Programmed cell death with a necrotic-like phenotype

Biomolecular Concepts

Volumn 4, Issue 3, 2013, Pages 259-275

  Morgan, Michael J ^a   Liu, Zheng Gang ^b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Caspase independent cell death; Necroptosis; Programmed cell death; Programmed necrosis

Indexed keywords

RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE;

ANIMAL; APOPTOSIS; CELL DEATH; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; NECROSIS; PHENOTYPE;

ANIMALS; APOPTOSIS; CELL DEATH; GENE EXPRESSION REGULATION; HUMANS; NECROSIS; PHENOTYPE; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES;

EID: 84881583186     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/bmc-2012-0056     Document Type: Review

References (199)

1. Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, Zitvogel L, Kroemer G. Cell death modalities: classification and pathophysiological implications. Cell Death Differ 2007; 14: 1237-43.
2. Schweichel J, Merker H. The morphology of various types of cell death in prenatal tissues. Teratology 1973; 7: 253-66.
3. Kroemer G, El-Deiry WS, Golstein P, Peter ME, Vaux D, Vandenabeele P, Zhivotovsky B, Blagosklonny MV, Malorni W, Knight RA, Piacentini M, Nagata S, Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 2005; 12: 1463-7.
4. Fiers W, Beyaert R, Declercq W, Vandenabeele P. More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene 1999; 18: 7719-30.
5. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239-57.
6. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, Dawson TM, Dawson VL, El-Deiry WS, Fulda S, Gottlieb E, Green DR, Hengartner MO, Kepp O, Knight RA, Kumar S, Lipton SA, Lu X, Madeo F, Malorni W, Mehlen P, Nunez G, Peter ME, Piacentini M, Rubinsztein DC, Shi Y, Simon HU, Vandenabeele P, White E, Yuan J, Zhivotovsky B, Melino G, Kroemer G. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012; 19: 107-20.
7. Pop C, Salvesen GS. Human caspases: activation, specificity, and regulation. J Biol Chem 2009; 284: 21777-81.
8. Salvesen GS, Ashkenazi A. SnapShot: caspases. Cell 2011; 147: 1197.
9. Dix MM, Simon GM, Cravatt BF. Global mapping of the topography and magnitude of proteolytic events in apoptosis. Cell 2008; 134: 679-91.
10. Mahrus S, Trinidad JC, Barkan DT, Sali A, Burlingame AL, Wells JA. Global Sequencing of proteolytic cleavage sites in apoptosis by specific Labeling of protein N termini. Cell 2008; 134: 866-76.
11. Shimbo K, Hsu GW, Nguyen H, Mahrus S, Trinidad JC, Burlingame AL, Wells JA. Quantitative profiling of caspasecleaved substrates reveals different drug-induced and cell-type patterns in apoptosis. Proc Natl Acad Sci USA 2012; 109: 12432-7.
12. Fischer U, Janicke RU, Schulze-Osthoff K. Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ 2003; 10: 76-100.
13. Galluzzi L, Kepp O, Trojel-Hansen C, Kroemer G. Mitochondrial control of cellular life, stress, and death. Circ Res 2012; 111: 1198-207.
14. Tait SWG, Green DR. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010; 11: 621-32.
15. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87: 99-163.
16. Reubold TF, Eschenburg S. A molecular view on signal transduction by the apoptosome. Cell Signal 2012; 24: 1420-5.
17. Crawford ED, Wells JA. Caspase substrates and cellular remodeling. Annu Rev Biochem 2011; 80: 1055-87.
18. Shamas-Din A, Brahmbhatt H, Leber B, Andrews DW. BH3-only proteins: orchestrators of apoptosis. Biochim Biophys Acta 2011; 1813: 508-20.
19. Chipuk JE, Green DR. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization ? Trends Cell Biol 2008; 18: 157-64.
20. Brenner D, Mak TW. Mitochondrial cell death effectors. Curr Opin Cell Biol 2009; 21: 871-7.
21. Dickens LS, Powley IR, Hughes MA, MacFarlane M. The ' complexities ' of life and death: death receptor signalling platforms. Exp Cell Res 2012; 318: 1269-77.
22. Lavrik IN, Krammer PH. Regulation of CD95/Fas signaling at the DISC. Cell Death Differ 2012; 19: 36-41.
23. Cabal-Hierro L, Lazo PS. Signal transduction by tumor necrosis factor receptors. Cell Signal 2012; 24: 1297-305.
24. Mahalingam D, Szegezdi E, Keane M, de Jong S, Samali A. TRAIL receptor signalling and modulation: are we on the right TRAIL ? Cancer Treatment Rev 2009; 35: 280-8.
25. Gyrd-Hansen M, Meier P. IAPs: from caspase inhibitors to modulators of NF-kappa B, inflammation and cancer. Nat Rev Cancer 2010; 10: 561-74.
