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<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Pharmacol.</journal-id>
<journal-title>Frontiers in Pharmacology</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Pharmacol.</abbrev-journal-title>
<issn pub-type="epub">1663-9812</issn>
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<publisher-name>Frontiers Media S.A.</publisher-name>
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<article-id pub-id-type="publisher-id">1385565</article-id>
<article-id pub-id-type="doi">10.3389/fphar.2024.1385565</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Pharmacology</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Induction of ferroptosis by natural products in non-small cell lung cancer: a comprehensive systematic review</article-title>
<alt-title alt-title-type="left-running-head">Zhang et al.</alt-title>
<alt-title alt-title-type="right-running-head">
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fphar.2024.1385565">10.3389/fphar.2024.1385565</ext-link>
</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" equal-contrib="yes">
<name>
<surname>Zhang</surname>
<given-names>Qiang</given-names>
</name>
<xref ref-type="author-notes" rid="fn001">
<sup>&#x2020;</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2104243/overview"/>
<role content-type="https://credit.niso.org/contributor-roles/Writing - review &#x26; editing/"/>
<role content-type="https://credit.niso.org/contributor-roles/funding-acquisition/"/>
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<contrib contrib-type="author" equal-contrib="yes">
<name>
<surname>Xia</surname>
<given-names>Yuting</given-names>
</name>
<xref ref-type="author-notes" rid="fn001">
<sup>&#x2020;</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Feiyan</given-names>
</name>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
<role content-type="https://credit.niso.org/contributor-roles/software/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Yang</surname>
<given-names>Dongfeng</given-names>
</name>
<uri xlink:href="https://loop.frontiersin.org/people/1400245/overview"/>
<role content-type="https://credit.niso.org/contributor-roles/investigation/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Liang</surname>
<given-names>Zongsuo</given-names>
</name>
<xref ref-type="corresp" rid="c001">&#x2a;</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2655626/overview"/>
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<aff>
<institution>Key Laboratory of Plant Secondary Metabolism and Regulation of Zhejiang Province</institution>, <institution>College of Life Sciences</institution>, <institution>Zhejiang Sci-Tech University</institution>, <addr-line>Hangzhou</addr-line>, <country>China</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>
<bold>Edited by:</bold> <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/299382/overview">Jianqiang Xu</ext-link>, Dalian University of Technology, China</p>
</fn>
<fn fn-type="edited-by">
<p>
<bold>Reviewed by:</bold> <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/1720160/overview">Xinhui Wang</ext-link>, Zhejiang University, China</p>
<p>
<ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/975651/overview">Charareh Pourzand</ext-link>, University of Bath, United Kingdom</p>
</fn>
<corresp id="c001">&#x2a;Correspondence: Zongsuo Liang, <email>liangzs2022@126.com</email>
</corresp>
<fn fn-type="equal" id="fn001">
<label>
<sup>&#x2020;</sup>
</label>
<p>These authors have contributed equally to this work and share first authorship</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>01</day>
<month>05</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>15</volume>
<elocation-id>1385565</elocation-id>
<history>
<date date-type="received">
<day>13</day>
<month>02</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>12</day>
<month>04</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Zhang, Xia, Wang, Yang and Liang.</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Zhang, Xia, Wang, Yang and Liang</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>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.</p>
</license>
</permissions>
<abstract>
<p>Lung cancer is one of the leading causes of cancer-related deaths worldwide that presents a substantial peril to human health. Non-Small Cell Lung Cancer (NSCLC) is a main subtype of lung cancer with heightened metastasis and invasion ability. The predominant treatment approaches currently comprise surgical interventions, chemotherapy regimens, and radiotherapeutic procedures. However, it poses significant clinical challenges due to its tumor heterogeneity and drug resistance, resulting in diminished patient survival rates. Therefore, the development of novel treatment strategies for NSCLC is necessary. Ferroptosis was characterized by iron-dependent lipid peroxidation and the accumulation of lipid reactive oxygen species (ROS), leading to oxidative damage of cells and eventually cell death. An increasing number of studies have found that exploiting the induction of ferroptosis may be a potential therapeutic approach in NSCLC. Recent investigations have underscored the remarkable potential of natural products in the cancer treatment, owing to their potent activity and high safety profiles. Notably, accumulating evidences have shown that targeting ferroptosis through natural compounds as a novel strategy for combating NSCLC holds considerable promise. Nevertheless, the existing literature on comprehensive reviews elucidating the role of natural products inducing the ferroptosis for NSCLC therapy remains relatively sparse. In order to furnish a valuable reference and support for the identification of natural products inducing ferroptosis in anti-NSCLC therapeutics, this article provided a comprehensive review explaining the mechanisms by which natural products selectively target ferroptosis and modulate the pathogenesis of NSCLC.</p>
</abstract>
<kwd-group>
<kwd>non-small cell lung cancer</kwd>
<kwd>ferroptosis</kwd>
<kwd>natural products</kwd>
<kwd>cancer treatment</kwd>
<kwd>drug development</kwd>
</kwd-group>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-at-acceptance</meta-name>
<meta-value>Pharmacology of Anti-Cancer Drugs</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1">
<title>1 Introduction</title>
<p>According to the latest data from the Global Cancer Observatory (GCO) (Cancer Today (iarc.fr)), in 2020, lung cancer ranked as the third most common cancer globally, with an incidence rate of approximately 22.4 cases per 100,000 population and a mortality rate of around 18% per 100,000 population (<xref ref-type="bibr" rid="B136">Sung et al., 2021</xref>) (<xref ref-type="fig" rid="F1">Figure 1</xref>). Non-Small Cell Lung Cancer (NSCLC) represents the predominant subtype of lung cancer, accounting for approximately 85% of cases, and it is characterized by a poor prognosis, with a 5-year survival rate of only 19% (<xref ref-type="bibr" rid="B120">Rodr&#xed;guez-Abreu et al., 2021</xref>; <xref ref-type="bibr" rid="B110">Mithoowani and Febbraro, 2022</xref>). Over the past few decades, various treatment modalities, including surgery, chemotherapy, radiation therapy, targeted therapy, and immunotherapy, have been employed in the clinical management of NSCLC (<xref ref-type="bibr" rid="B53">Hopstaken et al., 2021</xref>; <xref ref-type="bibr" rid="B109">Miller and Hanna, 2021</xref>; <xref ref-type="bibr" rid="B149">Wang et al., 2021</xref>; <xref ref-type="bibr" rid="B2">Alduais et al., 2023</xref>). Despite the significant advances achieved for these treatment strategies, the development of therapy resistance in NSCLC remains a considerable challenge (<xref ref-type="bibr" rid="B14">Brown et al., 2019</xref>; <xref ref-type="bibr" rid="B115">Patel and Weiss, 2020</xref>; <xref ref-type="bibr" rid="B113">Muthusamy et al., 2022</xref>), thus necessitating the exploration of novel therapeutic approaches for NSCLC.</p>
<fig id="F1" position="float">
<label>FIGURE 1</label>
<caption>
<p>Estimated age-standardized incidence and mortality rates (World) in 2020, World, both sexes, all ages.</p>
</caption>
<graphic xlink:href="fphar-15-1385565-g001.tif"/>
</fig>
