Volume 7 Issue 4
Sep.  2021
Turn off MathJax
Article Contents
Xiaoxuan Wang, Zicheng Liu, Lijuan Ma, Haijie Yu. Ferroptosis and its emerging role in tumor[J]. Biophysics Reports, 2021, 7(4): 280-294. doi: 10.52601/bpr.2021.210010
Citation: Xiaoxuan Wang, Zicheng Liu, Lijuan Ma, Haijie Yu. Ferroptosis and its emerging role in tumor[J]. Biophysics Reports, 2021, 7(4): 280-294. doi: 10.52601/bpr.2021.210010

Ferroptosis and its emerging role in tumor

doi: 10.52601/bpr.2021.210010
Funds:  This work was supported by Faculty Research Grant Projects of Macau University of Science and Technology, Macau, China (FRG-18-002-SKL and FRG-18-003-SKL), grants from the Macau Science and Technology Development Fund, Macau, China (0020/2019/A1 and 001/2020/ALC). All authors read and approved the final manuscript. X. Wang, Z. Liu and H. Yu. established the concept and drafted the manuscript; L. Ma revised the manuscript; Z. Liu prepared the graphic works; L. Ma and H. Yu revised and approved the manuscript.
More Information
  • Corresponding author: hjyu@must.edu.mo (H. Yu)
  • Received Date: 17 April 2021
  • Accepted Date: 22 August 2021
  • Available Online: 17 September 2021
  • Publish Date: 17 September 2021
  • Ferroptosis is a novel form of programmed cell death characterized by iron-dependent lipid peroxidation accumulation. It is morphologically, biochemically, and genetically distinct from other known cell death, such as apoptosis, necrosis, and pyroptosis. Its regulatory mechanisms include iron metabolism, fatty acid metabolism, mitochondrial respiration, and antioxidative systems eliminating lipid peroxidation, such as glutathione synthesis, selenium-dependent glutathione peroxidase 4, and ubiquinone. The disruption of cellular redox systems causes damage to the cellular membrane leading to ferroptotic cell death. Recent studies have shown that numerous pathological diseases, like tumors, neurodegenerative disorders, and ischemia-reperfusion injury are associated with ferroptosis. As such, pharmacological regulation of ferroptosis either by activation or by suppression will provide a vast potential for treatments of relevant diseases. This review will discuss the advanced progress in ferroptosis and its regulatory mechanisms from both the antioxidative and oxidative sides. In addition, the roles of ferroptosis in various tumorigenesis, development, and therapeutic strategies will be addressed, particularly to chemotherapy and immunotherapy, as well as the discoveries from Traditional Chinese Medicine. This review will lead us to have a comprehensive understanding of the future exploration of ferroptosis and cancer therapy.
  • loading
  • [1]
    Alvarez SW, Sviderskiy VO, Terzi EM, Papagiannakopoulos T, Moreira AL, Adams S, Sabatini DM, Birsoy K, Possemato R (2017) NFS1 undergoes positive selection in lung tumours and protects cells from ferroptosis. Nature 551(7682): 639−643 doi: 10.1038/nature24637
    [2]
    Arensman MD, Yang XS, Leahy DM, Toral-Barza L, Mileski M, Rosfjord EC, Wang F, Deng S, Myers JS, Abraham RT, Eng CH (2019) Cystine-glutamate antiporter xCT deficiency suppresses tumor growth while preserving antitumor immunity. Proc Natl Acad Sci USA 116(19): 9533−9542 doi: 10.1073/pnas.1814932116
    [3]
    Badgley MA, Kremer DM, Maurer HC, DelGiorno KE, Lee HJ, Purohit V, Sagalovskiy IR, Ma A, Kapilian J, Firl CEM, Decker AR, Sastra SA, Palermo CF, Andrade LR, Sajjakulnukit P, Zhang L, Tolstyka ZP, Hirschhorn T, Lamb C, Liu T, Gu W, Seeley ES, Stone E, Georgiou G, Manor U, Iuga A, Wahl GM, Stockwell BR, Lyssiotis CA, Olive KP (2020) Cysteine depletion induces pancreatic tumor ferroptosis in mice. Science 368(6486): 85−89 doi: 10.1126/science.aaw9872
    [4]
    Bai T, Lei P, Zhou H, Liang R, Zhu R, Wang W, Zhou L, Sun Y (2019) Sigma-1 receptor protects against ferroptosis in hepatocellular carcinoma cells. J Cell Mol Med 23(11): 7349−7359 doi: 10.1111/jcmm.14594
    [5]
    Basit F, van Oppen LM, Schockel L, Bossenbroek HM, van Emst-de Vries SE, Hermeling JC, Grefte S, Kopitz C, Heroult M, Hgm Willems P, Koopman WJ (2017) Mitochondrial complex I inhibition triggers a mitophagy-dependent ROS increase leading to necroptosis and ferroptosis in melanoma cells. Cell Death Dis 8(3): e2716 doi: 10.1038/cddis.2017.133
    [6]
    Basuli D, Tesfay L, Deng Z, Paul B, Yamamoto Y, Ning G, Xian W, McKeon F, Lynch M, Crum CP, Hegde P, Brewer M, Wang X, Miller LD, Dyment N, Torti FM, Torti SV (2017) Iron addiction: a novel therapeutic target in ovarian cancer. Oncogene 36(29): 4089−4099 doi: 10.1038/onc.2017.11
    [7]
    Bersuker K, Hendricks JM, Li Z, Magtanong L, Ford B, Tang PH, Roberts MA, Tong B, Maimone TJ, Zoncu R, Bassik MC, Nomura DK, Dixon SJ, Olzmann JA (2019) The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis. Nature 575(7784): 688−692 doi: 10.1038/s41586-019-1705-2
