Ferroptosis: Role of lipid peroxidation, iron and ferritinophagy

Biochimica et Biophysica Acta - General Subjects

Volumn 1861, Issue 8, 2017, Pages 1893-1900

  Latunde Dada, Gladys O ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Apoptosis; Autophagy; Ferritinophagy; Ferroptosis; Necrosis; Peroxidation

Indexed keywords

ADRENOYL MOIETY; AMINO ACID TRANSPORTER; ARACHIDONOYL MOIETY; CATIONIC AMINO ACID TRANSPORTER MEMBER 11; COPPER ZINC SUPEROXIDE DISMUTASE; FERRITIN; FUNCTIONAL GROUP; GLUTATHIONE; IRON; LIPOXYGENASE; MANGANESE SUPEROXIDE DISMUTASE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; PHOSPHORYLASE KINASE; PHOSPHORYLASE KINASE G2; PROTEIN P53; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG; CYSTEINE;

BIOACCUMULATION; CELL DEATH; FENTON REACTION; FERRITINOPHAGY; FERROPTOSIS; GENE SILENCING; HUMAN; HYDROXYLATION; IN VITRO STUDY; IRON DEPLETION; IRON OVERLOAD; IRON TRANSPORT; LIPID PEROXIDATION; MOLECULAR DYNAMICS; OXIDATION REDUCTION STATE; PEROXISOME; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; AUTOPHAGY; METABOLISM;

ANIMALS; AUTOPHAGY; CELL DEATH; CYSTEINE; FERRITINS; GLUTATHIONE; HUMANS; IRON; LIPID PEROXIDATION; REACTIVE OXYGEN SPECIES;

EID: 85019715011     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2017.05.019     Document Type: Review

References (57)