<p>Ferroptosis is a novel form of programmed cell death (PCD) that has been recently discovered and differs morphologically, biochemically, and genetically from apoptosis, autophagy, and necrotic (<xref ref-type="bibr" rid="B111">Mou et al., 2019</xref>; <xref ref-type="bibr" rid="B20">Chen et al., 2021b</xref>; <xref ref-type="bibr" rid="B185">Yuan et al., 2021</xref>). The presence of ferroptosis in cells is commonly linked to the accumulation of iron, disturbances in fatty acid metabolism, and lipid peroxidation (<xref ref-type="bibr" rid="B142">Ursini and Maiorino, 2020</xref>; <xref ref-type="bibr" rid="B171">Xu et al., 2021</xref>; <xref ref-type="bibr" rid="B180">Yao et al., 2021</xref>), which play crucial roles in initiating ferroptosis (<xref ref-type="bibr" rid="B76">Li and Li, 2020</xref>; <xref ref-type="bibr" rid="B189">Zhang et al., 2022</xref>). Previous studies have highlighted the significant role of ferroptosis in the pathogenesis of NSCLC, suggesting ferroptosis maybe a potential and novel approach for NSCLC treatment (<xref ref-type="bibr" rid="B94">Liu et al., 2021</xref>; <xref ref-type="bibr" rid="B96">Liu et al., 2022</xref>). The mediators or signal pathways regarding to ferroptosis in the pathological progression of NSCLC were presented in <xref ref-type="table" rid="T1">Table 1</xref>.</p>
<table-wrap id="T1" position="float">
<label>TABLE 1</label>
<caption>
<p>The mediators or signal pathways regarding to ferroptosis in the pathological progression of NSCLC.</p>
</caption>
<table>
<thead valign="top">
<tr>
<th align="center">Mediators or signal pathways</th>
<th align="center">Full name</th>
<th align="left">Mechanism</th>
<th align="center">References</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="center">FSP1</td>
<td align="center">S100 calcium binding protein A4</td>
<td align="left">FSP1 reduces ubiquinone (CoQ) to ubiquinol (CoQH2). As an antioxidant, CoQH2 inhibits lipid peroxidation and prevents ferroptosis</td>
<td align="center">
<xref ref-type="bibr" rid="B13">Bersuker et al. (2019)</xref>
</td>
</tr>
<tr>
<td align="center">Nrf-2/HMOX1</td>
<td align="center">NFE2 like bZIP transcription factor 2/heme oxygenase 1</td>
<td align="left">Acetaminophen sensitizing erastin-induced ferroptosis via modulation of Nrf-2/heme oxygenase-1 signaling pathway in non-small-cell lung cancer</td>
<td align="center">
<xref ref-type="bibr" rid="B35">Gai et al. (2020b)</xref>
</td>
</tr>
<tr>
<td align="center">HO-1</td>
<td align="center">heme oxygenase-1</td>
<td align="left">Lysosomal destabilizing drug Siramesine and the dual tyrosine kinase inhibitor Lapatinib induce a synergistic ferroptosis through reduced heme oxygenase-1(HO-1) levels</td>
<td align="center">
<xref ref-type="bibr" rid="B145">Villalpando-Rodriguez et al. (2019)</xref>
</td>
</tr>
<tr>
<td align="center">Notch3</td>
<td align="center">notch receptor 3</td>
<td align="left">Notch3 regulates ferroptosis via ROS-induced lipid peroxidation in NSCLC.</td>
<td align="center">
<xref ref-type="bibr" rid="B87">Li et al. (2022e)</xref>
</td>
</tr>
<tr>
<td align="center">TP53</td>
<td align="center">tumor protein p53</td>
<td align="left">Upregulation and activation of p53 by erastin-induced reactive oxygen species contribute to cytotoxic and cytostatic effects in A549 lung cancer cells</td>
<td align="center">
<xref ref-type="bibr" rid="B58">Huang et al. (2018)</xref>
</td>
</tr>
<tr>
<td align="center">P53RRA</td>
<td align="center">long intergenic non-protein coding RNA 472</td>
<td align="left">P53RRA promoted ferroptosis and apoptosis by affecting transcription of several metabolic genes</td>
<td align="center">
<xref ref-type="bibr" rid="B104">Mao et al. (2018)</xref>
</td>
</tr>
<tr>
<td align="center">NFS1</td>
<td align="center">NFS1 cysteine desulfurase</td>
<td align="left">NFS1 undergoes positive selection in lung tumours and protects cells from ferroptosis</td>
<td align="center">
<xref ref-type="bibr" rid="B3">Alvarez et al. (2017)</xref>
</td>
</tr>
<tr>
<td align="center">YAP</td>
<td align="center">Yes associated transcriptionalregulator ring finger protein 113A</td>
<td align="left">Intercellular interaction dictates cancer cell ferroptosis via NF2-YAP signaling</td>
<td align="center">
<xref ref-type="bibr" rid="B163">Wu et al. (2019)</xref>
</td>
</tr>
<tr>
<td align="center">RNF113A</td>
<td align="center">Lymphoid-specific helicase</td>
<td align="left">The X-linked trichothiodystrophy-causing gene RNF113A links the spliceosome to cell survival upon DNA damage</td>
<td align="center">
<xref ref-type="bibr" rid="B126">Shostak et al. (2020)</xref>
</td>
</tr>
<tr>
<td align="center">LCH</td>
<td align="center">serine/threonine/tyrosine kinase 1</td>
<td align="left">EGLN1/c-Myc Induced Lymphoid-Specific Helicase Inhibits Ferroptosis through Lipid Metabolic Gene Expression</td>
<td align="center">
<xref ref-type="bibr" rid="B67">Jiang et al. (2017)</xref>
</td>
</tr>
<tr>
<td align="center">STYK1</td>
<td align="center">NFE2 like bZIP transcription factor 2</td>
<td align="left">STYK1/NOK correlates with ferroptosis in non-small cell lung carcinoma</td>
<td align="center">
<xref ref-type="bibr" rid="B72">Lai et al. (2019)</xref>
</td>
</tr>
<tr>
<td align="center">Nrf2</td>
<td align="center">nuclear paraspeckle assembly transcript 1</td>
<td align="left">Nrf-2 regulates the sensitivity of human NSCLC cells to cystine deprivation-induced ferroptosis via FOCAD-FAK</td>
<td align="center">
<xref ref-type="bibr" rid="B56">Hu et al. (2020a)</xref>
</td>
</tr>
<tr>
<td align="center">NEAT1</td>
<td align="center">long intergenic non-protein coding RNA 336</td>
<td align="left">NEAT1 inhibits acyl-CoA synthetase long chain family member 4 (ACSL4) expression level to promotes ferroptosis sensitivity</td>
<td align="center">
<xref ref-type="bibr" rid="B162">Wu and Liu (2021)</xref>
</td>
</tr>
<tr>
<td align="center">LINC00336</td>
<td align="center">microRNA 324</td>
<td align="left">LINC00336 served as an endogenous sponge of microRNA 6852 (MIR6852) to regulate the ferroptosis</td>
<td align="center">
<xref ref-type="bibr" rid="B150">Wang et al. (2019)</xref>
</td>
</tr>
<tr>
<td align="center">MIR324</td>
<td align="center">microRNA 4443</td>
<td align="left">MIR324 direct targets GPX4 and reinstates ferroptosis sensitivity in cisplatin-resistant A549/DDP cells</td>
<td align="center">
<xref ref-type="bibr" rid="B31">Deng et al. (2021)</xref>
</td>
</tr>
<tr>
<td align="center">MIR4443</td>
<td align="center">microRNA 302a</td>
<td align="left">MIR4443 suppresses cisplatin-induced ferroptosis by modulating expression of apoptosis inducing factor mitochondria associated 2 (AIFM2) in an m6A-dependent manner</td>
<td align="center">
<xref ref-type="bibr" rid="B130">Song et al. (2021b)</xref>
</td>
</tr>
<tr>
<td align="center">MIR302A</td>
<td align="center">metallothionein 1D</td>
<td align="left">MIR302A participates ferroptosis process via targeting ferroportin in lung cancer cells</td>
<td align="center">
<xref ref-type="bibr" rid="B156">Wei et al. (2021)</xref>
</td>
</tr>
<tr>
<td align="center">MT1DP</td>
<td align="center" rowspan="2">epidermal growth factor receptor</td>
<td align="left">MT1DP sensitized A549 and H1299 cells to erastin-induced ferroptosis through downregulation of Nrf-2</td>
<td align="center">
<xref ref-type="bibr" rid="B34">Gai et al. (2020a)</xref>
</td>
</tr>
<tr>
<td align="center">EGFR</td>
<td align="left">Activation of EGFR pathway can increase Nrf-2 expression in which upregulates GPX4 expression and inhibits EGFR-tyrosine kinase inhibitor (TKI) -induced ferroptosis</td>
<td align="center">
<xref ref-type="bibr" rid="B100">Ma et al. (2021)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>In recent years, natural products from traditional herbal medicine have emerged as an increasingly important therapy in the prevention and treatment of NSCLC (<xref ref-type="bibr" rid="B193">Zhang et al., 2018</xref>; <xref ref-type="bibr" rid="B146">Wan et al., 2019</xref>; <xref ref-type="bibr" rid="B86">Li et al., 2021</xref>). Furthermore, there is a growing body of research focusing on the modulation of ferroptosis by natural products for the prevention and treatment of NSCLC (<xref ref-type="bibr" rid="B11">Batbold and Liu, 2021</xref>). This article discusses the molecular mechanisms underlying ferroptosis and highlights the mechanisms by which different types of natural products induce ferroptosis to exert anti-cancer effects on NSCLC. The aim is to further provide theoretical support for drug development and treatment strategies in NSCLC.</p>
</sec>
<sec id="s2">
<title>2 Mechanism of ferroptosis</title>
<p>Ferroptosis represents a distinct form of cell death, which was first proposed by Dixon et al., in 2012 (<xref ref-type="bibr" rid="B32">Dixon et al., 2012</xref>). Morphologically, ferroptosis is characterized by mitochondrial shrinkage, mitochondrial membrane rupture, increased membrane density, and reduced or vanished mitochondrial cristae (<xref ref-type="bibr" rid="B169">Xie et al., 2016</xref>). Biochemically, lipid peroxidation, iron metabolism, redox homeostasis and fatty acid supply are currently thought to be pivotal to the induction of ferroptosis. (<xref ref-type="bibr" rid="B80">Li et al., 2020</xref>; <xref ref-type="bibr" rid="B21">Chen et al., 2021c</xref>). The following part provides an overview of the extensively studied mechanisms underlying ferroptosis (<xref ref-type="fig" rid="F2">Figure 2</xref>).</p>
