Abstract
Cryopreservation is a technique to maintain biological materials’ physiological and genetic stability at an ultralow temperature. For commercially important livestock or aquatic species, gamete and embryo cryopreservation could play a significant role in breeding programs and commercial production. For example, it could help overcome key problems such as asynchronous maturation and an unbalanced sex ratio. However, the physiochemical stresses imposed by cryopreservation can negatively affect gametes and embryos, leading to a poor survival rate. Recent studies on cryoinjury have demonstrated that the cryosensitivity of lipids is one of the key causes of cryodamage in mammalians, as lipid compositions in membranes of gametes and embryos are closely related to their cryoresistance. In addition, the cryotolerance of gametes and embryos in some mammalian species has been improved by lipid modification. However, studies on the role of lipids in the cryopreservation of gametes, embryos, and larvae are rare in fish and shellfish. Therefore, this review focuses on recent methodological advances to improve cryotolerance by lipid modification, including lipid application or manipulation in human and livestock sperm, oocytes, and embryos, and how these novel approaches could improve cryopreservation techniques in aquatic species, especially for oocytes and embryos.
1 Introduction
Cryopreservation is a technique to store living materials (such as gametes, embryos, larvae, cells, and tissues) at an ultralow temperature to maintain their long-term physiological and genetic stability (Kopeika et al., 2015; Dhali et al., 2019). Cryopreservation of gametes, embryos and larvae (fish and shellfish) could play a significant role in reproductive and genetic improvement programs for commercially important livestock or aquatic species. It could also reduce the costs of transporting live animals for breeding and manage issues related to asynchronous maturation and unbalanced sex ratios (Huang et al., 2019; Díaz et al., 2021). The development of gamete and embryo cryopreservation protocols has been an integral step in advancing assisted reproductive technology (ART). From the first human infant derived from frozen sperm in 1953 () to the first human live birth after embryo cryopreservation in 1984 (Zeilmaker et al., 1984), ART in humans has become a mature technique. Cryopreservation techniques have also been greatly improved in livestock and pet animals (Galiguis et al., 2014; Mandal et al., 2014; Nagashima et al., 2015). In addition, the technical details of the governing factors and mechanisms contributing to cryoinjury have been gradually revealed (Kopeika et al., 2015; Dhali et al., 2019).
Several physical and chemical factors causing severe cryoinjuries have been reported in previous reviews in mammalian species (; Dhali et al., 2019). Among them, intracellular ice crystal formation, osmotic shock, free radicals such as reactive oxygen and nitrogen species (ROS and RNS), and lipid phase transition (LPT; a transition from a liquid phase to a crystalline-gel phase) are the primary factors causing cryoinjuries (Figueroa et al., 2019). Additionally, many adverse impacts of cryopreservation have been identified. For example, frozen-thawed sperm are characterized by lower motility, acrosome integrity, and mitochondrial membrane potential, resulting in low fertilization capacity (O’Connell et al., 2002; Ozkavukcu et al., 2008; Ugur et al., 2019). Fracture and membrane damage, mitochondrial dysfunction, and rupture and disruption of the cytoskeleton structure can negatively impact the further development of cryopreserved oocytes and embryos (Saunders and Parks, 1999; Kasai, 2002; Iussig et al., 2019; Gualtieri et al., 2021). At the molecular level, genomic DNA lesions and mitochondrial DNA damage have been detected in cryopreserved mammalian gametes and embryos (Lin and Tsai, 2012; Valcarce et al., 2013; Liu et al., 2016). Additionally, epigenetic and transcriptomic profiles are also susceptive to the stress caused by cryopreservation (Chatterjee et al., 2017; ).
Lipids are hydrophobic or amphiphilic molecules, including fatty acids (FAs), sterols, phospholipids (PLs) and triglycerides, and function as energy, signaling transduction, and cell membrane components (Fahy et al., 2009; Subramaniam et al., 2011). Lipid droplets (LDs) are also a significant component of oocytes, embryos and early-stage larvae in aquatic species. In gamete and embryo cryopreservation in mammalian species, among all chemical constituents, lipids such as the PLs - the main component of the plasma membrane, are the most susceptible to freezing damage (Quinn, 1985; Sieme et al., 2015). During the freezing process, LPT occurs, which is accompanied by the alteration in PLs structure and composition (Jung et al., 2014; Fang et al., 2016; Jung et al., 2021). The membrane then loses its high elasticity and becomes rigid, resulting in poor membrane permeability and hydrophobic molecule diffusion (). Ultimately, this process leads to the loss of cellular functionality (Hinkovska-Galcheva et al., 1989; Schuffner et al., 2001; Fang et al., 2016). Therefore, LPT at the nonphysiological temperature is considered one of the major causes of freezing damage. In general, mammalian gametes or embryos with lower LPT temperatures are likely to have better cryotolerance (Drobnis et al., 1993; Ghetler et al., 2005). Given that the LPT temperature is greatly dependent on lipid composition, features of the lipid profile are related to the cryoresistance of gametes and embryos. For example, the ratio between cholesterol and PL, and unsaturation rates are related to cryotolerance of spermatozoa (Waterhouse et al., 2006; Oldenhof et al., 2012), and lipid-rich oocytes or embryos usually exhibit high cryosensitivity. Therefore, lipid modification has become one of the key approaches to further improve post-thaw performances in mammalian gamete and embryo cryopreservation. For example, cryotolerance has been enhanced significantly by delipidation in lipid-rich oocytes and embryos () and membrane lipid replacement (MLR) in sperm (Vireque et al., 2016).
In aquatic animals, cryopreservation of oocytes, embryos and larvae is more challenging than sperm. Apart from their larger size and complex structure, the higher lipid content is another key factor that contributes to the chanlleges. For example, the egg lipid content is 32.4% on a wet weight basis in the whitefish Coregonus albula (V’uorela et al., 1979) and 38% on a dry weight basis in the Pacific oyster Magallana gigas (Massapina, 1999). These lipids serve as a vital energy reservoir for the early development of aquatic species as their digestive system has not fully evolved. Since lipid content and composition can affect cryotolerance, it is anticipated that lipid modification could play a similar role as in mammalians and improve the cryopreservation techniques in aquatic animals. Indeed, a few studies have demonstrated the potential of lipid modification in cryopreservation of gametes and larvae in aquatic animals. For instance, embryos produced from broodstock fed with diet supplemented with a fish oil showed a better permeability to cryoprotectants in Prochilodus lineatus (Costa et al., 2018). The supplement of exogenous lipids in cryoprotectants resulted in the improved performances in post-thaw fish sperm, and coral and oyster larvae (Cirino et al., 2021; Díaz et al., 2021; Zhu et al., 2023).
This review aims to update the recent development in lipid manipulation in the cryopreservation of sperm (both mammalian and aquatic species), oocytes (mammalian species), embryos (mammalian species), and larvae (aquatic species) and explore their applications to overcome some key challenges in aquatic species. In this review, we first discuss the effect and modification of lipids in the sperm, oocyte and embryo cryopreservation in mammalian species. We then present the recent development of lipid manipulation in cryopreservation of aquatic species. Finally we draw conclusions and propose future studies in aquatic species.
2 The effect of lipids on sperm cryopreservation in mammalian species
2.1 Current status of sperm cryopreservation
The cryopreservation of sperm is a reliable technique and has been extensively used in human ART and genetic germplasm conservation in livestock, and pet animals (Mandal et al., 2014).
This technique, however, has also showed several adverse effects on post-thaw spermatozoa, such as a decrease in motility and viability, the increase of single-strand DNA lesions, and the elevation of abnormal morphological characteristics (O’Connell et al., 2002; Ozkavukcu et al., 2008; Figueroa et al., 2019). It has been found that fluidity and permeability of the membrane serve a significant part in sperm cryoresistance and are related to the nature and percentage of PLs, polyunsaturated fatty acids (PUFAs), and cholesterol (Waterhouse et al., 2006; Oldenhof et al., 2012).
2.2 Plasma membrane lipid composition and sperm quality
Membrane lipid composition is diverse among organisms, cell type, organelle, membrane, bilayer-leaflet, and membrane subdomain levels (Harayama and Riezman, 2018). Compared with other tissues, spermatozoa membrane lipid is characterized by high PUFAs, especially dipolyunsaturated fatty acid (; Fang et al., 2016). Given the low LPT temperature of PUFAs and the kinks of double bonds in PUFAs hindering the acyl chains from packing, PUFAs increase overall membrane fluidity (Israelachvili et al., 1980; Sieme et al., 2015). In addition to the small size of spermatozoa, the high quantity of PUFAs also contributes to better cryoresistance in spermatozoa than in oocytes and embryos.
Spermatozoa membrane lipid composition varies between individuals, ages, and seasons (Kelso et al., 1996; ; ). These variations contribute to the difference in fresh sperm quality including motility and viability. In boar semen, for example, several lipid parameters such as the total lipid content, cholesterol, PL, n-3 PUFAs and Docosahexaenoic acid (DHA) are positively associated with sperm quality. On the other hand, saturated fatty acids (SFAs) and the ratio of n-6 to n-3 PUFAs are negatively correlated with sperm quality (). Similarly, in humans, PUFAs (especially DHA) play a significant role in normal sperm motility, concentration, and morphology, whereas monounsaturated fatty acids (MUFAs) adversely influence the quality parameters (; ).
2.3 Effect of cryopreservation on sperm lipid composition
The alteration of lipid composition in sperm can result in irreversible damage to the cellular membrane and the shift of cell homeostasis after cryopreservation (Schiller et al., 2000; Maldjian et al., 2005). In general, the changes can be summarized as follows: First, PUFAs and SFAs are commonly decreased and increased respectively as the result of lipid peroxidation after sperm cryopreservation in humans and domestic mammalians (; Schiller et al., 2000; Maldjian et al., 2005). Second, cryopreservation can reduce cholesterol levels (). Cholesterol plays a vital role in the structure and function of cell membranes, including the stability, permeability and fluidity of the cell membrane and the microenvironment of membrane proteins (Crockett, 1998; Partyka et al., 2016; Zhang et al., 2019). The loss of cholesterol can trigger the degeneration of the plasma membrane and apoptosis (). Third, the alteration of PLs composition and the translocation of membrane PLs have been found in frozen-thawed sperm (Schuffner et al., 2001; Fang et al., 2016). Normally, the distribution of PLs on the bilayer of the cellular membrane is asymmetric. For example, phosphatidylserine (PS), phosphatidylinositol (PI), and phosphatidylethanolamine (PE) are primarily distributed on the cytoplasmic leaflet, while Phosphatidylcholine (PC) and sphingomyelin (SM) are mainly located on the outer leaflet (Quinn, 2004; Fadeel and Xue, 2009).
The asymmetric distribution of PLs plays an important role in maintaining the physiological function of cells. Some specific proteins (e.g. protein kinase C, annexin, membrane skeletal proteins) are distributed on the cytoplasmic side by binding with PS (Manno et al., 2002). In the frozen-thawed sperm of ram, a significant reduction of PLs (PS, PI, PE, PG), an increase of diphosphatidylglycerol (DPG), and translocation of PLs between the cytoplasmic and outer layers were observed (Fang et al., 2016). Additionally, externalizations of PS and DPG were detected in cryopreserved ram sperm (Hinkovska-Galcheva et al., 1989; Schuffner et al., 2001). Hinkovska-Galcheva et al. (1989) suggested that the externalization of DPG inhibited the subsequent acrosome reaction and eventually impaired the fertilization capacity of sperm.
2.4 Lipid manipulation and sperm cryopreservation
Maintaining the lipid composition (PUFAs, cholesterol, PLs) and the physiological function of the membrane has been one of the key methods to improve the success rate of spermatozoa cryopreservation in many investigations (Ferreira et al., 2018). Egg yolk has become a common ingredient in the sperm extender in many mammalian species due to its protective influence (), which was first identified in bull semen (Phillips and Lardy, 1940). Despite the complex composition of egg yolks, low-density lipoprotein (LDL) plays a significant role in protecting spermatozoa in cryopreservation (Prapaiwan et al., 2015). In addition to egg yolk and LDL, other lipids, such as FAs and cholesterol, can also protect sperm during cryopreservation (Purdy and Graham, 2004; Moore et al., 2005; Hossain et al., 2007).
