Volume 14 Issue 10
Oct.  2024
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Shengli Ouyang, Zeyao Zeng, Jieyi He, Lianxiang Luo. Epigenetic regulation of targeted ferroptosis: A new strategy for drug development[J]. Journal of Pharmaceutical Analysis, 2024, 14(10): 101012. doi: 10.1016/j.jpha.2024.101012
Citation: Shengli Ouyang, Zeyao Zeng, Jieyi He, Lianxiang Luo. Epigenetic regulation of targeted ferroptosis: A new strategy for drug development[J]. Journal of Pharmaceutical Analysis, 2024, 14(10): 101012. doi: 10.1016/j.jpha.2024.101012

Epigenetic regulation of targeted ferroptosis: A new strategy for drug development

doi: 10.1016/j.jpha.2024.101012
  • Received Date: Jan. 28, 2024
  • Accepted Date: May 23, 2024
  • Rev Recd Date: May 20, 2024
  • Publish Date: May 28, 2024
  • Ferroptosis is a newly discovered form of cell death that is influenced by iron levels and is triggered by cellular metabolism and excessive lipid peroxidation. Epigenetic regulation plays a crucial role in the development and progression of diseases, making it essential to understand these mechanisms in order to identify potential targets for drug development and clinical treatment. The intersection of ferroptosis and epigenetics has opened up new avenues for research in drug development, offering innovative strategies for combating diseases. Recent studies have shown that epigenetic modifications can impact pathways related to ferroptosis, potentially leading to organ dysfunction. Despite the increasing focus on this relationship, the role of epigenetic regulation in drug development remains largely unexplored. This article explores current research on the interplay between epigenetic regulation and ferroptosis, delving into their regulatory mechanisms and discussing the effects of existing epigenetic modification regulators on diseases. Additionally, we highlight ongoing research on epigenetic factors involved in targeting ferroptosis in cancer, providing new insights for the development of cancer treatments.

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  • [1]
    S.J. Dixon, K.M. Lemberg, M.R. Lamprecht, et al., Ferroptosis: An iron-dependent form of nonapoptotic cell death, Cell 149 (2012) 1060-1072.
    [2]
    B.R. Stockwell, Ferroptosis turns 10: Emerging mechanisms, physiological functions, and therapeutic applications, Cell 185 (2022) 2401-2421.
    [3]
    D. Tang, X. Chen, R. Kang, et al., Ferroptosis: Molecular mechanisms and health implications, Cell Res. 31 (2021) 107-125.
    [4]
    L. Zhang, Q. Lu, C. Chang, Epigenetics in health and disease, Adv. Exp. Med. Biol. 1253 (2020) 3-55.
    [5]
    M.A. Dawson, T. Kouzarides, Cancer epigenetics: From mechanism to therapy, Cell 150 (2012) 12-27.
    [6]
    A. Cort, T. Ozben, L. Saso, et al., Redox control of multidrug resistance and its possible modulation by antioxidants, Oxid. Med. Cell. Longev. 2016 (2016), 4251912.
    [7]
    L. Rochette, G. Dogon, E. Rigal, et al., Lipid peroxidation and iron metabolism: Two corner stones in the homeostasis control of ferroptosis, Int. J. Mol. Sci. 24 (2022), 449.
    [8]
    E. Dai, X. Chen, A. Linkermann, et al., A guideline on the molecular ecosystem regulating ferroptosis, Nat. Cell Biol. (2024) 1447-1457.
    [9]
    D. Liang, A.M. Minikes, X. Jiang, Ferroptosis at the intersection of lipid metabolism and cellular signaling, Mol. Cell 82 (2022) 2215-2227.
    [10]
    B.T. Paul, D.H. Manz, F.M. Torti, et al., Mitochondria and Iron: Current questions, Expert Rev. Hematol. 10 (2017) 65-79.
    [11]
    M. Dodson, R. Castro-Portuguez, D.D. Zhang, NRF2 plays a critical role in mitigating lipid peroxidation and ferroptosis, Redox Biol. 23 (2019), 101107.
    [12]
    K. Pantopoulos, S.K. Porwal, A. Tartakoff, et al., Mechanisms of mammalian iron homeostasis, Biochemistry 51 (2012) 5705-5724.
    [13]
    G.J. Anderson, D.M. Frazer, Current understanding of iron homeostasis, Am. J. Clin. Nutr. 106 (2017) 1559S-1566S.
    [14]
    F. Zolea, A.M. Battaglia, E. Chiarella, et al., Ferritin heavy subunit silencing blocks the erythroid commitment of K562 cells via miR-150 up-regulation and GATA-1 repression, Int. J. Mol. Sci. 18 (2017), 2167.
    [15]
    J. Liu, R. Kang, D. Tang, Signaling pathways and defense mechanisms of ferroptosis, FEBS J. 289 (2022) 7038-7050.
    [16]
    Z. Zhang, M. Guo, Y. Li, et al., RNA-binding protein ZFP36/TTP protects against ferroptosis by regulating autophagy signaling pathway in hepatic stellate cells, Autophagy 16 (2020) 1482-1505.
    [17]
    J.D. Mancias, L. Pontano Vaites, S. Nissim, et al., Ferritinophagy via NCOA4 is required for erythropoiesis and is regulated by iron dependent HERC2-mediated proteolysis, elife 4 (2015), e10308.
    [18]
    W.E. Dowdle, B. Nyfeler, J. Nagel, et al., Selective VPS34 inhibitor blocks autophagy and uncovers a role for NCOA4 in ferritin degradation and iron homeostasis in vivo, Nat. Cell Biol. 16 (2014) 1069-1079.
    [19]
    C. Xu, S. Sun, T. Johnson, et al., The glutathione peroxidase Gpx4 prevents lipid peroxidation and ferroptosis to sustain Treg cell activation and suppression of antitumor immunity, Cell Rep. 35 (2021), 109235.