<fig id="F2" position="float">
<label>FIGURE 2</label>
<caption>
<p>Regulatory mechanism of ferroptosis. General mechanism of ferroptosis associated with System Xc<sup>&#x2212;</sup>, GPX4, accumulation of iron, and lipid peroxidation.</p>
</caption>
<graphic xlink:href="fphar-15-1385565-g002.tif"/>
</fig>
<sec id="s2-1">
<title>2.1 Inhibition of the cysteine-glutamate transporter system Xc<sup>&#x2212;</sup> induces ferroptosis</title>
<p>The system Xc<sup>-</sup> is a transport system involved in the regulation of cellular redox balance and the production of GSH (<xref ref-type="bibr" rid="B95">Liu et al., 2021</xref>). It is composed of two subunits: the light chain, known as xCT (SLC7A11), and the heavy chain, known as solute carrier family 3 member 2 (SLC3A2) (<xref ref-type="bibr" rid="B140">Tu et al., 2021</xref>). xCT is responsible for the transport of cystine (oxidized form of cysteine) into the cell, while SLC3A2 acts as a chaperone and stabilizes the expression of xCT on the cell surface (<xref ref-type="bibr" rid="B147">Wang et al., 2022</xref>). The function of system Xc<sup>-</sup> is to transport cystine into the cell in exchange for glutamate (Glu) export. Cystine is a disulfide form of the cysteine, which is essential for the synthesis of the antioxidant GSH. GSH helps to neutralize reactive oxygen species (ROS) and protects cells from oxidative damage (<xref ref-type="bibr" rid="B1">Albrecht et al., 2010</xref>). In the context of ferroptosis, system Xc<sup>-</sup> plays a central role in maintaining intracellular redox homeostasis. It imports cystine into the cell, which is subsequently reduced to cysteine. By promoting the availability of cystine, system Xc<sup>-</sup> supports the synthesis of GSH by catalyzing glutathione synthetase (GSS) and glycine (Gly). Throughout this process, GSH undergoes oxidation to form oxidized glutathione (GSSG). However, GSSG is subsequently converted back to its reduced form, GSH, with the assistance of an enzyme called glutathione reductase (GR). Therefore, inhibition or genetic depletion of system Xc<sup>-</sup> leads to impaired cystine uptake, reduced GSH synthesis, and increased vulnerability to lipid peroxidation, ultimately promoting ferroptosis (<xref ref-type="bibr" rid="B77">Li F. J. et al., 2022</xref>).</p>
</sec>
<sec id="s2-2">
<title>2.2 Inhibition of GPX4 induce ferroptosis</title>
<p>GPX4, a crucial antioxidant enzyme predominantly localized within cellular organelle membranes, plays a significant role in the elimination of lipid peroxides (<xref ref-type="bibr" rid="B108">Miao et al., 2022</xref>). Specifically, it exhibits the capacity to catalyze the reaction between GSH and lipid peroxidation during the process of ferroptosis. This enzyme facilitates the reduction of lipid peroxidation into benign alcohol forms, thereby impeding the buildup of lipid peroxidation (<xref ref-type="bibr" rid="B133">Sui et al., 2018</xref>). However, under conditions of inadequate intracellular GSH levels, the functionality of GPX4 becomes hindered, impeding the effective clearance of lipid peroxidation (<xref ref-type="bibr" rid="B170">Xu et al., 2021</xref>). During ferroptosis, the inhibition of system Xc<sup>-</sup> leads to a reduction in GSH synthesis, diminishes the substrate availability for GPX4 and reduces the elimination of lipid peroxidation, ultimately provokes the initiation of ferroptosis (<xref ref-type="bibr" rid="B123">Seibt et al., 2019</xref>).</p>
</sec>
<sec id="s2-3">
<title>2.3 Accumulation of iron</title>
<p>Iron is an essential bio-element within cells, participating in various physiological processes, including oxygen transport (<xref ref-type="bibr" rid="B91">Lipper et al., 2019</xref>), DNA synthesis (<xref ref-type="bibr" rid="B73">Lane et al., 2015</xref>), and energy production (<xref ref-type="bibr" rid="B52">Hentze et al., 2004</xref>). Under certain conditions, iron can also act as catalysts for cell death, promoting the occurrence of ferroptosis (<xref ref-type="bibr" rid="B101">Ma et al., 2022</xref>; <xref ref-type="bibr" rid="B5">Anandhan et al., 2023</xref>). Ferric ions (Fe<sup>3&#x002B;</sup>) are imported into the cell from the extracellular space through their binding to transferrin (TF), forming the complex &#x201c;TF&#x2013;Fe<sup>3&#x002B;</sup>&#x2013;TfR1&#x201d; with transferrin receptor 1 (TfR1) (<xref ref-type="bibr" rid="B47">Hadzhieva et al., 2014</xref>; <xref ref-type="bibr" rid="B10">Basuli et al., 2017</xref>). This process involving TF and TfR1 is crucial for the intracellular accumulation of lipid peroxides and the occurrence of ferroptosis. Within the endosome, Fe<sup>3&#x002B;</sup> are converted to ferrous ions (Fe<sup>2&#x002B;</sup>) by ferric reductases such as STEAP3 metalloreductase (<xref ref-type="bibr" rid="B183">Ye et al., 2022</xref>). Subsequently, Fe<sup>2&#x002B;</sup> are transported from the endosome to the labile iron pool (LIP) via the divalent metal transporter 1 (DMT1) (<xref ref-type="bibr" rid="B7">Aschner et al., 2022</xref>). In the cytosol, Fe<sup>2&#x002B;</sup> reacts with hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) through the Fenton reaction, leading to lipid peroxidation and the generation of ROS(<xref ref-type="bibr" rid="B92">Liu et al., 2022</xref>). Importantly, various cellular processes that influence iron uptake, storage, utilization, and release can impact cell sensitivity to ferroptosis. For instance, the degradation of ferritin induced by nuclear receptor coactivator 4 (NCOA4) also contributes to ferroptosis promotion (<xref ref-type="bibr" rid="B122">Santana-Codina et al., 2021</xref>). Conversely, reduced expression of solute carrier family 40 member 1 (SLC40A1) may result in intracellular Fe<sup>2&#x002B;</sup> accumulation, subsequently increase iron-dependent oxidative stress and facilitate ferroptosis (<xref ref-type="bibr" rid="B50">Hao et al., 2021</xref>).</p>
</sec>
<sec id="s2-4">
<title>2.4 Lipid peroxidation</title>
<p>Lipid metabolism plays a vital role in the occurrence of ferroptosis, which is characterized by the accumulation of lipid peroxides resulting from the oxidation of polyunsaturated fatty acids (PUFAs), a class of fatty acids characterized by the presence of multiple double bonds, including omega-3 and omega-6 fatty acids (<xref ref-type="bibr" rid="B24">Christie and Harwood, 2020</xref>), which plays essential roles in the composition of cell membranes and participate in numerous physiological processes within cells (<xref ref-type="bibr" rid="B159">Wiktorowska-Owczarek et al., 2015</xref>). During the process of lipid peroxidation, several enzymes involved in lipid metabolism act as positive regulators of ferroptosis. One such enzyme is Acyl-CoA synthetase long chain family member 4 (ACSL4), which participates in phospholipid metabolism and facilitates the synthesis of PUFA-CoA from PUFAs like arachidonoyl (AA) and adrenal (AdA), thereby activating PUFAs(<xref ref-type="bibr" rid="B33">Doll et al., 2017</xref>). Following ACSL4-driven esterification, lysophosphatidic transferase 3 (LPCAT3) incorporates PUFAs into phospholipids, forming phospholipids containing PUFAs (<xref ref-type="bibr" rid="B119">Reed et al., 2022</xref>). Subsequently, ALOX15 oxidizes these PUFA-PLs, generating lipid peroxides and ultimately leading to ferroptosis (<xref ref-type="bibr" rid="B103">Ma et al., 2022</xref>).</p>
</sec>
<sec id="s2-5">
<title>2.5 Others</title>
<p>Ferroptosis can also be regulated by several another protein. Recent publications are summarized in <xref ref-type="table" rid="T2">Table 2</xref>.</p>
<table-wrap id="T2" position="float">
<label>TABLE 2</label>
<caption>
<p>Mediators or modulators of ferroptosis.</p>
</caption>
<table>
<thead valign="top">
<tr>
<th align="center">Proteins</th>
<th align="left">Full names</th>
<th align="center">Mechanisms</th>
<th align="center">References</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="left">Panx 1</td>
<td align="left">Pannexin 1</td>
<td align="left">Panx 1 downregulates lipid peroxidation through the MAPK signal pathway</td>
<td align="center">
<xref ref-type="bibr" rid="B132">Su et al. (2019)</xref>
</td>
</tr>
<tr>
<td align="left">VDACs</td>
<td align="left">voltage-dependent amino channels</td>
<td align="left">Generation of mitochondrial ROS and mitochondrial dysfunction</td>
<td align="center">
<xref ref-type="bibr" rid="B91">Lipper et al. (2019)</xref>
</td>
</tr>
<tr>
<td align="left">HSPB1</td>
<td align="left">heat shock 27&#xa0;kDa protein 1</td>