26. Darding M, Meier P. IAPs: guardians of RIPK1. Cell Death Differ 2012; 19: 58-66.
27. Safa AR. c-FLIP, a master anti-apoptotic regulator. Exp Oncol 2012; 34: 176-84.
28. Ozturk S, Schleich K, Lavrik IN. Cellular FLICE-like inhibitory proteins (c-FLIPs): fine-tuners of life and death decisions. Exp Cell Res 2012; 318: 1324-31.
29. Kantari C, Walczak H. Caspase-8 and bid: caught in the act between death receptors and mitochondria. Biochim Biophys Acta 2011; 1813: 558-63.
30. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140: 313-26.
31. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
32. Yang ZF, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010; 22: 124-31.
33. Mizushima N. Autophagy: process and function. Gene Dev 2007; 21: 2861-73.
34. Mehrpour M, Esclatine A, Beau I, Codogno P. Overview of macroautophagy regulation in mammalian cells. Cell Res 2010; 20: 748-62.
35. Wirawan E, Berghe TV, Lippens S, Agostinis P, Vandenabeele P. Autophagy: for better or for worse. Cell Res 2012; 22: 43-61.
36. Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40: 280-93.
37. He CC, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43: 67-93.
38. Shaid S, Brandts CH, Serve H, Dikic I. Ubiquitination and selective autophagy. Cell Death Differ 2013; 20: 21-30.
39. Shen HM, Codogno P. Autophagic cell death Loch Ness monster or endangered species ? Autophagy 2011; 7: 457-65.
40. Shen SS, Kepp O, Kroemer G. The end of autophagic cell death ? Autophagy 2012; 8: 1-3.
41. Subramani S, Malhotra V. Non-autophagic roles of autophagyrelated proteins. EMBO Rep 2013; 14: 143-51.
42. Gump JM, Thorburn A. Autophagy and apoptosis: what is the connection ? Trends Cell Biol 2011; 21: 387-92.
43. Berry DL, Baehrecke EH. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 2007; 131: 1137-48.
44. Grooten J, Goossens V, Vanhaesebroeck B, Fiers W. Cell membrane permeabilization and cellular collapse, followed by loss of dehydrogenase activity: early events in tumour necrosis factor-induced cytotoxicity. Cytokine 1993; 5: 546-55.
45. Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W, Grooten J, Fiers W, Vandenabeele P. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 1998; 187: 1477-85.
46. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B, Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 2000; 1: 489-95.
47. Laster SM, Wood JG, Gooding LR. Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J Immunol 1988; 141: 2629-34.
48. Denecker G, Vercammen D, Steemans M, Vanden Berghe T, Brouckaert G, Van Loo G, Zhivotovsky B, Fiers W, Grooten J, Declercq W, Vandenabeele P. Death receptor-induced apoptotic and necrotic cell death: differential role of caspases and mitochondria. Cell Death Differ 2001; 8: 829-40.
49. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005; 1: 112-9.
50. Russell SW, Rosenau W, Lee JC. Cytolysis induced by human lymphotoxin. Am J Pathol 1972; 69: 103-18.
51. Sakon S, Xue X, Takekawa M, Sasazuki T, Okazaki T, Kojima Y, Piao JH, Yagita H, Okumura K, Doi T, Nakano H. NF-kappaB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J 2003; 22: 3898-909.
52. Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS, Tran JH, Nedospasov SA, Liu ZG. Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting proteinmediated cellular reactive oxygen species accumulation. J Biol Chem 2004; 279: 10822-8.
53. He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 2009; 137: 1100-11.
54. Morgan MJ, Liu ZG. Reactive oxygen species in TNFalphainduced signaling and cell death. Mol Cells 2010; 30: 1-12.
55. Devin A, Lin Y, Liu ZG. The role of the death-domain kinase RIP in tumour-necrosis-factor-induced activation of mitogen-activated protein kinases. EMBO Rep 2003; 4: 623-7.
56. Degterev A, Hitomi J, Germscheid M, Ch ' en IL, Korkina O, Teng X, Abbott D, Cuny GD, Yuan C, Wagner G, Hedrick SM, Gerber SA, Lugovskoy A, Yuan J. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 2008; 4: 313-21.
57. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009; 137: 1112-23.
58. Christofferson DE, Li Y, Hitomi J, Zhou W, Upperman C, Zhu H, Gerber SA, Gygi S, Yuan J. A novel role for RIP1 kinase in mediating TNFalpha production. Cell Death Dis 2012; 3: e320.
59. Biton S, Ashkenazi A. NEMO and RIP1 control cell fate in response to extensive DNA damage via TNF-alpha feedforward signaling. Cell 2011; 145: 92-103.
60. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009; 325: 332-6.