    [8]
    Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6): 394−424 doi: 10.3322/caac.21492
    [9]
    Brutsch SH, Wang CC, Li L, Stender H, Neziroglu N, Richter C, Kuhn H, Borchert A (2015) Expression of inactive glutathione peroxidase 4 leads to embryonic lethality, and inactivation of the Alox15 gene does not rescue such knock-in mice. Antioxid Redox Signal 22(4): 281−293 doi: 10.1089/ars.2014.5967
    [10]
    Chen D, Fan Z, Rauh M, Buchfelder M, Eyupoglu IY, Savaskan N (2017) ATF4 promotes angiogenesis and neuronal cell death and confers ferroptosis in a xCT-dependent manner. Oncogene 36(40): 5593−5608 doi: 10.1038/onc.2017.146
    [11]
    Chen P, Wu Q, Feng J, Yan L, Sun Y, Liu S, Xiang Y, Zhang M, Pan T, Chen X, Duan T, Zhai L, Zhai B, Wang W, Zhang R, Chen B, Han X, Li Y, Chen L, Liu Y, Huang X, Jin T, Zhang W, Luo H, Chen X, Li Y, Li Q, Li G, Zhang Q, Zhuo L, Yang Z, Tang H, Xie T, Ouyang X, Sui X (2020a) Erianin, a novel dibenzyl compound in Dendrobium extract, inhibits lung cancer cell growth and migration via calcium/calmodulin-dependent ferroptosis. Signal Transduct Target Ther 5(1): 51 doi: 10.1038/s41392-020-0149-3
    [12]
    Chen PH, Wu J, Ding CC, Lin CC, Pan S, Bossa N, Xu Y, Yang WH, Mathey-Prevot B, Chi JT (2020b) Kinome screen of ferroptosis reveals a novel role of ATM in regulating iron metabolism. Cell Death Differ 27(3): 1008−1022 doi: 10.1038/s41418-019-0393-7
    [13]
    Chu B, Kon N, Chen D, Li T, Liu T, Jiang L, Song S, Tavana O, Gu W (2019) ALOX12 is required for p53-mediated tumour suppression through a distinct ferroptosis pathway. Nat Cell Biol 21(5): 579−591 doi: 10.1038/s41556-019-0305-6
    [14]
    Citron ML, Berry DA, Cirrincione C, Hudis C, Winer EP, Gradishar WJ, Davidson NE, Martino S, Livingston R, Ingle JN, Perez EA, Carpenter J, Hurd D, Holland JF, Smith BL, Sartor CI, Leung EH, Abrams J, Schilsky RL, Muss HB, Norton L (2003) Randomized trial of dose-dense versus conventionally scheduled and sequential versus concurrent combination chemotherapy as postoperative adjuvant treatment of node-positive primary breast cancer: first report of Intergroup Trial C9741/Cancer and Leukemia Group B Trial 9741. J Clin Oncol 21(8): 1431−1439 doi: 10.1200/JCO.2003.09.081
    [15]
    Crofton J (1959) Chemotherapy of pulmonary tuberculosis. Br Med J 1(5138): 1610−1614 doi: 10.1136/bmj.1.5138.1610
    [16]
    Dai E, Han L, Liu J, Xie Y, Kroemer G, Klionsky DJ, Zeh HJ, Kang R, Wang J, Tang D (2020a) Autophagy-dependent ferroptosis drives tumor-associated macrophage polarization via release and uptake of oncogenic KRAS protein. Autophagy 16(11): 2069−2083 doi: 10.1080/15548627.2020.1714209
    [17]
    Dai E, Zhang W, Cong D, Kang R, Wang J, Tang D (2020b) AIFM2 blocks ferroptosis independent of ubiquinol metabolism. Biochem Biophys Res Commun 523(4): 966−971 doi: 10.1016/j.bbrc.2020.01.066
    [18]
    Dierge E, Debock E, Guilbaud C, Corbet C, Mignolet E, Mignard L, Bastien E, Dessy C, Larondelle Y, Feron O (2021) Peroxidation of n-3 and n-6 polyunsaturated fatty acids in the acidic tumor environment leads to ferroptosis-mediated anticancer effects. Cell Metab 33(8): 1701−1715 doi: 10.1016/j.cmet.2021.05.016
    [19]
    Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, Morrison B, 3 rd, Stockwell BR (2012) Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149(5): 1060−1072 doi: 10.1016/j.cell.2012.03.042
    [20]
    Dixon SJ, Winter GE, Musavi LS, Lee ED, Snijder B, Rebsamen M, Superti-Furga G, Stockwell BR (2015) Human haploid cell genetics reveals roles for lipid metabolism genes in nonapoptotic cell death. ACS Chem Biol 10(7): 1604−1609 doi: 10.1021/acschembio.5b00245
    [21]
    Doll S, Freitas FP, Shah R, Aldrovandi M, da Silva MC, Ingold I, Goya Grocin A, Xavier da Silva TN, Panzilius E, Scheel CH, Mourão A, Buday K, Sato M, Wanninger J, Vignane T, Mohana V, Rehberg M, Flatley A, Schepers A, Kurz A, White D, Sauer M, Sattler M, Tate EW, Schmitz W, Schulze A, O'Donnell V, Proneth B, Popowicz GM, Pratt DA, Angeli JPF, Conrad M (2019) FSP1 is a glutathione-independent ferroptosis suppressor. Nature 575(7784): 693−698 doi: 10.1038/s41586-019-1707-0
    [22]
    Doll S, Proneth B, Tyurina YY, Panzilius E, Kobayashi S, Ingold I, Irmler M, Beckers J, Aichler M, Walch A, Prokisch H, Trümbach D, Mao G, Qu F, Bayir H, Füllekrug J, Scheel CH, Wurst W, Schick JA, Kagan VE, Angeli JP, Conrad M (2017) ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat Chem Biol 13(1): 91−98 doi: 10.1038/nchembio.2239
    [23]