<td align="left">HSPB1 phosphorylation is downregulated and iron-mediated in the production of ROS</td>
<td align="center">
<xref ref-type="bibr" rid="B135">Sun et al. (2015)</xref>
</td>
</tr>
<tr>
<td align="left">VDR</td>
<td align="left">Vitamin D receptor</td>
<td align="left">VDR mediates the transcription of GPX4</td>
<td align="center">
<xref ref-type="bibr" rid="B57">Hu et al. (2020b)</xref>
</td>
</tr>
<tr>
<td align="left">CARS</td>
<td align="left">Cysteinyl-tRNA synthetase</td>
<td align="left">Involved in the synthesis of GSH</td>
<td align="center">
<xref ref-type="bibr" rid="B51">Hayano et al. (2016)</xref>
</td>
</tr>
<tr>
<td align="left">15LO</td>
<td align="left">15-lipoxygenases</td>
<td align="left">Catalyzes the formation of pro-ferroptotic 15-OOH-AA (HpETE)</td>
<td align="center">
<xref ref-type="bibr" rid="B131">Stoyanovsky et al. (2019)</xref>
</td>
</tr>
<tr>
<td align="left">PEBP1</td>
<td align="left">Phosphatidylethanolamine-binding protein 1</td>
<td align="left">Restrain the Ras/MEK/ERK cascade</td>
<td align="center">
<xref ref-type="bibr" rid="B158">Wenzel et al. (2017)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
</sec>
<sec id="s3">
<title>3 Natural products modulating ferroptosis for intervention in NSCLC</title>
<p>Natural products possess multiple pharmacological activities, particular in the treatment of tumors. Recently, researchers have identified certain natural products that can modulate ferroptosis to exert anti-tumor potential (<xref ref-type="bibr" rid="bib201">Yang et al., 2022</xref>). <xref ref-type="fig" rid="F3">Figure 3</xref> provides a compilation of natural products with their sources and chemical formulas, which induce ferroptosis to treat NSCLC. The regulatory targets and mechanisms of these natural products are illustrated in <xref ref-type="fig" rid="F4">Figure 4</xref> and presented in <xref ref-type="table" rid="T3">Table 3</xref>.</p>
<fig id="F3" position="float">
<label>FIGURE 3</label>
<caption>
<p>Chemical structures of natural products from traditional Chinese herbal medicine.</p>
</caption>
<graphic xlink:href="fphar-15-1385565-g003.tif"/>
</fig>
<fig id="F4" position="float">
<label>FIGURE 4</label>
<caption>
<p>The mechanism of natural products inducing ferroptosis in NSCLC. The activation of ROS or the inhibition of GPX4, GSH, SLC7A11 and transferrin by different natural products can induce ferroptosis to treat NSCLC.</p>
</caption>
<graphic xlink:href="fphar-15-1385565-g004.tif"/>
</fig>
<table-wrap id="T3" position="float">
<label>TABLE 3</label>
<caption>
<p>Natural products inducing ferroptosis in NSCLC.</p>
</caption>
<table>
<thead valign="top">
<tr>
<th align="left">Natural products</th>
<th align="center">Mechanisms</th>
<th align="left">References</th>
<th align="center">Effectiveness <italic>in vivo</italic>
</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="left">Timosaponin AIII</td>
<td align="left">Forms a complex with HSP90 and leads to degradation of GPX4</td>
<td align="left">
<xref ref-type="bibr" rid="B199">Zhou et al. (2023)</xref>
</td>
<td align="center">&#x2a;&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.001 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Curcumin</td>
<td align="left">Downregulation of SLC7A11</td>
<td align="left">
<xref ref-type="bibr" rid="B138">Tang et al. (2021)</xref>
</td>
<td align="center">&#x2a;&#x2a;&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.0001 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Sanguinarine</td>
<td align="left">Sanguinarine mediated the ubiquitination of GPX4 through Stub1</td>
<td align="left">
<xref ref-type="bibr" rid="B173">Xu et al. (2022)</xref>
</td>
<td align="center">&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.01 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Erianin</td>
<td align="left">Targeting the CaM signaling pathway and leading to ROS up Ginkgetin reduced the expression of SLC7A11 and GPX4</td>
<td align="left">
<xref ref-type="bibr" rid="B18">Chen et al. (2020a)</xref>
</td>
<td align="center">&#x2a;<italic>p</italic> &#x003c; 0.05 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Ginkgetin</td>
<td align="left">&#x3b1;-Hederin reduces the expression of GPX2/GSS/GSH</td>
<td align="left">
<xref ref-type="bibr" rid="B98">Lou et al. (2021b)</xref>
</td>
<td align="center">&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.01 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">&#x3b1;-Hederin</td>
<td align="left">Downregulation of GPX4</td>
<td align="left">
<xref ref-type="bibr" rid="B164">Wu et al. (2022a)</xref>
</td>
<td align="center">&#x2a;&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.001 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Dihydroisotanshinone I</td>
<td align="left">Downregulates SLC7A11 and results in a reduction in GSH</td>
<td align="left">
<xref ref-type="bibr" rid="B160">Wu et al. (2021)</xref>
</td>
<td align="center">&#x2a;<italic>p</italic> &#x003c; 0.05 <italic>versus</italic> control group in tumor metastasis (&#x3bc;m)</td>
</tr>
<tr>
<td align="left">Sulforaphane</td>
<td align="left">Downregulation of ferroportin</td>
<td align="left">
<xref ref-type="bibr" rid="B65">Jiang et al. (2016),</xref> <xref ref-type="bibr" rid="B61">Iida et al. (2021)</xref>
</td>
<td align="center">&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.01 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Cryptotanshinone</td>
<td align="left">Downregulates the protein and mRNA levels of Xct</td>
<td align="left">
<xref ref-type="bibr" rid="B17">Chen et al. (2014),</xref> <xref ref-type="bibr" rid="B118">Popa et al. (2021)</xref>
</td>
<td align="center">&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.01 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Artemisinin</td>
<td align="left">Upregulating Xct and downregulating SLC7A11</td>
<td align="left">
<xref ref-type="bibr" rid="B16">Chen et al. (2019),</xref> <xref ref-type="bibr" rid="B191">Zhang et al. (2021a)</xref>
</td>
<td align="center">&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.01 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Sinapine</td>
<td align="left">Inhibiting PRIM2/SLC7A11 Axis</td>
<td align="left">
<xref ref-type="bibr" rid="B124">Shao et al. (2022)</xref>
</td>
<td align="center">&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.01 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Dihydroartemisinin</td>
<td align="left">Increase the interaction between DRP1 and FIS1</td>
<td align="left">
<xref ref-type="bibr" rid="B184">Yuan et al. (2020),</xref> <xref ref-type="bibr" rid="B55">Hu et al. (2023)</xref>
</td>
<td align="center">&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.01 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Celastrol</td>
<td align="left">Increase ROS accumulation and GSH depletion</td>
<td align="left">
<xref ref-type="bibr" rid="B94">Liu et al. (2021a)</xref>
</td>
<td align="center">&#x2a;&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.001 <italic>versus</italic> control group in tumor volume (mm<sup>3</sup>)</td>
</tr>
<tr>
<td align="left">Betulin</td>
<td align="left">Increase the levels of total iron and reduce GSH levels</td>
<td align="left">
<xref ref-type="bibr" rid="B84">Li et al. (2022c),</xref> <xref ref-type="bibr" rid="B176">Yan et al. (2022)</xref>
</td>
<td align="center">&#x2a;&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.001 <italic>versus</italic> control group in tumor size (mm<sup>2</sup>)</td>
</tr>
<tr>
<td align="left">Capsaicin</td>
<td align="left"/>
<td align="left">
<xref ref-type="bibr" rid="B96">Liu et al. (2022b),</xref> <xref ref-type="bibr" rid="B30">Deng et al. (2023)</xref>
</td>
<td align="center">&#x2a;&#x2a;<italic>p</italic> &#x003c; 0.01 <italic>versus</italic> control group in maximal distances of metastasis (&#x3bc;m)</td>
</tr>
</tbody>
</table>
</table-wrap>
<sec id="s3-1">
<title>3.1 Timosaponin AIII</title>
<p>Timosaponin AIII(TA III) is a steroidal saponin and major active component derived from the traditional Chinese medicinal herb <italic>Schisandra chinensis</italic> (<xref ref-type="bibr" rid="B152">Wang et al., 2023</xref>). Timosaponin AIII exhibits various pharmacological activities, including anti-inflammatory (<xref ref-type="bibr" rid="B187">Yuan et al., 2016</xref>), anti-oxidant (<xref ref-type="bibr" rid="B66">Jiang et al., 2014</xref>), and anti-cancer effects (<xref ref-type="bibr" rid="B23">Chien et al., 2022</xref>). Zhou (<xref ref-type="bibr" rid="B199">Zhou et al., 2023</xref>) discovered that Timosaponin AIII can inhibit the proliferation and migration of NSCLC cells, induce cell cycle arrest at the G2/M phase, and trigger ROS release and iron accumulation. This process is accompanied by the generation of malondialdehyde (MDA) and the depletion of GSH. Furthermore, it was confirmed that heat shock protein 90 (HSP90) is a direct target of Timosaponin AIII. Timosaponin AIII forms a complex with HSP90, leading to the ubiquitination and degradation of GPX4, ultimately inducing ferroptosis. This study confirms that Timosaponin AIII can play a therapeutic role in NSCLC by inducing ferroptosis.</p>