Three main strategies are currently used to modify the lipid compositions to counteract the cryopreservation stress in mammalian sperm. The first is the supplementation of PUFAs in diet, which has enhanced the performance of post-thaw sperm in a few species, such as water buffalo, and goat (Souza et al., 2019; Silva et al., 2020). The second is the in vitro sperm incubation with exogenous lipids to improve sperm cryotolerance in humans, bovine, and swine (He et al., 2001; Röpke et al., 2011; Ferreira et al., 2018). The third and most common strategy is the supplementation of exogenous lipids in the cryopreservation extender, which can provide almost instantaneous protection from cold shock and freezing to increase the sperm cryoresistance (Quinn et al., 1980; He et al., 2001; Vireque et al., 2016).
While the mechanism of freezing protection of sperm by exogenous lipids is not fully understood, some theories have been proposed. First, a “loose interaction” between PL and membrane bilayers was inferred by Quinn et al. (1980) and Simpson et al. (1987) in ram and boar sperm, where the protection of PC against the cold shock was instantaneous and could be readily disrupted by a gentle wash. Second, the adhesion of PL micelles to and possible formation of PL protective film on the membrane surface have been suggested for the improvement of sperm cryotolerance in many studies (Ricker et al., 2006; Zhang et al., 2009; Vireque et al., 2016). Third, the monomeric transfer and the fusion between the liposome and sperm membrane bilayers were detected by Gadella et al. (1999) using 6-(7-nitrobenz-2-oxa-1,3-diazol-4-yl) amino-caproyl (C6NBD) labeled PLs in boar. The incorporation of exogenous lipids into the sperm has also been confirmed by 14C-labeled FAs and octadecyl rhodamine B (Neill and Masters, 1972; Vasquez and Roldan, 1997). Therefore, the properties of the sperm membrane can be modified by manipulating exogenous lipids, which could improve sperm cryotolerance.
It is worth noting that the application of antioxidants in combination with exogenous lipids could enhance sperm cryoresistance by neutralizing the ROS produced during cryopreservation as lipids (especially PUFAs) are highly susceptible to this chemical (Ortega Ferrusola et al., 2009; Towhidi and Parks, 2012; Towhidi et al., 2013).
3 The impact of lipids on oocyte and embryo cryopreservation in mammalian species
3.1 Current status of oocyte and embryo cryopreservation
Aside from maternal genetic material, oocytes provide essential nutrients, energy, and mitochondria for subsequent development after fertilization (Kopeika et al., 2015). On the other hand, the embryo contain genetic material from both maternal and paternal sides. Compared to sperm, the larger size of oocytes and embryos reduces their cryotolerance (Pai et al., 2021). As oocytes and embryos share similarities in freezing sensitivity, the methods to modify their lipid compositions are discussed together.
After decades of effort, the viability of post-thaw oocytes and embryos in mammalians has improved substantially (Tharasanit and Thuwanut, 2021). In human, for example, the live birth rates of cryopreserved embryos and oocytes reach 41% and 32%, respectively (Fraison et al., 2023). In bovine, this rate has been improved to the fresh control level of 53% (Gómez et al., 2020). Compared with sperm, the substantially lower surface-to-volume ratio and higher cytoplasmic lipid content in oocytes and embryos also contribute to their higher cryosensitivity in mammalians (). In oocytes and embryors, lipids also aggregate into LDs, which are often structurally bound to key cellular organelles, such as mitochondrion and endoplasmic reticulum (ER), cytoskeleton (microfilaments and microtubules), and cellular membrane (Guo et al., 2009; Zhou and Li, 2009). While this structural association has yet to be fully understood, the cluster of LDs, ER, and mitochondrion facilitate lipid metabolism (Guo et al., 2009). LDs normally contain triglycerides, PLs, sterols, and FAs (Dunning et al., 2014) and serve as an energy resource during the development of oocytes and embryos (Romek et al., 2011; ). The phase separation and further consolidation of LDs during cryopreservation could reduce the chance of successful cryopreservation of oocytes and embryos ().
3.2 Lipid composition and cryopreservation of oocytes and embryos
Similar to sperm, the occurrence of LTP during cryopreservation is the primary source of cryodamage of oocytes and embryos (; ), which can change the properties of cellular membrane and disrupt its function (Quinn, 1985; Van Meer et al., 2008). Changes in lipid composition have also been observed in post-thaw oocytes and embryos. For instance, in comparison with the fresh controls, the levels of certain PLs were significantly lower in post-thaw bovine embryos (three lysophosphatidylcholines; Janati Idrissi et al., 2021) and mouse oocytes [phosphatidic acid (PA), lysophosphatidic acid (LPA), lysophosphatidylglycerol (LPG); Jung et al., 2021].
Lipid content and composition in oocytes and embryos are species-specific and important for assessing their quality and potential cryotolerance (Pereira and Marques, 2008). Empirically, those species with lipid-rich oocytes and embryos (e.g. pig and domestic cat) have poor cryoresistance (Nagashima et al., 1999; Pereira and Marques, 2008; Galiguis et al., 2014). However, a higher proportion of unsaturated lipids can also produce a better cryosurvival rate due to lower LPT temperatures (). For example, in comparison with bovine or ovine, the higher survival rate of cryopreserved embryos of domestic cats is attributed to being richer in unsaturated lipids (Pope, 2014; ). Lipid compositions also vary among breeding strains, individuals and seasons (Zeron et al., 2001; Sudano et al., 2012). For example, by using the MALDI-MS/MS laser-induced fragmentation technique (LIFT), Sudano et al. (2012) revealed that embryos of Simmental subspecies showed a better cryosurvival rate than Nellore subspecies due to significant differences in particular PCs [e.g. PC(32:0), PC (34:1), PC (34:2) and PC (36:5)], and suggested these PCs be used as biomarkers to predict the outcome of cryopreservation.
3.3 Lipid modification and oocyte and embryo cryopreservation
The modification of lipid composition is an important strategy to further improve the cryopreservation technique in mammalian oocytes and embryos in recent years. The main strategies include: 1) nutritional management; 2) delipidation using mechanical methods; 3) delipidation using chemical methods; and 4) cholesterol level modification. They are summerized in Table 1.
Table 1
| Lipid modification strategy | Method | Material | Post-thaw parameter improved | Reference |
|---|---|---|---|---|
| Nutritional management | Application of serum-free culture medium | Bovine embryos | Survival rate Hatching rate | |
| Application of serum-free culture medium | Domestic cat embryos | Hatching rate | Murakami et al., 2011 | |
| Conjugated linoleic acid treatment | Bovine embryos | Intact embryos rate Re-expanded embryos rate | Pereira et al., 2007 | |
| Bovine embryos | Re-expansion rate | Leão et al., 2015 | ||
| Bovine oocytes | Survival rate Cleavage rate | Matos et al., 2015 | ||
| Docosahexaenoic acid or linolenic acid treatment | Bovine embryos | Survival rate | ||
| Oleic acid treatment | Bovine embryos | Survival rate | ||
| Delipidation using mechanical method | Centrifugation and micromanipulation | Porcine oocytes | Survival rate Germinal vesicle breakdown rate Metaphase II rate | Hara et al., 2005 |
| Porcine embryos | Blastocyst rate | Nagashima et al., 1999 | ||
| Bovine zygotes | Survival rate Hatching rate | Diez et al., 2001 | ||
| Centrifugation | Domestic cat oocytes | Degeneration rate (reduced) | Galiguis et al., 2014 | |
| Delipidation using chemical method | Forskolin treatment | Swamp buffalo embryos | Morula rate Blastocyst rate Hatched blastocyst rate Cell numbers of blastocyst | Panyaboriban et al., 2018 |
| Bovine embryos | Blastocyst rate Hatched blastocyst rate Cell numbers of blastocyst | Panyaboriban et al., 2018 | ||
| Porcine oocytes | Survival rate | Fu et al., 2011 | ||
| Bovine embryos | Re-expansion rates | Meneghel et al., 2017 | ||
| L-Carnitine treatment | Bovine embryos | Survival rate | Takahashi et al., 2013 | |
| Bovine embryos | Recovery rate Hatching rate | Ghanem et al., 2014 | ||
| Acetyl-L-carnitine treatment | Buffalo oocytes | Cleavage rate Morula rate Blastocyst rate Mitochondrial membrane potential | Xu et al., 2019 | |
| Phenazine ethosulfate treatment | Bovine embryos | Recovery rate Hatching rate | Ghanem et al., 2014 | |
| Porcine embryos | Blastocyst rate | Gajda et al., 2008 | ||
| Cholesterol level modification | Cholesterol-loaded methyl-β-cyclodextrin treatment | Bovine oocytes | Cleavage rate Eight-cell rate | Horvath and Seidel, 2006 |
| Cholesterol-loaded methyl-β-cyclodextrin treatment before vitrification Methyl-β-cyclodextrin treatment after thawing | Bovine oocytes | Sperm binding capacity Two-pronuclear rate Cleavage rate Blastocyst rate Cell numbers of blastocyst | Hao et al., 2021 |
Lipid modification for improving the cryopreservation of oocytes and embryos in mammalian species.
3.3.1 Nutritional management
The lipid composition of a female diet can affect the quality of oocytes and embryos (Childs et al., 2008a; Childs et al., 2008b; Wonnacott et al., 2010), which can affect their resistance to freezing. For instance, a diet with the addition of PUFAs can increase the quality of oocytes in ewes (Zeron et al., 2002). The increase of long-chain PUFA content in the follicle component could lower the midpoint of the LPT temperature of sheep oocytes and result in a better membrane integrity rate after chilling (Zeron et al., 2002).
As lipid is the primary energy resource for oocytes and embryos, the lipid content can be reduced if the nutrient restriction is applied in vitro (). Sudano et al. (2011) also found that when a high fetal calf serum (FCS) concentration was used in the culture medium, LDs accumulated in both fresh and post-thaw bovine embryos, leading to a lower re-expansion rate after vitrification. Compared to the whole sheep serum, delipidated sheep serum in the culture medium could reduce the LDs content of ovine cumulus-oocyte complexes (). The application of serum-free culture medium has improved the survival rates of post-thaw bovine and domestic cat embryos (; Murakami et al., 2011).
Some FAs have also been supplemented in the in vitro culture medium to improve the cryosurvival of mammalian oocytes and embryos by altering their lipid compositions (; Leão et al., 2015; ). For example, conjugated linoleic acid (CLA) could reduce the accumulation of lipids to large- and medium-size LDs by inhibiting the expression and activities of stearoyl–CoA desaturase and lipoprotein lipase (Pariza et al., 2001). CLA could also improve membrane fluidity by incorporation between CLA fatty acyl residues and SM or PC (Leão et al., 2015), and it has a better free radical scavenging property than linoleic acid or methyl linoleate (Fagali and Catalá, 2008). Due to these three functions, CLA-treated bovine embryos showed a higher survival rate after cryopreservation than the untreated control (Pereira et al., 2007; Leão et al., 2015). In addition to CLA, the supplementation of linolenic acid, docosahexaenoic acid (DHA), and oleic acid in the in vitro medium could also improve the cryosurvival of bovine embryos (; Karaşahin, 2019; ).
3.3.2 Delipidation using mechanical methods
The mechanical approach is an option to remove lipids in lipid-rich oocytes and embryos (Nagashima et al., 1994; Nagashima et al., 1999). LDs can be extruded by centrifugation under a hypertonic condition or removed by micromanipulation after polarization by centrifugation. Both methods have significantly improved the post-thaw survival rate and further developmental capacity of porcine oocytes, embryos, and domestic cat zygotes (Hara et al., 2005; Karja et al., 2006; Nagashima et al., 1994). Furthermore, when the lipid polarization method was used in domestic cat oocytes, the cryosurvival rate was improved in partially polarized cat oocytes (Galiguis et al., 2014). In contrast, the developmental competence was compromised in fully polarized oocytes, probably due to the adverse effect of lipid redistribution (Galiguis et al., 2014).
