Abstract
SIRT1 is a member of the sirtuin family functioning in the process of removal of acetyl groups from different proteins. This protein has several biological functions and is involved in the pathogenesis of metabolic diseases, malignancy, aging, neurodegenerative disorders and inflammation. Several long non-coding RNAs (lncRNAs), microRNAs (miRNAs) and circular RNAs (circRNAs) have been found to interact with SIRT1. These interactions have been assessed in the contexts of sepsis, cardiomyopathy, heart failure, non-alcoholic fatty liver disease, chronic hepatitis, cardiac fibrosis, myocardial ischemia/reperfusion injury, diabetes, ischemic stroke, immune-related disorders and cancers. Notably, SIRT1-interacting non-coding RNAs have been found to interact with each other. Several circRNA/miRNA and lncRNA/miRNA pairs that interact with SIRT1 have been identified. These axes are potential targets for design of novel therapies for different disorders. In the current review, we summarize the interactions between three classes of non-coding RNAs and SIRT1.
Introduction
As a member of the sirtuin family, Sirt1 has a function in removal of acetyl groups from different proteins. This nicotinamide adenosine dinucleotide (NAD)-dependent deacetylase has several biological functions and is involved in the pathogenesis of metabolic diseases, malignancy, aging, neurodegenerative disorders and inflammation (Rahman and Islam, 2011). SIRT1 has a lot of substrates including a number of transcription factors. These transcription factors include p53, FoxO family, HES1, HEY2, PPARγ, CTIP2, p300, PGC-1α, and NF-κB (Haigis and Guarente, 2006; Michan and Sinclair, 2007; Yamamoto et al., 2007; Pillarisetti, 2008). The enzymatic reaction catalyzed by SIRT1 leads to generation of nicotinamide and transfer of the acetyl group of the substrate to cleaved NAD, producing a distinctive metabolite, namely, O-acetyl-ADP ribose (Pillarisetti, 2008).
SIRT1 has an important role in the regulation of energy homeostasis in response to accessibility to nutrients. In the liver tissue, SIRT1 enhances expression of the nuclear receptor PPARα, thus regulating lipid homeostasis. Deletion of Sirt1 in this tissue has been shown to impair PPARα signaling and decrease ß-oxidation of fatty acids, resulting in the development of hepatic steatosis, induction of inflammatory responses in liver, and endoplasmic reticulum stress (Purushotham et al., 2009).
In addition to the regulation of metabolic pathways, SIRT1 is involved in the carcinogenic processes. Its expression has been found to be increased in both hematological malignancies (Bradbury et al., 2005) and solid tumors (Huffman et al., 2007; Stünkel et al., 2007). Possibly acting as an oncogene, SIRT1 interacts with p53 and induces its deacetylation at its C-terminal Lys382 residue (Vaziri et al., 2001), thus inactivating this tumor suppressor.
In fact, SIRT1 is involved in a variety of human disorders including malignant and nonmalignant conditions. Recently, researchers have focused on identification of the interaction between non-coding RNAs and SIRT1 in these disorders. These investigations have led to identification of a number of long non-coding RNAs (lncRNAs), microRNAs (miRNAs) and circular RNAs (circRNAs) that regulate expression of SIRT1. In the current review, we provide an overview of these non-coding RNAs.
SIRT1-interacting miRNAs
A class of non-coding RNAs known as miRNAs regulate gene expression by binding to specific target genes in distinct pathways, thereby modulating the expression of various genes (Ghafouri-Fard et al., 2021a; Hussen et al., 2021; Hussen et al., 2022a). Mature miRNAs are formed by further processing of pre-miRNAs, which are formed from the transcribed nucleic acids that make up primary miRNAs. Several miRNAs have been shown to target SIRT1, thus regulating its expression. Dysregulation of SIRT1-targeting miRNAs is involved in the pathogenesis of sepsis and its complications, non-alcoholic fatty liver disease (NAFLD), chronic hepatitis, hepatic and myocardial ischemia/reperfusion (I/R) injury, cardiac fibrosis, heart failure, myocardial infarction, osteoarthritis, kidney injury, diabetic nephropathy, cerebral I/R Injury, spinal cord injury, epilepsy and a number of malignant conditions (Table 1; Figure 1). In sepsis, upregulation of miR-181a (Wu Z. et al., 2021), miR-133a (Chen L. et al., 2020) and miR-195 (Yuan et al., 2020) has been shown to lead to downregulation of SIRT1 and aggravation of inflammatory responses. miR-29a, miR-34a and miR-182 are among SIRT1-interacting miRNAs being involved in the pathogenesis of hepatic disorders. For instance, miR-29a via modulating the GSK-3β/SIRT1 could ameliorate mouse non-alcoholic steatohepatitis (Yang et al., 2020). Alterations in the miR-34a/SIRT1/FXR/p53 axis have been found to induce NAFLD in rats (Alshehri et al., 2021). Moreover, miR-34a via mediating the SIRT1/p53 axis could enhance liver fibrosis in patients with chronic hepatitis (Li X. et al., 2020).