</sec>
<sec id="s3-2">
<title>3.2 Curcumin</title>
<p>Curcumin is a naturally occurring compound derived from turmeric (<xref ref-type="bibr" rid="B4">Anand et al., 2007</xref>). The curcumin possesses pharmacological properties such as immunomodulation (<xref ref-type="bibr" rid="B37">Gautam et al., 2007</xref>), anti-inflammatory (<xref ref-type="bibr" rid="B116">Peng et al., 2021</xref>), and anti-cancer activity (<xref ref-type="bibr" rid="B41">Gouda and Bhandary, 2019</xref>). In a study conducted by Tang (<xref ref-type="bibr" rid="B138">Tang et al., 2021</xref>), characteristic changes associated with ferroptosis were observed in response to curcumin treatment in NSCLC cells. These changes included increased intracellular accumulation of iron and MDA, depletion of GSH, downregulation of SLC7A11 and GPX4 protein levels, negative regulators of ferroptosis, accumulation of lipid peroxidation, curcumin-induced mitochondrial membrane rupture, and reduction of mitochondrial cristae. Furthermore, the curcumin-treated group exhibited increased accumulation of autolysosomes, along with elevated levels of autophagy biomarkers, such as Beclin1 and microtubule-associated protein 1 light chain 3 alpha (LC3). The study also demonstrated that the characteristic changes of ferroptosis were partially reversed when the curcumin-treated NSCLC cells group was treated with CQ (an inhibitor of autophagosome-lysosome fusion) or when the Beclin1 was silenced. In summary, these findings suggest that autophagy contributes to curcumin-induced ferroptosis in NSCLC cells, and inhibiting autophagy can alleviate cellular sensitivity to ferroptosis.</p>
</sec>
<sec id="s3-3">
<title>3.3 Sanguinarine</title>
<p>Sanguinarine is a natural small-molecule compound isolated from the bloodroot plant (<xref ref-type="bibr" rid="B97">Lou et al., 2021</xref>), which possesses anti-bacterial (<xref ref-type="bibr" rid="B190">Zhang et al., 2020</xref>), anti-inflammatory (<xref ref-type="bibr" rid="B114">Niu et al., 2012</xref>), and anti-cancer properties (<xref ref-type="bibr" rid="B38">Gaziano et al., 2016</xref>). Xu (<xref ref-type="bibr" rid="B173">Xu et al., 2022</xref>). conducted a study and found that sanguinarine inhibited the proliferation of NSCLC cells in a dose-dependent and time-dependent manner. In xenograft tumor animal models, sanguinarine effectively suppressed the growth and metastasis of NSCLC cells. Furthermore, it was discovered that sanguinarine induced intracellular accumulation of iron, increased levels of ROS and MDA, and reduced GSH levels. Sanguinarine mediated the ubiquitination and degradation of GPX4 through stress induced phosphoprotein 1 (STIP1) and U-Box containing protein 1 (Stub1), thereby triggering ferroptosis in NSCLC cells. Furthermore, overexpression of GPX4 partially restored the proliferative and invasive inhibitory effects of sanguinarine on NSCLC cells by suppressing ferroptosis. In conclusion, sanguinarine inhibits the growth and metastasis of NSCLC cells by regulating the Stub1/GPX4-dependent iron-dependent cell death pathway.</p>
</sec>
<sec id="s3-4">
<title>3.4 Erianin</title>
<p>Erianin, a natural benzylisoquinoline compound extracted from <italic>Dendrobium</italic> (<xref ref-type="bibr" rid="B78">Li et al., 2023</xref>), exhibits anti-cancer activity by inhibiting cell proliferation, inducing apoptosis (<xref ref-type="bibr" rid="B175">Xu et al., 2021</xref>), and autophagy (<xref ref-type="bibr" rid="B22">Chen et al., 2020</xref>) in various cancers such as cervical cancer (<xref ref-type="bibr" rid="B81">Li et al., 2018</xref>), colorectal cancer (<xref ref-type="bibr" rid="B107">Miao et al., 2023</xref>), prostate cancer (<xref ref-type="bibr" rid="B139">Trapika et al., 2021</xref>), and breast cancer (<xref ref-type="bibr" rid="B168">Xie et al., 2021</xref>). Chen (<xref ref-type="bibr" rid="B18">Chen et al., 2020</xref>) found that erianin arrested NSCLC cells in the G2/M phase, thereby inhibiting cell proliferation and metastasis. Further investigations revealed that erianin treatment induced accumulation of ROS, consumption of GSH, and occurrence of lipid peroxidation in NSCLC cells. However, the results were reversed by ferroptosis inhibitor. Calmodulin (CaM), a major endogenous calcium-regulating protein, plays a crucial role in regulating L-type voltage-dependent calcium channels, which are important for calcium and iron transport (<xref ref-type="bibr" rid="B188">Zeng et al., 2023</xref>). This study confirmed that erianin targeted the CaM signaling pathway, leading to ROS accumulation and upregulation of iron by modulating the calcium-CaM pathway, thereby inducing ferroptosis in NSCLC cells.</p>
</sec>
<sec id="s3-5">
<title>3.5 Ginkgetin</title>
<p>Ginkgetin is a natural flavonoid compound derived from the <italic>Ginkgo biloba</italic>. It exhibits pharmacological activities such as neuroprotection (<xref ref-type="bibr" rid="B128">Singh et al., 2019</xref>), cardiovascular protection (<xref ref-type="bibr" rid="B127">Silva and Martins, 2022</xref>), anti-oxidant (<xref ref-type="bibr" rid="B85">Li et al., 2022d</xref>), and anti-inflammatory effects (<xref ref-type="bibr" rid="B83">Li et al., 2022b</xref>). Additionally, research has shown that it exerts anti-cancer effects by inhibiting cell proliferation, angiogenesis, and inducing apoptosis in tumor cells (<xref ref-type="bibr" rid="B28">DeFeudis et al., 2003</xref>; <xref ref-type="bibr" rid="B182">Ye et al., 2007</xref>; <xref ref-type="bibr" rid="B9">Bai et al., 2015</xref>; <xref ref-type="bibr" rid="B48">Han et al., 2016</xref>; <xref ref-type="bibr" rid="B70">Kim et al., 2021</xref>). Lou (<xref ref-type="bibr" rid="B98">Lou J. S. et al., 2021</xref>) conducted a study and found that the combination of Ginkgetin with cisplatin enhanced the cytotoxicity against NSCLC cells. This combination treatment increasesthe accumulation of iron and the occurrence of lipid peroxidation. Further investigations revealed that Ginkgetin reduced the expression of SLC7A11 and GPX4, decreased the GSH/GSSG ratio, increased ROS formation, and reduced the activity of the Nrf-2/HO-1 signaling pathway. These actions collectively induced ferroptosis in NSCLC cells. These results suggest that the combination of Ginkgetin and cisplatin reduces NSCLC development by inducing ferroptosis.</p>
</sec>
<sec id="s3-6">
<title>3.6 Hederin</title>
<p>Hederin belongs to a class of saponin compounds found in the Ginkgo biloba plant, which belongs to the family <italic>Ginkgoaceae</italic> (<xref ref-type="bibr" rid="B64">Jeong et al., 2019</xref>). Numerous studies have indicated that &#x3b1;-Hederin has anti-tumor functions (<xref ref-type="bibr" rid="B12">Belmehdi et al., 2023</xref>). For instance, in colorectal cancer cells (<xref ref-type="bibr" rid="B134">Sun et al., 2019</xref>), &#x3b1;-Hederin inhibits the epithelial-mesenchymal transition induced by interleukin-6 and the activity of the JAK2/STAT3 signaling pathway, thereby suppressing cell migration and invasion. In gastric cancer cells (<xref ref-type="bibr" rid="B148">Wang et al., 2020</xref>), the combination of &#x3b1;-Hederin and cisplatin promotes apoptosis in gastric cancer cells through mitochondria-related apoptotic pathways. Wu (<xref ref-type="bibr" rid="B164">Wu et al., 2022</xref>) discovered that &#x3b1;-Hederin inhibits the proliferation and invasion of NSCLC cells in a dose-dependent manner both <italic>in vitro</italic> and <italic>in vivo</italic>. Subsequent proteomics, metabolomics, and high-throughput sequencing confirmed that &#x3b1;-Hederin treatment reduces the expression of GSH peroxidase 2 (GPX2) and GSS, inhibits the synthesis of GSH, disrupts the GSH redox system. After the administration of the ferroptosis inhibitor of ferrostatin-1, the study observed a partial restoration of &#x3b1;-Hederin-induced cell death. Meanwhile, ferrostatin-1 treatment recovered &#x3b1;-Hederin-induced disturbance in mitochondrial membrane potential. In summary, &#x3b1;-Hederin could induces ferroptosis in the treatment of NSCLC.</p>
</sec>
<sec id="s3-7">
<title>3.7 Dihydroisotanshinone I</title>