3.3.3 Delipidation using chemical methods
In comparison with mechanical delipidation, the in vitro chemical treatment is a more prevalent lipid modification method in cryopreservation of oocytes and embryos. Forsklin, L-carnitine, and Phenazine ethosulfate are the main chemicals used in the culture medium to enhance lipolysis ().
Forskolin
Forskolin triggers adenylate cyclase, which can raise the cyclic adenosine monophosphate (cAMP) level and induce lipolysis (Paschoal et al., 2016). When 10 μM forskolin was applied in the medium for in vitro maturation, the development competence of porcine oocytes was not impaired and showed higher resistance against cryopreservation (Fu et al., 2011). Likewise, after incubation with 5.0 μM forskolin for 24 hours, bovine embryos had less lipid and greater cryotolerance (Meneghel et al., 2017). Besides diminishing lipid content, forskolin could also attenuate cytoskeleton actin filament damages caused by vitrification in bovine oocytes (Meneghel et al., 2017).
L-carnitine
In animal cells, the primary role of L-carnitine is to transfer long-chain FAs across the inner mitochondrial membrane for the subsequent β-oxidation. It is, therefore, an enhancer of lipid metabolism (Longo et al., 2016; ). L-carnitine supplementation could increase the rate of zygote development to the blastocyst stage and improve the survival rate after cryopreservation in bovine (Takahashi et al., 2013). L-carnitine could also reduce ROS formation during vitrification (Sprícigo et al., 2017). Thus, the supplementation of L-carnitine could not only lower the density of LDs and modify the PL composition, but it could also enhance the physiological function of mitochondria (Somfai et al., 2011; Xu et al., 2019).
Phenazine ethosulfate
Phenazine ethosulfate (PES) can oxidize nicotinamide adenine dinucleotide phosphate hydrogen to nicotinamide adenine dinucleotide phosphate and arouse the pentose-phosphate pathway to generate more Adenosine triphosphate (ATP) through glucose metabolism (De La Torre-Sanchez et al., 2006; ). The lipid accumulation in bovine and porcine embryos could be inhibited when incubated with PES (De La Torre-Sanchez et al., 2006; Gajda et al., 2011). Ghanem et al. (2014) found that PES-treated bovine embryos showed enhanced cryotolerance.
3.3.4 Cholesterol level modification
A high ratio between cholesterol and PL in the cytoplasm membrane is usually associated with higher membrane fluidity, especially at low temperatures, meaning that cholesterol content in the membrane bilayer can affect the cryotolerance of oocytes (Horvath and Seidel, 2006). Methyl-β-cyclodextrin (MBC) is a water-soluble cyclic heptasaccharide that can be used to deliver hydrophobic substances, such as cholesterol or FAs, through its hydrophobic cylindrical cavity (). Horvath and Seidel (2006) showed that Cholesterol-loaded Methyl-β-cyclodextrin (CLC) treated oocytes had a better cleavage and 8-cells rate compared to untreated oocytes in bovine vitrification, although the advantage was not apparent in subsequent development. Conversely, found that CLC treatment did not significantly affect the cleavage and blastocyst rate in the same species. Nevertheless, the expression of some development-related genes (e.g. DNMT3A and BAX) indicates that oocytes treated by CLC could have a better quality, especially when they are vitrified at the germinal vesicle stage ().
4 Lipid manipulation in cryopreservation of aquatic species
4.1 Current status of cryopreservation of gametes, embryos and larvae
The first successful fish sperm cryopreservation in aquatic species was reported in 1953 (), almost at the same time as that of domestic mammalians. However, despite sperm cryopreservation having become a lucrative global industry in the livestock sector, it has not been widely applied to commercially important aquatic species (Tiersch et al., 2007; Migaud et al., 2013). The development of cryopreservation technique in oocytes, embryos, and larvae in aquatic species is still in its early stages, and has focused on the selection of cryoprotectant, optimization of freezing rate, and assessment of developmental stages suitable for freezing (Martínez-Páramo et al., 2017). The potential application of cryopreservation in the aquaculture industry is significant, as it could resolve key issues during seed production, such as the unbalanced sex ratio of broodstock, asynchronous sexual maturation, long-distance broodstock transportation, and seasonal constraints. This technique could also play an essential role in germplasm resource protection of rare breeding varieties and endangered species, especially in the face of natural disasters, environmental pollution, and disease outbreak (Liu et al., 2020a; Díaz et al., 2021).
To date, hundreds of fish sperm cryopreservation protocols have been reported and comprehensively reviewed by , Tsai and Lin (2012), and Martínez-Páramo et al. (2017). Sperm cryopreservation techniques have also been developed for most farmed and some ecologically important aquatic invertebrates (Diwan et al., 2020). The freezing of oocytes, embryos, and larvae in aquatic organisms is more challenging than that of spermatozoa. In comparison with sperm, the additional challenges are their poor membrane permeability, large size, high lipid content, and high sensitivity to temperature shock (Martínez-Páramo et al., 2017; Diwan et al., 2020). Although studies on cryopreservation of early-stage oocytes (Tsai et al., 2009), ovarian tissue fragments (), and primordial germ cells or a genital ridge (Kobayashi et al., 2007; Higaki et al., 2010; Inoue et al., 2012) have occurred in some fish species, these methods are subject to the success of subsequent in vitro maturation or transplantation. Compared with fish, the cryopreservation of oocytes, embryos and larvae of aquatic invertebrates is more promising due to their holoblastic cleavage, relatively less egg lipid content, and smaller size (Martínez-Páramo et al., 2017). To date, studies on larval cryopreservation have been reported in crustaceans (Subramoniam and Newton, 1993; Huang et al., 2017; Diwan et al., 2020) and echinoderms (Paredes, 2016; Dupré and Carvajal, 2019), and successful cryopreservation of oocytes, embryos and/or larvae has been published in mollusks (Tervit et al., 2005; Liu and Li, 2015; Liu et al., 2020b; Heres et al., 2021) and corals (Daly et al., 2018), although the post-thaw oocyte survival rates were low (Tervit et al., 2005; Liu and Li, 2015). Progresses of molluscan larval cryopreservation have been summarized recently by Yang and Huo (2022).
4.2 Lipid modification and cryopreservation
As with livestock, the relationship between gamete or embryo quality and lipid composition has been established in many aquatic species, especially those of commercial importance (Mansour et al., 2011; ; Glandon et al., 2016; Díaz et al., 2018). However, studies on lipid composition and cryopreservation are limited in aquatic species. Based on mammalian studies, it can be assumed that membrane fluidity, permeability, and lipid composition can play a similar role in the cryosurvival of gametes, embryos and larvae in aquatic animals, which has been demonstrated recently in Pacific oysters (Zhu et al., 2023). Therefore, lipid manipulations could enhance cryotolerance in aquatic species.
4.2.1 Lipid modification through nutritional management
To improve gamete quality, gamete lipid modification through dietary manipulation during broodstock conditioning is common in aquatic species (Helm et al., 1973; Fernández-Palacios et al., 1997; ; Ehteshami et al., 2011; Diogo et al., 2015; Valdebenito et al., 2015). Promising results have been reported in a few studies related to sperm or oocyte cryotolerance. For instance, a fish oil-supplement diet for broodstocks of Prochilodus lineatus led to a higher amount of total PUFAs, n-6 PUFAs, and long-chain PUFAs, and a lower amount of total MUFAs in the embryos. Those embryos also presented better permeability to cryoprotectants (1,2-Propanediol; Costa et al., 2018). Bivalves usually do not have sufficient capability to elongate and desaturate short-chain saturated FAs to long-chain PUFAs (de Moreno et al., 1976; de Moreno et al., 1977; Helm et al., 1991). Hence dietary lipid profiles can significantly affect the composition of FAs in bivalves (Langdon and Waldock, 1981; Dudognon et al., 2014). In Pacific oysters, when the broodstock was fed with microalgae containing a high fraction of PUFAs during cold preconditioning at 9 °C, the fertilization rate of post-thaw oocytes was significantly increased in comparison with the control (). These authors have proposed that the absolute content of PUFAs, rather than the ratios between PUFAs and MUFAs or SFAs, plays a vital role in cryotolerance of post-thaw oocytes.
4.2.2 Lipid modification and sperm cryopreservation
In addition to lipid modification through diet, there have been a few examples of improving sperm tolerance by supplementary FAs, cholesterol, and LDLs in fish sperm extenders (Table 2). According to Lahnsteiner et al. (2009), when FAs (including palmitic acid, arachidonic acid, linoleic acid, and arachidic acid) were added to the rainbow trout (Oncorhynchus mykiss) sperm motility-inhibiting extenders, the motility rate and the average path velocity were improved after 72 h storage at 4°C. However, their cryotolerance was not enhanced in the same study. On the contrary, when the arachidonic acids were used in the freezing medium of Atlantic salmon (Salmo salar), the membrane integrity and fertility rate of post-thaw sperm were significantly increased (Díaz et al., 2021). It is worth mentioning that the protective effect of egg yolk in the extender in the study by Lahnsteiner et al. (2009) was likely to be veiled by its LDL component (Pérez-Cerezales et al., 2010). The impact of cholesterol in sperm cryopreservation is species-specific. Its addition had no positive effect on the viability of cryopreserved sperm in S. Salar (Díaz et al., 2021), whereas showed significant improvement in cryoresistence in the common carp (Cyprinus carpio) when was used at a dose of 1.5 mg cholesterol per 120 × 106 spermatozoa (Yildiz et al., 2015).
Table 2
| Material cryopreserved | Species | Supplements - exogenous lipids and other chemicals | Base extenders/Cryoprotectants | Post-thaw parameters improved | Reference |
|---|---|---|---|---|---|
| Sperm | Prochilodus brevis | Egg yolk | 5% glucose 10% dimethyl sulfoxide | Membrane integrity | Torres et al., 2022 |
| Rasbora tawarensis | Egg yolk | Ringer’s solution /5% dimethyl sulfoxide | Mortility Fertilization rate Hatching rate | Muchlisin et al., 2020 | |
| Salmo salar | Arachidonic acid | Cortland® medium | Mortility Membrane integrity Mitochondrial membrane potential Fertility | Díaz et al., 2021 | |
| Oncorhynchus mykiss | Low density lipoprotein | Erdahl & Graham’s /7% dimethyl sulfoxide | Membrane integrity DNA integrity Eyed embryo survival rate | Pérez-Cerezales et al., 2010 | |
| Cyprinus carpio | Cholesterol-loaded cyclodextrin | 300 mM glucose, 10% dimethyl sulfoxide | Motility Duration of motility Vitality rate Fertilization rate | Yildiz et al., 2015 | |
| Larval cells | Mytilus trossulus | Lipid extract from Crenomytilus grayanus, vitamine C and vitamine E | 10% dimethyl sulfoxide 1.5% trehalose | Vitality rate Unsaturation index | Kostetsky et al., 2008 |
| Larval cells | Strongylocentrotus intermedius | Lipid extract from Crenomytilus grayanus, echinochrome | 6% dimethyl sulfoxide 4 mM trehalose | Survival rate RNA synthesis level | Odintsova et al., 2009 |
| Larvae | Seriatopora caliendrum | Erucic acid | 2 M ethylene glycol (EG), 1 M propylene glycol (PG), 40% (w/v) Ficoll, 10% gold nanoparticles | Survival rate | Cirino et al., 2021 |
| Larvae | Pocillopora verrucosa | Phosphatidylethanolamine | 2 M ethylene glycol (EG), 1 M propylene glycol (PG), 40% (w/v) Ficoll, 10% gold nanoparticles | Settlement rate | Cirino et al., 2021 |
| Trochophore larvae | Magallana gigas | 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine, α-tocopherol | 10% (v/v) ethylene glycol (EG) 5% (w/v) Ficoll (FIC) 0.2% (w/v) polyvinylpyrrolidone | D-stage larvae survival rate Spat yield | Zhu et al., 2023 |
Positive effects of exogenous lipid supplements in cryopreservation in aquatic animals.