TABLE 1
| Type of diseases | miRNA | Sample | Cell line | SIRT1 expression | Targets and pathways | Discussion | Ref |
|---|---|---|---|---|---|---|---|
| Sepsis | miR-181a (Up) | - | RAW264.7 | (Down) | Nrf2, p-65, NF-κβ, TNF-α, IL-1β, IL-6, Bcl-2, Bax | Inhibition of miR-181a via targeting SIRT1 by activating Nrf2 and inhibiting NF-κB could attenuate sepsis-induced inflammation and apoptosis | Wu et al. (2021a) |
| Sepsis | miR-133a (Up) | Serum samples: sepsis (n = 60), normal group (n = 30), C57BL/6J mice | RAW264.7 | (Down) | ALT, AST, IL-1β, IL-6, TNF-α | miR-133a by targeting SIRT1 could aggravate inflammatory responses in sepsis | Chen et al. (2020a) |
| Sepsis | miR-195 (Up) | - | NCM460 | (Down) | Bcl-2, Bax, elF2α, ATF4, CHOP, GRP78 | miR-195 via targeting the SIRT1/eIF2α axis could enhance intestinal epithelial cell apoptosis | Yuan et al. (2020) |
| Sepsis | miR-197 | H9c2 | (Down) | Bcl-2, Bax, IL-6, | miR-197 by modulating SIRT1 could participate cardiomyocyte injury | Liu et al. (2022a) | |
| IL-1β, Caspase-3, p53 | |||||||
| Septic cardiomyopathy | miR-22 (-) | miR-22-flox mice, αMHC-Cre mice, littermates wild-type (WT) mice | Cardiomyocyte | (Down) | TNF-α, IL-6, IL-1β, LC3-I/II, p62, Atg7, Caspase-3/9, Bax, Bcl-2 | Downregulation of miR-22 by targeting SIRT1 could alleviate septic cardiomyopathy | Wang et al. (2021a) |
| Non-alcoholic steatohepatitis (NAFLD) | miR-29a (-) | C57BL/6 mice | HepG2 | (-) | GSK-3β, CD36, PERK, IRE1α, XBP1s, CHOP | miR-29a via modulating the GSK-3β/SIRT1 could ameliorate mouse non-alcoholic steatohepatitis | Yang et al. (2020) |
| NAFLD | miR-34a (Up) | Wistar rats | - | (Down) | FXR, p53, ALT, AST, γ-GGT, | Alteration of miR-34a/SIRT1/FXR/p53 axis could induce NAFLD in rats | Alshehri et al. (2021) |
| TNF-α, IL-6, | |||||||
| Chronic hepatitis C (CHC) | miR-34a (Up) | CHC (n = 41), healthy control samples (n = 18) | - | (Down) | p53, TBA, AST, ALT | miR-34a via mediating the SIRT1/p53 axis could enhance liver fibrosis in patients with chronic hepatitis | Li et al. (2020a) |
| Hepatic I/R Injury | miR-182 (-) | Black/Swiss mice, C57BL/6J WT mice | Hepatocyte | (Down) | XBP1, NLRP3, ALT, IL-1β, TNF-α, IL-18, Caspase-1 | SIRT1 via modulating the miR-182-mediated XBP1/NLRP3 axis could alleviate hepatic IR injury | Li et al. (2021a) |
| Cardiac Fibrosis | miR-128 (Up) | C57BL/6 J mice | H9c2 | (Down) | PIK3R1, p53, p62, Bcl-2, Bax, | Downregulation of miR-128 via targeting the SIRT1/PIK3R1 axis could ameliorate cardiac dysfunction | Zhan et al. (2021) |
| Beclin-1, LC3-I/II, AKT, mTOR | |||||||
| Congestive heart failure (CHF) | miR-22 (-) | C57BL/6 mice | Cardiomyocyte | (Down) | PGC-1α, TFAM, p62, LC3-I/II | Downregulation of miR-22 by targeting SIRT1/PGC-1α could alleviate CHF. | Wang et al. (2021b) |
| HF | miR-199a (Up) | C57Bl/6J mice | CMs, CFs, CECs | (Down) | P300, Yy1, sST2 | miR199/SIRT1/P300 axis via upregulating the circulation of soluble sST2 isoform could modulate heart failure | Asensio-Lopez et al. (2021) |
| Myocardial I/R Injury | miR-29a (Up) | C57BL/J6 | H9c2 | (Down) | NLRP3, IL-1/6, IL-1β, TNF-α, eNOS, iNOS, Caspase-1 | Downregulation of miR-29a by targeting SIRT1 and inhibiting NLRP3-mediated pyroptosis could ameliorate myocardial I/R Injury | Ding et al. (2020) |
| Cardiotoxicity | miR-200a-3p (Up) | Wistar rats | H9c2, 293T | (-) | PEG3, NF-κβ, Bax, Bcl-2, IKK, p65, IκBα | miR-200a-3p via modulating SIRT1/NF-κB axis and by targeting PEG3 could aggravate cardiotoxicity | Fu et al. (2021) |
| Acute myocardial infarction (AMI) | miR-181a-5p (-) | - | H9C2 | (-) | Bcl-2, Bax, | miR-181a-5p via regulating SIRT1 could involve cardiomyocyte apoptosis induced by hypoxia–reoxygenation | Qi et al. (2020) |
| Caspase-3 | |||||||
| AMI | miR-124-3p (Up) | SD rats | H9C2 | (Down) | FGF21, CREB, PGC1-α, g IL-1α, IL-1β, IL-2/6, IFN-γ, TNF-α, Bax, Bcl-2, Caspase-3 | miR-124-3p via targeting SIRT1 by modulation FGF21/CREB/PGC1α axis could regulate cell apoptosis and oxidative stress of acute myocardial infarction | Wei et al. (2021) |
| Osteoarthritis (OA) | miR-30b-5p (Up) | OA tissue samples (n = 40) and adjacent (n = 15) normal tissue samples, SD rats | HC-A, | (Down) | FoxO3a, NLRP3, NF-κβ, IL-1β, IL-6/18, TNF-α, Bax, Caspase-1/3, MMP-3/13, ASC | NF-κB-inducible miR-30b-5p via modulating SIRT1-FoxO3a-mediated NLRP3 inflammasome could aggravate joint pain | Xu et al. (2021a) |
| OA | miR-122 (Up) | OA tissue samples (n = 29), normal cartilage tissue samples (n = 29) | - | (Down) | Collagen-II, Aggrecan, MMP-13, ADAMTS4 | miR-122 via targeting SIRT1 could regulate chondrocyte extracellular matrix degradation in osteoarthritis | Bai et al. (2020) |
| Kidney Injury | miR-34a (Up) | Kunming mice | - | (Down) | p53, TNF-α, IL-6, IL-1β, Caspase-9, Bax, Bcl-2 | miR-34a/SIRT1/p53 axis could modulate kidney injury | Hao et al. (2021) |
| Acute kidney injury (AKI) | miR-183-3p (Up) | SD rats | NRK-52E | (Down) | PUMA, FOXO3a, TGF-β1, a-SMA, Vimentin,E-Cadherin | Depletion of miR-183-3p via the SIRT1/PUMA/FOXO3a axis could improve renal tubulointerstitial fibrosis after AKI. | Li et al. (2021b) |
| Diabetic nephropathy (DN) | miR-150-5p (Up) | (n = 60) diabetes mellitus patients, C57BL/6J mice | Podocyte | (Down) | p53, p62, AMPK, p-cadherin, ZO-1, LC3-I/II | Downregulation of miR-150-5p by targeting the SIRT1/p53/AMPK axis could ameliorate diabetic nephropathy | Dong et al. (2021) |