    [20]
    W.S. Hambright, R.S. Fonseca, L. Chen, et al., Ablation of ferroptosis regulator glutathione peroxidase 4 in forebrain neurons promotes cognitive impairment and neurodegeneration, Redox Biol. 12 (2017) 8-17.
    [21]
    W.S. Yang, R. SriRamaratnam, M.E. Welsch, et al., Regulation of ferroptotic cancer cell death by GPX4, Cell 156 (2014) 317-331.
    [22]
    C.K. Singh, G. Chhabra, M.A. Ndiaye, et al., The role of sirtuins in antioxidant and redox signaling, Antioxid. Redox Signal. 28 (2018) 643-661.
    [23]
    C. Biswas, N. Shah, M. Muthu, et al., Nuclear heme oxygenase-1 (HO-1) modulates subcellular distribution and activation of Nrf2, impacting metabolic and anti-oxidant defenses, J. Biol. Chem. 289 (2014) 26882-26894.
    [24]
    X. Song, D. Long, Nrf2 and ferroptosis: A new research direction for neurodegenerative diseases, Front. Neurosci. 14 (2020), 267.
    [25]
    M. Conrad, A. Sandin, H. Forster, et al., 12/15-lipoxygenase-derived lipid peroxides control receptor tyrosine kinase signaling through oxidation of protein tyrosine phosphatases, Proc. Natl. Acad. Sci. U.S.A. 107 (2010) 15774-15779.
    [26]
    H. Sato, M. Tamba, T. Ishii, et al., Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins, J. Biol. Chem. 274 (1999) 11455-11458.
    [27]
    P. Koppula, Y. Zhang, L. Zhuang, et al., Amino acid transporter SLC7A11/xCT at the crossroads of regulating redox homeostasis and nutrient dependency of cancer, Cancer Commun. (Lond) 38 (2018), 12.
    [28]
    B.R. Stockwell, J.P. Friedmann Angeli, H. Bayir, et al., Ferroptosis: A regulated cell death nexus linking metabolism, redox biology, and disease, Cell 171 (2017) 273-285.
    [29]
    P. Koppula, L. Zhuang, B. Gan, Cystine transporter SLC7A11/xCT in cancer: Ferroptosis, nutrient dependency, and cancer therapy, Protein Cell 12 (2021) 599-620.
    [30]
    M.S. Kilberg, J. Shan, N. Su, ATF4-dependent transcription mediates signaling of amino acid limitation, Trends Endocrinol. Metab. 20 (2009) 436-443.
    [31]
    L. Wang, Y. Liu, T. Du, et al., ATF3 promotes erastin-induced ferroptosis by suppressing system Xc, Cell Death Differ. 27 (2020) 662-675.
    [32]
    H. Dong, Z. Qiang, D. Chai, et al., Nrf2 inhibits ferroptosis and protects against acute lung injury due to intestinal ischemia reperfusion via regulating SLC7A11 and HO-1, Aging 12 (2020) 12943-12959.
    [33]
    A.S. Agyeman, R. Chaerkady, P.G. Shaw, et al., Transcriptomic and proteomic profiling of KEAP1 disrupted and sulforaphane-treated human breast epithelial cells reveals common expression profiles, Breast Cancer Res. Treat. 132 (2012) 175-187.
    [34]
    N. Harada, M. Kanayama, A. Maruyama, et al., Nrf2 regulates ferroportin 1-mediated iron efflux and counteracts lipopolysaccharide-induced ferroportin 1 mRNA suppression in macrophages, Arch. Biochem. Biophys. 508 (2011) 101-109.
    [35]
    Z. Qiang, H. Dong, Y. Xia, et al., Nrf2 and STAT3 alleviates ferroptosis-mediated IIR-ALI by regulating SLC7A11, Oxid. Med. Cell. Longev. 2020 (2020), 5146982.
    [36]
    E.J. Hillmer, H. Zhang, H.S. Li, et al., STAT3 signaling in immunity, Cytokine Growth Factor Rev. 31 (2016) 1-15.
    [37]
    B. Zhou, J. Liu, R. Kang, et al., Ferroptosis is a type of autophagy-dependent cell death, Semin. Cancer Biol. 66 (2020) 89-100.
    [38]
    A.L. Levonen, A. Landar, A. Ramachandran, et al., Cellular mechanisms of redox cell signalling: Role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products, Biochem. J. 378 (2004) 373-382.
    [39]
    X. Sun, Z. Ou, R. Chen, et al., Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells, Hepatology 63 (2016) 173-184.
    [40]
    Z. Fan, A.K. Wirth, D. Chen, et al., Nrf2-Keap1 pathway promotes cell proliferation and diminishes ferroptosis, Oncogenesis 6 (2017), e371.
    [41]
    Y. Sun, L. He, T. Wang, et al., Activation of p62-Keap1-Nrf2 pathway protects 6-hydroxydopamine-induced ferroptosis in dopaminergic cells, Mol. Neurobiol. 57 (2020) 4628-4641.
    [42]
    Q. Dang, Z. Sun, Y. Wang, et al., Ferroptosis: A double-edged sword mediating immune tolerance of cancer, Cell Death Dis. 13 (2022), 925.
    [43]
    J.-Y. Lee, W.K. Kim, K.-H. Bae, et al., Lipid metabolism and ferroptosis, Biology 10 (2021), 184.
    [44]
    J. Cui, Y. Wang, X. Tian, et al., LPCAT3 is transcriptionally regulated by YAP/ZEB/EP300 and collaborates with ACSL4 and YAP to determine ferroptosis sensitivity, Antioxid. Redox Signal. 39 (2023) 491-511.
    [45]
    S.J. Dixon, G.E. Winter, L.S. Musavi, et al., Human haploid cell genetics reveals roles for lipid metabolism genes in nonapoptotic cell death, ACS Chem. Biol. 10 (2015) 1604-1609.