    Dolma S, Lessnick SL, Hahn WC, Stockwell BR (2003) Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell 3(3): 285−296 doi: 10.1016/S1535-6108(03)00050-3
    [24]
    Eaton JK, Furst L, Ruberto RA, Moosmayer D, Hilpmann A, Ryan MJ, Zimmermann K, Cai LL, Niehues M, Badock V, Kramm A, Chen S, Hillig RC, Clemons PA, Gradl S, Montagnon C, Lazarski KE, Christian S, Bajrami B, Neuhaus R, Eheim AL, Viswanathan VS, Schreiber SL (2020) Selective covalent targeting of GPX4 using masked nitrile-oxide electrophiles. Nat Chem Biol 16(5): 497−506 doi: 10.1038/s41589-020-0501-5
    [25]
    Efimova I, Catanzaro E, Van der Meeren L, Turubanova VD, Hammad H, Mishchenko TA, Vedunova MV, Fimognari C, Bachert C, Coppieters F, Lefever S, Skirtach AG, Krysko O, Krysko DV (2020) Vaccination with early ferroptotic cancer cells induces efficient antitumor immunity. J Immunother Cancer 8(2): e001369 doi: 10.1136/jitc-2020-001369
    [26]
    Eling N, Reuter L, Hazin J, Hamacher-Brady A, Brady NR (2015) Identification of artesunate as a specific activator of ferroptosis in pancreatic cancer cells. Oncoscience 2(5): 517−532 doi: 10.18632/oncoscience.160
    [27]
    Fan Z, Wirth AK, Chen D, Wruck CJ, Rauh M, Buchfelder M, Savaskan N (2017) Nrf2-Keap1 pathway promotes cell proliferation and diminishes ferroptosis. Oncogenesis 6(8): e371 doi: 10.1038/oncsis.2017.65
    [28]
    Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC (1998) Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci USA 95(3): 1148−1153 doi: 10.1073/pnas.95.3.1148
    [29]
    Frazer DM, Anderson GJ (2014) The regulation of iron transport. Biofactors 40(2): 206−214 doi: 10.1002/biof.1148
    [30]
    Friedmann Angeli JP, Schneider M, Proneth B, Tyurina YY, Tyurin VA, Hammond VJ, Herbach N, Aichler M, Walch A, Eggenhofer E, Basavarajappa D, Radmark O, Kobayashi S, Seibt T, Beck H, Neff F, Esposito I, Wanke R, Forster H, Yefremova O, Heinrichmeyer M, Bornkamm GW, Geissler EK, Thomas SB, Stockwell BR, O'Donnell VB, Kagan VE, Schick JA, Conrad M (2014) Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat Cell Biol 16(12): 1180−1191 doi: 10.1038/ncb3064
    [31]
    Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW, Annicchiarico-Petruzzelli M, Antonov AV, Arama E, Baehrecke EH, Barlev NA, Bazan NG, Bernassola F, Bertrand MJM, Bianchi K, Blagosklonny MV, Blomgren K, Borner C, Boya P, Brenner C, Campanella M, Candi E, Carmona-Gutierrez D, Cecconi F, Chan FKM, Chandel NS, Cheng EH, Chipuk JE, Cidlowski JA, Ciechanover A, Cohen GM, Conrad M, Cubillos-Ruiz JR, Czabotar PE, D’Angiolella V, Dawson TM, Dawson VL, De Laurenzi V, De Maria R, Debatin K-M, DeBerardinis RJ, Deshmukh M, Di Daniele N, Di Virgilio F, Dixit VM, Dixon SJ, Duckett CS, Dynlacht BD, El-Deiry WS, Elrod JW, Fimia GM, Fulda S, García-Sáez AJ, Garg AD, Garrido C, Gavathiotis E, Golstein P, Gottlieb E, Green DR, Greene LA, Gronemeyer H, Gross A, Hajnoczky G, Hardwick JM, Harris IS, Hengartner MO, Hetz C, Ichijo H, Jäättelä M, Joseph B, Jost PJ, Juin PP, Kaiser WJ, Karin M, Kaufmann T, Kepp O, Kimchi A, Kitsis RN, Klionsky DJ, Knight RA, Kumar S, Lee SW, Lemasters JJ, Levine B, Linkermann A, Lipton SA, Lockshin RA, López-Otín C, Lowe SW, Luedde T, Lugli E, MacFarlane M, Madeo F, Malewicz M, Malorni W, Manic G, Marine J-C, Martin SJ, Martinou J-C, Medema JP, Mehlen P, Meier P, Melino S, Miao EA, Molkentin JD, Moll UM, Muñoz-Pinedo C, Nagata S, Nuñez G, Oberst A, Oren M, Overholtzer M, Pagano M, Panaretakis T, Pasparakis M, Penninger JM, Pereira DM, Pervaiz S, Peter ME, Piacentini M, Pinton P, Prehn JHM, Puthalakath H, Rabinovich GA, Rehm M, Rizzuto R, Rodrigues CMP, Rubinsztein DC, Rudel T, Ryan KM, Sayan E, Scorrano L, Shao F, Shi Y, Silke J, Simon H-U, Sistigu A, Stockwell BR, Strasser A, Szabadkai G, Tait SWG, Tang D, Tavernarakis N, Thorburn A, Tsujimoto Y, Turk B, Vanden Berghe T, Vandenabeele P, Vander Heiden MG, Villunger A, Virgin HW, Vousden KH, Vucic D, Wagner EF, Walczak H, Wallach D, Wang Y, Wells JA, Wood W, Yuan J, Zakeri Z, Zhivotovsky B, Zitvogel L, Melino G, Kroemer G (2018) Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ 25(3): 486−541 doi: 10.1038/s41418-017-0012-4
    [32]
    Gao M, Monian P, Quadri N, Ramasamy R, Jiang X (2015) Glutaminolysis and transferrin regulate ferroptosis. Mol Cell 59(2): 298−308 doi: 10.1016/j.molcel.2015.06.011
    [33]
    Gong M, Hay S, Marshall KR, Munro AW, Scrutton NS (2007) DNA binding suppresses human AIF-M2 activity and provides a connection between redox chemistry, reactive oxygen species, and apoptosis. J Biol Chem 282(41): 30331−30340 doi: 10.1074/jbc.M703713200
    [34]
    Greenshields AL, Shepherd TG, Hoskin DW (2017) Contribution of reactive oxygen species to ovarian cancer cell growth arrest and killing by the anti-malarial drug artesunate. Mol Carcinog 56(1): 75−93 doi: 10.1002/mc.22474
