Mitochondrial regulation of cell death: A phylogenetically conserved control

Microbial Cell

Volumn 3, Issue 3, 2016, Pages 101-108

  Galluzzi, Lorenzo ^a,b,c,d,e   Kepp, Oliver ^a,b,c,d,e   Kroemer, Guido ^{a,b,c,d,e,f,g}  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e INSTITUT GUSTAVE ROUSSY   (France)

^f KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^g HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

Apoptosis; Autophagy; Autosis; Ferroptosis; MTP driven regulated necrosis; Necroptosis; Parthanatos; Pyroptosis

Indexed keywords

EID: 84991215710     PISSN: None     EISSN: 23112638     Source Type: Journal    
DOI: 10.15698/mic2016.03.483     Document Type: Article

References (99)

1. Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D, Alnemri ES, Altucci L, Andrews D, Annicchiarico-Petruzzelli M, Baehrecke EH, Bazan NG, Bertrand MJ, Bianchi K, Blagosklonny MV, Blomgren K, Borner C, Bredesen DE, Brenner C, Campanella M, Candi E, Cecconi F, Chan FK, Chandel NS, Cheng EH, Chipuk JE, Cidlowski JA, Ciechanover A, Dawson TM, Dawson VL, et al. (2015). Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ 22(1): 58-73.
2. Galluzzi L, Bravo-San Pedro JM, Kroemer G (2014). Organelle-specific initiation of cell death. Nat Cell Biol 16(8): 728-736.
3. Green DR, Galluzzi L, Kroemer G (2014). Cell biology. Metabolic control of cell death. Science 345(6203): 1250256.
4. Green DR, Levine B (2014). To be or not to be? How selective autophagy and cell death govern cell fate. Cell 157(1): 65-75.
5. Hetz C, Chevet E, Harding HP (2013). Targeting the unfolded protein response in disease. Nat Rev Drug Discov 12(9): 703-719.
6. Sica V, Galluzzi L, Bravo-San Pedro JM, Izzo V, Maiuri MC, Kroemer G (2015). Organelle-specific initiation of autophagy. Mol Cell 59(4): 522-539.
7. Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F, Codogno P, Debnath J, Gewirtz DA, Karantza V, Kimmelman A, Kumar S, Levine B, Maiuri MC, Martin SJ, Penninger J, Piacentini M, Rubinsztein DC, Simon HU, Simonsen A, Thorburn AM, Velasco G, Ryan KM, Kroemer G (2015). Autophagy in malignant transformation and cancer progression. EMBO J 34(7): 856-880.
8. Galluzzi L, Blomgren K, Kroemer G (2009). Mitochondrial membrane permeabilization in neuronal injury. Nat Rev Neurosci 10(7): 481-494.
9. Friese MA, Schattling B, Fugger L (2014). Mechanisms of neurodegeneration and axonal dysfunction in multiple sclerosis. Nat Rev Neurol 10(4): 225-238.
10. Brenner C, Galluzzi L, Kepp O, Kroemer G (2013). Decoding cell death signals in liver inflammation. J Hepatol 59(3): 583-594.
11. Fuchs Y, Steller H (2011). Programmed cell death in animal development and disease. Cell 147(4): 742-758.
12. Green DR, Victor B (2012). The pantheon of the fallen: why are there so many forms of cell death? Trends Cell Biol 22(11): 555-556.
13. Bender CE, Fitzgerald P, Tait SW, Llambi F, McStay GP, Tupper DO, Pellettieri J, Sanchez Alvarado A, Salvesen GS, Green DR (2012). Mitochondrial pathway of apoptosis is ancestral in metazoans. Proc Natl Acad Sci U S A 109(13): 4904-4909.
14. Degterev A, Yuan J (2008). Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 9(5): 378-390.
15. 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, et al. (2012). Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 19(1): 107-120.
16. Tait SW, Green DR (2010). Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11(9): 621-632.
17. Kroemer G, Galluzzi L, Brenner C (2007). Mitochondrial membrane permeabilization in cell death. Physiol Rev 87(1): 99-163.
18. Taylor RC, Cullen SP, Martin SJ (2008). Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 9(3): 231-241.
19. Wajant H (2002). The Fas signaling pathway: more than a paradigm. Science 296(5573): 1635-1636.
20. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G (2010). Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 11(10): 700-714.