4.2.3 Lipid modification and oocyte and larval cryopreservation
Total lipid extracts from aquatic invertebrates present cryoprotective abilities when they were added into the medium to cryopreserve molluscan primary larval cells (Odintsova et al., 2001; Odintsova et al., 2006; Kostetsky et al., 2008). For example, the post-thaw survival rate of Mytilus trossulus trochophore larval cells was increased from 5% to 13% by the addition of lipid extract of Crenomytilus grayanus, which was further improved to 35% when antioxidants (vitamin C and vitamin E) were supplemented (Kostetsky et al., 2008). The lipid profile analysis revealed that the addition of lipid extracts and antioxidants effectively increased percentages of MUFAs, PUFAs, n-3 PUFAs, n-6 PUFAs, and the unsaturation index and reduced the percentage of SFAs in the post-thaw larval cells (Kostetsky et al., 2008).
Attempts have also been made to alter the lipid composition of oocytes and larvae to improve cryoresistance. For example, Salinas-Flores et al. (2008) cultured the oocytes of M. gigas with CLC and MBC to increase and decrease the cholesterol level in the oocyte, respectively. Although the incorporation of cholesterol in oocytes was confirmed by fluorescence assessment, the treated and untreated oocytes showed similar post-thaw fertilization rates. In corals, Cirino et al. (2021) reported a methodology to improve the cryoresistance of coral larvae by adding exogenous lipids and gold nanoparticles to the vitrification solution. The vitality rate of vitrified Seriatopora caliendrum larvae was increased by erucic acid liposomes, whereas the settlement rate of vitrified Pocillopora verrucosa larvae was enhanced by PE liposomes. In addition, the survival rate of post-thaw M. gigas larvae was significantly improved by including 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine (POPC) and α-tocopherol in the cryopreservation medium (Zhu et al., 2023).
5 Conclusions and future research in aquatic species
The development of oocyte, embryo and larvae cryopreservation techniques is still in its early stages in aquatic organisms, although progresses have been made in some species, especially in bivalves. In comparison with mammalians, aquatic species possess even higher intracellular lipid content in oocytes, embryos and early-stage larvae (prior to feeding), which means that the cryopreservation of these materials might be more challenging. Therefore, the introduction of lipid modification might be a cornerstone in the development of cryopreservation techniques in aquatic species. The following will be the primary aspects the future studies should focus on.
While the relationship between lipid composition and gamete quality and/or development capability has been investigated in some species, most of these studies have not been focused on cryopreservation. Therefore, investigations on the relationship between specific lipid composition and cryotolerance would be a key research priority, which could be achieved by manipulating nutritional ingredients. Theoretically, when broodstock are fed with a diet rich in PUFAs during gametogenesis, they are likely to yield gametes with lower LPT, thus enhancing the cryoresistance of both gametes produced and the resulting embryos and larvae.
Given its effectiveness in larvae cryopreservation in some bivalve and coral species, the application of exogenous lipids (e.g. PLs, and lipid extract from hydrobiontes) in the cryoprotectant is likely to offer a new strategy to optimize existing or develop new larvae cryopreservation techniques. Due to the hydrophobic nature of exogenous lipids, they usually present in the form of liposomes in extenders or cryoprotectants. Their particle size and other properties could affect their interaction with plasma membrane and subsequently the cryopreservation outcomes. For example, sonicating the extender containing egg yolk has resulted in smaller liposomes and better post-thaw motility in donkey sperm compared to that without the treatment (Zhang et al., 2018). In the study by Cirino et al. (2021), the application of gold nanoparticles played a significant role in the success of coral larval cryopreservation because gold nanoparticles can change the biophysic features of liposomes such as zeta potential, temperature of LPT (Mady et al., 2012). Therefore, understanding the biophysical characteristics of liposomes and their effects on the cryopreserved materials will be beneficial for the further improvement of cryopreservation techniques.
Furthermore, partial removal of yolk through micromanipulation would be worth trying to improve the cryosurvival of oocytes, embryos, and larvae in aquatic animals when their cryopreservation has been investigated by optimizing other parameters. This method may not only hold significance academically but could also be critical to establish cryopreservation techniques, although the application of this technique might be limited to specific requirements such as gene banking and difficult to meet the quantity demands for commercial hatchery production. With the development of extended in vitro oocyte culture techniques in aquatic species, chemical delipidation and in virto lipid modulation could become practicable. This method would have broader applications than micromanipulation, since it could manipulate a larger quantity of materials.
As the vitrification method has been routinely used in the cryopreservation of oocyts and embryos in some mammalian species, including lipid-rich materials (; Du et al., 2021; Tharasanit and Thuwanut, 2021), and has also been successfully applied in a couple of coral species (Daly et al., 2018; Narida et al., 2023), the integratation of lipid modification and vitrification is likely to become a novel technological pathway for the cryopreservation of oocytes, embryos, and larvae in aquatic organisms.
Statements
Author contributions
XZ conceived and developed the idea and prepared the draft of the manuscript. YZ, YL, and YT helped for the collection of references and provided comments and suggestions to improve the manuscript. PM-E, JQ, and XL have critically gone through the draft and finalized the manuscript. All authors contributed to the article and approved the submitted version.
Acknowledgments
Mr. XZ is grateful for the financial support of the Australian Government Research Training Program Scholarship (AGRTPS) for his PhD study at Flinders University. Dr. YZ acknowledges the financial support provided by the Overseas Training Program for Colleges and Universities of Liaoning Province (2020GJWYB017).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
1
AardemaH.BertijnI.Van TolH.RijneveldA.VernooijJ.GadellaB. M.et al. (2022). Fatty acid supplementation during in vitro embryo production determines cryosurvival characteristics of bovine blastocysts. Front. Cell Dev. Biol.10. doi: 10.3389/fcell.2022.837405
2
AbeH.YamashitaS.SatohT.HoshiH. (2002). Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Mol. Reprod. Dev.61, 57–66. doi: 10.1002/mrd.1131
3
AdamsS. L.Salinas-FloresL.LimM. H. (2013). Diet conditioning of Pacific oyster, Crassostrea gigas , broodstock to improve oocyte cryopreservation success. J. Shellfish Res.32, 391–399. doi: 10.2983/035.032.0219
4
AitkenR. J. (2011). The capacitation-apoptosis highway: oxysterols and mamMalian sperm function. Biol. Reprod.85, 9–12. doi: 10.1095/biolreprod.111.092528
5
AksoyY.AksoyH.AltınkaynakK.AydınH. R.ÖzkanA. (2006). Sperm fatty acid composition in subfertile men. Prostaglandins Leukot. Essent. Fatty Acids75, 75–79. doi: 10.1016/j.plefa.2006.06.002
6
Al DarwichA.PerreauC.PetitM. H.PapillierP.DupontJ.GuillaumeD.et al. (2010). Effect of PUFA on embryo cryoresistance, gene expression and AMPKα phosphorylation in IVF-derived bovine embryos. Prostaglandins Other Lipid Mediators93, 30–36. doi: 10.1016/j.prostaglandins.2010.06.002
7
AlvarezJ. G.StoreyB. T. (1992). Evidence for increased lipid peroxidative damage and loss of superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during cryopreservation. J. Androl.13, 232–241.
8
Am-inN.KirkwoodR. N.TechakumphuM.TantasuparukW. (2011). Lipid profiles of sperm and seminal plasma from boars having normal or low sperm motility. Theriogenology75, 897–903. doi: 10.1016/j.theriogenology.2010.10.032
9
AmstislavskyS.MokrousovaV.BrusentsevE.OkotrubK.ComizzoliP. (2019). Influence of cellular lipids on cryopreservation of mamMalian oocytes and preimplantation embryos: a review. Biopreserv. Biobank.17, 76–83. doi: 10.1089/bio.2018.0039
10
AndersenJ. M.RønningP. O.HerningH.BekkenS. D.HaugenT. B.WitczakO. (2016). Fatty acid composition of spermatozoa is associated with BMI and with semen quality. Andrology4, 857–865. doi: 10.1111/andr.12227
11
AnilS.ZampollaT.ZhangT. (2011). Development of in vitro culture method for zebrafish ovarian tissue fragment. Cryobiology63, 311–312. doi: 10.1016/j.cryobiol.2011.09.025
12
AnzarM.RajapakshaK.BoswallL. (2019). Egg yolk-free cryopreservation of bull semen. PLoS One14, e0223977. doi: 10.1371/journal.pone.0223977
13
AravA.ZeronY.LeslieS. B.BehboodiE.AndersonG. B.CroweJ. H. (1996). Phase transition temperature and chilling sensitivity of bovine oocytes. Cryobiology33, 589–599. doi: 10.1006/cryo.1996.0062
14
ArcaronsN.MoratóR.VendrellM.YesteM.López-BejarM.RajapakshaK.et al. (2017). Cholesterol added prior to vitrification on the cryotolerance of immature and in vitro matured bovine oocytes. PLoS One12, e0184714. doi: 10.1371/journal.pone.0184714
15
Argov-ArgamanN.MahgreftheK.ZeronY.RothZ. (2013a). Season-induced variation in lipid composition is associated with semen quality in Holstein bulls. Reproduction145, 479–489. doi: 10.1530/REP-12-0498
16
Argov-ArgamanN.MahgreftheK.ZeronY.RothZ. (2013b). Variation in lipid profiles within semen compartments—the bovine model of aging. Theriogenology80, 712–721. doi: 10.1016/j.theriogenology.2013.05.024
17
AsturianoJ. F.SorberaL. A.CarrilloM.ZanuyS.RamosJ.NavarroJ. C.et al. (2001). Reproductive performance in male European sea bass (Dicentrarchus labrax, L.) fed two PUFA-enriched experimental diets: a comparison with males fed a wet diet. Aquaculture194, 173–190. doi: 10.1016/S0044-8486(00)00515-9
18