    [35]
    Guo J, Xu B, Han Q, Zhou H, Xia Y, Gong C, Dai X, Li Z, Wu G (2018) Ferroptosis: A novel anti-tumor action for cisplatin. Cancer Res Treat 50(2): 445−460 doi: 10.4143/crt.2016.572
    [36]
    Hangauer MJ, Viswanathan VS, Ryan MJ, Bole D, Eaton JK, Matov A, Galeas J, Dhruv HD, Berens ME, Schreiber SL, McCormick F, McManus MT (2017) Drug-tolerant persister cancer cells are vulnerable to GPX4 inhibition. Nature 551(7679): 247−250 doi: 10.1038/nature24297
    [37]
    Hao S, Yu J, He W, Huang Q, Zhao Y, Liang B, Zhang S, Wen Z, Dong S, Rao J, Liao W, Shi M (2017) Cysteine dioxygenase 1 mediates erastin-induced ferroptosis in human gastric cancer cells. Neoplasia 19(12): 1022−1032 doi: 10.1016/j.neo.2017.10.005
    [38]
    Hasegawa M, Takahashi H, Rajabi H, Alam M, Suzuki Y, Yin L, Tagde A, Maeda T, Hiraki M, Sukhatme VP, Kufe D (2016) Functional interactions of the cystine/glutamate antiporter, CD44v and MUC1-C oncoprotein in triple-negative breast cancer cells. Oncotarget 7(11): 11756−11769 doi: 10.18632/oncotarget.7598
    [39]
    Hellman NE, Gitlin JD (2002) Ceruloplasmin metabolism and function. Annu Rev Nutr 22: 439−458 doi: 10.1146/annurev.nutr.22.012502.114457
    [40]
    Hryniuk W, Bush H (1984) The importance of dose intensity in chemotherapy of metastatic breast cancer. J Clin Oncol 2(11): 1281−1288 doi: 10.1200/JCO.1984.2.11.1281
    [41]
    Hvidberg V, Maniecki MB, Jacobsen C, Hojrup P, Moller HJ, Moestrup SK (2005) Identification of the receptor scavenging hemopexin-heme complexes. Blood 106(7): 2572−2579 doi: 10.1182/blood-2005-03-1185
    [42]
    Imai H, Matsuoka M, Kumagai T, Sakamoto T, Koumura T (2017) Lipid peroxidation-dependent cell death regulated by GPx4 and ferroptosis. Curr Top Microbiol Immunol 403: 143−170
    [43]
    Ingold I, Berndt C, Schmitt S, Doll S, Poschmann G, Buday K, Roveri A, Peng X, Porto Freitas F, Seibt T, Mehr L, Aichler M, Walch A, Lamp D, Jastroch M, Miyamoto S, Wurst W, Ursini F, Arner ESJ, Fradejas-Villar N, Schweizer U, Zischka H, Friedmann Angeli JP, Conrad M (2018) Selenium utilization by GPX4 is required to prevent hydroperoxide-induced ferroptosis. Cell 172(3): 409−422 doi: 10.1016/j.cell.2017.11.048
    [44]
    Jia M, Qin D, Zhao C, Chai L, Yu Z, Wang W, Tong L, Lv L, Wang Y, Rehwinkel J, Yu J, Zhao W (2020) Redox homeostasis maintained by GPX4 facilitates STING activation. Nat Immunol 21(7): 727−735 doi: 10.1038/s41590-020-0699-0
    [45]
    Jiang L, Kon N, Li T, Wang SJ, Su T, Hibshoosh H, Baer R, Gu W (2015) Ferroptosis as a p53-mediated activity during tumour suppression. Nature 520(7545): 57−62 doi: 10.1038/nature14344
    [46]
    Jiang X, Stockwell BR, Conrad M (2021) Ferroptosis: mechanisms, biology and role in disease. Nat Rev Mol Cell Biol 22(4): 266−282 doi: 10.1038/s41580-020-00324-8
    [47]
    Jorgensen I, Miao EA (2015) Pyroptotic cell death defends against intracellular pathogens. Immunol Rev 265(1): 130−142 doi: 10.1111/imr.12287
    [48]
    Kagan VE, Mao G, Qu F, Angeli JP, Doll S, Croix CS, Dar HH, Liu B, Tyurin VA, Ritov VB, Kapralov AA, Amoscato AA, Jiang J, Anthonymuthu T, Mohammadyani D, Yang Q, Proneth B, Klein-Seetharaman J, Watkins S, Bahar I, Greenberger J, Mallampalli RK, Stockwell BR, Tyurina YY, Conrad M, Bayir H (2017) Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat Chem Biol 13(1): 81−90 doi: 10.1038/nchembio.2238
    [49]
    Kasukabe T, Honma Y, Okabe-Kado J, Higuchi Y, Kato N, Kumakura S (2016) Combined treatment with cotylenin A and phenethyl isothiocyanate induces strong antitumor activity mainly through the induction of ferroptotic cell death in human pancreatic cancer cells. Oncol Rep 36(2): 968−976 doi: 10.3892/or.2016.4867
    [50]
    Khoo KH, Verma CS, Lane DP (2014) Drugging the p53 pathway: understanding the route to clinical efficacy. Nat Rev Drug Discov 13(3): 217−236 doi: 10.1038/nrd4236
    [51]
    Kim EH, Shin D, Lee J, Jung AR, Roh JL (2018) CISD2 inhibition overcomes resistance to sulfasalazine-induced ferroptotic cell death in head and neck cancer. Cancer Lett 432: 180−190 doi: 10.1016/j.canlet.2018.06.018
    [52]
    Kim SE, Zhang L, Ma K, Riegman M, Chen F, Ingold I, Conrad M, Turker MZ, Gao M, Jiang X, Monette S, Pauliah M, Gonen M, Zanzonico P, Quinn T, Wiesner U, Bradbury MS, Overholtzer M (2016) Ultrasmall nanoparticles induce ferroptosis in nutrient-deprived cancer cells and suppress tumour growth. Nat Nanotechnol 11(11): 977−985 doi: 10.1038/nnano.2016.164
    [53]
    Kinowaki Y, Kurata M, Ishibashi S, Ikeda M, Tatsuzawa A, Yamamoto M, Miura O, Kitagawa M, Yamamoto K (2018) Glutathione peroxidase 4 overexpression inhibits ROS-induced cell death in diffuse large B-cell lymphoma. Lab Invest 98(5): 609−619 doi: 10.1038/s41374-017-0008-1