| DN | miR-34a (Up) | C57BL/6J mice | Podocyte | (Down) | p53, LC3A/B-I, LC3A/B-II | The p53/miR-34a/SIRT1 axis inhibition could ameliorate podocyte injury in DN. | Liang et al. (2021) |
| Cerebral I/R Injury | miR-19a/b-3p (Up) | SD rats | - | (Down) | FoxO3, SPHK1, NF-κβ p65, TNF-α, IL-6, IL-1β | miR-19a/b-3p via targeting the SIRT1/FoxO3/SPHK1 axis could promote inflammation during cerebral I/R injury | Zhou et al. (2021) |
| SCI | miR-324-5p (Up) | SD rats | PC12 | (Down) | Bcl-2, Caspase-3, Bax, TNF-α, IL-1β | Silencing miR-324-5p by modulating SIRT1 could alleviate rats SCI. | Wang et al. (2021c) |
| CCIS | miR-34c-5p (Up) | SD rats | - | (Down) | TNF-α, IL-6, IL-1β, STAT3 | Downregulation of miR-34c-5p via targeting the SIRT1/STAT3 axis could alleviate neuropathic pain | Mo et al. (2020) |
| Epilepsy | miR-135a-5p (Up) | - | BV2 | (-) | Caspase-3/9 | Downregulation of miR-135a-5p via targeting SIRT1 could protect glial cells against apoptosis in epilepsy | Wang et al. (2021d) |
| MDD | miR-138 (Up) | C57BL/6J mice | - | (Down) | PGC-1α, FNDC5, BDNF | miR-138 by targeting SIRT1 could enhance depressive-like behaviors in the hippocampus | Li et al. (2020b) |
| Migraine | miR-34a-5p (-) | SD rats | trigeminal ganglionic cells | (-) | COX2, PGE2, p65, NF-κβ, IL-1β, IL-13 | miR-34a-5p via inhibiting SIRT1 could enhance the IL-1β/COX2/PGE2 axis and stimulate the release of CGRP in trigeminal ganglion neurons in rats | Zhang et al. (2021a) |
| DFUs | miR-489-3p (-) | SD rats | HUVECs | (-) | VEGF, Bcl-2, Bax, Caspases-3/9, PI3K, AKT, eNOS, iNOS | Alteration in miR-489-3p/SIRT1 axis could enhance wound healing in DFU. | Huang et al. (2021a) |
| DR | miR-221 (Up) | - | hRMEC | (Down) | Nrf2, Caspase-3 Bax, Bcl-2, Keap-1 | Overexpression of miR-221 via inhibiting SIRT1 could enhance apoptosis of hRMEC. | Chen et al. (2020b) |
| ALI | miR-146a-3p (Up) | SD rats | BEAS-2B | (Down) | NF-κβ, TNF-α, IL-1β, IL-4, IL-6, IL-10 | Depletion of miR-146a-3p via upregulating SIRT1 and mediating NF-κB could attenuate ALI. | Yang and Li (2021) |
| UUO | miR-155-5p (Up) | - | NRK-49F | (Down) | α-SMA, Collage-I, Fibronectin | miR-155-5p via modulating SIRT1 promotes renal interstitial fibrosis | Wang et al. (2021e) |
| - | miR-217 (Up) | - | HUVECs | (-) | p53, SA-β-gal | miR-217 via modulating the SIRT1/p53 axis could enhance endothelial cell senescence | Wang et al. (2021f) |
| - | miR-204-5p (-) | C57BL/6J | HC11 | (-) | PPARγ | miR-204-5p by targeting SIRT1 could enhance lipid synthesis in mammary epithelial cells | Zhang et al. (2020a) |
| - | miR-128-3p (Up) | - | BMSCs | (-) | IL-6, IL-1β, MMP-9, MCP-1 | MiR-128-3p by regulating SIRT1 expression could mediate inflammatory responses in BMSCs | Wu et al. (2020) |
| - | miR‐34a‐5p, miR‐34a‐3p (-) | Human submandibular gland tissue samples (n = 114), human parotid gland tissue samples (n = 114), serum samples (n = 114), SD rats | SMG‐C6, | (-) | CTRP6, AMPK, TNF‐α, Bcl-2, Bax Caspase-3/8/9/12, Cytochrome-C, | CTRP6 via targeting the AMPK/SIRT1 axis by modulating miR‐34a‐5p expression could attenuate TNF‐α‐induced apoptosis | Qu et al. (2021) |
| - | miR-146a-5p (Up) | (n = 45) bone tissue samples, KO mice | MC3T3-E1 | (-) | Collagen-I | miR-146a-5p via targeting SIRT1 could regulate bone mass | Zheng et al. (2021) |
| PCa | miR-373 (-) | - | AsPC-1, | (-) | PGC-1α, NRF2, Bax, Bcl-2, Caspase-3/8/9, PARP, eNOS, iNOS | miR-373 via modulating the SIRT1/PGC-1α/NRF2 axis could suppress cell proliferation in pancreatic cancer cells | Yin et al. (2021) |
| PANC-1 | |||||||
| CRC | miR-34a (Up) | CRC tissue and ANT samples, DAB1/J mice, NOD-SCID mice | HCT-8, | (-) | NF-κβ, p65, B7-H3, TNF-α | miR-34a via modulating the SIRT1/NF-κB and B7-H3/TNF-α axis could induce immunosuppression in colorectal cancer | Meng et al. (2021) |
| HCT-116, | |||||||
| CHO, PBMCs | |||||||
| cSCC | miR-199a-5p (Down) | BALB/c nude mice | A431, NHSF | (Up) | CD44ICD, OCT4, SOX2, Nanog | miR-199a-5p by targeting SIRT1 and CD44ICD cleavage signaling could repress stemness of cSCC stem cells | Lu et al. (2020) |
SIRT1-interacting miRNAs.
FIGURE 1
SIRT1 works with a lot of molecules, some of which are transcription factors. p53, the FoxO family, HES1, HEY2, PPAR, CTIP2, p300, PGC-1, and NF-B are all transcription factors. Dysregulation of SIRT1-targeting miRNAs plays a role in the pathogenesis of sepsis and its complications, chronic hepatitis, ischemia/reperfusion (I/R) injury to the liver and heart, cardiac fibrosis, myocardial infarction, osteoarthritis, diabetic nephropathy, and a number of malignant diseases like colorectal cancer.
miR-128 has been shown to be involved in the pathogenesis of chronic angiotensin II infusion-induced cardiac remodeling through modulation of SIRT1. Silencing this miRNA in the heart tissues of mice could ameliorate angiotensin II-induced cardiac dysfunction, hypertrophy, fibrosis and oxidative stress damage. Angiotensin II could induce upregulation of miR-128 in cell culture. Treatment of cells with miR-128 antagomir could attenuate angiotensin II -induced apoptosis and oxidative damage possibly through targeting the SIRT1/p53 pathway. Suppression of this miRNA could also activate PIK3R1/Akt/mTOR pathway, restrain angiotensin II-induced autophagy in cardiomyocytes, and mitigate oxidative stress and apoptosis (Zhan et al., 2021).