BarberetJ.BarryF.ChouxC.GuillemanM.KarouiS.SimonotR.et al. (2020). What impact does oocyte vitrification have on epigenetics and gene expression? Clin. Epigenet.12, 121. doi: 10.1186/s13148-020-00911-8
19
Barceló-FimbresM.SeidelG. E. (2007). Effects of either glucose or fructose and metabolic regulators on bovine embryo development and lipid accumulation in vitro. Mol. Reprod. Dev.74, 1406–1418. doi: 10.1002/mrd.20700
20
BarreraN.dos Santos NetoP. C.CuadroF.BosolascoD.MuletA. P.CrispoM.et al. (2018). Impact of delipidated estrous sheep serum supplementation on in vitro maturation, cryotolerance and endoplasmic reticulum stress gene expression of sheep oocytes. PLoS One13, e0198742. doi: 10.1371/journal.pone.0198742
21
BeirãoJ.ZilliL.VilellaS.CabritaE.Fernández-DíezC.SchiavoneR.et al. (2012). Fatty acid composition of the head membrane and flagella affects Sparus aurata sperm quality. J. Appl. Ichthyol.28, 1017–1019. doi: 10.1111/jai.12085
22
BellM. V.DickJ. R.BudaCs. (1997). Molecular speciation of fish sperm phospholipids: Large amounts of dipolyunsaturated phosphatidylserine. Lipids32, 1085–1091. doi: 10.1007/s11745-997-0140-y
23
BlaxterJ. H. S. (1953). Sperm storage and cross-fertilization of spring and autumn spawning herring. Nature172, 1189–1190. doi: 10.1038/1721189b0
24
BorgesE. D.VirequeA. A. (2019). Updating the impact of lipid metabolism modulation and lipidomic profiling on oocyte cryopreservation. Euro. Med. J.4, 79–87. doi: 10.33590/emj/10310074
25
BrewsterM. E.LoftssonT. (2007). Cyclodextrins as pharmaceutical solubilizers. Adv. Drug Deliv. Rev.59, 645–666. doi: 10.1016/j.addr.2007.05.012
26
BungeR. G.ShermanJ. K. (1953). Fertilizing capacity of frozen human spermatozoa. Nature172, 767–768. doi: 10.1038/172767b0
27
CabritaE.SarasqueteC.Martínez-PáramoS.RoblesV.BeirãoJ.Pérez-CerezalesS.et al. (2010). Cryopreservation of fish sperm: applications and perspectives: Cryopreservation of fish sperm. J. Appl. Ichthyol.26, 623–635. doi: 10.1111/j.1439-0426.2010.01556.x
28
CeroliniS.KelsoK. A.NobleR. C.SpeakeB. K.PizziF.CavalchiniL. G. (1997). Relationship between spermatozoan lipid composition and fertility during aging of chickens. Biol. Reprod.57, 976–980. doi: 10.1095/biolreprod57.5.976
29
CeroliniS.MaldjianA.PizziF.GliozziT. (2001). Changes in sperm quality and lipid composition during cryopreservation of boar semen. Reproduction121, 395–401. doi: 10.1530/rep.0.1210395
30
ChatterjeeA.SahaD.NiemannH.GryshkovO.GlasmacherB.HofmannN. (2017). Effects of cryopreservation on the epigenetic profile of cells. Cryobiology74, 1–7. doi: 10.1016/j.cryobiol.2016.12.002
31
ChildsS.CarterF.LynchC. O.SreenanJ. M.LonerganP.HennessyA. A.et al. (2008a). Embryo yield and quality following dietary supplementation of beef heifers with n-3 polyunsaturated fatty acids (PUFA). Theriogenology70, 992–1003. doi: 10.1016/j.theriogenology.2008.06.008
32
ChildsS.HennessyA. A.SreenanJ. M.WathesD. C.ChengZ.StantonC.et al. (2008b). Effect of level of dietary n-3 polyunsaturated fatty acid supplementation on systemic and tissue fatty acid concentrations and on selected reproductive variables in cattle. Theriogenology70, 595–611. doi: 10.1016/j.theriogenology.2008.04.002
33
CirinoL.TsaiS.WangL.-H.ChenC.-S.HsiehW.-C.HuangC.-L.et al. (2021). Supplementation of exogenous lipids via liposomes improves coral larvae settlement post-cryopreservation and nano-laser warming. Cryobiology98, 80–86. doi: 10.1016/j.cryobiol.2020.12.004
34
CostaR.daS.SouzaF. M. S.SenhoriniJ. A.Bashiyo-SilvaC.Verissímo-SilveiraR.et al. (2018). Fatty acid influence on Prochilodus lineatus (Characiformes, Prochilodontidae) embryo cryopreservation parameters. Aquac. Res.49, 2714–2722. doi: 10.1111/are.13732
35
CrockettE. L. (1998). Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperature. Am. Zool.38, 291–304. doi: 10.1093/icb/38.2.291
36
DalyJ.ZuchowiczN.Nuñez LendoC. I.KhoslaK.LagerC.HenleyE. M.et al. (2018). Successful cryopreservation of coral larvae using vitrification and laser warming. Sci. Rep.8, 15714. doi: 10.1038/s41598-018-34035-0
37
De La Torre-SanchezJ. F.GardnerD. K.PreisK.GibbonsJ.SeidelG. E. (2006). Metabolic regulation of in vitro-produced bovine embryos. II. Effects of phenazine ethosulfate, sodium azide and 2,4-dinitrophenol during post-compaction development on glucose metabolism and lipid accumulation. Reprod. Fertil. Dev.18, 597. doi: 10.1071/RD05064
38
de MorenoJ. E. A.MorenoV. J.BrennerR. R. (1976). Lipid metabolism of the yellow clam, Mesodesma mactroides: 2-Polyunsaturated fatty acid metabolism. Lipids11, 561–566. doi: 10.1007/BF02532902
39
de MorenoJ. E. A.MorenoV. J.BrennerR. R. (1977). Lipid metabolism of the yellow clam, Mesodesma mactroides: 3-Saturated fatty acids and acetate metabolism. Lipids12, 804–808. doi: 10.1007/BF02533268
40
DhaliA. P.KolteA.MishraA. C.RoyS.BhattaR. (2019). “Cryopreservation of oocytes and embryos: current status and opportunities,” in Infertility, Assisted Reproductive Technologies and Hormone Assays. Ed. SheriffD.S. (London, United Kingdom: IntechOpen). doi: 10.5772/intechopen.81653
41
DíazR.Lee-EstévezM.FigueroaE.Ulloa-RodríguezP.SepúlvedaN.FariasJ. G. (2018). Study of the membrane lipid composition of Atlantic salmon ( Salmo salar ) spermatozoa and its relation with semen quality. Aquac. Res.49, 2603–2607. doi: 10.1111/are.13713
42
DíazR.QuiñonesJ.ShortS.ContrerasP.Ulloa-RodríguezP.Cancino-BaierD.et al. (2021). Effect of exogenous lipids on cryotolerance of Atlantic salmon (Salmo salar) spermatozoa. Cryobiology98, 25–32. doi: 10.1016/j.cryobiol.2021.01.004
43
DiezC.HeymanY.Le BourhisD.Guyader-JolyC.DegrouardJ.RenardJ. P. (2001). Delipidating in vitro-produced bovine zygotes: Effect on further development and consequences for freezability. Theriogenology55, 923–936. doi: 10.1016/S0093-691X(01)00454-X
44
DiogoP.MartinsG.GavaiaP.PintoW.DiasJ.CancelaL.et al. (2015). Assessment of nutritional supplementation in phospholipids on the reproductive performance of zebrafish, Danio rerio (Hamilton 1822). J. Appl. Ichthyol.31, 3–9. doi: 10.1111/jai.12733
45
DiwanA. D.HarkeS. N.GopalkrishnaPancheA. N. (2020). Cryobanking of fish and shellfish egg, embryos and larvae: an overview. Front. Mar. Sci.7. doi: 10.3389/fmars.2020.00251
46
DrobnisE. Z.CroweL. M.BergerT.AnchordoguyT. J.OverstreetJ. W.CroweJ. H. (1993). Cold shock damage is due to lipid phase transitions in cell membranes: A demonstration using sperm as a model. J. Exp. Zool.265, 432–437. doi: 10.1002/jez.1402650413
47
DuX.ZhuanQ.ChengK.LuoY.HouY.ZhuS.et al. (2021). Cryopreservation of porcine embryos: Recent updates and progress. Biopreserv. Biobank.19, 210–218. doi: 10.1089/bio.2020.0074
48
DudognonT.LambertC.QuereC.AuffretM.SoudantP.KraffeE. (2014). Mitochondrial activity, hemocyte parameters and lipid composition modulation by dietary conditioning in the Pacific oyster Crassostrea gigas. J. Comp. Physiol. B184, 303–317. doi: 10.1007/s00360-013-0800-1
49
DunningK. R.RussellD. L.RobkerR. L. (2014). Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation. Reproduction148, R15–R27. doi: 10.1530/REP-13-0251
50
DupréE.CarvajalJ. (2019). Cryopreservation of embryos and larvae of the edible sea urchin loxechinus albus (Molina 1782). Cryobiology86, 84–88. doi: 10.1016/j.cryobiol.2018.11.005
51
EhteshamiF.ChristianusA.RameshiH.HarminS. A.SaadC. R. (2011). The effects of dietary supplements of polyunsaturated fatty acid on pearl oyster, Pinctada margaritifera L., gonad composition and reproductive output: The effects of dietary supplements of PUFA on pearl oyster. Aquac. Res.42, 613–622. doi: 10.1111/j.1365-2109.2010.02658.x
52
FadeelB.XueD. (2009). The ins and outs of phospholipid asymmetry in the plasma membrane: roles in health and disease. Crit. Rev. Biochem. Mol. Biol.44, 264–277. doi: 10.1080/10409230903193307
53
FagaliN.CataláA. (2008). Antioxidant activity of conjugated linoleic acid isomers, linoleic acid and its methyl ester determined by photoemission and DPPH techniques. Biophys. Chem.137, 56–62. doi: 10.1016/j.bpc.2008.07.001
54
FahyE.SubramaniamS.MurphyR. C.NishijimaM.RaetzC. R. H.ShimizuT.et al. (2009). Update of the LIPID MAPS comprehensive classification system for lipids. J. Lipid Res.50, S9–S14. doi: 10.1194/jlr.R800095-JLR200
55
FangY.BlairH.ZhongR.SunH.ZhouD. (2016). Optimizing the freezing rate for ovine semen cryopreservation: phospholipid profiles and functions of the plasma membrane and quality and fertilization of spermatozoa. Small Rumin. Res.139, 46–51. doi: 10.1016/j.smallrumres.2016.04.012
56
Fernández-PalaciosH.IzquierdoM.RobainaL.ValenciaA.SalhiM.MonteroD. (1997). The effect of dietary protein and lipid from squid and fish meals on egg quality of broodstock for gilthead seabream (Sparus aurata). Aquaculture148, 233–246. doi: 10.1016/S0044-8486(96)01312-9
57
FerreiraG.CostaC.BassaizteguyV.SantosM.CardozoR.MontesJ.et al. (2018). InCubation of human sperm with micelles made from glycerophospholipid mixtures increases sperm motility and resistance to oxidative stress. PLoS One13, e0197897. doi: 10.1371/journal.pone.0197897
58
FigueroaE.Lee-EstevezM.ValdebenitoI.WatanabeI.OliveiraR. P. S.RomeroJ.et al. (2019). Effects of cryopreservation on mitochondrial function and sperm quality in fish. Aquaculture511, 634190. doi: 10.1016/j.aquaculture.2019.06.004
59
FraisonE.HuberlantS.LabruneE.CavalieriM.MontagutM.BrugnonF.et al. (2023). Live birth rate after female fertility preservation for cancer or haematopoietic stem cell transplantation: a systematic review and meta-analysis of the three main techniques; embryo, oocyte and ovarian tissue cryopreservation. Hum. Reprod.38, 489–502. doi: 10.1093/humrep/deac249
60
FuX.-W.WuG.-Q.LiJ.-J.HouY.-P.ZhouG.-B.Lun-Suoet al. (2011). Positive effects of Forskolin (stimulator of lipolysis) treatment on cryosurvival of in vitro matured porcine oocytes. Theriogenology75, 268–275. doi: 10.1016/j.theriogenology.2010.08.013
61
GadellaB. M.MillerN. G. A.ColenbranderB.Van GoldeL. M. G.HarrisonR. A. P. (1999). Flow cytometric detection of transbilayer movement of fluorescent phospholipid analogues across the boar sperm plasma membrane: Elimination of labeling artifacts. Mol. Reprod. Dev.53, 108–125. doi: 10.1002/(SICI)1098-2795(199905)53:1<108::AID-MRD13>3.0.CO;2-K
62
GajdaB.RomekM.GradI.KrzysztofowiczE.BrylaM.SmoragZ. (2011). Lipid content and cryotolerance of porcine embryos cultured with phenazine ethosulfate. Cryo Lett.32, 349–357.