    [54]
    Koppula P, Zhang Y, Zhuang L, Gan B (2018) Amino acid transporter SLC7A11/xCT at the crossroads of regulating redox homeostasis and nutrient dependency of cancer. Cancer Commun (Lond) 38(1): 12 doi: 10.1186/s40880-018-0288-x
    [55]
    Kraft VAN, Bezjian CT, Pfeiffer S, Ringelstetter L, Muller C, Zandkarimi F, Merl-Pham J, Bao X, Anastasov N, Kossl J, Brandner S, Daniels JD, Schmitt-Kopplin P, Hauck SM, Stockwell BR, Hadian K, Schick JA (2020) GTP cyclohydrolase 1/tetrahydrobiopterin counteract ferroptosis through lipid remodeling. ACS Cent Sci 6(1): 41−53 doi: 10.1021/acscentsci.9b01063
    [56]
    Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigó R, Gladyshev VN (2003) Characterization of mammalian selenoproteomes. Science 300(5624): 1439−1443 doi: 10.1126/science.1083516
    [57]
    Kwiecien S, Jasnos K, Magierowski M, Sliwowski Z, Pajdo R, Brzozowski B, Mach T, Wojcik D, Brzozowski T (2014) Lipid peroxidation, reactive oxygen species and antioxidative factors in the pathogenesis of gastric mucosal lesions and mechanism of protection against oxidative stress-induced gastric injury. J Physiol Pharmacol 65(5): 613−622
    [58]
    Kwon MY, Park E, Lee SJ, Chung SW (2015) Heme oxygenase-1 accelerates erastin-induced ferroptotic cell death. Oncotarget 6(27): 24393−24403 doi: 10.18632/oncotarget.5162
    [59]
    Lee H, Zandkarimi F, Zhang Y, Meena JK, Kim J, Zhuang L, Tyagi S, Ma L, Westbrook TF, Steinberg GR, Nakada D, Stockwell BR, Gan B (2020a) Energy-stress-mediated AMPK activation inhibits ferroptosis. Nat Cell Biol 22(2): 225−234 doi: 10.1038/s41556-020-0461-8
    [60]
    Lee J, You JH, Shin D, Roh JL (2020b) Inhibition of glutaredoxin 5 predisposes cisplatin-resistant head and neck cancer cells to ferroptosis. Theranostics 10(17): 7775−7786 doi: 10.7150/thno.46903
    [61]
    Li J, Cao F, Yin HL, Huang ZJ, Lin ZT, Mao N, Sun B, Wang G (2020) Ferroptosis: past, present and future. Cell Death Dis 11(2): 88 doi: 10.1038/s41419-020-2298-2
    [62]
    Lin R, Zhang Z, Chen L, Zhou Y, Zou P, Feng C, Wang L, Liang G (2016) Dihydroartemisinin (DHA) induces ferroptosis and causes cell cycle arrest in head and neck carcinoma cells. Cancer Lett 381(1): 165−175 doi: 10.1016/j.canlet.2016.07.033
    [63]
    Lin W, Wang C, Liu G, Bi C, Wang X, Zhou Q, Jin H (2020) SLC7A11/xCT in cancer: biological functions and therapeutic implications. Am J Cancer Res 10(10): 3106−3126
    [64]
    Liou GY, Storz P (2010) Reactive oxygen species in cancer. Free Radic Res 44(5): 479−496 doi: 10.3109/10715761003667554
    [65]
    Liu B, Zhao C, Li H, Chen X, Ding Y, Xu S (2018) Puerarin protects against heart failure induced by pressure overload through mitigation of ferroptosis. Biochem Biophys Res Commun 497(1): 233−240 doi: 10.1016/j.bbrc.2018.02.061
    [66]
    Louandre C, Marcq I, Bouhlal H, Lachaier E, Godin C, Saidak Z, Francois C, Chatelain D, Debuysscher V, Barbare JC, Chauffert B, Galmiche A (2015) The retinoblastoma (Rb) protein regulates ferroptosis induced by sorafenib in human hepatocellular carcinoma cells. Cancer Lett 356(2 Pt B): 971−977
    [67]
    Luo M, Wu L, Zhang K, Wang H, Zhang T, Gutierrez L, O'Connell D, Zhang P, Li Y, Gao T, Ren W, Yang Y (2018) miR-137 regulates ferroptosis by targeting glutamine transporter SLC1A5 in melanoma. Cell Death Differ 25(8): 1457−1472 doi: 10.1038/s41418-017-0053-8
    [68]
    Ma S, Henson ES, Chen Y, Gibson SB (2016) Ferroptosis is induced following siramesine and lapatinib treatment of breast cancer cells. Cell Death Dis 7: e2307 doi: 10.1038/cddis.2016.208
    [69]
    Magtanong L, Ko PJ, To M, Cao JY, Forcina GC, Tarangelo A, Ward CC, Cho K, Patti GJ, Nomura DK, Olzmann JA, Dixon SJ (2019) Exogenous monounsaturated fatty acids promote a ferroptosis-resistant cell state. Cell Chem Biol 26(3): 420−432 doi: 10.1016/j.chembiol.2018.11.016
    [70]
    Mao C, Liu X, Zhang Y, Lei G, Yan Y, Lee H, Koppula P, Wu S, Zhuang L, Fang B, Poyurovsky MV, Olszewski K, Gan B (2021) DHODH-mediated ferroptosis defence is a targetable vulnerability in cancer. Nature 593(7860): 586−590 doi: 10.1038/s41586-021-03539-7
    [71]
    Matsushita M, Freigang S, Schneider C, Conrad M, Bornkamm GW, Kopf M (2015) T cell lipid peroxidation induces ferroptosis and prevents immunity to infection. J Exp Med 212(4): 555−568 doi: 10.1084/jem.20140857
    [72]
    Miess H, Dankworth B, Gouw AM, Rosenfeldt M, Schmitz W, Jiang M, Saunders B, Howell M, Downward J, Felsher DW, Peck B, Schulze A (2018) The glutathione redox system is essential to prevent ferroptosis caused by impaired lipid metabolism in clear cell renal cell carcinoma. Oncogene 37(40): 5435−5450 doi: 10.1038/s41388-018-0315-z