SIRT1-interacting miRNAs are also involved in the pathogenic processes in the acute myocardial infarction. Suppression of miR-29a has been shown to protect against myocardial I/R injury through influencing expression of SIRT1 and subduing oxidative stress and NLRP3-associated pyroptosis (Ding et al., 2020). In addition, miR-200a-3p has been found to aggravate doxorubicin-induced cardiotoxic effects through targeting PEG3 via SIRT1/NF-κB signaling pathway (Fu et al., 2021). miR-181a-5p is another miRNA which participates in the cardiomyocyte apoptosis induced by hypoxia–reoxygenation via regulation of SIRT1 (Qi et al., 2020). Moreover, an experiment in an animal model of acute myocardial infarction has shown that miR-124-3p targets SIRT1 to influence cell apoptosis, inflammatory responses, and oxidative stress through regulation of the FGF21/CREB/PGC1α axis (Wei et al., 2021). Besides, miRNAs that modulate expression of SIRT1 can affect pathogenesis of heart failure. For instance, downregulation of miR-22 by targeting SIRT1/PGC-1α could alleviate this disorder (Wang et al., 2021b). Finally, miR199/SIRT1/P300 axis has apotential function in the patheticlogy of this disorder (Asensio-Lopez et al., 2021).
Lastly, three SIRT1-interacting miRNAs have been revealed to participate in the carcinogenesis. miR-373 is a tumor suppressor miRNA that inhibits proliferation of pancreatic cancer cells through influencing activity of SIRT1/PGC-1α/NRF2 axis (Yin et al., 2021). On the other hand, miR-34a acts as an immunosuppressive miRNA in colorectal cancer via regulation of SIRT1/NF-κB/B7-H3/TNF-α axis (Meng et al., 2021). Lastly, miR-199a-5p has a role in repression of stemness of squamous cell carcinoma cells through influencing activity of SIRT1 and CD44ICD cleavage signaling (Lu et al., 2020).
SIRT1-interacting circRNAs
Circular RNAs (CircRNAs) are common in all animals, from viruses to mammals. They are single-stranded, endogenous covalently closed RNA molecules with highly stability. The biosynthesis, regulation, localization, destruction, and modification of circRNAs have all seen great progress (Sayad et al., 2022). CircRNAs play a role in a wide range of human disorders, particularly malignancies (Ghafouri-Fard et al., 2021b; Ghafouri-Fard et al., 2022). The impact of SIRT1-interacting circRNAs in the regulation of SIRT1 has been assessed in diabetes and its complications, rheumatoid arthritis, chronic cerebral ischemia, osteoarthritis, intervertebral disc degeneration as well as malignant disorders, particularly glioma (Table 2). All of these circRNAs have been shown to act as molecular sponges for miRNAs to subsequently affect expression of miRNAs targets (Figure 2). For instance, hsa_circ_0115355 has been found to regulate activity of miR-145/SIRT1 axis, thus enhancing function of pancreatic ß cells in patients with type 2 diabetes mellitus (Dai et al., 2022). CircHIPK3 is another circRNA which participates in the pathogenesis of diabetic complications. Expression of this circRNA has been significantly reduced in HK-2 cells following exposure with high glucose. Forced upregulation of circHIPK3 could reverse high glucose-induced pathologic events in HK-2 cells. SIRT1 has been found to be the target of miR-326 and miR-487a-3p, two downstream genes of circHIPK3. Silencing of these two miRNAs could induce proliferation and decrease apoptosis in high glucose-induced HK-2 cells. Taken together, upregulation of circHIPK3 can reduce the effects of high glucose in HK-2 cells via sponging miR-326 or miR-487a-3p and influencing expression of SIRT1 (Zhuang et al., 2021).
TABLE 2
| Type of diseases | Circular-RNAs | Sample | Cell line | SIRT1 expression | Targets and pathways | Discussion | Ref |
|---|---|---|---|---|---|---|---|
| T2DM | hsa_circ_0115355 (Down) | Serum samples of T2DM patients (n = 20) | INS-1 | (Down) | miR-145 | hsa_circ_0115355 via targeting the miR-145/SIRT1 axis could enhance pancreatic ß-cell function | Dai et al. (2022) |
| DN | HIPK3 (Down) | - | HK-2 | (Down) | miR-326, | Circ-HIPK3 via modulating the miR-326/miR-487a-3p/SIRT1 axis could alleviate high glucose toxicity to HK-2 Cells | Zhuang et al. (2021) |
| miR-487a-3p, | |||||||
| Caspase-3, | |||||||
| Bax, Bcl-2 | |||||||
| RA | hsa_circ_0044235 (Down) | Serum samples of RA (n = 48), healthy control group (n = 36), DBA/1 J mice | FLSs | (Down) | miR-135b-5p, Caspase-1, | hsa_circ_0044235 could regulate pyroptosis via modulating miR-135b-5p-SIRT1 axis | Chen et al. (2021) |
| TNF-α, IL-6, | |||||||
| IL-1β, NLRP3 | |||||||
| CCI | circ_0000296 (Down) | C57BL/6J mice | HT22 | (Down) | miR-194-5p, Runx3 | Upregulation of circ_0000296 via miR-194-5p/Runx3 axis could increase transcription of SIRT1 and inhibit apoptosis of hippocampal neurons | Huang et al. (2021b) |
| OA | Circ_0001103 (Down) | OA samples (n = 30), normal tissues (n = 10), OA serum (n = 10) and normal (n = 10) samples | Chondrocyte | (Down) | miR-375, IL-1β, COL2A1, ADAMTS4 | Circ_0001103 via targeting miR-375 by upregulating SIRT1 could alleviate IL-1β-induced chondrocyte cell injuries | Zhang et al. (2021b) |
| IDD | CIDN (Down) | IDD tissue samples (n = 30) and healthy control tissues (n = 50), SD rats | NP | (Down) | miR-34a-5p, | Circ-CIDN via the miR-34a-5p/SIRT1 axis could mitigate compression loading-induced damage | Xiang et al. (2020) |
| MMP-3/13, Bax, caspase-3, Bcl-2, | |||||||
| Collagen-II | |||||||
| GC | NOP10 (Up) | 10 pairs of GC and ANT samples | GES-1, AGS, | (Up) | miR-204, NF-κβ, E-cadherin, p65, Vimentin, Bcl-2, Caspase-3, Bax | Circ-NOP10 by regulating the miR-204/SIRT1 axis could mediate gastric cancer progression | Xu et al. (2021b) |
| MNK-45, | |||||||
| HGC-27, | |||||||
| BGC-823 | |||||||
| Glioma | Circ-0082374 (Up) | glioma samples (n = 42), non-cancer tissue samples (n = 28), BALB/c nude mice | A172, BT325, | (-) | miR-326, | Knockdown of Circ-0082374 by modulating the miR-326/SIRT1 axis could inhibit viability, migration, invasion, and glycolysis of glioma cells | Wang et al. (2020) |
| LN229, U251, | MMP-9, | ||||||
| SHG44, HA1800 | E-cadherin, Vimentin |
SIRT1-interacting circRNAs.