1. Hanson, B., Necroptosis: a new way of dying?. Cancer Biol. Ther., 2016, 1–12.
2. Xie, Y., Hou, W., Song, X., Yu, Y., Huang, J., Sun, X., Kang, R., Tang, D., Ferroptosis: process and function. Cell Death Differ. 23 (2016), 369–379.
3. 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., Morrison, B. III, Stockwell, B.R., Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149 (2012), 1060–1072.
4. Dolma, S., Lessnick, S.L., Hahn, W.C., Stockwell, B.R., Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell 3 (2003), 285–296.
5. Sato, H., Shiiya, A., Kimata, M., Maebara, K., Tamba, M., Sakakura, Y., Makino, N., Sugiyama, F., Yagami, K., Moriguchi, T., Takahashi, S., Bannai, S., Redox imbalance in cystine/glutamate transporter-deficient mice. J. Biol. Chem. 280 (2005), 37423–37429.
6. Gao, M., Monian, P., Quadri, N., Ramasamy, R., Jiang, X., Glutaminolysis and transferrin regulate ferroptosis. Mol. Cell 59 (2015), 298–308.
7. 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.
8. Jiang, L., Hickman, J.H., Wang, S.J., Gu, W., Dynamic roles of p53-mediated metabolic activities in ROS-induced stress responses. Cell Cycle 14 (2015), 2881–2885.
9. Doll, S., Proneth, B., Tyurina, Y.Y., Panzilius, E., Kobayashi, S., Ingold, I., Irmler, M., Beckers, J., Aichler, M., Walch, A., Prokisch, H., Trumbach, D., Mao, G., Qu, F., Bayir, H., Fullekrug, J., Scheel, C.H., Wurst, W., Schick, J.A., Kagan, V.E., Angeli, J.P., Conrad, M., ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat. Chem. Biol. 13 (2017), 91–98.
10. Yang, W.S., Stockwell, B.R., Ferroptosis: death by lipid peroxidation. Trends Cell Biol. 26 (2016), 165–176.
11. Friedman, B.I., Schaefer, J.W., Schiff, L., Olaniyan, M.F.A.A., Increased iron-59 absorption in patients with hepatic cirrhosis. J. Nucl. Med. 7 (1966), 594–602.
12. Seiler, A., Schneider, M., Forster, H., Roth, S., Wirth, E.K., Culmsee, C., Plesnila, N., Kremmer, E., Radmark, O., Wurst, W., Bornkamm, G.W., Schweizer, U., Conrad, M., Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab. 8 (2008), 237–248.
13. Wirth, E.K., Conrad, M., Winterer, J., Wozny, C., Carlson, B.A., Roth, S., Schmitz, D., Bornkamm, G.W., Coppola, V., Tessarollo, L., Schomburg, L., Kohrle, J., Hatfield, D.L., Schweizer, U., Neuronal selenoprotein expression is required for interneuron development and prevents seizures and neurodegeneration. FASEB J. 24 (2010), 844–852.
14. Doll, S., Conrad, M., Iron and ferroptosis: a still ill-defined liaison. IUBMB Life, 2017.
15. Chen, L., Hambright, W.S., Na, R., Ran, Q., Ablation of the ferroptosis inhibitor glutathione peroxidase 4 in neurons results in rapid motor neuron degeneration and paralysis. J. Biol. Chem. 290 (2015), 28097–28106.
16. Frey, P.A., Reed, G.H., The ubiquity of iron. ACS Chem. Biol. 7 (2012), 1477–1481.
17. Petrat, F., Rauen U, de GH: determination of the chelatable iron pool of isolated rat hepatocytes by digital fluorescence microscopy using the fluorescent probe, phen green SK. Hepatology 29 (1999), 1171–1179.
18. Dixon, S.J., Stockwell, B.R., The role of iron and reactive oxygen species in cell death. Nat. Chem. Biol. 10 (2014), 9–17.
19. Yang, W.S., SriRamaratnam, R., Welsch, M.E., Shimada, K., Skouta, R., Viswanathan, V.S., Cheah, J.H., Clemons, P.A., Shamji, A.F., Clish, C.B., Brown, L.M., Girotti, A.W., Cornish, V.W., Schreiber, S.L., Stockwell, B.R., Regulation of ferroptotic cancer cell death by GPX4. Cell 156 (2014), 317–331.
20. Yang, W.S., Kim, K.J., Gaschler, M.M., Patel, M., Shchepinov, M.S., Stockwell, B.R., Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E4966–E4975.
21. Kagan, V.E., Mao, G., Qu, F., Angeli, J.P., Doll, S., Croix, C.S., Dar, H.H., Liu, B., Tyurin, V.A., Ritov, V.B., Kapralov, A.A., Amoscato, A.A., Jiang, J., Anthonymuthu, T., Mohammadyani, D., Yang, Q., Proneth, B., Klein-Seetharaman, J., Watkins, S., Bahar, I., Greenberger, J., Mallampalli, R.K., Stockwell, B.R., Tyurina, Y.Y., Conrad, M., Bayir, H., Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat. Chem. Biol. 13 (2017), 81–90.