    [73]
    Nguyen HP, Yi D, Lin F, Viscarra JA, Tabuchi C, Ngo K, Shin G, Lee AY, Wang Y, Sul HS (2020) Aifm2, a NADH oxidase, supports robust glycolysis and is required for cold- and diet-induced thermogenesis. Mol Cell 77(3): 600−617 doi: 10.1016/j.molcel.2019.12.002
    [74]
    Nie J, Lin B, Zhou M, Wu L, Zheng T (2018) Role of ferroptosis in hepatocellular carcinoma. J Cancer Res Clin Oncol 144(12): 2329−2337 doi: 10.1007/s00432-018-2740-3
    [75]
    O'Toole SA, Beith JM, Millar EK, West R, McLean A, Cazet A, Swarbrick A, Oakes SR (2013) Therapeutic targets in triple negative breast cancer. J Clin Pathol 66(6): 530−542 doi: 10.1136/jclinpath-2012-201361
    [76]
    Ohgami RS, Campagna DR, McDonald A, Fleming MD (2006) The Steap proteins are metalloreductases. Blood 108(4): 1388−1394 doi: 10.1182/blood-2006-02-003681
    [77]
    Ou W, Mulik RS, Anwar A, McDonald JG, He X, Corbin IR (2017) Low-density lipoprotein docosahexaenoic acid nanoparticles induce ferroptotic cell death in hepatocellular carcinoma. Free Radic Biol Med 112: 597−607 doi: 10.1016/j.freeradbiomed.2017.09.002
    [78]
    Ou Y, Wang SJ, Li D, Chu B, Gu W (2016) Activation of SAT1 engages polyamine metabolism with p53-mediated ferroptotic responses. Proc Natl Acad Sci USA 113(44): E6806−E6812 doi: 10.1073/pnas.1607152113
    [79]
    Parzych KR, Klionsky DJ (2014) An overview of autophagy: morphology, mechanism, and regulation. Antioxid Redox Signal 20(3): 460−473 doi: 10.1089/ars.2013.5371
    [80]
    Probst L, Dachert J, Schenk B, Fulda S (2017) Lipoxygenase inhibitors protect acute lymphoblastic leukemia cells from ferroptotic cell death. Biochem Pharmacol 140: 41−52 doi: 10.1016/j.bcp.2017.06.112
    [81]
    Roh JL, Kim EH, Jang H, Shin D (2017) Nrf2 inhibition reverses the resistance of cisplatin-resistant head and neck cancer cells to artesunate-induced ferroptosis. Redox Biol 11: 254−262 doi: 10.1016/j.redox.2016.12.010
    [82]
    Roh JL, Kim EH, Jang HJ, Park JY, Shin D (2016) Induction of ferroptotic cell death for overcoming cisplatin resistance of head and neck cancer. Cancer Lett 381(1): 96−103 doi: 10.1016/j.canlet.2016.07.035
    [83]
    Sato H, Tamba M, Ishii T, Bannai S (1999) Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem 274(17): 11455−11458 doi: 10.1074/jbc.274.17.11455
    [84]
    Sato M, Kusumi R, Hamashima S, Kobayashi S, Sasaki S, Komiyama Y, Izumikawa T, Conrad M, Bannai S, Sato H (2018a) The ferroptosis inducer erastin irreversibly inhibits system x(c)- and synergizes with cisplatin to increase cisplatin's cytotoxicity in cancer cells. Sci Rep 8(1): 968 doi: 10.1038/s41598-018-19213-4
    [85]
    Shah R, Shchepinov MS, Pratt DA (2018) Resolving the role of lipoxygenases in the initiation and execution of ferroptosis. ACS Cent Sci 4(3): 387−396 doi: 10.1021/acscentsci.7b00589
    [86]
    Shang Y, Luo M, Yao F, Wang S, Yuan Z, Yang Y (2020) Ceruloplasmin suppresses ferroptosis by regulating iron homeostasis in hepatocellular carcinoma cells. Cell Signal 72: 109633 doi: 10.1016/j.cellsig.2020.109633
    [87]
    Shimada K, Skouta R, Kaplan A, Yang WS, Hayano M, Dixon SJ, Brown LM, Valenzuela CA, Wolpaw AJ, Stockwell BR (2016) Global survey of cell death mechanisms reveals metabolic regulation of ferroptosis. Nat Chem Biol 12(7): 497−503 doi: 10.1038/nchembio.2079
    [88]
    Shin D, Kim EH, Lee J, Roh JL (2018) Nrf2 inhibition reverses resistance to GPX4 inhibitor-induced ferroptosis in head and neck cancer. Free Radic Biol Med 129: 454−462 doi: 10.1016/j.freeradbiomed.2018.10.426
    [89]
    Siegel RL, Miller KD, Jemal A (2016) Cancer statistics, 2016. CA Cancer J Clin 66(1): 7−30 doi: 10.3322/caac.21332
    [90]
    Siegel RL, Miller KD, Jemal A (2019) Cancer statistics, 2019. CA Cancer J Clin 69(1): 7−34 doi: 10.3322/caac.21551
    [91]
    Song X, Wang X, Liu Z, Yu Z (2020) Role of GPX4-mediated ferroptosis in the sensitivity of triple negative breast cancer cells to gefitinib. Front Oncol 10: 597434 doi: 10.3389/fonc.2020.597434
    [92]
    Soula M, Weber RA, Zilka O, Alwaseem H, La K, Yen F, Molina H, Garcia-Bermudez J, Pratt DA, Birsoy K (2020) Metabolic determinants of cancer cell sensitivity to canonical ferroptosis inducers. Nat Chem Biol 16(12): 1351−1360 doi: 10.1038/s41589-020-0613-y
    [93]
    Stockwell BR, Friedmann Angeli JP, Bayir H, Bush AI, Conrad M, Dixon SJ, Fulda S, Gascón S, Hatzios SK, Kagan VE, Noel K, Jiang X, Linkermann A, Murphy ME, Overholtzer M, Oyagi A, Pagnussat GC, Park J, Ran Q, Rosenfeld CS, Salnikow K, Tang D, Torti FM, Torti SV, Toyokuni S, Woerpel KA, Zhang DD (2017) Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell 171(2): 273−285 doi: 10.1016/j.cell.2017.09.021