    [46]
    T. Grenier-Larouche, A. Galinier, L. Casteilla, et al., Omental adipocyte hypertrophy relates to coenzyme Q10 redox state and lipid peroxidation in obese women, J. Lipid Res. 56 (2015) 1985-1992.
    [47]
    K. Bersuker, J.M. Hendricks, Z. Li, et al., The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis, Nature 575 (2019) 688-692.
    [48]
    P. Koppula, G. Lei, Y. Zhang, et al., A targetable CoQ-FSP1 axis drives ferroptosis-and radiation-resistance in KEAP1 inactive lung cancers, Nat. Commun. 13 (2022), 2206.
    [49]
    A. Latremoliere, M. Costigan, GCH1, BH4 and pain, Curr. Pharm. Biotechnol. 12 (2011) 1728-1741.
    [50]
    T. Harada, H. Kagamiyama, K. Hatakeyama, Feedback regulation mechanisms for the control of GTP cyclohydrolase I activity, Science 260 (1993) 1507-1510.
    [51]
    T. Yoneyama, J.M. Brewer, K. Hatakeyama, GTP cyclohydrolase I feedback regulatory protein is a pentamer of identical subunits. Purification, cDNA cloning, and bacterial expression, J. Biol. Chem. 272 (1997) 9690-9696.
    [52]
    Q. Hu, W. Wei, D. Wu, et al., Blockade of GCH1/BH4 axis activates ferritinophagy to mitigate the resistance of colorectal cancer to erastin-induced ferroptosis, Front. Cell Dev. Biol. 10 (2022), 810327.
    [53]
    S.J.F. Cronin, C. Seehus, A. Weidinger, et al., The metabolite BH4 controls T cell proliferation in autoimmunity and cancer, Nature 563 (2018) 564-568.
    [54]
    V.A.N. Kraft, C.T. Bezjian, S. Pfeiffer, et al., GTP cyclohydrolase 1/tetrahydrobiopterin counteract ferroptosis through lipid remodeling, ACS Cent. Sci. 6 (2020) 41-53.
    [55]
    J. Xue, C. Yu, W. Sheng, et al., The Nrf2/GCH1/BH4 axis ameliorates radiation-induced skin injury by modulating the ROS cascade, J. Invest. Dermatol. 137 (2017) 2059-2068.
    [56]
    Y. Pei, Y. Qian, H. Wang, et al., Epigenetic regulation of ferroptosis-associated genes and its implication in cancer therapy, Front. Oncol. 12 (2022), 771870.
    [57]
    K.M. Schachtschneider, Y. Liu, L.A. Rund, et al., Impact of neonatal iron deficiency on hippocampal DNA methylation and gene transcription in a porcine biomedical model of cognitive development, BMC Genomics 17 (2016), 856.
    [58]
    L.M. Iyer, S. Abhiman, L. Aravind, Natural history of eukaryotic DNA methylation systems, Prog. Mol. Biol. Transl. Sci. 101 (2011) 25-104.
    [59]
    K. Kawai, Y.-S. Li, M.-F. Song, et al., DNA methylation by dimethyl sulfoxide and methionine sulfoxide triggered by hydroxyl radical and implications for epigenetic modifications, Bioorg. Med. Chem. Lett. 20 (2010) 260-265.
    [60]
    R.D. Horniblow, P. Pathak, D.L. Balacco, et al., Iron-mediated epigenetic activation of NRF2 targets, J. Nutr. Biochem. 101 (2022), 108929.
    [61]
    Q. Ye, M. Trivedi, Y. Zhang, et al., Brain iron loading impairs DNA methylation and alters GABAergic function in mice, FASEB J. 33 (2019) 2460-2471.
    [62]
    S. Zhang, W. Chang, H. Wu, et al., Pan-cancer analysis of iron metabolic landscape across the Cancer Genome Atlas, J. Cell. Physiol. 235 (2020) 1013-1024.
    [63]
    R. Wei, H. Qiu, J. Xu, et al., Expression and prognostic potential of GPX1 in human cancers based on data mining, Ann. Transl. Med. 8 (2020), 124.
    [64]
    N.A.B. Schumann, A.S. Mendonca, M.M. Silveira, et al., Procaine and S-adenosyl-l-homocysteine affect the expression of genes related to the epigenetic machinery and change the DNA methylation status of in vitro cultured bovine skin fibroblasts, DNA Cell Biol. 39 (2020) 37-49.
    [65]
    W. Shen, C. Gao, R. Cueto, et al., Homocysteine-methionine cycle is a metabolic sensor system controlling methylation-regulated pathological signaling, Redox Biol. 28 (2020), 101322.
    [66]
    X. Zhang, Z. Huang, Z. Xie, et al., Homocysteine induces oxidative stress and ferroptosis of nucleus pulposus via enhancing methylation of GPX4, Free Radic. Biol. Med. 160 (2020) 552-565.
    [67]
    Z. Zhang, C. Fu, J. Liu, et al., Hypermethylation of the Nrf2 promoter induces ferroptosis by inhibiting the Nrf2-GPX4 axis in COPD, Int. J. Chron. Obstruct. Pulmon. Dis. 16 (2021) 3347-3362.
    [68]
    J.-Y. Lee, M. Nam, H.Y. Son, et al., Polyunsaturated fatty acid biosynthesis pathway determines ferroptosis sensitivity in gastric cancer, Proc. Natl. Acad. Sci. U.S.A. 117 (2020) 32433-32442.
    [69]
    Q. Shi, R. Liu, L. Chen, Ferroptosis inhibitor ferrostatin-1 alleviates homocysteine-induced ovarian granulosa cell injury by regulating TET activity and DNA methylation, Mol. Med. Rep. 25 (2022), 130.
    [70]
    E. Logie, B. Van Puyvelde, B. Cuypers, et al., Ferroptosis induction in multiple myeloma cells triggers DNA methylation and histone modification changes associated with cellular senescence, Int. J. Mol. Sci. 22 (2021), 12234.