<p>Dihydroisotanshinone I (DTI), a diterpenoid compound belonging to the tanshinone class, is extracted from the medicinal herb <italic>Salvia miltiorrhiza</italic> (<xref ref-type="bibr" rid="B54">Hsu et al., 2021</xref>). <italic>Salvia miltiorrhiza</italic> has been widely used in traditional Chinese medicine and possess diverse pharmacological activities and therapeutic potential (<xref ref-type="bibr" rid="B167">XD et al., 2019</xref>; <xref ref-type="bibr" rid="bib202">He et al., 2024</xref>). Research studies have demonstrated that DTIDTI exhibits anti-oxidant (<xref ref-type="bibr" rid="B62">Ip et al., 2002</xref>), and anti-cancer properties (<xref ref-type="bibr" rid="B161">Wu et al., 2017</xref>; <xref ref-type="bibr" rid="B89">Lin et al., 2019</xref>). Wu (<xref ref-type="bibr" rid="B160">Wu et al., 2021</xref>)have shown that DTI inhibits the growth of A549 cells and H460 cells via inducing ferroptosis. The underlying mechanism involves the downregulation of GPX4 protein and GSH levels, accumulation of MDA,ROS, leading toand lipid peroxidation and finally induction of ferroptosis in NSCLC.</p>
</sec>
<sec id="s3-8">
<title>3.8 Sulforaphane</title>
<p>Sulforaphane belongs to the class of compounds known as isothiocyanates and is predominantly found in vegetables of the Brassicaceae family, particularly in cruciferous vegetables such as cauliflower, cabbage, and broccoli (<xref ref-type="bibr" rid="B143">Vanduchova et al., 2019</xref>). Extensive research has demonstrated that sulforaphane exerts its beneficial effects through multiple mechanisms, including the activation of intracellular antioxidant enzymes (<xref ref-type="bibr" rid="B63">Ishida et al., 2021</xref>), modulation of cellular signaling pathways (<xref ref-type="bibr" rid="B195">Zhang et al., 2022c</xref>), and anti-cancer activities (<xref ref-type="bibr" rid="B121">Russo et al., 2018</xref>). Studies conducted by Yuko Iida (<xref ref-type="bibr" rid="B61">Iida et al., 2021</xref>) have shown that sulforaphane significantly inhibits the growth of NSCLC cells, and this growth inhibition can be reversed by ferroptosis inhibitors offerrostatin-1. Furthermore, treatment of NSCLC cells with sulforaphane leads to an increase in iron and ROS levels, as well as collection of lipid peroxidation products, all of which can be attenuated by ferroptosis inhibitors. Subsequent investigations revealed that sulforaphane specifically downregulates the expression of the SLC7A11, resulting in a reduction in GSH accumulation. Collectively, Sulforaphane inhibits the growth of NSCLC cells via inducing ferroptosis.</p>
</sec>
<sec id="s3-9">
<title>3.9 Cryptotanshinone</title>
<p>Cryptotanshinone (CTN) is a diterpenoid monomer and a lipophilic component extracted from the dried roots and rhizomes of the traditional Chinese herb <italic>S. miltiorrhiza</italic> (<xref ref-type="bibr" rid="B79">Li et al., 2021</xref>; <xref ref-type="bibr" rid="bib203">Zhang et al., 2023</xref>). CTN has been proven to possess various biological activities, including antioxidant (<xref ref-type="bibr" rid="B44">Guo et al., 2022</xref>), anti-tumor (<xref ref-type="bibr" rid="B26">Dalil et al., 2022</xref>), antibacterial (<xref ref-type="bibr" rid="B198">Zhong et al., 2021</xref>), and anti-inflammatory effects (<xref ref-type="bibr" rid="B165">Wu et al., 2020</xref>). Li (<xref ref-type="bibr" rid="B118">Popa et al., 2021</xref>) discovered that CTN effectively suppresses NSCLC cells invasion, proliferation and tumorigenesis. The treatment of CTN resulted in increased iron accumulation within the cells and decreased the expression levelof GPX4 protein. Furthermore, CTN elicited an upregulation of Cytoglobin, a protein known to induce ferroptosis, while downregulats ferroportin expression. Moreover, study demonstrated that CTN induces iron-dependent lipid peroxidation by inhibiting the function of TfR1. These data suggest that the induction of ferroptosis in NSCLC cells, achieved by increasing iron accumulation, Cytoglobin, and iron-dependent lipid peroxidation, or by downregulating the expression levels of ferroportin and GPX4, may be an important mechanism through which CTN attenuates NSCLC.</p>
</sec>
<sec id="s3-10">
<title>3.10 Artemisinin</title>
<p>Artemisinin is a sesquiterpene lactone isolated from the <italic>Artemisia annual</italic> (<xref ref-type="bibr" rid="B102">Ma et al., 2020</xref>). It is widely used for the treatment of malaria (<xref ref-type="bibr" rid="B137">Talman et al., 2019</xref>). Apart from its well-known role in treating malaria, artemisinin has been reported in numerous studies to possess additional pharmacological activities, including anti-schistosomiasis (<xref ref-type="bibr" rid="B117">P&#xe9;rez del Villar et al., 2012</xref>),anti-cancer (<xref ref-type="bibr" rid="B69">Kiani et al., 2020</xref>),anti-inflammation (<xref ref-type="bibr" rid="B186">Yuan et al., 2019</xref>),anti-virus (<xref ref-type="bibr" rid="B155">Wani et al., 2021</xref>). Zhang (<xref ref-type="bibr" rid="B191">Zhang et al., 2021</xref>) discovered that artemisinin downregulates the protein and mRNA levels of xCT. Furthermore, artemisinin upregulates the mRNA level of TfR1, Therefore, Zhang hypothesis that Artemisinin may induces ferroptosis in NSCLC. Consequently, the cell death caused by artemisinin can be partially reversed by N-Acetyl-L-cysteine (NAC), a ROS scavenger, and ferrostatin-1, a ferroptosis inhibitor. The findings demonstrate that the inhibitory effect of artemisinin on NSCLC cells is at least partially attributed to the induction of ferroptosis.</p>
</sec>
<sec id="s3-11">
<title>3.11 Sinapine</title>
<p>Sinapine belongs to the class of compounds known as phenethylamines particularly in abundance in sources such as barley, mustard seeds, peas, and rapeseeds (<xref ref-type="bibr" rid="B27">Dang et al., 2023</xref>). It exhibits numerous pharmacological activities, such like antioxidant (<xref ref-type="bibr" rid="B181">Yates et al., 2019</xref>), anti-inflammatory (<xref ref-type="bibr" rid="B82">Li et al., 2019</xref>), and anti-cancer activities (<xref ref-type="bibr" rid="B45">Guo et al., 2014</xref>). In the realm of cancer research, Sinapine has shown promise as an anti-cancer agent, displaying inhibitory effects on various cancer cells, including breast cancer (<xref ref-type="bibr" rid="B46">Guo et al., 2016</xref>) and colorectal cancer (<xref ref-type="bibr" rid="B179">Yang et al., 2023</xref>). Notably, Shao (<xref ref-type="bibr" rid="B124">Shao et al., 2022</xref>) found that Sinapine play the anti-tumor effects on NSCLC cells. Induce ferroptosis by increasing intracellular ferrous iron, lipid peroxidation, and ROS in NSCLC cells. Also, treatment with Sinapine upregulates transferrin and transferrin receptor, and inhibits either of them attenuated the ferroptosis induced by Sinapine. Additionally, Sinapine treatment led to a p53-dependent downregulation of SLC7A11. Furthermore, Sinapine also play the inhibition role in the growth of NSCLC <italic>in vivo</italic>. In conclusion, the findings highlight that Sinapine could be a promising therapeutic approach via triggers ferroptosis in NSCLC.</p>
</sec>
<sec id="s3-12">
<title>3.12 Dihydroartemisinin</title>
<p>Dihydroartemisinin (DHA) is a derivative of artemisinin, which is a compound extracted from the <italic>Artemisia annua</italic> plant (<xref ref-type="bibr" rid="B25">Dai et al., 2021</xref>). DHA exhibits its antimalarial activity by rapidly and effectively clearing the malaria parasite from the bloodstream (<xref ref-type="bibr" rid="B49">Hanboonkunupakarn and White, 2022</xref>). In addition to its antimalarial properties, DHA has been demonstrated anti-inflammatory (<xref ref-type="bibr" rid="B177">Yang et al., 2022</xref>),anti-cancer (<xref ref-type="bibr" rid="B8">Bai et al., 2021</xref>) and immunomodulatory (<xref ref-type="bibr" rid="B36">Gao et al., 2020</xref>) properties. In DNA replication, the protein encoded by the DNA primase subunit 2 (PRIM2) gene plays a critical role. PRIM2 functions by catalyzing the synthesis of RNA primers, which act as the starting points for DNA synthesis (<xref ref-type="bibr" rid="B157">Wei and Lozano-Dur&#xe1;n, 2023</xref>). Yuan&#x2019;s study (<xref ref-type="bibr" rid="B184">Yuan et al., 2020</xref>) revealed that DHA reduced the expression of PRIM2, and silencing PRIM2 mimicked the inhibitory effects of DHA on cell proliferation and colony formation, while promoting cell death in NCSLC cells. Additionally, the study found that DHA treatment and the absence of PRIM2 led to a series of ferroptosis characteristic in NSCLC cells. Mechanistically, the combination of DHA treatment and the absence of PRIM2 decrease the level of GSH, increasecellular lipid ROS and MDA levels, as well as downregulats SLC7A11 and &#x3b2;-catenin expressions in NCSLC cells.</p>
</sec>
<sec id="s3-13">
<title>3.13 Celastrol</title>