FIGURE 2
CircRNAs have been proven to serve as molecular sponges for miRNAs, thereby influencing the expression of miRNA targets. SIRT1 has been found to be the target of miRNA genes, which were already being sponged by different types of circRNAs that prevented or enhanced gene expression.
Hsa_circ_0044235 is another circRNA which has been shown to be downregulated in patients with rheumatoid arthritis (RA). Downregulation of this circRNA has been correlated with low levels of SIRT1 expression in these patients. Overexpression of hsa_circ_0044235 could attenuate joint inflammation, cell apoptosis, and joint injury, and reduce NLRP3-mediated pyroptosis but increasing SIRT1 expression. Upregulation of this circRNA could also inhibit caspase-1 content. Mechanistically, hsa_circ_0044235 increases expression of SIRT1 through sponging miR-135b-5p (Chen et al., 2021).
CircularNOP10 and circ0082374 are two putative oncogenic circRNAs that regulate expression of SIRT1. CircularNOP10 has a role in induction of progression of gastric cancer through regulation of miR-204/SIRT1 pathway (Xu J. et al., 2021). In glioma cells, circ0082374 has a role in induction of cell viability, migration, invasion and glycolysis through regulation of miR-326/SIRT1 axis (Wang et al., 2020).
SIRT1-interacting lncRNAs
Transcripts larger than 200 nt are known as long non-coding RNAs (lnRNAs), which cannot code for proteins and may possess small open reading frames (ORFs). Because they interact with various proteins, mRNAs and DNA sequences, lncRNAs play significant roles in a number of disorders (Sabaie et al., 2021; Hussen et al., 2022b). GAS5, LincRNA‐p21, MCM3AP-AS1, TUG1, SNHG7, SNHG8, SNHG10, SNHG15, Oip5-as1, ILF3-AS1, ANRIL, UCA1 and KCNQ1OT1 are examples of lncRNAs that regulate expression of SIRT1 through sponging miRNAs. These lncRNAs can affect pathogenesis of RA, atherosclerosis, sepsis-associated renal injury (SARI), diabetic nephropathy, ischemic stroke and a number of malignant conditions (Table 3). For instance, GAS5 via regulating the miR-222-3p/Sirt1 axis could alleviate RA (Yang et al., 2021). Moreover, GAS5 via inhibiting the miR-579-3p and activating the SIRT1/PGC-1α/Nrf2 axis could reduce cell pyroptosis in SARI (Ling et al., 2021). In the context of osteoarthritis, MCM3AP-AS1 via modulating the miR-138-5p/SIRT1 axis could protect chondrocytes from IL-1β-induced inflammation (Shi et al., 2021).
TABLE 3
| Type of diseases | LncRNA | Sample | Cell line | SIRT1 expression | Target and pathways | Discussion | Ref |
|---|---|---|---|---|---|---|---|
| RA | GAS5 (Down) | Serum samples of RA patients (n = 35) and Serum samples of healthy control (n = 35) | RA-FLSs | (Down) | miR-222-3p, TNF-α,IL-1β, IL-6, Bcl-2, Bax, Caspase-3/9 | GAS5 via regulating the miR-222-3p/Sirt1 axis could alleviate RA. | Yang et al. (2021) |
| Atherosclerosis | LincRNA‐p21 (Down) | Serum samples of AS patients (n = 25), C57BL/6 mice | HAECs, | (Down) | miR-221, Pcsk9, Caspase-3, Bcl-2, Bax | LncRNA-p21 via modulating the miR-221/SIRT1/Pcsk9 axis could alleviate atherosclerosis progression | Wang et al. (2021g) |
| 293T | |||||||
| SARI | GAS5 (Down) | C57BL/6 mice | HK-2 | (Down) | miR-579-3p, Nrf2, IL-1β, IL-18, NLRP3, PGC-1α, Caspase-1, | GAS5 via inhibiting the miR-579-3p by activating the SIRT1/PGC-1α/Nrf2 axis could reduce cell pyroptosis in SARI. | Ling et al. (2021) |
| OA | MCM3AP-AS1 (Down) | 30 pairs of OA and ANTs | CHON-001, ATDC5 | (Down) | miR-138-5p, | MCM3AP-AS1 via modulating the miR-138-5p/SIRT1 axis could protect chondrocytes from IL-1β-induced inflammation | Shi et al. (2021) |
| IL-6, IL-8, | |||||||
| TNF-α | |||||||
| Sepsis | TUG1 (Down) | C57BL/6 mice | RAW264.7 | (Down) | miR-9-5p, TNF-α, MCP-1, IL-6, IL-10, iNOS, Arg-1, | TUG1 via impairing miR-9-5p targeted SIRT1 inhibition could confer anti-inflammatory macrophage polarization in sepsis effects | Ma et al. (2021) |
| DN | TUG1 (Down) | - | HK-2 | SIRT1 (Down) | miR-29c-3p, ERS, Bax, Bcl-2, caspase-3/12, GRP78, CHOP, PERK, eIF-2α | The TUG1/miR-29c-3p/SIRT1 axis could regulate endoplasmic reticulum stress-mediated cell injury in DN. | Wang et al. (2021h) |
| Ischemic Stroke | SNHG8 (-) | C57BL/6 mice | BMEC | (Down) | miR‐425‐5p, NF‐κβ, caspase-3, ZO-1, Occludin, TNF-α, IL-1β, IL-6 | SNHG8 via regulating miR‐425‐5p mediated SIRT1/NF‐κβ axis could attenuate blood-brain barrier damage | Tian et al. (2021) |
| Ischemic Stroke | SNHG7 (Down) | C57BL/6 mice | PC12, | (Down) | miR-9 | SNHG7 by targeting the miR-9/SIRT1 axis could alleviate damage in PC12 Cells | Zhou et al. (2020) |