    [71]
    J. Zhang, M. Gao, Y. Niu, et al., From DNMT1 degrader to ferroptosis promoter: Drug repositioning of 6-thioguanine as a ferroptosis inducer in gastric cancer, Biochem. Biophys. Res. Commun. 603 (2022) 75-81.
    [72]
    J. Lee, J.H. You, M.S. Kim, et al., Epigenetic reprogramming of epithelial-mesenchymal transition promotes ferroptosis of head and neck cancer, Redox Biol. 37 (2020), 101697.
    [73]
    K.D. Meyer, Y. Saletore, P. Zumbo, et al., Comprehensive analysis of mRNA methylation reveals enrichment in 3’ UTRs and near stop codons, Cell 149 (2012) 1635-1646.
    [74]
    X. Chen, Y.-Z. Sun, H. Liu, et al., RNA methylation and diseases: Experimental results, databases, Web servers and computational models, Brief. Bioinform. 20 (2019) 896-917.
    [75]
    P. Boccaletto, F. Stefaniak, A. Ray, et al., MODOMICS: A database of RNA modification pathways. 2021 update, Nucleic Acids Res. 50 (2022) D231-D235.
    [76]
    P.V. Sergiev, N.A. Aleksashin, A.A. Chugunova, et al., Structural and evolutionary insights into ribosomal RNA methylation, Nat. Chem. Biol. 14 (2018) 226-235.
    [77]
    Y. Pan, P. Ma, Y. Liu, et al., Multiple functions of m6A RNA methylation in cancer, J. Hematol. Oncol. 11 (2018), 48.
    [78]
    L. He, H. Li, A. Wu, et al., Functions of N6-methyladenosine and its role in cancer, Mol. Cancer 18 (2019), 176.
    [79]
    J. Han, J.-Z. Wang, X. Yang, et al., METTL3 promote tumor proliferation of bladder cancer by accelerating pri-miR221/222 maturation in m6A-dependent manner, Mol. Cancer 18 (2019), 110.
    [80]
    M. Cheng, L. Sheng, Q. Gao, et al., The m6A methyltransferase METTL3 promotes bladder cancer progression via AFF4/NF-κB/MYC signaling network, Oncogene 38 (2019) 3667-3680.
    [81]
    H. Yang, Y. Hu, M. Weng, et al., Hypoxia inducible lncRNA-CBSLR modulates ferroptosis through m6A-YTHDF2-dependent modulation of CBS in gastric cancer, J. Adv. Res. 37 (2021) 91-106.
    [82]
    F.-H. Ji, X.-H. Fu, G.-Q. Li, et al., FTO prevents thyroid cancer progression by SLC7A11 m6A methylation in a ferroptosis-dependent manner, Front. Endocrinol. 13 (2022), 857765.
    [83]
    J. Ye, X. Chen, X. Jiang, et al., RNA demethylase ALKBH5 regulates hypopharyngeal squamous cell carcinoma ferroptosis by posttranscriptionally activating NFE2L2/NRF2 in an m6 A-IGF2BP2-dependent manner, J. Clin. Lab. Anal. 36 (2022), e24514.
    [84]
    J. Liu, Z. Ren, L. Yang, et al., The NSUN5-FTH1/FTL pathway mediates ferroptosis in bone marrow-derived mesenchymal stem cells, Cell Death Discov. 8 (2022), 99.
    [85]
    H. Ling, M. Li, C. Yang, et al., Glycine increased ferroptosis via SAM-mediated GPX4 promoter methylation in rheumatoid arthritis, Rheumatology (Oxford) 61 (2022) 4521-4534.
    [86]
    J.E. Wilusz, H. Sunwoo, D.L. Spector, Long noncoding RNAs: Functional surprises from the RNA world, Genes Dev. 23 (2009) 1494-1504.
    [87]
    R. Zhang, T. Pan, Y. Xiang, et al., Curcumenol triggered ferroptosis in lung cancer cells via lncRNA H19/miR-19b-3p/FTH1 axis, Bioact. Mater. 13 (2021) 23-36.
    [88]
    Y. Luo, S. Huang, J. Wei, et al., Long noncoding RNA LINC01606 protects colon cancer cells from ferroptotic cell death and promotes stemness by SCD1-Wnt/β-catenin-TFE3 feedback loop signalling, Clin. Transl. Med. 12 (2022), e752.
    [89]
    Y. Zhang, M. Luo, X. Cui, et al., Long noncoding RNA NEAT1 promotes ferroptosis by modulating the miR-362-3p/MIOX axis as a ceRNA, Cell Death Differ. 29 (2022) 1850-1863.
    [90]
    J. Lu, F. Xu, H. Lu, LncRNA PVT1 regulates ferroptosis through miR-214-mediated TFR1 and p53, Life Sci. 260 (2020), 118305.
    [91]
    Y. Zhang, S. Guo, S. Wang, et al., LncRNA OIP5-AS1 inhibits ferroptosis in prostate cancer with long-term cadmium exposure through miR-128-3p/SLC7A11 signaling, Ecotoxicol. Environ. Saf. 220 (2021), 112376.
    [92]
    Y.Z. Li, H.C. Zhu, Y. Du, et al., Silencing lncRNA SLC16A1-AS1 induced ferroptosis in renal cell carcinoma through miR-143-3p/SLC7A11 signaling, Technol. Cancer Res. Treat. 21 (2022), 15330338221077803.
    [93]
    J. Krol, I. Loedige, W. Filipowicz, The widespread regulation of microRNA biogenesis, function and decay, Nat. Rev. Genet. 11 (2010) 597-610.
    [94]
    M. Luo, L. Wu, K. Zhang, et al., miR-137 regulates ferroptosis by targeting glutamine transporter SLC1A5 in melanoma, Cell Death Differ. 25 (2018) 1457-1472.