22. D'Herde, K., Krysko, D.V., Ferroptosis: oxidized PEs trigger death. Nat. Chem. Biol. 13 (2017), 4–5.
23. Friedmann Angeli, J.P., Schneider, M., Proneth, B., Tyurina, Y.Y., Tyurin, V.A., Hammond, V.J., 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, G.W., Geissler, E.K., Thomas, S.B., Stockwell, B.R., O'Donnell, V.B., Kagan, V.E., Schick, J.A., Conrad, M., Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat. Cell Biol. 16 (2014), 1180–1191.
24. Carlson, B.A., Tobe, R., Yefremova, E., Tsuji, P.A., Hoffmann, V.J., Schweizer, U., Gladyshev, V.N., Hatfield, D.L., Conrad, M., Glutathione peroxidase 4 and vitamin E cooperatively prevent hepatocellular degeneration. Redox Biol. 9 (2016), 22–31.
25. Wortmann, M., Schneider, M., Pircher, J., Hellfritsch, J., Aichler, M., Vegi, N., Kolle, P., Kuhlencordt, P., Walch, A., Pohl, U., Bornkamm, G.W., Conrad, M., Beck, H., Combined deficiency in glutathione peroxidase 4 and vitamin E causes multiorgan thrombus formation and early death in mice. Circ. Res. 113 (2013), 408–417.
26. Gout, P.W., Simms, C.R., Robertson, M.C., In vitro studies on the lymphoma growth-inhibitory activity of sulfasalazine. Anti-Cancer Drugs 14 (2003), 21–29.
27. Sun, X., Ou, Z., Chen, R., Niu, X., Chen, D., Kang, R., Tang, D., Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology 63 (2016), 173–184.
28. 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., Morrison, B. III, Stockwell, B.R., Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149 (2012), 1060–1072.
29. Siddiq, A., Aminova, L.R., Troy, C.M., Suh, K., Messer, Z., Semenza, G.L., Ratan, R.R., Selective inhibition of hypoxia-inducible factor (HIF) prolyl-hydroxylase 1 mediates neuroprotection against normoxic oxidative death via HIF- and CREB-independent pathways. J. Neurosci. 29 (2009), 8828–8838.
30. Arrigo, A.P., Virot, S., Chaufour, S., Firdaus, W., Kretz-Remy, C., Diaz-Latoud, C., Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing iron intracellular levels. Antioxid. Redox Signal. 7 (2005), 414–422.
31. Chen, H., Zheng, C., Zhang, Y., Chang, Y.Z., Qian, Z.M., Shen, X., Heat shock protein 27 downregulates the transferrin receptor 1-mediated iron uptake. Int. J. Biochem. Cell Biol. 38 (2006), 1402–1416.
32. Sun, X., Ou, Z., Xie, M., Kang, R., Fan, Y., Niu, X., Wang, H., Cao, L., Tang, D., HSPB1 as a novel regulator of ferroptotic cancer cell death. Oncogene 34 (2015), 5617–5625.
33. Murphy, T.H., Miyamoto, M., Sastre, A., Schnaar, R.L., Coyle, J.T., Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress. Neuron 2 (1989), 1547–1558.
34. Zaman, K., Ryu, H., Hall, D., O'Donovan, K., Lin, K.I., Miller, M.P., Marquis, J.C., Baraban, J.M., Semenza, G.L., Ratan, R.R., Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia-inducible factor-1 and ATF-1/CREB and increased expression of glycolytic enzymes, p21(waf1/cip1), and erythropoietin. J. Neurosci. 19 (1999), 9821–9830.
35. Speer, R.E., Karuppagounder, S.S., Basso, M., Sleiman, S.F., Kumar, A., Brand, D., Smirnova, N., Gazaryan, I., Khim, S.J., Ratan, R.R., Hypoxia-inducible factor prolyl hydroxylases as targets for neuroprotection by “antioxidant” metal chelators: from ferroptosis to stroke. Free Radic. Biol. Med. 62 (2013), 26–36.
36. Takahashi-Makise, N., Ward, D.M., Kaplan, J., On the mechanism of iron sensing by IRP2: new players, new paradigms. Nat. Chem. Biol. 5 (2009), 874–875.
37. Lavaute, T., Smith, S., Cooperman, S., Iwai, K., Land, W., Meyron-Holtz, E., Drake, S.K., Miller, G., Abu-Asab, M., Tsokos, M., Switzer, R. III, Grinberg, A., Love, P., Tresser, N., Rouault, T.A., Targeted deletion of the gene encoding iron regulatory protein-2 causes misregulation of iron metabolism and neurodegenerative disease in mice. Nat. Genet. 27 (2001), 209–214.
38. Salvatore, M.F., Fisher, B., Surgener, S.P., Gerhardt, G.A., Rouault, T., Neurochemical investigations of dopamine neuronal systems in iron-regulatory protein 2 (IRP-2) knockout mice. Brain Res. Mol. Brain Res. 139 (2005), 341–347.
39. MacDonald, M.J., Hasan, N.M., Ansari, I.U., Longacre, M.J., Kendrick, M.A., Stoker, S.W., Discovery of a genetic metabolic cause for Mauriac syndrome in type 1 diabetes. Diabetes 65 (2016), 2051–2059.