61. Sun X, Yin J, Starovasnik MA, Fairbrother WJ, Dixit VM. Identification of a novel homotypic interaction motif required for the phosphorylation of receptor-interacting protein (RIP) by RIP3. J Biol Chem 2002; 277: 9505-11.
62. Li J, McQuade T, Siemer AB, Napetschnig J, Moriwaki K, Hsiao YS, Damko E, Moquin D, Walz T, McDermott A, Chan FK, Wu H. The RIP1/ RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 2012; 150: 339-50.
63. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010; 11: 700-14.
64. Zhao J, Jitkaew S, Cai Z, Choksi S, Li Q, Luo J, Liu ZG. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc Natl Acad Sci USA 2012; 109: 5322-7.
65. Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X, Wang X. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012; 148: 213-27.
66. Takeda K, Komuro Y, Hayakawa T, Oguchi H, Ishida Y, Murakami S, Noguchi T, Kinoshita H, Sekine Y, Iemura S, Natsume T, Ichijo H. Mitochondrial phosphoglycerate mutase 5 uses alternate catalytic activity as a protein serine/threonine phosphatase to activate ASK1. Proc Natl Acad Sci USA 2009; 106: 12301-5.
67. Wang Z, Jiang H, Chen S, Du F, Wang X. The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 2012; 148: 228-43.
68. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science 2012; 337: 1062-5.
69. Whelan RS, Konstantinidis K, Wei AC, Chen Y, Reyna DE, Jha S, Yang Y, Calvert JW, Lindsten T, Thompson CB, Crow MT, Gavathiotis E, Dorn GW, O ' Rourke B, Kitsis RN. Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci USA 2012; 109: 6566-71.
70. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, Gillard JW, Jaquith JB, Morris SJ, Barker PA. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 2008; 30: 689-700.
71. Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E, Haas TL, Webb AI, Rickard JA, Anderton H, Wong WW, Nachbur U, Gangoda L, Warnken U, Purcell AW, Silke J, Walczak H. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 2011; 471: 591-6.
72. Bertrand MJ, Lippens S, Staes A, Gilbert B, Roelandt R, De Medts J, Gevaert K, Declercq W, Vandenabeele P. cIAP1/2 are direct E3 ligases conjugating diverse types of ubiquitin chains to receptor interacting proteins kinases 1 to 4 (RIP1-4). PLoS One 2011; 6: e22356.
73. Li HX, Kobayashi M, Blonska M, You Y, Lin X. Ubiquitination of RIP is required for tumor necrosis factor alpha-induced NF-kappa B activation. J Biol Chem 2006; 281: 13636-43.
74. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 2006; 22: 245-57.
75. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008; 133: 693-703.
76. Vanlangenakker N, Vanden Berghe T, Bogaert P, Laukens B, Zobel K, Deshayes K, Vucic D, Fulda S, Vandenabeele P, Bertrand MJ. cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ 2011; 18: 656-65.
77. O ' Donnell MA, Hase H, Legarda D, Ting AT. NEMO Inhibits Programmed Necrosis in an NFkappaB-independent manner by restraining RIP1. PLoS One 2012; 7: e41238.
78. Kovalenko A, Chable-Bessia C, Cantarella G, Israel A, Wallach D, Courtois G. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 2003; 424: 801-5.
79. Wertz IE, O ' Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, Ma A, Koonin EV, Dixit VM. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004; 430: 694-9.
80. Heyninck K, Denecker G, De Valck D, Fiers W, Beyaert R. Inhibition of tumor necrosis factor-induced necrotic cell death by the zinc finger protein A20. Anticancer Res 1999; 19: 2863-8.
81. Storz P, Doppler H, Ferran C, Grey ST, Toker A. Functional dichotomy of A20 in apoptotic and necrotic cell death. Biochem J 2005; 387: 47-55.
82. Vanlangenakker N, Bertrand MJ, Bogaert P, Vandenabeele P, Vanden Berghe T. TNF-induced necroptosis in L929 cells is tightly regulated by multiple TNFR1 complex I and II members. Cell Death Dis 2011; 2: e230.
83. Narayan N, Lee IH, Borenstein R, Sun J, Wong R, Tong G, Fergusson MM, Liu J, Rovira, II, Cheng HL, Wang G, Gucek M, Lombard D, Alt FW, Sack MN, Murphy E, Cao L, Finkel T. The NAD-dependent deacetylase SIRT2 is required for programmed necrosis. Nature 2012; 492: 199-204.
84. Lin Y, Devin A, Rodriguez Y, Liu ZG. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev 1999; 13: 2514-26.
85. Feng S, Yang Y, Mei Y, Ma L, Zhu DE, Hoti N, Castanares M, Wu M. Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain. Cell Signal 2007; 19: 2056-67.
