How do we fit ferroptosis in the family of regulated cell death?

Cell Death and Differentiation

Volumn 24, Issue 12, 2017, Pages 1991-1998

  Fearnhead, Howard O ^a   Vandenabeele, Peter ^b,c   Berghe, Tom Vanden ^b,c  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSOME; INFLAMMASOME; TUMOR NECROSIS FACTOR; IRON;

BIOLOGICAL ACTIVITY; COMPLEX FORMATION; CYTOKINE PRODUCTION; FERROPTOSIS; HUMAN; LIPID PEROXIDATION; MOLECULAR WEIGHT; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; PYROPTOSIS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; APOPTOSIS; CELL DEATH; GENETICS; METABOLISM;

APOPTOSIS; CELL DEATH; HUMANS; IRON;

EID: 85034030884     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2017.149     Document Type: Review

References (112)

1. Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ 2015; 22: 58-73.
2. Meier P, Finch A, Evan G. Apoptosis in development. Nature 2000; 407: 796-801.
3. Lauber K, Bohn E, Krober SM, Xiao YJ, Blumenthal SG, Lindemann RK et al. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 2003; 113: 717-730.
4. Li F, Huang Q, Chen J, Peng Y, Roop DR, Bedford JS et al. Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci Signal 2010; 3: ra13.
5. Chera S, Ghila L, Dobretz K, Wenger Y, Bauer C, Buzgariu W et al. Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev Cell 2009; 17: 279-289.
6. Galliot B. Injury-induced asymmetric cell death as a driving force for head regeneration in Hydra. Dev Genes Evol 2013; 223: 39-52.
7. Green DR, Victor B. The pantheon of the fallen: why are there so many forms of cell death? Trends Cell Biol 2012; 22: 555-556.
8. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 1997; 185: 1481-1486.
9. Grootjans S, Vanden Berghe T, Vandenabeele P. Initiation and execution mechanisms of necroptosis: an overview. Cell Death Differ 2017; 24: 1184-1195.
10. Sun L, Wang H, Wang Z, He S, Chen S, Liao D et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012; 148: 213-227.
11. Cao JY, Dixon SJ. Mechanisms of ferroptosis. Cell Mol Life Sci 2016; 73: 2195-2209.
12. Yang WS, Stockwell BR. Ferroptosis: death by lipid peroxidation. Trends Cell Biol 2016; 26: 165-176.
13. Dixon SJ. Ferroptosis: bug or feature? Immunol Rev 2017; 277: 150-157.
14. Friedmann Angeli JP, Shah R, Pratt DA, Conrad M. Ferroptosis inhibition: mechanisms and opportunities. Trends Pharmacol Sci 2017; 14: 489-498.
15. Friedmann Angeli JP, Schneider M, Proneth B, Tyurina YY, Tyurin VA, Hammond VJ et al. Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat Cell Biol 2014; 16: 1180-1191.
16. Linkermann A, Skouta R, Himmerkus N, Mulay SR, Dewitz C, De Zen F et al. Synchronized renal tubular cell death involves ferroptosis. Proc Natl Acad Sci USA 2014; 111: 16836-16841.
17. Crawford ED, Wells JA. Caspase substrates and cellular remodeling. Annu Rev Biochem 2011; 80: 1055-1087.
18. Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol 2014; 15: 135-147.
19. Tanzer MC, Tripaydonis A, Webb AI, Young SN, Varghese LN, Hall C et al. Necroptosis signalling is tuned by phosphorylation of MLKL residues outside the pseudokinase domain activation loop. Biochem J 2015; 471: 255-265.
20. Murphy JM, Czabotar PE, Hildebrand JM, Lucet IS, Zhang JG, Alvarez-Diaz S et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 2013; 39: 443-453.
21. Cai Z, Jitkaew S, Zhao J, Chiang HC, Choksi S, Liu J et al. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol 2014; 16: 55-65.
22. Petrie EJ, Hildebrand JM, Murphy JM. Insane in the membrane: a structural perspective of MLKL function in necroptosis. Immunol Cell Biol 2017; 95: 152-159.
23. Tanzer MC, Matti I, Hildebrand JM, Young SN, Wardak A, Tripaydonis A et al. Evolutionary divergence of the necroptosis effector MLKL. Cell Death Differ 2016; 23: 1185-1197.
24. Wu J, Huang Z, Ren J, Zhang Z, He P, Li Y et al. Mlkl knockout mice demonstrate the indispensable role of Mlkl in necroptosis. Cell Res 2013; 23: 994-1006.