    [95]
    C. Ding, X. Ding, J. Zheng, et al., miR-182-5p and miR-378a-3p regulate ferroptosis in I/R-induced renal injury, Cell Death Dis. 11 (2020), 929.
    [96]
    H. Zhang, T. Deng, R. Liu, et al., CAF secreted miR-522 suppresses ferroptosis and promotes acquired chemo-resistance in gastric cancer, Mol. Cancer 19 (2020), 43.
    [97]
    W. Zhou, Z. Cai, J. Liu, et al., Circular RNA: Metabolism, functions and interactions with proteins, Mol. Cancer 19 (2020), 172.
    [98]
    S. Chen, Z. Zhang, B. Zhang, et al., CircCDK14 promotes tumor progression and resists ferroptosis in glioma by regulating PDGFRA, Int. J. Biol. Sci. 18 (2022) 841-857.
    [99]
    C. Wu, M. Du, R. Yu, et al., A novel mechanism linking ferroptosis and endoplasmic reticulum stress via the circPtpn14/miR-351-5p/5-LOX signaling in melatonin-mediated treatment of traumatic brain injury, Free Radic. Biol. Med. 178 (2022) 271-294.
    [100]
    H. Zhang, Z. Ge, Z. Wang, et al., Circular RNA RHOT1 promotes progression and inhibits ferroptosis via mir-106a-5p/STAT3 axis in breast cancer, Aging 13 (2021) 8115-8126.
    [101]
    Y. Luo, G. Niu, H. Yi, et al., Nanomedicine promotes ferroptosis to inhibit tumour proliferation in vivo, Redox Biol. 42 (2021), 101908.
    [102]
    M.D. Stewart, J. Li, J. Wong, Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment, Mol. Cell. Biol. 25 (2005) 2525-2538.
    [103]
    J.E. Audia, R.M. Campbell, Histone modifications and cancer, Cold Spring Harb. Perspect. Biol. 8 (2016), a019521.
    [104]
    T. Lan, T.T. Sun, C. Wei, et al., Epigenetic regulation of ferroptosis in central nervous system diseases, Mol. Neurobiol. 60 (2023) 3584-3599.
    [105]
    B.R. Sabari, D. Zhang, C.D. Allis, et al., Metabolic regulation of gene expression through histone acylations, Nat. Rev. Mol. Cell Biol. 18 (2017) 90-101.
    [106]
    M. Zille, A. Kumar, N. Kundu, et al., Ferroptosis in neurons and cancer cells is similar but differentially regulated by histone deacetylase inhibitors, eNeuro 6 (2019) ENEURO.0263-ENEURO.0218.2019.
    [107]
    L. Liu, Y. Li, D. Cao, et al., SIRT3 inhibits gallbladder cancer by induction of AKT-dependent ferroptosis and blockade of epithelial-mesenchymal transition, Cancer Lett. 510 (2021) 93-104.
    [108]
    F. Fan, P. Liu, R. Bao, et al., A dual PI3K/HDAC inhibitor induces immunogenic ferroptosis to potentiate cancer immune checkpoint therapy, Cancer Res. 81 (2021) 6233-6245.
    [109]
    X. Wang, K. Liu, H. Gong, et al., Death by histone deacetylase inhibitor quisinostat in tongue squamous cell carcinoma via apoptosis, pyroptosis, and ferroptosis, Toxicol. Appl. Pharmacol. 410 (2021), 115363.
    [110]
    T. Zhang, B. Sun, C. Zhong, et al., Targeting histone deacetylase enhances the therapeutic effect of Erastin-induced ferroptosis in EGFR-activating mutant lung adenocarcinoma, Transl. Lung Cancer Res. 10 (2021) 1857-1872.
    [111]
    Y. Liu, X. Duan, C. Zhang, et al., KAT6B may be applied as a potential therapeutic target for glioma, J. Oncol. 2022 (2022), 2500092.
    [112]
    H. Li, W. Liu, X. Zhang, et al., Ketamine suppresses proliferation and induces ferroptosis and apoptosis of breast cancer cells by targeting KAT5/GPX4 axis, Biochem. Biophys. Res. Commun. 585 (2021) 111-116.
    [113]
    S. Sui, J. Zhang, S. Xu, et al., Ferritinophagy is required for the induction of ferroptosis by the bromodomain protein BRD4 inhibitor (+)-JQ1 in cancer cells, Cell Death Dis. 10 (2019), 331.
    [114]
    S.-H. Luo, J.-M. Tian, Y. Chu, et al., The BRD4-SRPK2-SRSF2 signal modulates the splicing efficiency of ACSL3 pre-mRNA and influences erastin-induced ferroptosis in osteosarcoma cells, Cell Death Dis. 14 (2023), 760.
    [115]
    X. Cui, X. Yun, M. Sun, et al., HMGCL-induced β-hydroxybutyrate production attenuates hepatocellular carcinoma via DPP4-mediated ferroptosis susceptibility, Hepatol. Int. 17 (2023) 377-392.
    [116]
    X. Zhang, S. Sui, L. Wang, et al., Inhibition of tumor propellant glutathione peroxidase 4 induces ferroptosis in cancer cells and enhances anticancer effect of cisplatin, J. Cell. Physiol. 235 (2020) 3425-3437.
    [117]
    Y. Chen, X. Yi, B. Huo, et al., BRD4770 functions as a novel ferroptosis inhibitor to protect against aortic dissection, Pharmacol. Res. 177 (2022), 106122.
    [118]
    T. Liu, P. Xu, S. Ke, et al., Histone methyltransferase SETDB1 inhibits TGF-β-induced epithelial-mesenchymal transition in pulmonary fibrosis by regulating SNAI1 expression and the ferroptosis signaling pathway, Arch. Biochem. Biophys. 715 (2022), 109087.