86. O ' Donnell MA, Perez-Jimenez E, Oberst A, Ng A, Massoumi R, Xavier R, Green DR, Ting AT. Caspase 8 inhibits programmed necrosis by processing CYLD. Nat Cell Biol 2011; 13: 1437-42.
87. Bonnet MC, Preukschat D, Welz PS, van Loo G, Ermolaeva MA, Bloch W, Haase I, Pasparakis M. The adaptor protein FADD protects epidermal keratinocytes from necroptosis in vivo and prevents skin inflammation. Immunity 2011; 35: 572-82.
88. Ch ' en IL, Tsau JS, Molkentin JD, Komatsu M, Hedrick SM. Mechanisms of necroptosis in T cells. J Exp Med 2011; 208: 633-41.
89. Dillon CP, Oberst A, Weinlich R, Janke LJ, Kang TB, Ben-Moshe T, Mak TW, Wallach D, Green DR. Survival function of the FADD-CASPASE-8-cFLIP(L) complex. Cell Rep 2012; 1: 401-7.
90. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, Caspary T, Mocarski ES. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011; 471: 368-72.
91. Lu JV, Weist BM, van Raam BJ, Marro BS, Nguyen LV, Srinivas P, Bell BD, Luhrs KA, Lane TE, Salvesen GS, Walsh CM. Complementary roles of Fas-associated death domain (FADD) and receptor interacting protein kinase-3 (RIPK3) in T-cell homeostasis and antiviral immunity. Proc Natl Acad Sci USA 2011; 108: 15312-7.
92. Moulin M, Anderton H, Voss AK, Thomas T, Wong WW, Bankovacki A, Feltham R, Chau D, Cook WD, Silke J, Vaux DL. IAPs limit activation of RIP kinases by TNF receptor 1 during development. EMBO J 2012; 31: 1679-91.
93. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C, Hakem R, Salvesen GS, Green DR. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011; 471: 363-7.
94. Zhang HB, Zhou XH, McQuade T, Li JH, Chan FKM, Zhang JK. Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 2011; 471: 373-6.
95. Upton JW, Kaiser WJ, Mocarski ES. Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 2010; 7: 302-13.
96. Vanden Berghe T, Vanlangenakker N, Parthoens E, Deckers W, Devos M, Festjens N, Guerin CJ, Brunk UT, Declercq W, Vandenabeele P. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ 2010; 17: 922-30.
97. Upton JW, Kaiser WJ, Mocarski ES. DAI/ZBP1/DLM-1 Complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 2012; 11: 290-7.
98. Goossens V, Grooten J, De Vos K, Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci USA 1995; 92: 8115-9.
99. Ventura JJ, Cogswell P, Flavell RA, Baldwin AS Jr, Davis RJ. JNK potentiates TNF-stimulated necrosis by increasing the production of cytotoxic reactive oxygen species. Genes Dev 2004; 18: 2905-15.
100. Schulze-Osthoff K, Bakker AC, Vanhaesebroeck B, Beyaert R, Jacob WA, Fiers W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J Biol Chem 1992; 267: 5317-23.
101. Schulze-Osthoff K, Beyaert R, Vandevoorde V, Haegeman G, Fiers W. Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene-inductive effects of TNF. EMBO J 1993; 12: 3095-104.
102. Goossens V, De Vos K, Vercammen D, Steemans M, Vancompernolle K, Fiers W, Vandenabeele P, Grooten J. Redox regulation of TNF signaling. BioFactors (Oxford, England) 1999; 10: 145-56.
103. Festjens N, Kalai M, Smet J, Meeus A, Van Coster R, Saelens X, Vandenabeele P. Butylated hydroxyanisole is more than a reactive oxygen species scavenger. Cell Death Differ 2006; 13: 166-9.
104. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T, Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005; 434: 652-8.
105. Li Y, Johnson N, Capano M, Edwards M, Crompton M. Cyclophilin-D promotes the mitochondrial permeability transition but has opposite effects on apoptosis and necrosis. Biochem J 2004; 383: 101-9.
106. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci USA 2005; 102: 12005-10.
107. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005; 434: 658-62.
108. Sato T, Machida T, Takahashi S, Murase K, Kawano Y, Hayashi T, Iyama S, Takada K, Kuribayashi K, Sato Y, Kobune M, Takimoto R, Matsunaga T, Kato J, Niitsu Y. Apoptosis supercedes necrosis in mitochondrial DNA-depleted Jurkat cells by cleavage of receptorinteracting protein and inhibition of lysosomal cathepsin. J Immunol 2008; 181: 197-207.
109. Luke CJ, Pak SC, Askew YS, Naviglia TL, Askew DJ, Nobar SM, Vetica AC, Long OS, Watkins SC, Stolz DB, Barstead RJ, Moulder GL, Bromme D, Silverman GA. An intracellular serpin regulates necrosis by inhibiting the induction and sequelae of lysosomal injury. Cell 2007; 130: 1108-19.