| Cerebral I/R Injury | SNHG15 (Up) | - | SH-SY5Y | (-) | miR-141, TNF-α, IL-1β, IL-6, iNOS, p65 | SNHG15 by targeting the miR-141/SIRT1 axis could enhance oxidative stress damage | Kang et al. (2021) |
| Myocardial I/R Injury | Oip5-as1 (Down) | SD rats | NRVMs, | (Down) | miR-29a, AMPK, PGC1α, LDH, ROS, Bax, Bcl-2, Cyt-c, caspase-3, 15-F2t-isoprostane, SOD, GPx | Oip5-as1 via activating the SIRT1/AMPK/PGC1α axis by sponging miR-29a could attenuate myocardial I/R injury | Niu et al. (2020) |
| H9c2 | |||||||
| MI | ILF3-AS1 (Down) | - | H9c2, | (-) | miR-212-3p, PI3K, AKT, Bcl-2, Bax, caspase-3/9 | ILF3-AS1 via targeting the miR-212-3p/SIRT1 axis and the PI3K/Akt pathway could regulate MI. | Zhang et al. (2020c) |
| 293T | |||||||
| AMI | ANRIL (Up) | - | H9c2 | (-) | miR‐7‐5p, Bcl-2, Bax, Caspase-3/9, HIF-1α | ANRIL via targeting the miR‐7‐5p/SIRT1 axis could protect H9c2 cells against hypoxia‐induced injury | Shu et al. (2020) |
| Diabetes | TUG1 (Down) | C57BL/6J mice | 3T3-L1 | (Down) | miR-204, AMPK, ACC, ATGL, PGC-1α, PPARα, UCP-1 | TUG1 via targeting SIRT1 by regulating miR-204 could enhance brown remodeling of white adipose tissue in diabetic mice | Zhang et al. (2020d) |
| NSCLC | SNHG10 (Down) | 60 pairs of NSCLC and ANT samples | H1581, H1703 | (-) | miR-543 | SNHG10 via sponging miR-543 could upregulate tumor suppressive SIRT1 in NSCLC. | Zhang et al. (2020b) |
| HCC | SNHG7 (Up) | 25 pairs of HCC and ANT samples | THLE-3, | (Up) | miR-34a, NLRP3, Caspase-1, IL-1β | SNHG7 via targeting the miR-34a/SIRT1 axis could inhibit NLRP3-dependent pyroptosis | Chen et al. (2020c) |
| 293T, HepG2, | |||||||
| SK-hep-1 | |||||||
| CRC | GAS5 (Down) | 75 pairs of CRC and ANT samples, Wistar rats | HT29, | (Up) | miR-34a, mTOR, LC3 I/II. Beclin-1, Bcl-2, Bax | GAS5 via targeting the miR-34a/mTOR/SIRT1 axis could inhibit malignant progression in CRC. | Zhang et al. (2021c) |
| HCT116, | |||||||
| SW480, | |||||||
| SW620 | |||||||
| AML | UCA1 (Up) | Serum samples: AML (n = 27), normal (n = 9) | KG‐1a, THP‐1, | (-) | miR‐204, Caspase-3, iNOS, COX-2 | Silencing UCA1 via targeting miR‐204 by repressing SIRT1 could accelerate apoptosis in pediatric AML. | Liang et al. (2020) |
| HS‐5 | |||||||
| RB | KCNQ1OT1 (UP) | 3 pairs of RB and ANTs, nude mice | hTERT RPE-1, Y79, WERI-Rb-1 | (Down) | miR-124, | KCNQ1OT1 by targeting the miR-124/SP1 axis could modulate RB cell proliferation and invasion | Zhang et al. (2021d) |
| SP1, Cyclin-D1, | |||||||
| Caspase-3, Vimentin, | |||||||
| E/N-cadherin, |
SIRT1-interacting lncRNAs.
SIRT1-interacting lncRNAs have also been shown to affect pathogenesis of malignant conditions. For instance, SNHG10 has been found to sponge miR-543 in non small cell lung cancer (Zhang Z. et al., 2020). Moreover, SNHG7 has been demonstrated to inhibit NLRP3-associated pyroptosis through regulating miR-34a/SIRT1 axis in liver cancer (Chen Z. et al., 2020). GAS5 can inhibit malignant progression of colorecatl cancer cells through regulating macroautophagy and forming a negative feedback loop with the miR-34a/mTOR/SIRT1 axis (Zhang HG. et al., 2021). On the other hand, UCA1 has a role in induction of cell proliferation and suppression of apoptosis through affecting expression of SIRT1 and miR‐204 in pediatric AML (Liang et al., 2020). The known interactions that SIRT1 has with a variety of lnRNAs are illustrated in Figure 3.
FIGURE 3
There are numerous ways in which SIRT1 and the other lnRNAs interact, and it has been demonstrated that these interactions have an impact on pathogenesis conditions.
A number of therapeutic agents such as anthocyanins, ginsenoside-R3, dexmedetomidine hydrochloride, berberine, sorafenib, 17β-Estradiol, phenylpyridinium, tetrahydroxy stilbene glycoside, cisplatin, resveratrol, sulforaphane and liraglutide have been found to affect expression of non-coding RNAs/SIRT1 axes (Table 4). For instance, experiments in animal model of asthma have shown that anthocyanins suppresses inflammatory responses in airways through decreasing activity of NF-κB pathway via the miR-138-5p/SIRT1 axis (Liu Y. et al., 2022). Moreover, ginsenoside Rg3 can alleviate sepsis-related hepatic injury through modulation of TUG1/miR-200c-3p/SIRT1 axis (Wu P. et al., 2021). TUG1/miR-194/SIRT1 axis has been found to be targeted by dexmedetomidine hydrochloride to inhibit hepatocytes apoptosis and inflammatory responses (Gu et al., 2021). Additionally, the effects of berberine in amelioration of hepatic insulin resistance have been revealed to be mediated through regulation of miR-146b/SIRT1 axis (Sui et al., 2021).