    [119]
    Y. Cao, F. Luo, J. Peng, et al., KMT2B-dependent RFK transcription activates the TNF-α/NOX2 pathway and enhances ferroptosis caused by myocardial ischemia-reperfusion, J. Mol. Cell. Cardiol. 173 (2022) 75-91.
    [120]
    J. Wang, X. Yin, W. He, et al., SUV39H1 deficiency suppresses clear cell renal cell carcinoma growth by inducing ferroptosis, Acta Pharm. Sin. B 11 (2021) 406-419.
    [121]
    Y. Wang, Y. Zhao, H. Wang, et al., Histone demethylase KDM3B protects against ferroptosis by upregulating SLC7A11, FEBS Open Bio 10 (2020) 637-643.
    [122]
    M. Chen, Y. Jiang, Y. Sun, KDM4A-mediated histone demethylation of SLC7A11 inhibits cell ferroptosis in osteosarcoma, Biochem. Biophys. Res. Commun. 550 (2021) 77-83.
    [123]
    K. Xu, X. Liu, B. Wen, et al., GSK-J4, a specific histone lysine demethylase 6A inhibitor, ameliorates lipotoxicity to cardiomyocytes via preserving H3K27 methylation and reducing ferroptosis, Front. Cardiovasc. Med. 9 (2022), 907747.
    [124]
    R. Feng, Y. Xiong, Y. Lei, et al., Lysine-specific demethylase 1 aggravated oxidative stress and ferroptosis induced by renal ischemia and reperfusion injury through activation of TLR4/NOX4 pathway in mice, J. Cell. Mol. Med. 26 (2022) 4254-4267.
    [125]
    A. Li, Y. He, S. Sun, et al., Lysine-specific demethylase 1 inhibitors protect cochlear spiral ganglion neurons against cisplatin-induced damage, Neuroreport 26 (2015) 539-547.
    [126]
    Y. Liu, L. Ouyang, C. Mao, et al., PCDHB14 promotes ferroptosis and is a novel tumor suppressor in hepatocellular carcinoma, Oncogene 41 (2022) 3570-3583.
    [127]
    T. Zhu, B. Liu, D. Wu, et al., Autophagy regulates VDAC3 ubiquitination by FBXW7 to promote erastin-induced ferroptosis in acute lymphoblastic leukemia, Front. Cell Dev. Biol. 9 (2021), 740884.
    [128]
    Y. Wang, D. Chen, H. Xie, et al., AUF1 protects against ferroptosis to alleviate sepsis-induced acute lung injury by regulating NRF2 and ATF3, Cell. Mol. Life Sci. 79 (2022), 228.
    [129]
    Y. Yang, M. Luo, K. Zhang, et al., Nedd4 ubiquitylates VDAC2/3 to suppress erastin-induced ferroptosis in melanoma, Nat. Commun. 11 (2020), 433.
    [130]
    Y. Wang, Y. Liu, J. Liu, et al., NEDD4L-mediated LTF protein degradation limits ferroptosis, Biochem. Biophys. Res. Commun. 531 (2020) 581-587.
    [131]
    L. Liu, C. Zhang, S. Qu, et al., ESR1 inhibits ionizing radiation-induced ferroptosis in breast cancer cells via the NEDD4L/CD71 pathway, Arch. Biochem. Biophys. 725 (2022), 109299.
    [132]
    S. Chillappagari, R. Belapurkar, A. Moller, et al., SIAH2-mediated and organ-specific restriction of HO-1 expression by a dual mechanism, Sci. Rep. 10 (2020), 2268.
    [133]
    S. An, M. Hu, Quercetin promotes TFEB nuclear translocation and activates lysosomal degradation of ferritin to induce ferroptosis in breast cancer cells, Comput. Intell. Neurosci. 2022 (2022), 5299218.
    [134]
    H. Nishizawa, M. Matsumoto, T. Shindo, et al., Ferroptosis is controlled by the coordinated transcriptional regulation of glutathione and labile iron metabolism by the transcription factor BACH1, J. Biol. Chem. 295 (2020) 69-82.
    [135]
    R. Gao, R.K.R. Kalathur, M. Coto-Llerena, et al., YAP/TAZ and ATF4 drive resistance to Sorafenib in hepatocellular carcinoma by preventing ferroptosis, EMBO Mol. Med. 13 (2021), e14351.
    [136]
    J. Liu, X. Song, F. Kuang, et al., NUPR1 is a critical repressor of ferroptosis, Nat. Commun. 12 (2021), 647.
    [137]
    Z. Wang, X. Chen, N. Liu, et al., A nuclear long non-coding RNA LINC00618 accelerates ferroptosis in a manner dependent upon apoptosis, Mol. Ther. 29 (2021) 263-274.
    [138]
    Y. Jiang, C. Mao, R. Yang, et al., EGLN1/c-Myc induced Lymphoid-specific helicase inhibits ferroptosis through lipid metabolic gene expression changes, Theranostics 7 (2017) 3293-3305.
    [139]
    R. Kang, G. Kroemer, D. Tang, The tumor suppressor protein p53 and the ferroptosis network, Free Radic. Biol. Med. 133 (2019) 162-168.
    [140]
    L. Jiang, N. Kon, T. Li, et al., Ferroptosis as a p53-mediated activity during tumour suppression, Nature 520 (2015) 57-62.
    [141]
    C. Mao, X. Wang, Y. Liu, et al., A G3BP1-Interacting lncRNA promotes ferroptosis and apoptosis in cancer via nuclear sequestration of p53, Cancer Res. 78 (2018) 3484-3496.
    [142]
    W. Li, W. Li, Y. Wang, et al., Inhibition of DNMT-1 alleviates ferroptosis through NCOA4 mediated ferritinophagy during diabetes myocardial ischemia/reperfusion injury, Cell Death Discov. 7 (2021), 267.