63
GajdaB.SmoragZ.BrylaM. (2008). Effect of phenazine ethosulfate on porcine blastocyst development, apoptosis, and cryotolerance after open pulled straw vitrification. Reprod. Fertil. Dev.20, 118. doi: 10.1071/RDv20n1Ab75
64
GaliguisJ.GómezM. C.LeiboS. P.PopeC. E. (2014). Birth of a domestic cat kitten produced by vitrification of lipid polarized in vitro matured oocytes. Cryobiology68, 459–466. doi: 10.1016/j.cryobiol.2014.02.012
65
GhanemN.HaA.-N.FakruzzamanMd.BangJ.-I.LeeS.-C.KongI.-K. (2014). Differential expression of selected candidate genes in bovine embryos produced in vitro and cultured with chemicals modulating lipid metabolism. Theriogenology82, 238–250. doi: 10.1016/j.theriogenology.2014.03.024
66
GhetlerY.YavinS.ShalgiR.AravA. (2005). The effect of chilling on membrane lipid phase transition in human oocytes and zygotes. Hum. Reprod.20, 3385–3389. doi: 10.1093/humrep/dei236
67
GlandonH. L.MichaelisA. K.PolitanoV. A.AlexanderS. T.VlahovichE. A.ReeceK. S.et al. (2016). Impact of environment and ontogeny on relative fecundity and egg quality of female oysters (Crassostrea virginica) from four sites in northern chesapeake bay. Biol. Bull.231, 185–198. doi: 10.1086/691066
68
GómezE.CarroceraS.MartínD.Pérez-JánezJ. J.PrendesJ.PrendesJ. M.et al. (2020). Efficient one-step direct transfer to recipients of thawed bovine embryos cultured in vitro and frozen in chemically defined medium. Theriogenology146, 39–47. doi: 10.1016/j.theriogenology.2020.01.056
69
GualtieriR.KalthurG.BarbatoV.Di NardoM.AdigaS. K.TaleviR. (2021). Mitochondrial dysfunction and oxidative stress caused by cryopreservation in reproductive cells. Antioxidants10, 337. doi: 10.3390/antiox10030337
70
GuoY.CordesK. R.FareseR. V.WaltherT. C. (2009). Lipid droplets at a glance. J. Cell Sci.122, 749–752. doi: 10.1242/jcs.037630
71
HaoT.ZhangP.HaoH.DuW.PangY.ZhaoS.et al. (2021). The combination treatment of cholesterol-loaded methyl-β-cyclodextrin and methyl-β-cyclodextrin significantly improves the fertilization capacity of vitrified bovine oocytes by protecting fertilization protein JUNO. Reprod. Dom. Anim.56, 519–530. doi: 10.1111/rda.13890
72
HaraK.AbeY.KumadaN.AonoN.KobayashiJ.MatsumotoH.et al. (2005). Extrusion and removal of lipid from the cytoplasm of porcine oocytes at the germinal vesicle stage: Centrifugation under hypertonic conditions influences vitrification. Cryobiology50, 216–222. doi: 10.1016/j.cryobiol.2005.01.003
73
HarayamaT.RiezmanH. (2018). Understanding the diversity of membrane lipid composition. Nat. Rev. Mol. Cell Biol.19, 281–296. doi: 10.1038/nrm.2017.138
74
HeL.BaileyJ. L.BuhrM. M. (2001). Incorporating lipids into boar sperm decreases chilling sensitivity but not capacitation potential. Biol. Reprod.64, 69–79. doi: 10.1095/biolreprod64.1.69
75
HelmM. M.HollandD. L.StephensonR. R. (1973). The effect of supplementary algal feeding of a hatchery breeding stock of ostrea edulis l. on larval vigour. J. Mar. Biol. Assoc. U. K.53, 673–684. doi: 10.1017/S0025315400058872
76
HelmM. M.HollandD. L.UttingS. D.EastJ. (1991). Fatty acid composition of early non-feeding larvae of the European flat oyster, Ostrea edulis. J. Mar. Biol. Assoc. U. K.71, 691–705. doi: 10.1017/S0025315400053248
77
HeresP.TroncosoJ.ParedesE. (2021). Larval cryopreservation as new management tool for threatened clam fisheries. Sci. Rep.11, 15428. doi: 10.1038/s41598-021-94197-2
78
HigakiS.EtoY.KawakamiY.YamahaE.KagawaN.KuwayamaM.et al. (2010). Production of fertile zebrafish (Danio rerio) possessing germ cells (gametes) originated from primordial germ cells recovered from vitrified embryos. REPRODUCTION139, 733–740. doi: 10.1530/REP-09-0549
79
Hinkovska-GalchevaV.PetkovaD.KoumanovK. (1989). Changes in the phospholipid composition and phospholipid asymmetry of ram sperm plasma membranes after cryopreservation. Cryobiology26, 70–75. doi: 10.1016/0011-2240(89)90034-5
80
HorvathG.SeidelG. E. (2006). Vitrification of bovine oocytes after treatment with cholesterol-loaded methyl-β-cyclodextrin. Theriogenology66, 1026–1033. doi: 10.1016/j.theriogenology.2006.03.004
81
HossainM. S.TareqK. M. A.HammanoK.-I.TsujiiH. (2007). Effect of fatty acids on boar sperm motility, viability and acrosome reaction: Fatty acids induce acrosome reaction. Reprod. Med. Biol.6, 235–239. doi: 10.1111/j.1447-0578.2007.00191.x
82
HuangZ.GaoL.HouY.ZhuS.FuX. (2019). Cryopreservation of farm animal gametes and embryos: recent updates and progress. Front. Agr. Sci. Eng.6, 42. doi: 10.15302/J-FASE-2018231
83
HuangX.ZhuangP.FengG.ZhaoF.LiuJ.ZhangT.et al. (2017). Cryopreservation of Chinese mitten crab, Eriocheir sinensis H. Milne Edwards 1853 (Decapoda, Brachyura), embryos by vitrification. Crustaceana90, 1765–1777. doi: 10.1163/15685403-00003730
84
InoueD.FujimotoT.KawakamiY.YasuiG. S.YamahaE.AraiK. (2012). Vitrification of primordial germ cells using whole embryos for gene-banking in loach, Misgurnus anguillicaudatus. J. Appl. Ichthyol.28, 919–924. doi: 10.1111/jai.12058
85
IsraelachviliJ. N.MarčeljaS.HornR. G. (1980). Physical principles of membrane organization. Quart. Rev. Biophys.13, 121–200. doi: 10.1017/S0033583500001645
86
IussigB.MaggiulliR.FabozziG.BertelleS.VaiarelliA.CimadomoD.et al. (2019). A brief history of oocyte cryopreservation: Arguments and facts. Acta Obstet. Gynecol. Scand.98, 550–558. doi: 10.1111/aogs.13569
87
Janati IdrissiS.Le BourhisD.LefevreA.EmondP.Le BerreL.DesnoësO.et al. (2021). Lipid profile of bovine grade-1 blastocysts produced either in vivo or in vitro before and after slow freezing process. Sci. Rep.11, 11618. doi: 10.1038/s41598-021-90870-8
88
JungG. T.LeeJ. H.ParkD.AhnJ. M.UmD.-E.ShinH.et al. (2021). Lipidomic changes in mouse oocytes vitrified in PEG 8000-supplemented vitrification solutions. Cryobiology99, 140–148. doi: 10.1016/j.cryobiol.2020.11.004
89
JungJ.ShinH.BangS.MokH. J.SuhC. S.KimK. P.et al. (2014). Analysis of the phospholipid profile of metaphase II mouse oocytes undergoing vitrification. PLoS One9, e102620. doi: 10.1371/journal.pone.0102620
90
KaraşahinT. (2019). The effect of oleic and linoleic acid addition to the culture media on bovine embryonic development following vitrification. Pol. J. Vet. Sci.22, 661–666. doi: 10.24425/pjvs.2019.129978
91
KarjaN. W. K.OtoiT.WongsrikeaoP.MurakamiM.AgungB.FahrudinM.et al. (2006). In vitro development and post-thaw survival of blastocysts derived from delipidated zygotes from domestic cats.Theriogenology65, 415–423. doi: 10.1016/j.theriogenology.2005.04.029.
92
KasaiM. (2002). Advances in the cryopreservation of mamMalian oocytes and embryos: Development of ultrarapid vitrification: Ultrarapid vitrification of oocytes/embryos. Reprod. Med. Biol.1, 1–9. doi: 10.1046/j.1445-5781.2002.00004.x
93
KelsoK. A.CeroliniS.NobleR. C.SparksN. H. C.SpeakeB. K. (1996). Lipid and antioxidant changes in semen of broiler fowl from 25 to 60 weeks of age. Reproduction106, 201–206. doi: 10.1530/jrf.0.1060201
94
KobayashiT.TakeuchiY.TakeuchiT.YoshizakiG. (2007). Generation of viable fish from cryopreserved primordial germ cells. Mol. Reprod. Dev.74, 207–213. doi: 10.1002/mrd.20577
95
KopeikaJ.ThornhillA.KhalafY. (2015). The effect of cryopreservation on the genome of gametes and embryos: principles of cryobiology and critical appraisal of the evidence. Hum. Reprod. Update21, 209–227. doi: 10.1093/humupd/dmu063
96
KostetskyE. Y.BorodaA. V.OdintsovaN. A. (2008). Changes in the lipid composition of mussel (Mytilus trossulus) embryo cells during cryopreservation. Biophysics53, 299–303. doi: 10.1134/S000635090804012X
97
LahnsteinerF.MansourN.McNivenM. A.RichardsonG. F. (2009). Fatty acids of rainbow trout (Oncorhynchus mykiss) semen: Composition and effects on sperm functionality. Aquaculture298, 118–124. doi: 10.1016/j.aquaculture.2009.08.034
98
LangdonC. J.WaldockM. J. (1981). The effect of algal and artificial diets on the growth and fatty acid composition of Crassostrea gigas Spat. J. Mar. Biol. Assoc. U. K.61, 431–448. doi: 10.1017/S0025315400047056
99
LeãoB. C. S.Rocha-FrigoniN. A. S.CabralE. C.CoelhoM. B.FerreiraC. R.EberlinM. N.et al. (2015). Improved embryonic cryosurvival observed after in vitro supplementation with conjugated linoleic acid is related to changes in the membrane lipid profile. Theriogenology84, 127–136. doi: 10.1016/j.theriogenology.2015.02.023
100
LinC.TsaiS. (2012). The effect of cryopreservation on DNA damage, gene expression and protein abundance in vertebrate. Ital. J. Anim. Sci.11, e21. doi: 10.4081/ijas.2012.e21
101
LiuT.GaoJ.ZhouN.MoM.WangX.ZhangX.et al. (2016). The effect of two cryopreservation methods on human sperm DNA damage. Cryobiology72, 210–215. doi: 10.1016/j.cryobiol.2016.04.004
102
LiuY.GluisM.Miller-EzzyP.HanJ.QinJ.ZhanX.et al. (2020a). Development of a programmable freezing technique on larval cryopreservation in the Pacific oyster Crassostrea gigas. Aquaculture523, 735199. doi: 10.1016/j.aquaculture.2020.735199
103
LiuY.GluisM.Miller-EzzyP.QinJ.HanJ.ZhanX.et al. (2020b). Development of a programmable freezing technique on larval cryopreservation in Mytilus galloprovincialis. Aquaculture516, 734554. doi: 10.1016/j.aquaculture.2019.734554
104
LiuY.LiX. (2015). Successful oocyte cryopreservation in the blue mussel Mytilus galloprovincialis. Aquaculture438, 55–58. doi: 10.1016/j.aquaculture.2015.01.002
105
LongoN.FrigeniM.PasqualiM. (2016). Carnitine transport and fatty acid oxidation. Biochim. Biophys. Acta Mol. Cell Res.1863, 2422–2435. doi: 10.1016/j.bbamcr.2016.01.023
106
MadyM. M.FathyM. M.YoussefT.KhalilW. M. (2012). Biophysical characterization of gold nanoparticles-loaded liposomes. Phys. Med.28, 288–295. doi: 10.1016/j.ejmp.2011.10.001
