p53 Suppresses Metabolic Stress-Induced Ferroptosis in Cancer Cells

Cell Reports

Volumn 22, Issue 3, 2018, Pages 569-575

  Tarangelo, Amy ^a   Magtanong, Leslie ^b   Bieging Rolett, Kathryn T ^a   Li, Yang ^a   Ye, Jiangbin ^a   Attardi, Laura D ^a   Dixon, Scott J ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

cancer; cell death; cystine; ferroptosis; glutathione; metabolism; p53; reactive oxygen species

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1A; GLUTATHIONE; PROTEIN P53; REACTIVE OXYGEN METABOLITE; TP53 PROTEIN, HUMAN; TRP53 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CANCER CELL; CONTROLLED STUDY; CRISPR-CAS9 SYSTEM; DEPLETION; EMBRYO; FERROPTOSIS; GENE EDITING; HUMAN; HUMAN CELL; MALE; METABOLIC STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIME LAPSE IMAGING; WILD TYPE; ANIMAL; APOPTOSIS; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GLUTATHIONE; HUMANS; MICE; NEOPLASMS; REACTIVE OXYGEN SPECIES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 85041647871     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.12.077     Document Type: Article

References (24)

1. Abbas, T., Dutta, A., p21 in cancer: intricate networks and multiple activities. Nat. Rev. Cancer 9 (2009), 400–414.
2. Bieging, K.T., Mello, S.S., Attardi, L.D., Unravelling mechanisms of p53-mediated tumour suppression. Nat. Rev. Cancer 14 (2014), 359–370.
3. Brady, C.A., Jiang, D., Mello, S.S., Johnson, T.M., Jarvis, L.A., Kozak, M.M., Kenzelmann Broz, D., Basak, S., Park, E.J., McLaughlin, M.E., et al. Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 145 (2011), 571–583.
4. Chen, W., Sun, Z., Wang, X.-J., Jiang, T., Huang, Z., Fang, D., Zhang, D.D., Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol. Cell 34 (2009), 663–673.
5. Dixon, S.J., Lemberg, K.M., Lamprecht, M.R., Skouta, R., Zaitsev, E.M., Gleason, C.E., Patel, D.N., Bauer, A.J., Cantley, A.M., Yang, W.S., et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149 (2012), 1060–1072.
6. Dixon, S.J., Patel, D.N., Welsch, M., Skouta, R., Lee, E.D., Hayano, M., Thomas, A.G., Gleason, C.E., Tatonetti, N.P., Slusher, B.S., Stockwell, B.R., Pharmacological inhibition of cystine-glutamate exchange induces endoplasmic reticulum stress and ferroptosis. eLife, 3, 2014, e02523.
7. Ewald, J.C., Kuehne, A., Zamboni, N., Skotheim, J.M., The yeast cyclin-dependent kinase routes carbon fluxes to fuel cell cycle progression. Mol. Cell 62 (2016), 532–545.
8. Forcina, G.C., Conlon, M., Wells, A., Cao, J.Y., Dixon, S.J., Systematic quantification of population cell death kinetics in mammalian cells. Cell Syst. 4 (2017), 600–610.e6.
9. Jennis, M., Kung, C.-P., Basu, S., Budina-Kolomets, A., Leu, J.I.-J., Khaku, S., Scott, J.P., Cai, K.Q., Campbell, M.R., Porter, D.K., et al. An African-specific polymorphism in the TP53 gene impairs p53 tumor suppressor function in a mouse model. Genes Dev. 30 (2016), 918–930.
10. Jiang, L., Kon, N., Li, T., Wang, S.-J., Su, T., Hibshoosh, H., Baer, R., Gu, W., Ferroptosis as a p53-mediated activity during tumour suppression. Nature 520 (2015), 57–62.
11. Johnson, L., Mercer, K., Greenbaum, D., Bronson, R.T., Crowley, D., Tuveson, D.A., Jacks, T., Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410 (2001), 1111–1116.
12. Johnson, T.M., Hammond, E.M., Giaccia, A., Attardi, L.D., The p53QS transactivation-deficient mutant shows stress-specific apoptotic activity and induces embryonic lethality. Nat. Genet. 37 (2005), 145–152.
13. Kruiswijk, F., Labuschagne, C.F., Vousden, K.H., p53 in survival, death and metabolic health: a lifeguard with a licence to kill. Nat. Rev. Mol. Cell Biol. 16 (2015), 393–405.
14. Lewerenz, J., Sato, H., Albrecht, P., Henke, N., Noack, R., Methner, A., Maher, P., Mutation of ATF4 mediates resistance of neuronal cell lines against oxidative stress by inducing xCT expression. Cell Death Differ. 19 (2012), 847–858.
15. Li, T., Kon, N., Jiang, L., Tan, M., Ludwig, T., Zhao, Y., Baer, R., Gu, W., Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 149 (2012), 1269–1283.
16. Maddocks, O.D.K., Berkers, C.R., Mason, S.M., Zheng, L., Blyth, K., Gottlieb, E., Vousden, K.H., Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature 493 (2013), 542–546.
17. Paek, A.L., Liu, J.C., Loewer, A., Forrester, W.C., Lahav, G., Cell-to-cell variation in p53 dynamics leads to fractional killing. Cell 165 (2016), 631–642.
18. Pfister, N.T., Prives, C., Transcriptional regulation by wild-type and cancer-related mutant forms of p53. Cold Spring Harb. Perspect. Med., 7, 2017, a026054.
19. Piskounova, E., Agathocleous, M., Murphy, M.M., Hu, Z., Huddlestun, S.E., Zhao, Z., Leitch, A.M., Johnson, T.M., DeBerardinis, R.J., Morrison, S.J., Oxidative stress inhibits distant metastasis by human melanoma cells. Nature 527 (2015), 186–191.
20. Stockwell, B.R., Friedmann Angeli, J.P., Bayir, H., Bush, A.I., Conrad, M., Dixon, S.J., Fulda, S., Gascón, S., Hatzios, S.K., Kagan, V.E., et al. Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell 171 (2017), 273–285.
21. Tarunina, M., Jenkins, J.R., Human p53 binds DNA as a protein homodimer but monomeric variants retain full transcription transactivation activity. Oncogene 8 (1993), 3165–3173.
22. Vassilev, L.T., Vu, B.T., Graves, B., Carvajal, D., Podlaski, F., Filipovic, Z., Kong, N., Kammlott, U., Lukacs, C., Klein, C., et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303 (2004), 844–848.
23. Wang, S.-J., Li, D., Ou, Y., Jiang, L., Chen, Y., Zhao, Y., Gu, W., Acetylation is crucial for p53-mediated ferroptosis and tumor suppression. Cell Rep. 17 (2016), 366–373.
24. Xie, Y., Zhu, S., Song, X., Sun, X., Fan, Y., Liu, J., Zhong, M., Yuan, H., Zhang, L., Billiar, T.R., et al. The tumor suppressor p53 limits ferroptosis by blocking DPP4 activity. Cell Rep. 20 (2017), 1692–1704.