    [143]
    H. Yang, L. Zhao, Y. Gao, et al., Pharmacotranscriptomic analysis reveals novel drugs and gene networks regulating ferroptosis in cancer, Cancers 12 (2020), 3273.
    [144]
    K. Miyamoto, M. Watanabe, S. Boku, et al., xCT inhibition increases sensitivity to vorinostat in a ROS-dependent manner, Cancers 12 (2020), 827.
    [145]
    T. Oliveira, E. Hermann, D. Lin, et al., HDAC inhibition induces EMT and alterations in cellular iron homeostasis to augment ferroptosis sensitivity in SW13 cells, Redox Biol. 47 (2021), 102149.
    [146]
    B.K. Flesner, S.R. Kumar, J.N. Bryan, 6-Thioguanine and zebularine down-regulate DNMT1 and globally demethylate canine malignant lymphoid cells, BMC Vet. Res. 10 (2014), 290.
    [147]
    Z. Yuan, S. Chen, C. Gao, et al., Development of a versatile DNMT and HDAC inhibitor C02S modulating multiple cancer hallmarks for breast cancer therapy, Bioorg. Chem. 87 (2019) 200-208.
    [148]
    W.A. Kwon, H.K. Seo, Novel G9a/DNMT first-in-class dual reversible inhibitor has potent antitumor effect in bladder cancer, Transl. Cancer Res. 9 (2020) 1319-1321.
    [149]
    A. Sfera, K.G. Thomas, C.V. Andronescu, et al., Bromodomains in human-immunodeficiency virus-associated neurocognitive disorders: A model of ferroptosis-induced neurodegeneration, Front. Neurosci. 16 (2022), 904816.
    [150]
    J. Qiao, Y. Chen, Y. Mi, et al., NR5A2 synergizes with NCOA3 to induce breast cancer resistance to BET inhibitor by upregulating NRF2 to attenuate ferroptosis, Biochem. Biophys. Res. Commun. 530 (2020) 402-409.
    [151]
    C. Yang, T. Lu, M. Liu, et al., Tiliroside targets TBK1 to induce ferroptosis and sensitize hepatocellular carcinoma to sorafenib, Phytomedicine 111 (2023), 154668.
    [152]
    Y. Peng, N. Li, F. Tang, et al., Corosolic acid sensitizes ferroptosis by upregulating HERPUD1 in liver cancer cells, Cell Death Discov. 8 (2022), 376.
    [153]
    Y. Ding, X. Chen, C. Liu, et al., Identification of a small molecule as inducer of ferroptosis and apoptosis through ubiquitination of GPX4 in triple negative breast cancer cells, J. Hematol. Oncol. 14 (2021), 19.
    [154]
    W. Zhang, B. Jiang, Y. Liu, et al., Bufotalin induces ferroptosis in non-small cell lung cancer cells by facilitating the ubiquitination and degradation of GPX4, Free Radic. Biol. Med. 180 (2022) 75-84.
    [155]
    Y. Liu, L. He, B. Liu, et al., Pharmacological inhibition of sphingolipid synthesis reduces ferroptosis by stimulating the HIF-1 pathway, iScience 25 (2022), 104533.
    [156]
    G. Li, S. Lin, Z. Yu, et al., A PARP1 PROTAC as a novel strategy against PARP inhibitor resistance via promotion of ferroptosis in p53-positive breast cancer, Biochem. Pharmacol. 206 (2022), 115329.
    [157]
    L.S. Chan, J. Liu, M.S.C. Li, et al., Selenite as a dual apoptotic and ferroptotic agent synergizes with EGFR and KRAS inhibitors with epigenetic interference, Clin. Epigenetics 15 (2023), 36.
    [158]
    Y. Wang, S. Yan, X. Liu, et al., PRMT4 promotes ferroptosis to aggravate doxorubicin-induced cardiomyopathy via inhibition of the Nrf2/GPX4 pathway, Cell Death Differ. 29 (2022) 1982-1995.
    [159]
    H. Zhao, X. Li, L. Yang, et al., Isorhynchophylline relieves ferroptosis-induced nerve damage after intracerebral hemorrhage via miR-122-5p/TP53/SLC7A11 pathway, Neurochem. Res. 46 (2021) 1981-1994.
    [160]
    M. Szyf, Prospects for the development of epigenetic drugs for CNS conditions, Nat. Rev. Drug Discov. 14 (2015) 461-474.
    [161]
    S. Moufarrij, M. Dandapani, E. Arthofer, et al., Epigenetic therapy for ovarian cancer: Promise and progress, Clin. Epigenetics 11 (2019), 7.
    [162]
    J.S. Smolen, D. Aletaha, A. Barton, et al., Rheumatoid arthritis, Nat. Rev. Dis. Primers 4 (2018), 18001.
    [163]
    C.D. DiNardo, B.A. Jonas, V. Pullarkat, et al., Azacitidine and venetoclax in previously untreated acute myeloid leukemia, N. Engl. J. Med. 383 (2020) 617-629.
    [164]
    L. Falchi, H. Ma, S. Klein, et al., Combined oral 5-azacytidine and romidepsin are highly effective in patients with PTCL: A multicenter phase 2 study, Blood 137 (2021) 2161-2170.
    [165]
    G. Garcia-Manero, E.A. Griffiths, D.P. Steensma, et al., Oral cedazuridine/decitabine for MDS and CMML: A phase 2 pharmacokinetic/pharmacodynamic randomized crossover study, Blood 136 (2020) 674-683.
    [166]
    M.A. Sekeres, J. Taylor, Diagnosis and treatment of myelodysplastic syndromes: A review, JAMA 328 (2022) 872-880.
    [167]
    L.C. Stork, Y. Matloub, E. Broxson, et al., Oral 6-mercaptopurine versus oral 6-thioguanine and veno-occlusive disease in children with standard-risk acute lymphoblastic leukemia: Report of the children’s oncology group CCG-1952 clinical trial, Blood 115 (2010) 2740-2748.