110. Los M, Mozoluk M, Ferrari D, Stepczynska A, Stroh C, Renz A, Herceg Z, Wang ZQ, Schulze-Osthoff K. Activation and caspasemediated inhibition of PARP: a molecular switch between fibroblast necrosis and apoptosis in death receptor signaling. Mol Biol Cell 2002; 13: 978-88.
111. Xu Y, Huang S, Liu ZG, Han J. Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/ TRAF2-mediated JNK1 activation. J Biol Chem 2006; 281: 8788-95.
112. Delavallee L, Cabon L, Galan-Malo P, Lorenzo HK, Susin SA. AIF-mediated caspase-independent necroptosis: a new chance for targeted therapeutics. IUBMB Life 2011; 63: 221-32.
113. Moubarak RS, Yuste VJ, Artus C, Bouharrour A, Greer PA, Menissier-de Murcia J, Susin SA. Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol Cell Biol 2007; 27: 4844-62.
114. David KK, Andrabi SA, Dawson TM, Dawson VL. Parthanatos, a messenger of death. Front Biosci 2009; 14: 1116-28.
115. Shen HM, Liu ZG. JNK signaling pathway is a key modulator in cell death mediated by reactive oxygen and nitrogen species. Free Radic Biol Med 2006; 40: 928-39.
116. Kinnally KW, Peixoto PM, Ryu SY, Dejean LM. Is mPTP the gatekeeper for necrosis, apoptosis, or both ? Biochim Biophys Acta 2011; 1813: 616-22.
117. Halestrap AP. What is the mitochondrial permeability transition pore ? J Mol Cell Cardiol 2009; 46: 821-31.
118. Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 2012; 149: 1536-48.
119. Boya P, Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene 2008; 27: 6434-51.
120. Kreuzaler P, Watson CJ. Killing a cancer: what are the alternatives ? Nat Rev Cancer 2012; 12: 411-24.
121. Artal-Sanz M, Samara C, Syntichaki P, Tavernarakis N. Lysosomal biogenesis and function is critical for necrotic cell death in Caenorhabditis elegans. J Cell Biol 2006; 173: 231-9.
122. Tu HC, Ren D, Wang GX, Chen DY, Westergard TD, Kim H, Sasagawa S, Hsieh JJ, Cheng EH. The p53-cathepsin axis cooperates with ROS to activate programmed necrotic death upon DNA damage. Proc Natl Acad Sci USA 2009; 106: 1093-8.
123. Kurz T, Terman A, Gustafsson B, Brunk UT. Lysosomes in iron metabolism, ageing and apoptosis. Histochem Cell Biol 2008; 129: 389-406.
124. Kurz T, Gustafsson B, Brunk UT. Intralysosomal iron chelation protects against oxidative stress-induced cellular damage. FEBS J 2006; 273: 3106-17.
125. Krishnakumar R, Kraus WL. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell 2010; 39: 8-24.
126. Bai P, Canto C. The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab 2012; 16: 290-5.
127. Berger NA. Symposium-cellular-response to DNA damage-the role of poly(ADP-ribose)-poly(ADP-ribose) in the cellular-response to DNA damage. Radiat Res 1985; 101: 4-15.
128. Ha HC, Snyder SH. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA 1999; 96: 13978-82.
129. Oleinick NL, Evans HH. Poly(ADP-ribose) and the response of cells to ionizing-radiation. radiat res 1985; 101: 29-46.
130. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 2011; 27: 441-64.
131. Ying WH, Alano CC, Garnier P, Swanson RA. NAD( + ) as a metabolic link between DNA damage and cell death. J Neurosci Res 2005; 79: 216-23.
132. Alano CC, Ying WH, Swanson RA. Poly(ADP-ribose) polymerase-1-mediated cell death in astrocytes requires NAD( + ) depletion and mitochondrial permeability transition. J Biol Chem 2004; 279: 18895-902.
133. Hafner AV, Dai J, Gomes AP, Xiao CY, Palmeira CM, Rosenzweig A, Sinclair DA. Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging 2010; 2: 914-23.
134. Shulga N, Wilson-Smith R, Pastorino JG. Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria. J Cell Sci 2010; 123: 894-902.
135. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002; 297: 259-63.
136. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397: 441-6.
137. Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, Dawson VL. Apoptosis-inducing factor mediates poly(ADPribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 2006; 103: 18314-9.
138. Wang Y, Kim NS, Haince JF, Kang HC, David KK, Andrabi SA, Poirier GG, Dawson VL, Dawson TM. Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci Signal 2011; 4: ra20.