25. Yoon S, Kovalenko A, Bogdanov K, Wallach D. MLKL, the protein that mediates necroptosis, also regulates endosomal trafficking and extracellular vesicle generation. Immunity 2017; 47: 51-65.
26. Gong YN, Guy C, Olauson H, Becker JU, Yang M, Fitzgerald P et al. ESCRT-III acts downstream of MLKL to regulate necroptotic cell death and its consequences. Cell 2017; 169: 286-300 e216.
27. Dondelinger Y, Hulpiau P, Saeys Y, Bertrand MJ, Vandenabeele P. An evolutionary perspective on the necroptotic pathway. Trends Cell Biol 2016; 26: 721-732.
28. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozoren N, Jagirdar R et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonellainfected macrophages. Nat Immunol 2006; 7: 576-582.
29. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 2006; 7: 569-575.
30. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 2010; 107: 3076-3080.
31. Miao EA, Warren SE. Innate immune detection of bacterial virulence factors via the NLRC4 inflammasome. J Clin Immunol 2010; 30: 502-506.
32. He WT, Wan H, Hu L, Chen P, Wang X, Huang Z et al. Gasdermin D is an executor of pyroptosis and required for interleukin-1beta secretion. Cell Res 2015; 25: 1285-1298.
33. Chen X, He WT, Hu L, Li J, Fang Y, Wang X et al. Pyroptosis is driven by non-selective gasdermin-D pore and its morphology is different from MLKL channel-mediated necroptosis. Cell Res 2016; 26: 1007-1020.
34. Sborgi L, Ruhl S, Mulvihill E, Pipercevic J, Heilig R, Stahlberg H et al. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J 2016; 35: 1766-1778.
35. Ding J, Wang K, Liu W, She Y, Sun Q, Shi J et al. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 2016; 535: 111-116.
36. Shi J, Gao W, Shao F. Pyroptosis: gasdermin-mediated programmed necrotic cell death. Trends Biochem Sci 2016; 42: 245-254.
37. Clem RJ, Fechheimer M, Miller LK. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 1991; 254: 1388-1390.
38. Chen P, Tian J, Kovesdi I, Bruder JT. Interaction of the adenovirus 14. 7-kDa protein with FLICE inhibits Fas ligand-induced apoptosis. J Biol Chem 1998; 273: 5815-5820.
39. Taylor JM, Barry M. Near death experiences: poxvirus regulation of apoptotic death. Virology 2006; 344: 139-150.
40. Skaletskaya A, Bartle LM, Chittenden T, McCormick AL, Mocarski ES, Goldmacher VS. A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc Natl Acad Sci USA 2001; 98: 7829-7834.
41. Lagunoff M, Carroll PA. Inhibition of apoptosis by the gamma-herpesviruses. Int Rev Immunol 2003; 22: 373-399.
42. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009; 137: 1112-1123.
43. Omoto S, Guo H, Talekar GR, Roback L, Kaiser WJ, Mocarski ES. Suppression of RIP3-dependent necroptosis by human cytomegalovirus. J Biol Chem 2015; 290: 11635-11648.
44. Upton JW, Kaiser WJ, Mocarski ES. Cytomegalovirus M45 cell death suppression requires receptor-interacting protein (RIP) homotypic interaction motif (RHIM)-dependent interaction with RIP1. J Biol Chem 2008; 283: 16966-16970.
45. Guo H, Omoto S, Harris PA, Finger JN, Bertin J, Gough PJ et al. Herpes simplex virus suppresses necroptosis in human cells. Cell Host Microbe 2015; 17: 243-251.
46. Miao EA, Leaf IA, Treuting PM, Mao DP, Dors M, Sarkar A et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 2010; 11: 1136-1142.
47. Brodsky IE, Palm NW, Sadanand S, Ryndak MB, Sutterwala FS, Flavell RA et al. AYersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 2010; 7: 376-387.
48. Dewoody R, Merritt PM, Houppert AS, Marketon MM. YopK regulates the Yersinia pestis type III secretion system from within host cells. Mol Microbiol 2011; 79: 1445-1461.
49. Doitsh G, Galloway NL, Geng X, Yang Z, Monroe KM, Zepeda O et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014; 505: 509-514.
50. Vanden Berghe T, Kalai M, Denecker G, Meeus A, Saelens X, Vandenabeele P. Necrosis is associated with IL-6 production but apoptosis is not. Cell Signal 2006; 18: 328-335.
51. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 2012; 149: 1060-1072.
52. Tonnus W, Linkermann A. The in vivo evidence for regulated necrosis. Immunol Rev 2017; 277: 128-149.
53. Yang WS, SriRamaratnam R, Welsch ME, Shimada K, Skouta R, Viswanathan VS et al. Regulation of ferroptotic cancer cell death by GPX4. Cell 2014; 156: 317-331.
54. Wong-Ekkabut J, Xu Z, Triampo W, Tang IM, Tieleman DP, Monticelli L. Effect of lipid peroxidation on the properties of lipid bilayers: a molecular dynamics study. Biophys J 2007; 93: 4225-4236.
55. Yin H, Xu L, Porter NA. Free radical lipid peroxidation: mechanisms and analysis. Chem Rev 2011; 111: 5944-5972.
56. Grimsrud PA, Xie H, Griffin TJ, Bernlohr DA. Oxidative stress and covalent modification of protein with bioactive aldehydes. J Biol Chem 2008; 283: 21837-21841.
57. Wong CM, Marcocci L, Liu L, Suzuki YJ. Cell signaling by protein carbonylation and decarbonylation. Antioxid Redox Signal 2010; 12: 393-404.
58. Dalleau S, Baradat M, Gueraud F, Huc L. Cell death and diseases related to oxidative stress: 4-hydroxynonenal (HNE) in the balance. Cell Death Differ 2013; 20: 1615-1630.
59. Aryal B, Jeong J, Rao VA. Doxorubicin-induced carbonylation and degradation of cardiac myosin binding protein C promote cardiotoxicity. Proc Natl Acad Sci USA 2014; 111: 2011-2016.
60. Dixon SJ, Patel DN, Welsch M, Skouta R, Lee ED, Hayano M et al. Pharmacological inhibition of cystine-glutamate exchange induces endoplasmic reticulum stress and ferroptosis. Elife 2014; 3: e02523.
61. Zilka O, Shah R, Li B, Friedmann Angeli JP, Griesser M, Conrad M et al. On the mechanism of cytoprotection by ferrostatin-1 and liproxstatin-1 and the role of lipid peroxidation in ferroptotic cell death. ACS Cent Sci 2017; 3: 232-243.
62. Yang WS, Kim KJ, Gaschler MM, Patel M, Shchepinov MS, Stockwell BR. Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc Natl Acad Sci USA 2016; 113: E4966-E4975.
63. Kagan VE, Mao G, Qu F, Angeli JP, Doll S, Croix CS et al. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat Chem Biol 2017; 13: 81-90.
64. Doll S, Proneth B, Tyurina YY, Panzilius E, Kobayashi S, Ingold I et al. ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat Chem Biol 2017; 13: 91-98.
65. Pallast S, Arai K, Wang X, Lo EH, van Leyen K. 12/15-Lipoxygenase targets neuronal mitochondria under oxidative stress. J Neurochem 2009; 111: 882-889.
66. Khanna S, Roy S, Ryu H, Bahadduri P, Swaan PW, Ratan RR et al. Molecular basis of vitamin E action: tocotrienol modulates 12-lipoxygenase, a key mediator of glutamateinduced neurodegeneration. J Biol Chem 2003; 278: 43508-43515.
67. Khanna S, Roy S, Slivka A, Craft TK, Chaki S, Rink C et al. Neuroprotective properties of the natural vitamin E alpha-tocotrienol. Stroke 2005; 36: 2258-2264.
68. Distefano AM, Martin MV, Cordoba JP, Bellido AM, D'Ippolito S, Colman SL et al. Heat stress induces ferroptosis-like cell death in plants. J Cell Biol 2017; 216: 463-476.
69. Dixon SJ, Stockwell BR. The role of iron and reactive oxygen species in cell death. Nat Chem Biol 2014; 10: 9-17.
70. Gao M, Monian P, Quadri N, Ramasamy R, Jiang X. Glutaminolysis and transferrin regulate ferroptosis. Mol Cell 2015; 59: 298-308.
71. Seiler A, Schneider M, Forster H, Roth S, Wirth EK, Culmsee C et al. Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependentand AIF-mediated cell death. Cell Metab 2008; 8: 237-248.
72. Kang Y, Tiziani S, Park G, Kaul M, Paternostro G. Cellular protection using Flt3 and PI3Kalpha inhibitors demonstrates multiple mechanisms of oxidative glutamate toxicity. Nat Commun 2014; 5: 3672.