107
MaldjianA.PizziF.GliozziT.CeroliniS.PennyP.NobleR. (2005). Changes in sperm quality and lipid composition during cryopreservation of boar semen. Theriogenology63, 411–421. doi: 10.1016/j.theriogenology.2004.09.021
108
MandalR.BadyakarD.ChakrabartyJ. (2014). Role of membrane lipid fatty acids in sperm cryopreservation. Arch. Androl.2014, 1–9. doi: 10.1155/2014/190542
109
MannoS.TakakuwaY.MohandasN. (2002). Identification of a functional role for lipid asymmetry in biological membranes: Phosphatidylserine-skeletal protein interactions modulate membrane stability. Proc. Natl. Acad. Sci. U.S.A.99, 1943–1948. doi: 10.1073/pnas.042688399
110
MansourN.LahnsteinerF.McNivenM. A.RichardsonG. F.PelletierC. S. (2011). Relationship between fertility and fatty acid profile of sperm and eggs in Arctic char, Salvelinus alpinus. Aquaculture318, 371–378. doi: 10.1016/j.aquaculture.2011.05.023
111
Martínez-PáramoS.HorváthÁ.LabbéC.ZhangT.RoblesV.HerráezP.et al. (2017). Cryobanking of aquatic species. Aquaculture472, 156–177. doi: 10.1016/j.aquaculture.2016.05.042
112
MassapinaC. (1999). Oocyte and embryo quality in Crassostrea gigas (Portuguese strain) during a spawning period in Algarve, South Portugal. Aquat. Living Resour.12, 327–333. doi: 10.1016/S0990-7440(99)00115-1
113
MatosJ. E.MarquesC. C.MouraT. F.BaptistaM. C.HortaA. E. M.SoveralG.et al. (2015). Conjugated linoleic acid improves oocyte cryosurvival through modulation of the cryoprotectants influx rate. Reprod. Biol. Endocrinol.13, 60. doi: 10.1186/s12958-015-0059-3
114
MeneghelM.Dall’AcquaP. C.AmbrogiM.LeãoB. C. S.Rocha-FrigoniN. A. S.MingotiG. Z. (2017). Lipid content and cryotolerance of in vitro-produced bovine embryos treated with forskolin before vitrification. Pesq. Vet. Bras.37, 395–400. doi: 10.1590/s0100-736x2017000400015
115
MigaudH.BellG.CabritaE.McAndrewB.DavieA.BobeJ.et al. (2013). Gamete quality and broodstock management in temperate fish. Rev. Aquac.5, S194–S223. doi: 10.1111/raq.12025
116
MooreA. I.SquiresE. L.GrahamJ. K. (2005). Adding cholesterol to the stallion sperm plasma membrane improves cryosurvival. Cryobiology51, 241–249. doi: 10.1016/j.cryobiol.2005.07.004
117
MuchlisinZ. A.SarahP. I.AldilaD. F.ErianiK.HasriI.BatubaraA. S.et al. (2020). Effect of Dimethyl sulfoxide (DMSO) and egg yolk on sperm motility, fertility and hatching rates of depik Rasbora tawarensis (Pisces: Cyprinidae) eggs after short-term cryopreservation. Aquac. Res.51, 1700–1705. doi: 10.1111/are.14516
118
MurakamiM.DongY. J.SuzukiT.TaniguchiM.KaedeiY.SatoY.et al. (2011). Development and subsequent cryotolerance of domestic cat embryos cultured in serum-free and serum-containing media. Cryobiology63, 170–174. doi: 10.1016/j.cryobiol.2011.06.002
119
NagashimaH.D.A. CameronR.KuwayamaM.YoungM.BeebeL.W. BlackshawA.et al. (1999). Survival of porcine delipated oocytes and embryos after cryopreservation by freezing or vitrification. J. Reprod. Dev.45, 167–176. doi: 10.1262/jrd.45.167
120
NagashimaH.KashiwazakiN.AshmanR. J.GrupenC. G.SeamarkR. F.NottleM. B. (1994). Removal of cytoplasmic lipid enhances the tolerance of porcine embryos to chilling. Biol. Reprod.51, 618–622. doi: 10.1095/biolreprod51.4.618
121
NagashimaJ. B.SylvesterS. R.NelsonJ. L.CheongS. H.MukaiC.LamboC.et al. (2015). Live births from domestic dog (Canis familiaris) embryos produced by in vitro fertilization. PLoS One10, e0143930. doi: 10.1371/journal.pone.0143930
122
NaridaA.TsaiS.HsiehW.-C.WenZ.-H.WangL.-H.HuangC.-L.et al. (2023). First successful production of adult corals derived from cryopreserved larvae. Front. Mar. Sci.10. doi: 10.3389/fmars.2023.1172102
123
NeillA. R.MastersC. J. (1972). Metabolism of fatty acids by bovine spermatozoa. Biochem. J.127, 375–385. doi: 10.1042/bj1270375
124
O’ConnellM.McClureN.LewisS. E. M. (2002). The effects of cryopreservation on sperm morphology, motility and mitochondrial function. Hum. Reprod.17, 704–709. doi: 10.1093/humrep/17.3.704
125
OdintsovaN. A.AgeenkoN. V.KiselevK. V.SaninaN. M.KostetskyE. Y. (2006). Analysis of marine hydrobiont lipid extracts as possible cryoprotective agents. Int. J. Refrig.29, 387–395. doi: 10.1016/j.ijrefrig.2005.07.010
126
OdintsovaN. A.BorodaA. V.VelanskyP. V.KostetskyE. (2009). The fatty acid profile changes in marine invertebrate larval cells during cryopreservation. Cryobiology59, 335–343. doi: 10.1016/j.cryobiol.2009.09.006
127
OdintsovaN.KiselevK.SaninaN.KostetskyE. (2001). Cryopreservation of primary cell cultures of marine invertebrates. Cryo Lett.22, 299–310.
128
OldenhofH.FriedelK.AkhoondiM.GojowskyM.WolkersW. F.SiemeH. (2012). Membrane phase behavior during cooling of stallion sperm and its correlation with freezability. Mol. Membr. Biol.29, 95–106. doi: 10.3109/09687688.2012.674161
129
Ortega FerrusolaC.González FernándezL.MorrellJ. M.Salazar SandovalC.Macías GarcíaB.Rodríguez-MartinezH.et al. (2009). Lipid peroxidation, assessed with BODIPY-C11, increases after cryopreservation of stallion spermatozoa, is stallion-dependent and is related to apoptotic-like changes. Reproduction138, 55–63. doi: 10.1530/REP-08-0484
130
OzkavukcuS.ErdemliE.IsikA.OztunaD.KarahuseyinogluS. (2008). Effects of cryopreservation on sperm parameters and ultrastructural morphology of human spermatozoa. J. Assist. Reprod. Genet.25, 403–411. doi: 10.1007/s10815-008-9232-3
131
PaiH.BaidR.PalshetkarN.PaiA.PaiR.PalshetkarR. (2021). Oocyte cryopreservation - current scenario and future perspectives: A narrative review. J. Hum. Reprod. Sci.14, 340. doi: 10.4103/jhrs.jhrs_173_21
132
PanyaboribanS.TharasanitT.ChankitisakulV.Swangchan-UthaiT.TechakumphuM. (2018). Treatment with chemical delipidation forskolin prior to cryopreservation improves the survival rates of swamp buffalo (Bubalus bubalis) and bovine (Bos indicus) in vitro produced embryos. Cryobiology84, 46–51. doi: 10.1016/j.cryobiol.2018.08.003
133
ParedesE. (2016). Biobanking of a marine invertebrate model organism: the sea urchin. J. Mar. Sci. Eng.4, 7. doi: 10.3390/jmse4010007
134
ParizaM. W.ParkY.CookM. E. (2001). The biologically active isomers of conjugated linoleic acid. Prog. Lipid Res.40, 283–298. doi: 10.1016/S0163-7827(01)00008-X
135
PartykaA.Bonarska-KujawaD.SporniakM.StrojeckiM.NiżańskiW. (2016). Modification of membrane cholesterol and its impact on frozen–thawed chicken sperm characteristics. Zygote24, 714–723. doi: 10.1017/S0967199416000022
136
PaschoalD.SudanoM.MazieroR.GuastaliM.MagalhãesL.Landim-AlvarengaF.et al. (2016). Cryopreservation of in vitro produced bovine embryos after lipid decrease with forskolin. Reprod. Fertil. Dev.28, 212. doi: 10.1071/RDv28n2Ab165
137
PereiraR. M.BaptistaM. C.VasquesM. I.HortaA. E. M.PortugalP. V.BessaR. J. B.et al. (2007). Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t,12c CLA). Anim. Reprod. Sci.98, 293–301. doi: 10.1016/j.anireprosci.2006.03.015
138
PereiraR. M.MarquesC. C. (2008). Animal oocyte and embryo cryopreservation. Cell Tissue Bank.9, 267–277. doi: 10.1007/s10561-008-9075-2
139
Pérez-CerezalesS.Martínez-PáramoS.BeirãoJ.HerráezM. P. (2010). Evaluation of DNA damage as a quality marker for rainbow trout sperm cryopreservation and use of LDL as cryoprotectant. Theriogenology74, 282–289. doi: 10.1016/j.theriogenology.2010.02.012
140
PhillipsP. H.LardyH. A. (1940). A yolk-buffer pabulum for the preservation of bull semen. J. Dairy Sci.23, 399–404. doi: 10.3168/jds.S0022-0302(40)95541-2
141
PopeC. E. (2014). Aspects of in vivo oocyte production, blastocyst development, and embryo transfer in the cat. Theriogenology81, 126–137. doi: 10.1016/j.theriogenology.2013.09.006
142
PrapaiwanN.TharasanitT.PunjachaipornpolS.YamtangD.RoongsitthichaiA.MoonarmartW.et al. (2015). Low-density lipoprotein improves motility and plasma membrane integrity of cryopreserved canine epididymal spermatozoa. Asian Australas. J. Anim. Sci.29, 646–651. doi: 10.5713/ajas.15.0572
143
PurdyP. H.GrahamJ. K. (2004). Effect of adding cholesterol to bull sperm membranes on sperm capacitation, the acrosome reaction, and fertility. Biol. Reprod.71, 522–527. doi: 10.1095/biolreprod.103.025577
144
QuinnP. J. (1985). A lipid-phase separation model of low-temperature damage to biological membranes. Cryobiology22, 128–146. doi: 10.1016/0011-2240(85)90167-1
145
QuinnP. J. (2004). “Plasma membrane phospholipid asymmetry,” in Phospholipid Metabolism in Apoptosis Subcellular Biochemistry. Eds. QuinnP. J.KaganV. E. (Boston: Kluwer Academic Publishers), 39–60. doi: 10.1007/0-306-47931-1_3
146
QuinnP. J.ChowP. Y. W.WhiteI. G. (1980). Evidence that phospholipid protects ram spermatozoa from cold shock at a plasma membrane site. Reproduction60, 403–407. doi: 10.1530/jrf.0.0600403
147
RickerJ. V.LinforJ. J.DelfinoW. J.KysarP.ScholtzE. L.TablinF.et al. (2006). Equine sperm membrane phase behavior: the effects of lipid-based cryoprotectants. Biol. Reprod.74, 359–365. doi: 10.1095/biolreprod.105.046185
148
RomekM.GajdaB.KrzysztofowiczE.KepczynskiM.SmoragZ. (2011). New technique to quantify the lipid composition of lipid droplets in porcine oocytes and pre-implantation embryos using Nile Red fluorescent probe. Theriogenology75, 42–54. doi: 10.1016/j.theriogenology.2010.06.040
149
RöpkeT.OldenhofH.LeidingC.SiemeH.BollweinH.WolkersW. F. (2011). Liposomes for cryopreservation of bovine sperm. Theriogenology76, 1465–1472. doi: 10.1016/j.theriogenology.2011.06.015
150
Salinas-FloresL.AdamsS. L.LimM. H. (2008). Cholesterol addition and removal in pacific oyster oocytes does not improve cryopreservation success. CryoLetters29, 391–398.