139. Jouan-Lanhouet S, Arshad MI, Piquet-Pellorce C, Martin-Chouly C, Le Moigne-Muller G, Van Herreweghe F, Takahashi N, Sergent O, Lagadic-Gossmann D, Vandenabeele P, Samson M, Dimanche-Boitrel MT. TRAIL induces necroptosis involving RIPK1/ RIPK3-dependent PARP-1 activation. Cell Death Differ 2012; 19: 2003-14.
140. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, Xavier RJ, Yuan J. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 2008; 135: 1311-23.
141. Wang YF, Kim NS, Li XL, Greer PA, Koehler RC, Dawson VL, Dawson TM. Calpain activation is not required for AIF translocation in PARP-1-dependent cell death (parthanatos). J Neurochem 2009; 110: 687-96.
142. Dutta C, Day T, Kopp N, van Bodegom D, Davids MS, Ryan J, Bird L, Kommajosyula N, Weigert O, Yoda A, Fung H, Brown JR, Shapiro GI, Letai A, Weinstock DM. BCL2 suppresses PARP1 function and nonapoptotic cell death. Cancer Res 2012; 72: 4193-203.
143. Ye K. PARP inhibitor tilts cell death from necrosis to apoptosis in cancer cells. Cancer Biol Ther 2008; 7: 942-4.
144. Tentori L, Balduzzi A, Portarena I, Levati L, Vernole P, Gold B, Bonmassar E, Graziani G. Poly (ADP-ribose) polymerase inhibitor increases apoptosis and reduces necrosis induced by a DNA minor groove binding methyl sulfonate ester. Cell Death Differ 2001; 8: 817-28.
145. Eliasson MJ, Sampei K, Mandir AS, Hurn PD, Traystman RJ, Bao J, Pieper A, Wang ZQ, Dawson TM, Snyder SH, Dawson VL. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med 1997; 3: 1089-95.
146. Zheng J, Devalaraja-Narashimha K, Singaravelu K, Padanilam BJ. Poly(ADP-ribose) polymerase-1 gene ablation protects mice from ischemic renal injury. Am J Physiol Renal Physiol 2005; 288: F387-98.
147. Yang Z, Zingarelli B, Szabo C. Effect of genetic disruption of poly (ADP-ribose) synthetase on delayed production of inflammatory mediators and delayed necrosis during myocardial ischemia-reperfusion injury. Shock 2000; 13: 60-6.
148. Soriano FG, Liaudet L, Szabo E, Virag L, Mabley JG, Pacher P, Szabo C. Resistance to acute septic peritonitis in poly(ADPribose) polymerase-1-deficient mice. Shock 2002; 17: 286-92.
149. Liaudet L, Soriano FG, Szabo E, Virag L, Mabley JG, Salzman AL, Szabo C. Protection against hemorrhagic shock in mice genetically deficient in poly(ADP-ribose)polymerase. Proc Natl Acad Sci USA 2000; 97: 10203-8.
150. Mota RA, Hernandez-Espinosa D, Galbis-Martinez L, Ordonez A, Minano A, Parrilla P, Vicente V, Corral J, Yelamos J. Poly(ADP-ribose) polymerase-1 inhibition increases expression of heat shock proteins and attenuates heat stroke-induced liver injury. Crit Care Med 2008; 36: 526-34.
151. Saito Y, Nishio K, Ogawa Y, Kimata J, Kinumi T, Yoshida Y, Noguchi N, Niki E. Turning point in apoptosis/necrosis induced by hydrogen peroxide. Free Radic Res 2006; 40: 619-30.
152. Takeda M, Shirato I, Kobayashi M, Endou H. Hydrogen peroxide induces necrosis, apoptosis, oncosis and apoptotic oncosis of mouse terminal proximal straight tubule cells. Nephron 1999; 81: 234-8.
153. Teramoto S, Tomita T, Matsui H, Ohga E, Matsuse T, Ouchi Y. Hydrogen peroxide-induced apoptosis and necrosis in human lung fibroblasts: protective roles of glutathione. Jpn J Pharmacol 1999; 79: 33-40.
154. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, Minowa O, Miyazono K, Noda T, Ichijo H. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2001; 2: 222-8.
155. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005; 120: 649-61.
156. Chang L, Kamata H, Solinas G, Luo JL, Maeda S, Venuprasad K, Liu YC, Karin M. The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover. Cell 2006; 124: 601-13.
157. Ventura JJ, Hubner A, Zhang C, Flavell RA, Shokat KM, Davis RJ. Chemical genetic analysis of the time course of signal transduction by JNK. Mol Cell 2006; 21: 701-10.
158. Morgan MJ, Kim Y-S. Nox1, Reactive oxygen species, JNK, and necrotic cell death. In: Shen HM, Vandenabeele P, editors. Cell death: necrotic cell death. New York, NY: Springer/Humana Press 2013 [in press].