73. Woolley JF, Naughton R, Stanicka J, Gough DR, Bhatt L, Dickinson BC et al. H2O2 production downstream of FLT3 is mediated by p22phox in the endoplasmic reticulum and is required for STAT5 signalling. PLoS ONE 2012; 7: e34050.
74. Ong Q, Guo S, Zhang K, Cui B. U0126 protects cells against oxidative stress independent of its function as a MEK inhibitor. ACS Chem Neurosci 2015; 6: 130-137.
75. Wang H, An P, Xie E, Wu Q, Fang X, Gao H et al. Characterization of ferroptosis in murine models of hemochromatosis. Hepatology 2017; 66: 449-465.
76. Jiang L, Kon N, Li T, Wang SJ, Su T, Hibshoosh H et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature 2015; 520: 57-62.
77. Li T, Kon N, Jiang L, Tan M, Ludwig T, Zhao Y et al. Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 2012; 149: 1269-1283.
78. Wang SJ, Li D, Ou Y, Jiang L, Chen Y, Zhao Y et al. Acetylation is crucial for p53-mediated eerroptosis and tumor suppression. Cell Rep 2016; 17: 366-373.
79. Cramer SL, Saha A, Liu J, Tadi S, Tiziani S, Yan W et al. Systemic depletion of L-cyst(e)ine with cyst(e)inase increases reactive oxygen species and suppresses tumor growth. Nat Med 2017; 23: 120-127.
80. Ou Y, Wang SJ, Li D, Chu B, Gu W. Activation of SAT1 engages polyamine metabolism with p53-mediated ferroptotic responses. Proc Natl Acad Sci USA 2016; 113: E6806-E6812.
81. Wijnhoven SW, Zwart E, Speksnijder EN, Beems RB, Olive KP, Tuveson DA et al. Mice expressing a mammary gland-specific R270H mutation in the p53 tumor suppressor gene mimic human breast cancer development. Cancer Res 2005; 65: 8166-8173.
82. Jennis M, Kung CP, Basu S, Budina-Kolomets A, Leu JI, Khaku S et al. An African-specific polymorphism in the TP53 gene impairs p53 tumor suppressor function in a mouse model. Genes Dev 2016; 30: 918-930.
83. Xie Y, Song X, Sun X, Huang J, Zhong M, Lotze MT et al. Identification of baicalein as a ferroptosis inhibitor by natural product library screening. Biochem Biophys Res Commun 2016; 473: 775-780.
84. Dixon SJ, Winter GE, Musavi LS, Lee ED, Snijder B, Rebsamen M et al. Human haploid cell genetics reveals roles for lipid metabolism genes in nonapoptotic cell death. ACS Chem Biol 2015; 10: 1604-1609.
85. Doll S, Proneth B, Tyurina YY, Panzilius E, Kobayashi S, Ingold I et al. ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat Chem Biol 2017; 13: 91-98.
86. Hayano M, Yang WS, Corn CK, Pagano NC, Stockwell BR. Loss of cysteinyl-tRNA synthetase (CARS) induces the transsulfuration pathway and inhibits ferroptosis induced by cystine deprivation. Cell Death Differ 2016; 23: 270-278.
87. Monteiro HP, Winterbourn CC. 6-Hydroxydopamine releases iron from ferritin and promotes ferritin-dependent lipid peroxidation. Biochem Pharmacol 1989; 38: 4177-4182.
88. Ben-Shachar D, Eshel G, Finberg JP, Youdim MB. The iron chelator desferrioxamine (Desferal) retards 6-hydroxydopamine-induced degeneration of nigrostriatal dopamine neurons. J Neurochem 1991; 56: 1441-1444.
89. Cadet JL, Katz M, Jackson-Lewis V, Fahn S. Vitamin E attenuates the toxic effects of intrastriatal injection of 6-hydroxydopamine (6-OHDA) in rats: behavioral and biochemical evidence. Brain Res 1989; 476: 10-15.
90. Sawyer DB, Peng X, Chen B, Pentassuglia L, Lim CC. Mechanisms of anthracycline cardiac injury: can we identify strategies for cardioprotection? Prog Cardiovasc Dis 2010; 53: 105-113.
91. Herman EH, Zhang J, Ferrans VJ. Comparison of the protective effects of desferrioxamine and ICRF-187 against doxorubicin-induced toxicity in spontaneously hypertensive rats. Cancer Chemother Pharmacol 1994; 35: 93-100.