TABLE 4
| Type of diseases | Drug | Non-coding RNAs | Sample | Cell line | SIRT1 expression | Target | Discussion | Ref |
|---|---|---|---|---|---|---|---|---|
| Asthma | Anthocyanins (Anth) | miR-138-5p (Up) | Balb/c mice; treated with 250 mg/kg Anth before each atomization for 1 h | HBE; treated with 10 μg/mL Anth for 1 h | (-) | NF-κβ p65, | Anth via targeting the miR-138-5p/SIRT1 axis by downregulating NF-κβ could inhibit airway inflammation in asthmatic mice | Liu et al. (2022b) |
| IL-4/5/13, | ||||||||
| IFN-γ | ||||||||
| Sepsis | Ginsenoside-R3 (Rg3) | TUG1 (-), miR-200c-3p | C57BL/6 mice; treated with 20 mg/kg Rg3, I.P, for 1 h | Hepatocyte; pretreated with 25 μM Rg3 for 6 h | (Down) | LC3-I/II, p62, Beclin-1, | Rg3 by modulating the TUG1/miR-200c-3p/SIRT1 axis could alleviate septic liver injury | Wu et al. (2021b) |
| PGC1-α, | ||||||||
| AMPK | ||||||||
| LI | Dexmedetomidine hydrochloride (DEX) | TUG1 (-), miR-194 | - | WRL-68; pretreated with 0.01, 0.1, and 1, 5 nM DEX for 1 h | (Down) | Bax, Bcl-2, | DEX by activating the TUG1/miR-194/SIRT1 axis could inhibit hepatocyte inflammation and apoptosis | Gu et al. (2021) |
| TNF-α, | ||||||||
| IL-1β, IL-6 | ||||||||
| Insulin resistance | Berberine (BBR) | miR-146b (-) | C57BL/6J mice; treated with 5, 10 mg/kg/day, I.P, for 4 weeks, | HepG2; treated with 5–30 µM BBR for 24h and 48 h | (Down) | FOXO1 | BBR by regulating the miR-146b/SIRT1 axis could ameliorate hepatic insulin resistance | Sui et al. (2021) |
| Liver cancer | Sorafenib | miR-425 (-) | TCGA and GEO databases | HepG2, PLC, Hep3B, Huh7, MIHA; treated with 10 µM for 48 h | (-) | LC3-I/II, | miR-425 via SIRT1 to promote sorafenib resistance could regulate lipophagy in liver cancer | Sun et al. (2021) |
| ATGL | ||||||||
| PMOP | 17β-Estradiol (E2) | H19 (Down), miR-532-3p | Bone tissue (n = 10), serum samples (n = 10), control group (n = 10), Wistar rats; treated with 0.5 mg/kg/day E2 subcutaneously | BMSCs; treated with 10–7 M E2 for 14 days | (Down) | ALP, RUNX2, | E2 via targeting the miR-532-3p/SIRT1 axis could enhance the expression of H19 to regulate osteogenic differentiation | Li et al. (2021c) |
| PD | Phenylpyridinium (MPP) | miR-132 (-) | FVB littermate wild-type mice | SH-SY5Y; treated with 1.25 and 2.5 mM MPP, for 12, 24, 48 h | (Down) | p53, | Upregulation of miR-132 via activating the SIRT1/p53 axis could induce PD. | Qazi et al. (2021) |
| NF-κB | ||||||||
| - | Tetrahydroxy Stilbene Glycoside (TSG) | miR-34a (Up) | - | HUVECs; pretreated with 20, 40 μg/ml TSG for 24 h | (Down) | PAI-1, p21 | TSG via targeting the miR-34a/SIRT1 axis could attenuate endothelial cell premature senescence | Zhang et al. (2022) |
| AKI | Cisplatin (DDP) | miR-132-3p (-) | C57BL/6J mice; treated with 20 mg/kg DDP for 24, 48 h | HK-2; treated with 5 μg/ml DDP for 24, 48 h | (Down) | NF-κβ, | miR-132-3p via targeting NF-κβ by modulating SIRT1 could promote DDP-induced apoptosis in renal tubular epithelial cells | Han et al. (2021) |
| BLC | DDP | MST1P2 (-), miR‐133b | - | SW 780/DDP, RT4/DDP | (-) | p53, | LncRNA MST1P2/miR‐133b axis via the SIRT1/p53 axis can influence chemoresistance to DDP‐based therapy | Chen et al. (2020d) |
| Caspase-3 | ||||||||
| - | Resveratrol (RSV) | miR-155 (-) | - | N9; treated with 10 µM RSV for 1 h | (-) | AMPK, NLRP3, NF-κβ, | RSV via targeting the SIRT1/AMPK axis could inhibit NLRP3 inflammasome-induced pyroptosis and miR-155 expression in microglia | Tufekci et al. (2021) |
| IL-1β, IL-18 | ||||||||
| - | Sulforaphane (SFN) | miR-34a (Up) | HUVECs; pretreated with 1.0 μmol/l SFN for 4, 8, 12 h | (-) | Nrf2, | SFN via modulating the miR-34a/SIRT1 axis by upregulating Nrf2 could protect endothelial cells from oxidative stress | Li et al. (2021d) | |
| ARE | ||||||||
| DN | Liraglutide (LRG) | miR-34a (-) | SD rats; treated with 6 mg LRG subcutaneously for 12 weeks | - | (-) | AST, ALT, HIF-1α, | LRG via targeting the miR-34a/SIRT1 axis could regulate kidney and liver in DN rats | Xiao et al. (2021) |
| Egr-1, | ||||||||
| TGF-β1 |
Effects of drugs on SIRT1-interacting ncRNAs.