<p>Celastrol is a prominent bioactive compound extracted from the root bark of Tripterygium wilfordii, a plant belonging to the <italic>Celastraceae</italic> family (<xref ref-type="bibr" rid="B174">Xu et al., 2021</xref>). It falls within the class of pentacyclic triterpenoids, possessing a triterpene framework and exhibiting noteworthy biological activity (<xref ref-type="bibr" rid="B88">Li et al., 2022f</xref>), such like anti-cancer (<xref ref-type="bibr" rid="B172">Xu et al., 2023</xref>), anti-inflammatory effect in liver fibrosis (<xref ref-type="bibr" rid="B153">Wang et al., 2020</xref>), and potential pharmacological treatment of obesity (<xref ref-type="bibr" rid="B93">Liu et al., 2015</xref>). In a study conducted by Liu(<xref ref-type="bibr" rid="B94">Liu et al., 2021</xref>), it was observed that the combination of erastin,a ferroptosis inducer, and celastrol induced cell death in NSCLC cells at concentrations that were not toxic individually. The co-treatment with celastrol and erastin resulted in promotion of ROS generation, disturbance of mitochondrial membrane potential, augmentation of the interaction between dynamin-related protein 1 (DRP1) and mitochondrial fission, mitochondrial 1 (FIS1), and stimulation of mitochondrial fission. Of these, the above results suggest that Celastrol may be a natural compound that effectively induces ferroptosis.</p>
</sec>
<sec id="s3-14">
<title>3.14 Betulin</title>
<p>Betulin is a natural triterpene compound that occurs in the bark of specific tree species, including white and silver birch trees (<xref ref-type="bibr" rid="B29">Demets et al., 2022</xref>). The emerging evidence has shown that Betulinpossesses various advantageous properties, including anti-inflammatory (<xref ref-type="bibr" rid="B141">Tuli et al., 2021</xref>), anti-oxidant (<xref ref-type="bibr" rid="B43">G&#xfc;nther et al., 2021</xref>), and anti-cancer (<xref ref-type="bibr" rid="B151">Wang et al., 2017</xref>). Yan (<xref ref-type="bibr" rid="B176">Yan et al., 2022</xref>) found that betulin in combination with Gefitinib exhibited antagonistic effects on cellular viability on NSCLC cells of A549 and H460. However, the ferroptosis inhibitors of ferrostatin-1, liproxstatin-1 and deferoxamine can completely rescue the viability of A549 and H460 after treatment of betulin in combination with Gefitinib. Moreover, in order to confirm whether ferroptosis contributes to the death under the treatment of betulin in combination with gefetinib, the author performed a series of experiments and found that combination induced ROS accumulation, lipid peroxidation, and GSH depletion. The expression of SLC7A11, GPX4 and ferritin heavy chain 1 (FTH1), negative regulators of ferroptosis, was decreased under the combination treatment of betulin and gefetinib. Whereas, the positive regulatory protein of ferroptosis heme oxygenase 1(HO-1) was increased. , Therefore, Betulin may be a potential therapeutic agent for NSCLC via inducing ferroptosis.</p>
</sec>
<sec id="s3-15">
<title>3.15 Capsaicin</title>
<p>Capsaicin, a natural compound present in chili peppers, in fruits of the capsicum genus like cayenne peppers and jalapenos (<xref ref-type="bibr" rid="B15">Chapa-Oliver and Mej&#xed;a-Teniente, 2016</xref>), has attracted attention for its potential health benefits (<xref ref-type="bibr" rid="B125">Sharma et al., 2013</xref>). Research suggests that capsaicin may contributes to improved cardiovascular health (<xref ref-type="bibr" rid="B112">Munjuluri et al., 2021</xref>) and possess anti-microbial properties (<xref ref-type="bibr" rid="B39">Goci et al., 2021</xref>). In a study conducted by Liu(<xref ref-type="bibr" rid="B96">Liu et al., 2022</xref>), it was observed that capsaicin exhibited significant inhibitory effects on the proliferation of NSCLC cells. Mechanismlly, capsaicin increased the levels of total iron and ferrous ions, while reducing GSH levels in the treated cells compared to the control group. Additionally, both mRNA and protein levels of SLC7A11 and GPX4 showed significant decreases in NSCLC cells treated with capsaicin compared to the control group. In summary, the treatment potential of capsaicin in NSCLC cells lies in its ability to induce ferroptosis.</p>
</sec>
<sec id="s3-16">
<title>3.16 Chinese medicine and preparations</title>
<p>In addition, several studies have indicated that certain Chinese medicine and preparations possess the potential therapeutic ability to stimulate ferroptosis to exhibit potential benefits in the treatment of NSCLC. <italic>Hedyotis diffusa</italic> (HD), a species of flowering plant in the family <italic>Rubiaceae,</italic> is a traditional Chinese herbal medicine, which exhibits numerous pharmacological activities, including antioxidant (<xref ref-type="bibr" rid="B99">Lu et al., 2000</xref>), anti-inflammatory (<xref ref-type="bibr" rid="B60">Hung et al., 2022</xref>), and anti-cancer (<xref ref-type="bibr" rid="B166">Wu et al., 2022</xref>). It contains various bioactive compounds, including iridoids, flavonoids, triterpenoids, and phenolic acids, which are believed to contribute to its medicinal effects (<xref ref-type="bibr" rid="B192">Zhang et al., 2021</xref>). Huang (<xref ref-type="bibr" rid="B59">Huang et al., 2022</xref>)found that HD can inhibit NSCLC cells growth and induce characteristics of ferroptosis, including increase in mitochondrial membrane density, shrunken mitochondria, and decline of cristae. Moreover, HD increase cellular Lipid ROS, the Fe<sup>2&#x002B;</sup> fluorescence intensity and MDA levels. Mechanically, HD-induced ferroptosis in lung adenocarcinoma cells may be related to the voltage dependent anion channel 2/3(VDAC2/3) pathway, (<xref ref-type="bibr" rid="B178">Yang et al., 2020</xref>),a group of specific channel proteins, facilitates the exchange of metabolites and ions across the outer mitochondrial membrane and may regulate mitochondrial functions. Furthermore, HD exerts its regulatory effects on the BCL2 apoptosis regulator (Bcl2)/BCL2 associated X, apoptosis regulator (Bax) protein complex, thereby modulating the functional dynamics of VDAC2/3. This modulation results in the activation of VDAC2/3 channels, facilitating the translocation of ions and facilitating the intracellular accumulation of ROS. Above all, HD could induce ferroptosis via Bcl2 inhibition to promote Bax regulation of VDAC2/3 to attentus the NSCLC cells growth. Zhao (<xref ref-type="bibr" rid="B197">Zhao et al., 2022</xref>) showed that Fuzheng Kang&#x2019;ai (FZKA) decoction significantly suppressed the expression of GPX4 and system Xc<sup>&#x2212;</sup> and conducted a reduction in the GSH/GSSG ratio to induce ferroptosis in NSCLC treatment. Importantly, the induction of ferroptosis in NSCLC cells by FZKA decoction was significantly reversed when GPX4 was overexpressed. These findings were further confirmed <italic>in vivo</italic> animal model, validating the observed effects of FZKA on ferroptosis in NSCLC cells.</p>
</sec>
</sec>
<sec id="s4">
<title>4 Conclusion and prospects</title>
<p>Ferroptosis is a novel form of cell death that distinguishes itself from apoptosis, necroptosis, and autophagy. Multiple evidences have indicated the significant role of ferroptosis in regulating tumor cell growth and drug resistance, making it a potential new target for anti-tumor interventions (<xref ref-type="bibr" rid="B19">Chen et al., 2021a</xref>; <xref ref-type="bibr" rid="B129">Song et al., 2021</xref>; <xref ref-type="bibr" rid="B154">Wang et al., 2022</xref>). Therefore, ferroptosis inducers hold great promise as highly prospective agents for cancer diagnosis and therapeutic intervention, and they are also of significant importance in the development of anti-cancer drugs (<xref ref-type="bibr" rid="B75">Lei et al., 2022</xref>). Here, we have summarized the characteristic ferroptosis inducers and their main anti-cancer mechanisms in <xref ref-type="sec" rid="s9">Supplementary Table</xref>, aiming to provide support for the clinical development of anti-cancer drugs.</p>