    [94]
    Sui X, Zhang R, Liu S, Duan T, Zhai L, Zhang M, Han X, Xiang Y, Huang X, Lin H, Xie T (2018) RSL3 drives ferroptosis through GPX4 inactivation and ROS production in colorectal cancer. Front Pharmacol 9: 1371 doi: 10.3389/fphar.2018.01371
    [95]
    Tarangelo A, Magtanong L, Bieging-Rolett KT, Li Y, Ye J, Attardi LD, Dixon SJ (2018) p53 suppresses metabolic stress-induced ferroptosis in cancer cells. Cell Rep 22(3): 569−575 doi: 10.1016/j.celrep.2017.12.077
    [96]
    Tesfay L, Paul BT, Konstorum A, Deng Z, Cox AO, Lee J, Furdui CM, Hegde P, Torti FM, Torti SV (2019) Stearoyl-CoA desaturase 1 protects ovarian cancer cells from ferroptotic cell death. Cancer Res 79(20): 5355−5366 doi: 10.1158/0008-5472.CAN-19-0369
    [97]
    Timmerman LA, Holton T, Yuneva M, Louie RJ, Padro M, Daemen A, Hu M, Chan DA, Ethier SP, van 't Veer LJ, Polyak K, McCormick F, Gray JW (2013) Glutamine sensitivity analysis identifies the xCT antiporter as a common triple-negative breast tumor therapeutic target. Cancer Cell 24(4): 450−465 doi: 10.1016/j.ccr.2013.08.020
    [98]
    Tsoi J, Robert L, Paraiso K, Galvan C, Sheu KM, Lay J, Wong DJL, Atefi M, Shirazi R, Wang X, Braas D, Grasso CS, Palaskas N, Ribas A, Graeber TG (2018) Multi-stage differentiation defines melanoma subtypes with differential vulnerability to drug-induced iron-dependent oxidative stress. Cancer Cell 33(5): 890−904 doi: 10.1016/j.ccell.2018.03.017
    [99]
    Venkatesh D, O'Brien NA, Zandkarimi F, Tong DR, Stokes ME, Dunn DE, Kengmana ES, Aron AT, Klein AM, Csuka JM, Moon SH, Conrad M, Chang CJ, Lo DC, D'Alessandro A, Prives C, Stockwell BR (2020) MDM2 and MDMX promote ferroptosis by PPARalpha-mediated lipid remodeling. Genes Dev 34(7-8): 526−543 doi: 10.1101/gad.334219.119
    [100]
    Viswanathan VS, Ryan MJ, Dhruv HD, Gill S, Eichhoff OM, Seashore-Ludlow B, Kaffenberger SD, Eaton JK, Shimada K, Aguirre AJ, Viswanathan SR, Chattopadhyay S, Tamayo P, Yang WS, Rees MG, Chen S, Boskovic ZV, Javaid S, Huang C, Wu X, Tseng YY, Roider EM, Gao D, Cleary JM, Wolpin BM, Mesirov JP, Haber DA, Engelman JA, Boehm JS, Kotz JD, Hon CS, Chen Y, Hahn WC, Levesque MP, Doench JG, Berens ME, Shamji AF, Clemons PA, Stockwell BR, Schreiber SL (2017) Dependency of a therapy-resistant state of cancer cells on a lipid peroxidase pathway. Nature 547(7664): 453−457 doi: 10.1038/nature23007
    [101]
    Wang L, Liu Y, Du T, Yang H, Lei L, Guo M, Ding HF, Zhang J, Wang H, Chen X, Yan C (2020) ATF3 promotes erastin-induced ferroptosis by suppressing system Xc(.). Cell Death Differ 27(2): 662−675 doi: 10.1038/s41418-019-0380-z
    [102]
    Warner GJ, Berry MJ, Moustafa ME, Carlson BA, Hatfield DL, Faust JR (2000) Inhibition of selenoprotein synthesis by selenocysteine tRNA[Ser]Sec lacking isopentenyladenosine. J Biol Chem 275(36): 28110−28119 doi: 10.1074/jbc.M001280200
    [103]
    Weiwer M, Bittker JA, Lewis TA, Shimada K, Yang WS, MacPherson L, Dandapani S, Palmer M, Stockwell BR, Schreiber SL, Munoz B (2012) Development of small-molecule probes that selectively kill cells induced to express mutant RAS. Bioorg Med Chem Lett 22(4): 1822−1826 doi: 10.1016/j.bmcl.2011.09.047
    [104]
    Wen Q, Liu J, Kang R, Zhou B, Tang D (2019) The release and activity of HMGB1 in ferroptosis. Biochem Biophys Res Commun 510(2): 278−283 doi: 10.1016/j.bbrc.2019.01.090
    [105]
    Wenzel SE, Tyurina YY, Zhao J, St Croix CM, Dar HH, Mao G, Tyurin VA, Anthonymuthu TS, Kapralov AA, Amoscato AA, Mikulska-Ruminska K, Shrivastava IH, Kenny EM, Yang Q, Rosenbaum JC, Sparvero LJ, Emlet DR, Wen X, Minami Y, Qu F, Watkins SC, Holman TR, VanDemark AP, Kellum JA, Bahar I, Bayır H, Kagan VE (2017) PEBP1 wardens ferroptosis by enabling lipoxygenase generation of lipid death signals. Cell 171(3): 628−641 doi: 10.1016/j.cell.2017.09.044
    [106]
    Wohlhieter CA, Richards AL, Uddin F, Hulton CH, Quintanal-Villalonga A, Martin A, de Stanchina E, Bhanot U, Asher M, Shah NS, Hayatt O, Buonocore DJ, Rekhtman N, Shen R, Arbour KC, Donoghue M, Poirier JT, Sen T, Rudin CM (2020) Concurrent mutations in STK11 and KEAP1 promote ferroptosis protection and SCD1 dependence in lung cancer. Cell Rep 33(9): 108444 doi: 10.1016/j.celrep.2020.108444
    [107]
    Wong RS (2011) Apoptosis in cancer: from pathogenesis to treatment. J Exp Clin Cancer Res 30: 87 doi: 10.1186/1756-9966-30-87
    [108]
    Woo JH, Shimoni Y, Yang WS, Subramaniam P, Iyer A, Nicoletti P, Rodriguez Martinez M, Lopez G, Mattioli M, Realubit R, Karan C, Stockwell BR, Bansal M, Califano A (2015) Elucidating compound mechanism of action by network perturbation analysis. Cell 162(2): 441−451 doi: 10.1016/j.cell.2015.05.056
    [109]