40. Maichele, A.J., Burwinkel, B., Maire, I., Sovik, O., Kilimann, M.W., Mutations in the testis/liver isoform of the phosphorylase kinase gamma subunit (PHKG2) cause autosomal liver glycogenosis in the gsd rat and in humans. Nat. Genet. 14 (1996), 337–340.
41. Jennis, M., Kung, C.P., Basu, S., Budina-Kolomets, A., Leu, J.I., Khaku, S., Scott, J.P., Cai, K.Q., Campbell, M.R., Porter, D.K., Wang, X., Bell, D.A., Li, X., Garlick, D.S., Liu, Q., Hollstein, M., George, D.L., Murphy, M.E., An African-specific polymorphism in the TP53 gene impairs p53 tumor suppressor function in a mouse model. Genes Dev. 30 (2016), 918–930.
42. 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.
43. Ou, Y., Wang, S.J., Li, D., Chu, B., Gu, W., Activation of SAT1 engages polyamine metabolism with p53-mediated ferroptotic responses. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E6806–E6812.
44. Shen, J., Sheng, X., Chang, Z., Wu, Q., Wang, S., Xuan, Z., Li, D., Wu, Y., Shang, Y., Kong, X., Yu, L., Li, L., Ruan, K., Hu, H., Huang, Y., Hui, L., Xie, D., Wang, F., Hu, R., Iron metabolism regulates p53 signaling through direct heme-p53 interaction and modulation of p53 localization, stability, and function. Cell Rep. 7 (2014), 180–193.
45. Dowdle, W.E., Nyfeler, B., Nagel, J., Elling, R.A., Liu, S., Triantafellow, E., Menon, S., Wang, Z., Honda, A., Pardee, G., Cantwell, J., Luu, C., Cornella-Taracido, I., Harrington, E., Fekkes, P., Lei, H., Fang, Q., Digan, M.E., Burdick, D., Powers, A.F., Helliwell, S.B., D'Aquin, S., Bastien, J., Wang, H., Wiederschain, D., Kuerth, J., Bergman, P., Schwalb, D., Thomas, J., Ugwonali, S., Harbinski, F., Tallarico, J., Wilson, C.J., Myer, V.E., Porter, J.A., Bussiere, D.E., Finan, P.M., Labow, M.A., Mao, X., Hamann, L.G., Manning, B.D., Valdez, R.A., Nicholson, T., Schirle, M., Knapp, M.S., Keaney, E.P., Murphy, L.O., 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.
46. Mancias, J.D., Wang, X., Gygi, S.P., Harper, J.W., Kimmelman, A.C., Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 509 (2014), 105–109.
47. Gao, M., Monian, P., Pan, Q., Zhang, W., Xiang, J., Jiang, X., Ferroptosis is an autophagic cell death process. Cell Res. 26 (2016), 1021–1032.
48. Kroemer, G., Marino, G., Levine, B., Autophagy and the integrated stress response. Mol. Cell 40 (2010), 280–293.
49. Hou, W., Xie, Y., Song, X., Sun, X., Lotze, M.T., Zeh, H.J. III, Kang, R., Tang, D., Autophagy promotes ferroptosis by degradation of ferritin. Autophagy 12 (2016), 1425–1428.
50. Chance, B., GREENSTEIN, D.S., HIGGINS, J., YANG, C.C., The mechanism of catalase action. II. Electric analog computer studies. Arch. Biochem. Biophys. 37 (1952), 322–339.
51. Persson, H.L., Yu, Z., Tirosh, O., Eaton, J.W., Brunk, U.T., Prevention of oxidant-induced cell death by lysosomotropic iron chelators. Free Radic. Biol. Med. 34 (2003), 1295–1305.
52. Yu, Z., Persson, H.L., Eaton, J.W., Brunk, U.T., Intralysosomal iron: a major determinant of oxidant-induced cell death. Free Radic. Biol. Med. 34 (2003), 1243–1252.
53. Bresgen, N., Jaksch, H., Bauer, H.C., Eckl, P., Krizbai, I., Tempfer, H., Astrocytes are more resistant than cerebral endothelial cells toward geno- and cytotoxicity mediated by short-term oxidative stress. J. Neurosci. Res. 84 (2006), 1821–1828.
54. Bresgen, N., Jaksch, H., Lacher, H., Ohlenschlager, I., Uchida, K., Eckl, P.M., Iron-mediated oxidative stress plays an essential role in ferritin-induced cell death. Free Radic. Biol. Med. 48 (2010), 1347–1357.
55. Pietrangelo, A., Iron, friend or foe? “Freedom” makes the difference. J. Hepatol. 32 (2000), 862–864.
56. Wang, H., An, P., Xie, E., Wu, Q., Fang, X., Gao, H., Zhang, Z., Li, Y., Wang, X., Zhang, J., Li, G., Yang, L., Liu, W., Min, J., Wang, F., Characterization of ferroptosis in murine models of hemochromatosis. Hepatology, 2017.
57. Yu, H., Guo, P., Xie, X., Wang, Y., Chen, G., Ferroptosis, a new form of cell death, and its relationships with tumourous diseases. J. Cell. Mol. Med., 2016.