Discussion
SIRT1 has a role as a deacetylase and is able to deacetylate a range of substrates. Thus, it participates in the regulation of a wide array of physiological processes such as gene expression, metabolic pathways and aging (Haigis and Guarente, 2006; Michan and Sinclair, 2007). This protein has functional interactions with lncRNAs, miRNAs and circRNAs. In fact, a complicated network exists between these non-coding RNAs and SIRT1. Hsa_circ_0115355/miR-326, hsa_circ_0115355/miR-487a-3p, HIPK3/miR-145, hsa_circ_0044235/miR-135b-5p, circ_0000296/miR-194-5p, circ_0001103/miR-375, CIDN/miR-34a-5p, NOP10/miR-204, circ-0082374/miR-324 are examples of circRNA/miRNA pairs that interact with SIRT1. Similarly, GAS5/miR-222-3p, GAS5/miR-579-3p, GAS5/miR-34a, MCM3AP-AS1/miR-138-5p, TUG1/miR-9-5p, TUG1/miR-29c-3p, TUG1/miR-204, SNHG8/miR‐425‐5p, SNHG7/miR-9, SNHG7/miR-34a, SNHG15/miR-141, SNHG10/miR-543, Oip5-as1/miR-29a, ILF3-AS1/miR-212-3p, ANRIL/miR-7-5p, UCA1/miR-204 and KCNQ1OT1/miR-124 are lncRNA/miRNA pairs that regulate expression of SIRT1 in different contexts. These interactions are possibly involved in the pathoetiology of a number of human disorders such as sepsis, cardiomyopathy, heart failure, non-alcoholic fatty liver disease, chronic hepatitis, cardiac fibrosis, myocardial ischemia/reperfusion injury, diabetes, ischemic stroke, immune-related disorders and cancers. In cancers, SIRT1-interacting non-coding RNAs not only affect cell proliferation but also regulate stemness and immunosuppressive responses in the tumor niche.
SIRT1 is a potential target for design of novel therapies. Most importantly, a number of drugs used for treatment of diverse asthma, sepsis, liver injury, insulin resistance, postmenopausal osteoporosis, Parkinson’s disease, diabetic nephropathy and cancers exert their effects through modulation of non-coding RNAs/SIRT1 axis. Thus, identification of the interactions between non-coding RNAs and SIRT1 has practical significance in design of novel therapeutic strategies for diverse disorders. Remarkably, non-coding RNAs that modulate expression of SIRT1 are putative modulators of the response of patients to different drugs.
Statements
Acknowledgments
The authors would like to thank the clinical Research Development Unit (CRDU) of Loghman Hakim Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran for their support, cooperation and assistance throughout the period of study.
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.
Glossary
| ANT | Adjacent normal tissue |
| PPARα | peroxisome proliferators-activated receptor a |
| CTRP6 | C1q/Tumor Necrosis Factor‐Related Protein‐6 |
| HMGCoAR | β-Hydroxy ß-Methylglutaryl-CoA Reductase |
| hUC-MSCs | Human Umbilical Cord-Derived Mesenchymal Stem Cell |
| HBE | Human Bronchial Epithelial |
| hTERT RPE-1 | Human Retinal Pigment Epithelial Cell Line |
| FLSs | Fibroblast-Like Synoviocytes |
| PBMCs | Human Peripheral Blood Mononuclear Cells |
| BMSCs | Human Bone Marrow Mesenchymal Stem Cells |
| ALP | Alkaline Phosphatase |
| MPO | Myeloperoxidase |
| CECs | Cardiac Endothelial Cells |
| CFs | Cardiac Fibroblasts |
| CMs | Cardiomyocytes |
| CGRP | Calcitonin Generated Peptide |
| PGE2 | Prostaglandin E2 |
| BMEC | Microvascular Endothelial Cell |
| HASMCs | Human Aortic Smooth Muscle Cells |
| HIF-1α | Hypoxia-Inducible Factor-1 a |
| Egr-1 | Early Growth Response-1 |
| UA | Uric Acid |
| UREA | Urea |
| Nrf2 | Nuclear Factor Erythroid-2-Related Factor 2 |
| ARE | Antioxidant Response Element |
| NRVMs | Neonatal Rats Ventricular Myocytes |
| BMSCs | Bone Marrow Mesenchymal Stem Cells |
| hRMEC | Human Retinal Microvascular Endothelial Cells |
| CUMS | Chronic Unpredictable Mild Stress |
| HBDH | Hydroxybutyratse Dehydrogenase |
| CK-MB | Creatine Kinase MB Activity |
| NHSF | Normal Human Skin Fibroblast |
| RA | Rheumatoid Arthritis |
| AS | Atherosclerosis |
| SARI | Sepsis-associated renal injury |
| AML | Pediatric acute myeloid leukemia |
| HCC | Hepatocellular carcinoma |
| NSCLC | Non-small cell lung cancer |
| I/R | Ischemia-reperfusion |
| NAFLD | Non-Alcoholic Fatty Liver Disease |
| CHC | Chronic Hepatitis C |
| SCMP | Septic Cardiomyopathy |
| CHF | Congestive Heart Failure |
| HF | Heart Failure |
| MI | Myocardial Injury |
| AMI | Acute Myocardial Infarction |
| AKI | Osteoarthritis (OA), Acute Kidney Injury |
| DN | Diabetic Nephropathy |
| DR | Diabetic Retinopathy |
| SCI | Spinal Cord Injury |
| CCIS | Chronic Constriction Injury of Sciatic Nerve |
| MDD | Major Depressive Disorder |
| DFUs | Diabetic Foot Ulcers |
| ALI | Acute Lung Injury |
| UUO | Unilateral Ureteral Obstruction |
| PCa | Pancreatic Cancer |
| CRC | Colorectal Cancer |
| cSCC | Cutaneous Squamous Cell Carcinoma |
| RB | retinoblastoma |
| T2DM | Type 2 Diabetes Mellitus |
| CCI | Chronic Cerebral Ischemia |
| IDD | Intervertebral Disc Degeneration |
| GC | Gastric Cancer |
| LI | Liver Injury |
| HIR | Hepatic Insulin Resistance |
| PMOP | Postmenopausal osteoporosis |
| PD | Parkinson’s Disease |
| BLC | Bladder Cancer |
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Summary
Keywords
SIRT1, lncRNA, miRNA, circRNA, biomar
Citation
Ghafouri-Fard S, Shoorei H, Hussen BM, Poornajaf Y, Taheri M and Sharifi G (2023) Interaction between SIRT1 and non-coding RNAs in different disorders. Front. Genet. 14:1121982. doi: 10.3389/fgene.2023.1121982
Received
12 December 2022
Accepted
16 June 2023
Published
27 June 2023
Volume
14 - 2023
Edited by
Liqi Shu, Brown University, United States
Reviewed by
Roopa Biswas, Uniformed Services University of the Health Sciences, United States
Amin Safa, Complutense University of Madrid, Spain
Updates
Copyright
© 2023 Ghafouri-Fard, Shoorei, Hussen, Poornajaf, Taheri and Sharifi.
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: Mohammad Taheri, Mohammad.taheri@uni-jena.de; Guive Sharifi, gibnow@yahoo.com
Disclaimer
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