159. Chambers JW, LoGrasso PV. Mitochondrial c-Jun N-terminal kinase (JNK) signaling initiates physiological changes resulting in amplification of reactive oxygen species generation. J Biol Chem 2011; 286: 16052-62.
160. Goossens V, Stange G, Moens K, Pipeleers D, Grooten J. Regulation of tumor necrosis factor-induced, mitochondriaand reactive oxygen species-dependent cell death by the electron flux through the electron transport chain complex I. Antioxid Redox Signal 1999; 1: 285-95.
161. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis 2007; 12: 913-22.
162. Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 2007; 47: 143-83.
163. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 2004; 4: 181-9.
164. Brown DI, Griendling KK. Nox proteins in signal transduction. Free Radic Biol Med 2009; 47: 1239-53.
165. Morgan MJ, Kim YS, Liu ZG. TNFalpha and reactive oxygen species in necrotic cell death. Cell Res 2008; 18: 343-9.
166. Byun HS, Won M, Park KA, Kim YR, Choi BL, Lee H, Hong JH, Piao L, Park J, Kim JM, Kweon GR, Kang SH, Han J, Hur GM. Prevention of TNF-induced necrotic cell death by rottlerin through a Nox1 NADPH oxidase. Exp Mol Med 2008; 40: 186-95.
167. Kim YS, Morgan MJ, Choksi S, Liu ZG. TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol Cell 2007; 26: 675-87.
168. Yazdanpanah B, Wiegmann K, Tchikov V, Krut O, Pongratz C, Schramm M, Kleinridders A, Wunderlich T, Kashkar H, Utermohlen O, Bruning JC, Schutze S, Kronke M. Riboflavin kinase couples TNF receptor 1 to NADPH oxidase. Nature 2009; 460: 1159-63.
169. Park KJ, Lee CH, Kim A, Jeong KJ, Kim CH, Kim YS. Death receptors 4 and 5 activate Nox1 NADPH oxidase through riboflavin kinase to induce reactive oxygen species-mediated apoptotic cell death. J Biol Chem 2012; 287: 3313-25.
170. Li WG, Miller FJ Jr, Zhang HJ, Spitz DR, Oberley LW, Weintraub NL. H 2 O(2)-induced O(2) production by a non-phagocytic NAD(P)H oxidase causes oxidant injury. J Biol Chem 2001; 276: 29251-6.
171. Lee SB, Bae IH, Bae YS, Um HD. Link between mitochondria and NADPH oxidase 1 isozyme for the sustained production of reactive oxygen species and cell death. J Biol Chem 2006; 281: 36228-35.
172. Pantano C, Anathy V, Ranjan P, Heintz NH, Janssen-Heininger YM. Nonphagocytic oxidase 1 causes death in lung epithelial cells via a TNF-RI-JNK signaling axis. Am J Respir Cell Mol Biol 2007; 36: 473-9.
173. Hanawa N, Shinohara M, Saberi B, Gaarde WA, Han D, Kaplowitz N. Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminopheninduced liver injury. J Biol Chem 2008; 283: 13565-77.
174. Bogoyevitch MA, Kobe B. Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol Mol Biol Rev 2006; 70: 1061-95.
175. Hubner A, Cavanagh-Kyros J, Rincon M, Flavell RA, Davis RJ. Functional cooperation of the proapoptotic Bcl2 family proteins Bmf and Bim in vivo. Mol Cell Biol 2010; 30: 98-105.
176. Kim BJ, Ryu SW, Song BJ. JNK-and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 2006; 281: 21256-65.
177. Tsuruta F, Sunayama J, Mori Y, Hattori S, Shimizu S, Tsujimoto Y, Yoshioka K, Masuyama N, Gotoh Y. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 2004; 23: 1889-99.
178. Cho Y, McQuade T, Zhang H, Zhang J, Chan FK. RIP1-dependent and independent effects of necrostatin-1 in necrosis and T cell activation. PLoS One 2011; 6: e23209.
179. Benakis C, Bonny C, Hirt L. JNK inhibition and inflammation after cerebral ischemia. Brain Behav Immun 2010; 24: 800-11.
180. Nijboer CH, van der Kooij MA, van Bel F, Ohl F, Heijnen CJ, Kavelaars A. Inhibition of the JNK/AP-1 pathway reduces neuronal death and improves behavioral outcome after neonatal hypoxic-ischemic brain injury. Brain Behav Immun 2010; 24: 812-21.
181. Kaiser RA, Liang Q, Bueno O, Huang Y, Lackey T, Klevitsky R, Hewett TE, Molkentin JD. Genetic inhibition or activation of JNK1/2 protects the myocardium from ischemia-reperfusioninduced cell death in vivo. J Biol Chem 2005; 280: 32602-8.