<p>The current study summarized the introduction and mechanism of ferroptosis. The mechanism of ferroptosis mainly involves four processes: GPX4, system Xc<sup>&#x2212;</sup>, iron metabolism, and lipid peroxidation. In the field of NCSLC research, the ferroptosis as a novel cellular death mechanism has gathered significant attention in recent years (<xref ref-type="bibr" rid="B194">Zhang et al., 2022b</xref>; <xref ref-type="bibr" rid="B196">Zhao et al., 2023</xref>). We summarized relevant targets or pathways of ferroptosis in NCSLC therapy as shown in <xref ref-type="table" rid="T1">Table 1</xref>. Additionally, natural products have made certain progress in the prevention and treatment of NCSLC by regulating ferroptosis process. However, the investigation into the modulation of ferroptosis in NSCLC using natural products is currently in its initial exploratory phase, with certain limitations evident in existing research studies. Firstly, most studies have only explored the molecular mechanisms by which natural product from traditional Chinese medicine induces ferroptosis through a single pathway. Nevertheless, traditional Chinese medicine formulas and patent medicines widely used in clinical practice possess the characteristics of &#x201c;multiple components, multiple targets, and multiple effects&#x201d; (<xref ref-type="bibr" rid="bib204">Yan et al., 2022</xref>). In future research, we should explore the molecular mechanisms of traditional Chinese medicine in regulating ferroptosis from multiple pathways and perspectives, construct &#x201c;components-targets/pathways-disease&#x201d; pharmacological network, and conduct relevant clinical trials.</p>
<p>Secondly, natural products are typically complex mixtures with diverse chemical structures and compositions, which increases the complexity of studying their pharmacological activities and tissue specificity (<xref ref-type="bibr" rid="bib205">Xia et al., 2022</xref>). These complexities may make it difficult to accurately assess the absorption, distribution, metabolism, and excretion properties of drugs. Based on this, we need to strengthen the exploration of the potential of nanotechnology (<xref ref-type="bibr" rid="B68">Kaur et al., 2022</xref>), encapsulation (<xref ref-type="bibr" rid="B90">Linh et al., 2022</xref>), and targeted delivery systems (<xref ref-type="bibr" rid="B40">Gorain et al., 2022</xref>) to improve the pharmacokinetics and tissue specificity of natural products.</p>
<p>Thirdly, certain natural products may cause adverse reactions in the digestive system, such as nausea, vomiting, diarrhea, gastrointestinal discomfort, etc. (<xref ref-type="bibr" rid="B106">Menniti-Ippolito et al., 2008</xref>; <xref ref-type="bibr" rid="B144">Vasudeva et al., 2012</xref>; <xref ref-type="bibr" rid="B200">Zorzela et al., 2021</xref>; <xref ref-type="bibr" rid="B6">Andrade et al., 2022</xref>). Therefore, the importance of conducting controlled clinical trials should be emphasized to evaluate the safety of treatment methods based on natural products for NSCLC patients.</p>
<p>Finally, it is also necessary to consider combining natural products with other treatment modalities, including chemotherapy drugs such as sulfasalazine (<xref ref-type="bibr" rid="B74">Lay et al., 2007</xref>), sorafenib (<xref ref-type="bibr" rid="B42">Groenendijk et al., 2015</xref>), zalcitabine (<xref ref-type="bibr" rid="B105">McNeill and Wilson, 2007</xref>), and cisplatin (<xref ref-type="bibr" rid="B71">Kryczka et al., 2021</xref>), which all can be purposed to induce ferroptosis, to improve the efficiency of natural product-based treatments for NSCLC. We believe that with the progress ferroptosis of research, new effective strategies for the treatment of NSCLC can be provided.</p>
</sec>
</body>
<back>
<sec id="s5">
<title>Author contributions</title>
<p>QZ: Writing&#x2013;original draft, Validation. YX: Data curation, Software, Writing&#x2013;original draft. FW: Investigation, Writing&#x2013;original draft. DY: Methodology, Writing&#x2013;review and editing. ZL: Writing&#x2013;review and editing, Funding acquisition.</p>
</sec>
<sec id="s6" sec-type="funding-information">
<title>Funding</title>
<p>The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was funded by the R &#x26; D project of &#x201c;Jianbing&#x201d; and &#x201c;Lingyan&#x201d; in Zhejiang Province (2022C02023) and the Key Science and Technology Project of New Agricultural Variety Breeding of Zhejiang Province (2021C02074).</p>
</sec>
<sec id="s7" sec-type="COI-statement">
<title>Conflict of interest</title>
<p>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.</p>
</sec>
<sec id="s8" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>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.</p>
</sec>
<sec id="s9">
<title>Supplementary material</title>
<p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="https://www.frontiersin.org/articles/10.3389/fphar.2024.1385565/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fphar.2024.1385565/full&#x23;supplementary-material</ext-link>
</p>
<supplementary-material xlink:href="Table1.docx" id="SM1" mimetype="application/docx" xmlns:xlink="http://www.w3.org/1999/xlink"/>
</sec>
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<sec id="s10">
<title>Glossary</title>
<table-wrap id="udT1" position="float">
<table>
<tbody valign="top">
<tr>
<td align="left">
<bold>ACSL4</bold>
</td>
<td align="left">Acyl-CoA synthetase long chain family member 4</td>
</tr>
<tr>
<td align="left">
<bold>AA</bold>
</td>
<td align="left">arachidonoyl</td>
</tr>
<tr>
<td align="left">
<bold>AdA</bold>
</td>
<td align="left">adrenal</td>
</tr>
<tr>
<td align="left">
<bold>CTN</bold>
</td>
<td align="left">Cryptotanshinone</td>
</tr>
<tr>
<td align="left">
<bold>CaM</bold>
</td>
<td align="left">Calmodulin</td>
</tr>
<tr>
<td align="left">
<bold>CoQ</bold>
</td>
<td align="left">Coenzyme Q</td>
</tr>
<tr>
<td align="left">
<bold>DTI</bold>
</td>
<td align="left">Dihydroisotanshinone I</td>
</tr>
<tr>
<td align="left">
<bold>DMT1</bold>
</td>
<td align="left">divalent metal transporter 1</td>
</tr>
<tr>
<td align="left">
<bold>DHA</bold>
</td>
<td align="left">Dihydroartemisinin</td>
</tr>
<tr>
<td align="left">
<bold>DRP1</bold>
</td>
<td align="left">dynamin-related protein 1</td>
</tr>
<tr>
<td align="left">
<bold>Fe</bold>
<sup>
<bold>3&#x002B;</bold>
</sup>
</td>
<td align="left">Ferric ions</td>
</tr>
<tr>
<td align="left">
<bold>Fe</bold>
<sup>
<bold>2&#x002B;</bold>
</sup>
</td>
<td align="left">ferrous ions</td>
</tr>
<tr>
<td align="left">
<bold>FZKA</bold>
</td>
<td align="left">Fuzheng Kang&#x2019;ai</td>
</tr>
<tr>
<td align="left">
<bold>FIS1</bold>
</td>
<td align="left">fission 1 protein</td>
</tr>
<tr>
<td align="left">
<bold>GSH</bold>
</td>
<td align="left">glutathione</td>
</tr>
<tr>
<td align="left">
<bold>GCO</bold>
</td>
<td align="left">Global Cancer Observatory</td>
</tr>
<tr>
<td align="left">
<bold>GSSG</bold>
</td>
<td align="left">oxidized glutathione</td>
</tr>
<tr>
<td align="left">
<bold>GR</bold>
</td>
<td align="left">glutathione reductase</td>
</tr>
<tr>
<td align="left">
<bold>Gly</bold>
</td>
<td align="left">glycine</td>
</tr>
<tr>
<td align="left">
<bold>GSS</bold>
</td>
<td align="left">glutathione synthetase</td>
</tr>
<tr>
<td align="left">
<bold>GPX4</bold>
</td>
<td align="left">glutathione peroxidase 4</td>
</tr>
<tr>
<td align="left">
<bold>glutamate</bold>
</td>
<td align="left">Glu</td>
</tr>
<tr>
<td align="left">
<bold>GPX2</bold>
</td>
<td align="left">GSH peroxidase 2</td>
</tr>
<tr>
<td align="left">
<bold>HD</bold>
</td>
<td align="left">Hedyotis diffusa</td>
</tr>
<tr>
<td align="left">
<bold>HSP90</bold>
</td>
<td align="left">heat shock protein 90</td>
</tr>
<tr>
<td align="left">
<bold>LPCAT3</bold>
</td>
<td align="left">lysophosphatidic transferase 3</td>
</tr>
<tr>
<td align="left">
<bold>MDA</bold>
</td>
<td align="left">malondialdehyde</td>
</tr>
<tr>
<td align="left">
<bold>Nrf-2</bold>
</td>
<td align="left">NFE2 like bZIP transcription factor 2</td>
</tr>
<tr>
<td align="left">
<bold>NCOA4</bold>
</td>
<td align="left">nuclear receptor coactivator 4</td>
</tr>
<tr>
<td align="left">
<bold>NAC</bold>
</td>
<td align="left">N-Acetyl-L-cysteine</td>
</tr>
<tr>
<td align="left">
<bold>NSCLC</bold>
</td>
<td align="left">Non-Small Cell Lung Cancer</td>
</tr>
<tr>
<td align="left">
<bold>PCD</bold>
</td>
<td align="left">programmed cell death</td>
</tr>
<tr>
<td align="left">
<bold>PUFAs</bold>
</td>
<td align="left">polyunsaturated fatty acids</td>
</tr>
<tr>
<td align="left">
<bold>PRIM2</bold>
</td>
<td align="left">DNA primase subunit 2</td>
</tr>
<tr>
<td align="left">
<bold>ROS</bold>
</td>
<td align="left">reactive oxygen species</td>
</tr>
<tr>
<td align="left">
<bold>Stub1</bold>
</td>
<td align="left">U-Box containing protein 1</td>
</tr>
<tr>
<td align="left">
<bold>SLC3A2</bold>
</td>
<td align="left">solute carrier family 3 member 2</td>
</tr>
<tr>
<td align="left">
<bold>SLC40A1</bold>
</td>
<td align="left">solute carrier family 40 member 1</td>
</tr>
<tr>
<td align="left">
<bold>TA III</bold>
</td>
<td align="left">Timosaponin AIII</td>
</tr>
<tr>
<td align="left">
<bold>TfR1</bold>
</td>
<td align="left">transferrin receptor</td>
</tr>
<tr>
<td align="left">
<bold>VDAC</bold>
</td>
<td align="left">voltage-dependent anion channel</td>
</tr>
<tr>
<td align="left">
<bold>xCT</bold>
</td>
<td align="left">SLC7A11</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
</back>
</article>