92. Henriksson R, Grankvist K. Protective effect of iron chelators on epirubicin-induced fibroblast toxicity. Cancer Lett 1988; 43: 179-183.
93. Stuart MJ, deAlarcon PA, Barvinchak MK. Inhibition of adriamycin-induced human platelet lipid peroxidation by vitamin E. Am J Hematol 1978; 5: 297-303.
94. Bus JS, Aust SD, Gibson JE. Paraquat toxicity: proposed mechanism of action involving lipid peroxidation. Environ Health Perspect 1976; 16: 139-146.
95. Van der Wal NA, Smith LL, van Oirschot JF, van Asbeck BS. Effect of iron chelators on paraquat toxicity in rats and alveolar type II cells. Am Rev Respir Dis 1992; 145: 180-186.
96. Suntres ZE, Shek PN. Liposomal alpha-tocopherol alleviates the progression of paraquatinduced lung damage. J Drug Target 1995; 2: 493-500.
97. Yonaha M, Saito M, Sagai M. Stimulation of lipid peroxidation by methyl mercury in rats. Life Sci 1983; 32: 1507-1514.
98. Lin TH, Huang YL, Huang SF. Lipid peroxidation in liver of rats administrated with methyl mercuric chloride. Biol Trace Elem Res 1996; 54: 33-41.
99. LeBel CP, Ali SF, Bondy SC. Deferoxamine inhibits methyl mercury-induced increases in reactive oxygen species formation in rat brain. Toxicol Appl Pharmacol 1992; 112: 161-165.
100. Andersen HR, Andersen O. Effects of dietary alpha-tocopherol and beta-carotene on lipid peroxidation induced by methyl mercuric chloride in mice. Pharmacol Toxicol 1993; 73: 192-201.
101. Fraga CG, Zamora R, Tappel AL. Damage to protein synthesis concurrent with lipid peroxidation in rat liver slices: effect of halogenated compounds, peroxides, and vitamin E1. Arch Biochem Biophys 1989; 270: 84-91.
102. Casini AF, Maellaro E, Pompella A, Ferrali M, Comporti M. Lipid peroxidation, protein thiols and calcium homeostasis in bromobenzene-induced liver damage. Biochem Pharmacol 1987; 36: 3689-3695.
103. Coleman JB, Casini AF, Serroni A, Farber JL. Evidence for the participation of activated oxygen species and the resulting peroxidation of lipids in the killing of cultured hepatocytes by aryl halides. Toxicol Appl Pharmacol 1990; 105: 393-402.
104. Maellaro E, Casini AF, Del Bello B, Comporti M. Lipid peroxidation and antioxidant systems in the liver injury produced by glutathione depleting agents. Biochem Pharmacol 1990; 39: 1513-1521.
105. Hashimoto S, Glende EA Jr., Recknagel RO. Hepatic lipid peroxidation in acute fatal human carbon tetrachloride poisoning. N Engl J Med 1968; 279: 1082-1085.
106. Younes M, Siegers CP. The role of iron in the paracetamol-and CCl4-induced lipid peroxidation and hepatotoxicity. Chem Biol Interact 1985; 55: 327-334.
107. Miyazawa T, Suzuki T, Fujimoto K, Kaneda T. Phospholipid hydroperoxide accumulation in liver of rats intoxicated with carbon tetrachloride and its inhibition by dietary alphatocopherol. J Biochem 1990; 107: 689-693.
108. Stacey NH, Cantilena LR Jr., Klaassen CD. Cadmium toxicity and lipid peroxidation in isolated rat hepatocytes. Toxicol Appl Pharmacol 1980; 53: 470-480.
109. Yiin SJ, Sheu JY, Lin TH. Lipid peroxidation in rat adrenal glands after administration cadmium and role of essential metals. J Toxicol Environ Health A 2001; 62: 47-56.
110. Fariss MW. Cadmium toxicity: unique cytoprotective properties of alpha tocopheryl succinate in hepatocytes. Toxicology 1991; 69: 63-77.
111. Cojocel C, Hannemann J, Baumann K. Cephaloridine-induced lipid peroxidation initiated by reactive oxygen species as a possible mechanism of cephaloridine nephrotoxicity. Biochim Biophys Acta 1985; 834: 402-410.
112. Cojocel C, Laeschke KH, Inselmann G, Baumann K. Inhibition of cephaloridine-induced lipid peroxidation. Toxicology 1985; 35: 295-305.