182. Kelliher MA, Grimm S, Ishida Y, Kuo F, Stanger BZ, Leder P. The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity 1998; 8: 297-303.
183. Xu XS, Chua KW, Chua CC, Liu CF, Hamdy RC, Chua BHL. Synergistic protective effects of humanin and necrostatin-1 on hypoxia and ischemia/reperfusion injury. Brain Res 2010; 1355: 189-94.
184. Northington FJ, Chavez-Valdez R, Graham EM, Razdan S, Gauda EB, Martin LJ. Necrostatin decreases oxidative damage, inflammation, and injury after neonatal HI. J Cereb Blood Flow Metab 2011; 31: 178-89.
185. You ZR, Savitz SI, Yang JS, Degterev A, Yuan JY, Cuny GD, Moskowitz MA, Whalen MJ. Necrostatin-1 reduces histopathology and improves functional outcome after controlled cortical impact in mice. J Cereb Blood Flow Metab 2008; 28: 1564-73.
186. Lim SY, Davidson SM, Mocanu MM, Yellon DM, Smith CC. The cardioprotective effect of necrostatin requires the cyclophilin-D component of the mitochondrial permeability transition pore. Cardiovasc Drugs Ther 2007; 21: 467-9.
187. Smith CCT, Davidson SM, Lim SY, Simpkin JC, Hothersall JS, Yellon DM. Necrostatin: a potentially novel cardioprotective agent? Cardiovasc Drug Ther 2007; 21: 227-33.
188. Oerlemans MIFJ, Liu J, Arslan F, den Ouden K, van Middelaar BJ, Doevendans PA, Sluijter JPG. Inhibition of RIP1-dependent necrosis prevents adverse cardiac remodeling after myocardial ischemia-reperfusion in vivo. Basic Res Cardiol 2012; 107: 270.
189. Zhu S, Zhang Y, Bai G, Li H. Necrostatin-1 ameliorates symptoms in R6/2 transgenic mouse model of Huntington ' s disease. Cell Death Dis 2011; 2: e115.
190. Linkermann A, Brasen JH, Himmerkus N, Liu SY, Huber TB, Kunzendorf U, Krautwald S. Rip1 (receptor-interacting protein kinase 1) mediates necroptosis and contributes to renal ischemia/reperfusion injury. Kidney Int 2012; 81: 751-61.
191. Takahashi N, Duprez L, Grootjans S, Cauwels A, Nerinckx W, DuHadaway JB, Goossens V, Roelandt R, Van Hauwermeiren F, Libert C, Declercq W, Callewaert N, Prendergast GC, Degterev A, Yuan J, Vandenabeele P. Necrostatin-1 analogues: critical issues on the specificity, activity and in vivo use in experimental disease models. Cell Death Dis 2012; 3: e437.
192. Degterev A, Maki JL, Yuan J. Activity and specificity of necrostatin-1, small-molecule inhibitor of RIP1 kinase. Cell Death Differ 2013; 20: 366.
193. Vandenabeele P, Grootjans S, Callewaert N, Takahashi N. Necrostatin-1 blocks both RIPK1 and IDO: consequences for the study of cell death in experimental disease models. Cell Death Differ 2013; 20: 185-7.
194. Linkermann A, Brasen JH, De Zen F, Weinlich R, Schwendener RA, Green DR, Kunzendorf U, Krautwald S. Dichotomy between RIP1-and RIP3-mediated necroptosis in tumor necrosis factoralpha-induced shock. Mol Med 2012; 18: 577-86.
195. Trichonas G, Murakami Y, Thanos A, Morizane Y, Kayama M, Debouck CM, Hisatomi T, Miller JW, Vavvas DG. Receptor interacting protein kinases mediate retinal detachmentinduced photoreceptor necrosis and compensate for inhibition of apoptosis. Proc Natl Acad Sci USA 2010; 107: 21695-700.
196. Murakami Y, Matsumoto H, Roh M, Suzuki J, Hisatomi T, Ikeda Y, Miller JW, Vavvas DG. Receptor interacting protein kinase mediates necrotic cone but not rod cell death in a mouse model of inherited degeneration. Proc Natl Acad Sci USA 2012; 109: 14598-603.
197. Roychowdhury S, McMullen MR, Pisano SG, Liu XL, Nagy LE. Absence of receptor interacting protein kinase 3 prevents ethanol-induced liver injury. Hepatology 2012; 56: 981A-A.
198. Lin J, Li H, Yang M, Ren J, Huang Z, Han F, Huang J, Ma J, Zhang D, Zhang Z, Wu J, Huang D, Qiao M, Jin G, Wu Q, Huang Y, Du J, Han J. A Role of RIP3-mediated macrophage necrosis in atherosclerosis development. Cell Rep 2013; 3: 200-10.
199. Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar typhimurium . Nat Immunol 2012; 13: 954-62.