    Xie Y, Hou W, Song X, Yu Y, Huang J, Sun X, Kang R, Tang D (2016) Ferroptosis: process and function. Cell Death Differ 23(3): 369−379 doi: 10.1038/cdd.2015.158
    [110]
    Xie Y, Zhu S, Song X, Sun X, Fan Y, Liu J, Zhong M, Yuan H, Zhang L, Billiar TR, Lotze MT, Zeh HJ, 3 rd, Kang R, Kroemer G, Tang D (2017) The tumor suppressor p53 limits ferroptosis by blocking DPP4 activity. Cell Rep 20(7): 1692−1704 doi: 10.1016/j.celrep.2017.07.055
    [111]
    Yagoda N, von Rechenberg M, Zaganjor E, Bauer AJ, Yang WS, Fridman DJ, Wolpaw AJ, Smukste I, Peltier JM, Boniface JJ, Smith R, Lessnick SL, Sahasrabudhe S, Stockwell BR (2007) RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447(7146): 864−868
    [112]
    Yamaguchi Y, Kasukabe T, Kumakura S (2018) Piperlongumine rapidly induces the death of human pancreatic cancer cells mainly through the induction of ferroptosis. Int J Oncol 52(3): 1011−1022
    [113]
    Yanatori I, Kishi F (2019) DMT1 and iron transport. Free Radic Biol Med 133: 55−63 doi: 10.1016/j.freeradbiomed.2018.07.020
    [114]
    Yang WH, Ding CC, Sun T, Rupprecht G, Lin CC, Hsu D, Chi JT (2019) The Hippo Pathway effector TAZ regulates ferroptosis in renal cell carcinoma. Cell Rep 28(10): 2501−2508 doi: 10.1016/j.celrep.2019.07.107
    [115]
    Yang WS, Kim KJ, Gaschler MM, Patel M, Shchepinov MS, Stockwell BR (2016) Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc Natl Acad Sci USA 113(34): E4966−4975 doi: 10.1073/pnas.1603244113
    [116]
    Yang WS, SriRamaratnam R, Welsch ME, Shimada K, Skouta R, Viswanathan VS, Cheah JH, Clemons PA, Shamji AF, Clish CB, Brown LM, Girotti AW, Cornish VW, Schreiber SL, Stockwell BR (2014) Regulation of ferroptotic cancer cell death by GPX4. Cell 156(1-2): 317−331 doi: 10.1016/j.cell.2013.12.010
    [117]
    Yang WS, Stockwell BR (2008) Synthetic lethal screening identifies compounds activating iron-dependent, nonapoptotic cell death in oncogenic-RAS-harboring cancer cells. Chem Biol 15(3): 234−245 doi: 10.1016/j.chembiol.2008.02.010
    [118]
    Yang Y, Luo M, Zhang K, Zhang J, Gao T, Connell DO, Yao F, Mu C, Cai B, Shang Y, Chen W (2020) Nedd4 ubiquitylates VDAC2/3 to suppress erastin-induced ferroptosis in melanoma. Nat Commun 11(1): 433 doi: 10.1038/s41467-020-14324-x
    [119]
    Yehuda S, Rabinovitz S, Carasso RL, Mostofsky DI (2002) The role of polyunsaturated fatty acids in restoring the aging neuronal membrane. Neurobiol Aging 23(5): 843−853 doi: 10.1016/S0197-4580(02)00074-X
    [120]
    Yoo SE, Chen L, Na R, Liu Y, Rios C, Van Remmen H, Richardson A, Ran Q (2012) Gpx4 ablation in adult mice results in a lethal phenotype accompanied by neuronal loss in brain. Free Radic Biol Med 52(9): 1820−1827 doi: 10.1016/j.freeradbiomed.2012.02.043
    [121]
    Yu B, Choi B, Li W, Kim DH (2020a) Magnetic field boosted ferroptosis-like cell death and responsive MRI using hybrid vesicles for cancer immunotherapy. Nat Commun 11(1): 3637 doi: 10.1038/s41467-020-17380-5
    [122]
    Yu Y, Jiang L, Wang H, Shen Z, Cheng Q, Zhang P, Wang J, Wu Q, Fang X, Duan L, Wang S, Wang K, An P, Shao T, Chung RT, Zheng S, Min J, Wang F (2020b) Hepatic transferrin plays a role in systemic iron homeostasis and liver ferroptosis. Blood 136(6): 726−739 doi: 10.1182/blood.2019002907
    [123]
    Zhang H, Deng T, Liu R, Ning T, Yang H, Liu D, Zhang Q, Lin D, Ge S, Bai M, Wang X, Zhang L, Li H, Yang Y, Ji Z, Wang H, Ying G, Ba Y (2020) CAF secreted miR-522 suppresses ferroptosis and promotes acquired chemo-resistance in gastric cancer. Mol Cancer 19(1): 43 doi: 10.1186/s12943-020-01168-8
    [124]
    Zhang K, Wu L, Zhang P, Luo M, Du J, Gao T, O'Connell D, Wang G, Wang H, Yang Y (2018a) miR-9 regulates ferroptosis by targeting glutamic-oxaloacetic transaminase GOT1 in melanoma. Mol Carcinog 57(11): 1566−1576 doi: 10.1002/mc.22878
    [125]
    Zhang Y, Shi J, Liu X, Feng L, Gong Z, Koppula P, Sirohi K, Li X, Wei Y, Lee H, Zhuang L, Chen G, Xiao ZD, Hung MC, Chen J, Huang P, Li W, Gan B (2018b) BAP1 links metabolic regulation of ferroptosis to tumour suppression. Nat Cell Biol 20(10): 1181−1192 doi: 10.1038/s41556-018-0178-0
    [126]
    Zou Y, Palte MJ, Deik AA, Li H, Eaton JK, Wang W, Tseng YY, Deasy R, Kost-Alimova M, Dancik V, Leshchiner ES, Viswanathan VS, Signoretti S, Choueiri TK, Boehm JS, Wagner BK, Doench JG, Clish CB, Clemons PA, Schreiber SL (2019) A GPX4-dependent cancer cell state underlies the clear-cell morphology and confers sensitivity to ferroptosis. Nat Commun 10(1): 1617 doi: 10.1038/s41467-019-09277-9
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(2)  / Tables(1)

    Article Metrics

    Article views (1950) PDF downloads(90) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return