    [168]
    Y.H. Kim, M. Bagot, L. Pinter-Brown, et al., Mogamulizumab versus vorinostat in previously treated cutaneous T-cell lymphoma (MAVORIC): An international, open-label, randomised, controlled phase 3 trial, Lancet Oncol. 19 (2018) 1192-1204.
    [169]
    M.J. Burke, J.K. Lamba, S. Pounds, et al., A therapeutic trial of decitabine and vorinostat in combination with chemotherapy for relapsed/refractory acute lymphoblastic leukemia, Am. J. Hematol. 89 (2014) 889-895.
    [170]
    P. Chinnaiyan, S. Chowdhary, L. Potthast, et al., Phase I trial of vorinostat combined with bevacizumab and CPT-11 in recurrent glioblastoma, Neuro-oncology 14 (2012) 93-100.
    [171]
    O.A. O’Connor, S. Horwitz, T. Masszi, et al., Belinostat in patients with relapsed or refractory peripheral T-cell lymphoma: Results of the pivotal phase II BELIEF (CLN-19) study, J. Clin. Oncol. 33 (2015) 2492-2499.
    [172]
    W. Yeo, H.C. Chung, S.L. Chan, et al., Epigenetic therapy using belinostat for patients with unresectable hepatocellular carcinoma: A multicenter phase I/II study with biomarker and pharmacokinetic analysis of tumors from patients in the mayo phase II consortium and the cancer therapeutics research group, J. Clin. Oncol. 30 (2012) 3361-3367.
    [173]
    H. Fredly, H. Reikvam, B.T. Gjertsen, et al., Disease-stabilizing treatment with all-trans retinoic acid and valproic acid in acute myeloid leukemia: Serum hsp70 and hsp90 levels and serum cytokine profiles are determined by the disease, patient age, and anti-leukemic treatment, Am. J. Hematol. 87 (2012) 368-376.
    [174]
    B.E. Nelson, A.M. Tsimberidou, X. Fu, et al., A phase I trial of bevacizumab and temsirolimus in combination with valproic acid in advanced solid tumors, Oncologist 28 (2023) 1100-e1292.
    [175]
    Y. Zhang, Y. Gu, H. Ren, et al., Gut microbiome-related effects of berberine and probiotics on type 2 diabetes (the PREMOTE study), Nat. Commun. 11 (2020), 5015.
    [176]
    S.A. Harrison, P.J. Ruane, B.L. Freilich, et al., Efruxifermin in non-alcoholic steatohepatitis: A randomized, double-blind, placebo-controlled, phase 2a trial, Nat. Med. 27 (2021) 1262-1271.
    [177]
    K.H. Hsieh, Effects of PAF antagonist, BN52021, on the PAF-, methacholine-, and allergen-induced bronchoconstriction in asthmatic children, Chest 99 (1991) 877-882.
    [178]
    N. Rothammer, M.S. Woo, S. Bauer, et al., G9a dictates neuronal vulnerability to inflammatory stress via transcriptional control of ferroptosis, Sci. Adv. 8 (2022), eabm5500.
    [179]
    E.J. Daly, M.H. Trivedi, A. Janik, et al., Efficacy of esketamine nasal spray plus oral antidepressant treatment for relapse prevention in patients with treatment-resistant depression: A randomized clinical trial, JAMA Psychiatry 76 (2019) 893-903.
    [180]
    Rde S. Pereira, Regression of gastroesophageal reflux disease symptoms using dietary supplementation with melatonin, vitamins and aminoacids: Comparison with omeprazole, J. Pineal Res. 41 (2006) 195-200.
    [181]
    Z.-L. Jin, W.-Y. Gao, S.-J. Liao, et al., Paeonol inhibits the progression of intracerebral haemorrhage by mediating the HOTAIR/UPF1/ACSL4 axis, ASN Neuro 13 (2021), 17590914211010647.
    [182]
    J. Li, S.-H. Deng, J. Li, et al., Obacunone alleviates ferroptosis during lipopolysaccharide-induced acute lung injury by upregulating Nrf2-dependent antioxidant responses, Cell. Mol. Biol. Lett. 27 (2022), 29.
    [183]
    S. Feng, Y. Yuan, Z. Lin, et al., Low-dose hypomethylating agents cooperate with ferroptosis inducers to enhance ferroptosis by regulating the DNA methylation-mediated MAGEA6-AMPK-SLC7A11-GPX4 signaling pathway in acute myeloid leukemia, Exp. Hematol. Oncol. 13 (2024), 19.
    [184]
    Y. Li, K. Li, W. Zhao, et al., VPA improves ferroptosis in tubular epithelial cells after cisplatin-induced acute kidney injury, Front. Pharmacol. 14 (2023), 1147772.
    [185]
    X. Li, J. Chen, W. Feng, et al., Berberine ameliorates iron levels and ferroptosis in the brain of 3×Tg-AD mice, Phytomedicine 118 (2023), 154962.
    [186]
    A. Wu, B. Feng, J. Yu, et al., Fibroblast growth factor 21 attenuates iron overload-induced liver injury and fibrosis by inhibiting ferroptosis, Redox Biol. 46 (2021),102131.
    [187]
    J. Chen, Z. Ou, T. Gao, et al., Ginkgolide B alleviates oxidative stress and ferroptosis by inhibiting GPX4 ubiquitination to improve diabetic nephropathy, Biomed. Pharmacother. 156 (2022), 113953.
    [188]
    G.N. He, N.R. Bao, S. Wang, et al., Ketamine induces ferroptosis of liver cancer cells by targeting lncRNA PVT1/miR-214-3p/GPX4, Drug Des. Devel. Ther. 15 (2021) 3965-3978.
    [189]
    L. Ye, Y. Xu, L. Wang, et al., Downregulation of CYP2E1 is associated with poor prognosis and tumor progression of gliomas, Cancer Med. 10 (2021) 8100-8113.
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