151
SaundersK. M.ParksJ. E. (1999). Effects of cryopreservation procedures on the cytology and fertilization rate of in vitro-matured bovine oocytes. Biol. Reprod.61, 178–187. doi: 10.1095/biolreprod61.1.178
152
SchillerJ.ArnholdJ.GlanderH.-J.ArnoldK. (2000). Lipid analysis of human spermatozoa and seminal plasma by MALDI-TOF mass spectrometry and NMR spectroscopy — effects of freezing and thawing. Chem. Phys. Lipids.106, 145–156. doi: 10.1016/S0009-3084(00)00148-1
153
SchuffnerA.MorshediM.OehningerS. (2001). Cryopreservation of fractionated, highly motile human spermatozoa: effect on membrane phosphatidylserine externalization and lipid peroxidation. Hum. Reprod.16, 2148–2153. doi: 10.1093/humrep/16.10.2148
154
SiemeH.OldenhofH.WolkersW. (2015). Sperm membrane behaviour during cooling and cryopreservation. Reprod. Domest. Anim.50, 20–26. doi: 10.1111/rda.12594
155
SilvaL. K. X.LourençoJ. B.da SilvaA. O. A.de SousaJ. S.SilvaA. G. M. E.Dos ReisA. N.et al. (2020). Increased quality of in natura and cryopreserved semen of water buffaloes supplemented with saturated and unsaturated fatty acids from the palm oil industry. Anim. Reprod.17, e20200522. doi: 10.1590/1984-3143-ar2020-0522
156
SimpsonA. M.SwanM. A.WhiteI. G. (1987). Susceptibility of epididymal boar sperm to cold shock and protective action of phosphatidylcholine. Gamete Res.17, 355–373. doi: 10.1002/mrd.1120170408
157
SomfaiT.KanedaM.AkagiS.WatanabeS.HaraguchiS.MizutaniE.et al. (2011). Enhancement of lipid metabolism with L-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes. Reprod. Fertil. Dev.23, 912. doi: 10.1071/RD10339
158
SouzaR. S.BarbosaL. P.AguiarC. S.VieiraR. L. A.RibeiroM. O.AraújoR.C.d. S.et al. (2019). Cryopreservation of semen from goats fed a diet supplemented with flaxseed. Rev. Bras. saúde Prod. anim.20, e0112020. doi: 10.1590/s1519-9940210112020
159
SprícigoJ. F.MoratóR.ArcaronsN.YesteM.DodeM. A.López-BejarM.et al. (2017). Assessment of the effect of adding L-carnitine and/or resveratrol to maturation medium before vitrification on in vitro-matured calf oocytes. Theriogenology89, 47–57. doi: 10.1016/j.theriogenology.2016.09.035
160
SubramaniamS.FahyE.GuptaS.SudM.ByrnesR. W.CotterD.et al. (2011). Bioinformatics and systems biology of the lipidome. Chem. Rev.111, 6452–6490. doi: 10.1021/cr200295k
161
SubramoniamT.NewtonS. S. (1993). Cryopreservation of penaeid prawn embryos. Curr. Sci.65, 176–178.
162
SudanoM. J.PaschoalD. M.da Silva RascadoT.MagalhãesL. C. O.CrocomoL. F.de Lima-NetoJ. F.et al. (2011). Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology75, 1211–1220. doi: 10.1016/j.theriogenology.2010.11.033
163
SudanoM. J.SantosV. G.TataA.FerreiraC. R.PaschoalD. M.MaChadoR.et al. (2012). Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts. Biol. Reprod.87, 1–11. doi: 10.1095/biolreprod.112.102897
164
TakahashiT.InabaY.SomfaiT.KanedaM.GeshiM.NagaiT.et al. (2013). Supplementation of culture medium with L-carnitine improves development and cryotolerance of bovine embryos produced in vitro. Reprod. Fertil. Dev.25, 589. doi: 10.1071/RD11262
165
TervitH. R.AdamsS. L.RobertsR. D.McGowanL. T.PughP. A.SmithJ. F.et al. (2005). Successful cryopreservation of Pacific oyster (Crassostrea gigas) oocytes. Cryobiology51, 142–151. doi: 10.1016/j.cryobiol.2005.06.001
166
TharasanitT.ThuwanutP. (2021). Oocyte cryopreservation in domestic animals and humans: principles, techniques and updated outcomes. Animals11, 2949. doi: 10.3390/ani11102949
167
TierschT. R.YangH.JenkinsJ. A.DongQ. (2007). Sperm cryopreservation in fish and shellfish. Soc Reprod. Fertil. Suppl.65, 493–508.
168
TorresT. M.Almeida-MonteiroP. S. D.NascimentoR. V. D.PereiraV. A.FerreiraY. M.LobatoJ. S.et al. (2022). Sperm cryopreservation of Prochilodus brevis using different concentrations of non-permeable cryoprotectants. Anim. Reprod.19, e20210083. doi: 10.1590/1984-3143-ar2021-0083
169
TowhidiA.ParksJ. E. (2012). Effect of n-3 fatty acids and α-tocopherol on post-thaw parameters and fatty acid composition of bovine sperm. J. Assist. Reprod. Genet.29, 1051–1056. doi: 10.1007/s10815-012-9834-7
170
TowhidiA.ZeinoaldiniS.ArdebiliR.Dadashpour DavachiN.NasiriA. H. (2013). Combined n-3 fatty acids and α-tocopherol supplementation improved the ovine sperm cryosurvival. Iran. J. Biotechnol.11, 238–243. doi: 10.5812/ijb.14469
171
TsaiS.LinC. (2012). Advantages and applications of cryopreservation in fisheries science. Braz. Arch. Biol. Technol.55, 425–434. doi: 10.1590/S1516-89132012000300014
172
TsaiS.RawsonD. M.ZhangT. (2009). Studies on chilling sensitivity of early stage zebrafish (Danio rerio) ovarian follicles. Cryobiology58, 279–286. doi: 10.1016/j.cryobiol.2009.02.002
173
UgurM. R.Saber AbdelrahmanA.EvansH. C.GilmoreA. A.HititM.ArifiantiniR. I.et al. (2019). Advances in cryopreservation of bull sperm. Front. Vet. Sci.6. doi: 10.3389/fvets.2019.00268
174
ValcarceD. G.Cartón-GarcíaF.RiescoM. F.HerráezM. P.RoblesV. (2013). Analysis of DNA damage after human sperm cryopreservation in genes crucial for fertilization and early embryo development. Andrology1, 723–730. doi: 10.1111/j.2047-2927.2013.00116.x
175
ValdebenitoI. I.GallegosP. C.EfferB. R. (2015). Gamete quality in fish: evaluation parameters and determining factors. Zygote23, 177–197. doi: 10.1017/S0967199413000506
176
Van MeerG.VoelkerD. R.FeigensonG. W. (2008). Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol.9, 112–124. doi: 10.1038/nrm2330
177
VasquezJ. M.RoldanE. R. S. (1997). Phospholipid metabolism in boar spermatozoa and role of diacylglycerol species in the De Novo formation of phosphatidylcholine. Mol. Reprod. Dev.47, 105–112. doi: 10.1002/(SICI)1098-2795(199705)47:1<105::AID-MRD14>3.0.CO;2-0
178
VirequeA. A.TataA.SilvaO. F. L. L. O.LoTurcoE. G.AzzoliniA.FerreiraC. R.et al. (2016). Effects of n-6 and n-3 polyunsaturated acid-rich soybean phosphatidylcholine on membrane lipid profile and cryotolerance of human sperm. Fertil. Steril.106, 273–283.e6. doi: 10.1016/j.fertnstert.2016.03.044
179
V’uorelaR.KaitarantaJ.LinkoR. R. (1979). Proximate composition of fish roe in relation to maturity. Food Res. Int.12, 186–188. doi: 10.1016/S0315-5463(79)73133-6
180
WaterhouseK. E.HofmoP. O.TverdalA.MillerR. R. (2006). Within and between breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction131, 887–894. doi: 10.1530/rep.1.01049
181
WonnacottK. E.KwongW. Y.HughesJ.SalterA. M.LeaR. G.GarnsworthyP. C.et al. (2010). Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction139, 57–69. doi: 10.1530/REP-09-0219
182
XuH.-Y.GengS.-S.LiT.-T.FuQ.LuS.-S.LiangX.-W.et al. (2019). Maturation of buffalo oocytes in vitro with acetyl-L-carnitine improves cryotolerance due to changes in mitochondrial function and the membrane lipid profile. Reprod. Fertil. Dev.31, 386. doi: 10.1071/RD18102
183
YangH.HuoY. (2022). Review of molluscan larval cryopreservation and application to germplasm cryobanking and commercial seed production. Aquaculture547, 737491. doi: 10.1016/j.aquaculture.2021.737491
184
YildizC.YavasI.BozkurtY.AksoyM. (2015). Effect of cholesterol-loaded cyclodextrin on cryosurvival and fertility of cryopreserved carp (Cyprinus carpio) sperm. Cryobiology70, 190–194. doi: 10.1016/j.cryobiol.2015.01.009
185
ZeilmakerG. H.AlberdaA. T.van GentI.RijkmansC. M. P. M.DrogendijkA. C. (1984). Two pregnancies following transfer of intact frozen-thawed embryos. Fertil. Steril.42, 293–296. doi: 10.1016/S0015-0282(16)48029-5
186
ZeronY.OcheretnyA.KedarO.BorochovA.SklanD.AravA. (2001). Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction121, 447–454. doi: 10.1530/rep.0.1210447
187
ZeronY.SklanD.AravA. (2002). Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes. Mol. Reprod. Dev.61, 271–278. doi: 10.1002/mrd.1156
188
ZhangS. S.HuJ. H.LiQ. W.JiangZ. L.ZhangX. Y. (2009). The cryoprotective effects of soybean lecithin on boar spermatozoa quality. Afr. J. Biotechnol.8, 6476–6480. doi: 10.5897/AJB09.1070
189
ZhangJ.LiQ.WuY.WangD.XuL.ZhangY.et al. (2019). Cholesterol content in cell membrane maintains surface levels of ErbB2 and confers a therapeutic vulnerability in ErbB2-positive breast cancer. Cell Commun. Signal.17, 15. doi: 10.1186/s12964-019-0328-4
190
ZhangH.YeH.ShaoY.WuS.YuJ.JiC.et al. (2018). The effects of egg yolk concentration and particle size on donkey semen preservation. J. Equine. Vet. Sci.65, 19–24. doi: 10.1016/j.jevs.2018.03.002
191
ZhouG.LiN. (2009). Cryopreservation of porcine oocytes: recent advances. Mol. Hum. Reprod.15, 279–285. doi: 10.1093/molehr/gap016
192
ZhuX.Miller-EzzyP.GluisM.ZhaoY.QinJ.TangY.et al. (2023). Effects of phosphatidylcholine and tocopherol during larval cryopreservation of Pacific oysters (Magallana gigas). Aquaculture574, 739650. doi: 10.1016/j.aquaculture.2023.739650
Summary
Keywords
cryopreservation, lipid application, sperm, oocyte, embryo, larva, aquaculture
Citation
Zhu X, Miller-Ezzy P, Zhao Y, Qin J, Tang Y, Liu Y and Li X (2023) Lipid modification to improve cryotolerance of gametes, embryos and larvae and its potential application in aquaculture species: a review. Front. Mar. Sci. 10:1235958. doi: 10.3389/fmars.2023.1235958
Received
07 June 2023
Accepted
28 August 2023
Published
11 September 2023
Volume
10 - 2023
Edited by
Khor Waiho, University of Malaysia Terengganu, Malaysia
Reviewed by
Estefania Paredes, University of Vigo, Spain; Maocang Yan, Zhejiang Mariculture Research Institute, China
Updates
Copyright
© 2023 Zhu, Miller-Ezzy, Zhao, Qin, Tang, Liu and Li.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Xiaoxu Li, xiaoxu.li@sa.gov.au; Yibing Liu, liuyibing@ouc.edu.cn
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.