21. Linkermann A, Green DR (2014). Necroptosis. N Engl J Med 370(5): 455-465.
22. Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P (2014). Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol 15(2): 135-147.
23. Galluzzi L, Kepp O, Krautwald S, Kroemer G, Linkermann A (2014). Molecular mechanisms of regulated necrosis. Semin Cell Dev Biol 35:24-32.
24. Bonora M, Wieckowski MR, Chinopoulos C, Kepp O, Kroemer G, Galluzzi L, Pinton P (2015). Molecular mechanisms of cell death: central implication of ATP synthase in mitochondrial permeability transition. Oncogene 34(12): 1475-1486.
25. Linkermann A, Skouta R, Himmerkus N, Mulay SR, Dewitz C, De Zen F, Prokai A, Zuchtriegel G, Krombach F, Welz PS, Weinlich R, Vanden Berghe T, Vandenabeele P, Pasparakis M, Bleich M, Weinberg JM, Reichel CA, Brasen JH, Kunzendorf U, Anders HJ, Stockwell BR, Green DR, Krautwald S (2014). Synchronized renal tubular cell death involves ferroptosis. Proc Natl Acad Sci U S A 111(47): 16836-16841.
26. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, Morrison B, 3rd, Stockwell BR (2012). Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149(5): 1060-1072.
27. Liu Y, Shoji-Kawata S, Sumpter RM, Jr., Wei Y, Ginet V, Zhang L, Posner B, Tran KA, Green DR, Xavier RJ, Shaw SY, Clarke PG, Puyal J, Levine B (2013). Autosis is a Na+,K+-ATPase-regulated form of cell death triggered by autophagy-inducing peptides, starvation, and hy-poxia-ischemia. Proc Natl Acad Sci U S A 110(51): 20364-20371.
28. Liu Y, Levine B (2015). Autosis and autophagic cell death: the dark side of autophagy. Cell Death Differ 22(3): 367-376.
29. Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu J, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX, Fitzgerald L, Zhang Y, Bertram EM, Goodnow CC, Dixit VM (2015). Caspase-11 cleaves gasdermin D for non-canonical inflammasome signaling. Nature.
30. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F (2015). Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature.
31. Lim Y, Kumar S (2015). A single cut to pyroptosis. Oncotarget 6(35): 36926-36927.
32. Galluzzi L, Kepp O, Kroemer G (2012). Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol 13(12): 780-788.
33. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996). Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86(1): 147-157.
34. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X (1997). Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90(3): 405-413.
35. Galluzzi L, Kepp O, Trojel-Hansen C, Kroemer G (2012). Nonapoptotic functions of apoptosis-regulatory proteins. EMBO Rep 13(4): 322-330.
36. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ (2001). Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292(5517): 727-730.
37. Czabotar PE, Lessene G, Strasser A, Adams JM (2014). Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol 15(1): 49-63.
38. Chipuk JE, Green DR (2008). How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol 18(4): 157-164.
39. Edlich F, Banerjee S, Suzuki M, Cleland MM, Arnoult D, Wang C, Neutzner A, Tjandra N, Youle RJ (2011). Bcl-x(L) retrotranslocates Bax from the mitochondria into the cytosol. Cell 145(1): 104-116.
40. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G (1995). Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182(2): 367-377.
41. Zamzami N, Marchetti P, Castedo M, Zanin C, Vayssiere JL, Petit PX, Kroemer G (1995). Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J Exp Med 181(5): 1661-1672.
42. Segawa K, Kurata S, Yanagihashi Y, Brummelkamp TR, Matsuda F, Nagata S (2014). Caspase-mediated cleavage of phospholipid flippase for apoptotic phosphatidylserine exposure. Science 344(6188): 1164-1168.
43. Suzuki J, Denning DP, Imanishi E, Horvitz HR, Nagata S (2013). Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science 341(6144): 403-406.
44. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nunez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G, Nomenclature Committee on Cell D (2009). Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16(1): 3-11.
45. Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A, Nagata S (1998). A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391(6662): 43-50.
46. Huang Q, Li F, Liu X, Li W, Shi W, Liu FF, O'Sullivan B, He Z, Peng Y, Tan AC, Zhou L, Shen J, Han G, Wang XJ, Thorburn J, Thorburn A, Jime-no A, Raben D, Bedford JS, Li CY (2011). Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat Med 17(7): 860-866.
47. Gibert B, Mehlen P (2015). Dependence Receptors and Cancer: Addiction to Trophic Ligands. Cancer Res 75(24): 5171-5175.
48. Fombonne J, Bissey PA, Guix C, Sadoul R, Thibert C, Mehlen P (2012). Patched dependence receptor triggers apoptosis through ubiquitination of caspase-9. Proc Natl Acad Sci U S A 109(26): 10510-10515.
49. Mille F, Thibert C, Fombonne J, Rama N, Guix C, Hayashi H, Corset V, Reed JC, Mehlen P (2009). The Patched dependence receptor triggers apoptosis through a DRAL-caspase-9 complex. Nat Cell Biol 11(6): 739-746.
50. Guenebeaud C, Goldschneider D, Castets M, Guix C, Chazot G, Delloye-Bourgeois C, Eisenberg-Lerner A, Shohat G, Zhang M, Laudet V, Kimchi A, Bernet A, Mehlen P (2010). The dependence receptor UNC5H2/B triggers apoptosis via PP2A-mediated dephosphorylation of DAP kinase. Mol Cell 40(6): 863-876.
51. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J, Scaffidi C, Bretz JD, Zhang M, Gentz R, Mann M, Krammer PH, Peter ME, Dixit VM (1996). FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death--inducing signaling complex. Cell 85(6): 817-827.
52. Medema JP, Scaffidi C, Kischkel FC, Shevchenko A, Mann M, Krammer PH, Peter ME (1997). FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J 16(10): 2794-2804.
53. Schutze S, Tchikov V, Schneider-Brachert W (2008). Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat Rev Mol Cell Biol 9(8): 655-662.
54. Barnhart BC, Alappat EC, Peter ME (2003). The CD95 type I/type II model. Semin Immunol 15(3): 185-193.
55. Li H, Zhu H, Xu CJ, Yuan J (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94(4): 491-501.
56. Yin XM, Wang K, Gross A, Zhao Y, Zinkel S, Klocke B, Roth KA, Korsmeyer SJ (1999). Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400(6747): 886-891.
57. Jost PJ, Grabow S, Gray D, McKenzie MD, Nachbur U, Huang DC, Bouillet P, Thomas HE, Borner C, Silke J, Strasser A, Kaufmann T (2009). XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 460(7258): 1035-1039.
58. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, Xavier RJ, Yuan J (2008). Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135(7): 1311-1323.
59. 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 (2008). Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4(5): 313-321.
60. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J (2005). Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1(2): 112-119.
61. Dillon CP, Oberst A, Weinlich R, Janke LJ, Kang TB, Ben-Moshe T, Mak TW, Wallach D, Green DR (2012). Survival function of the FADD-CASPASE-8-cFLIP(L) complex. Cell Rep 1(5): 401-407.
62. Weinlich R, Oberst A, Dillon CP, Janke LJ, Milasta S, Lukens JR, Rodriguez DA, Gurung P, Savage C, Kanneganti TD, Green DR (2013). Protective roles for caspase-8 and cFLIP in adult homeostasis. Cell Rep 5(2): 340-348.
63. Galluzzi L, Kepp O, Kroemer G (2014). MLKL regulates necrotic plasma membrane permeabilization. Cell Res 24(2): 139-140.
64. Chen X, Li W, Ren J, Huang D, He WT, Song Y, Yang C, Li W, Zheng X, Chen P, Han J (2014). Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res 24(1): 105-121.
65. Cai Z, Jitkaew S, Zhao J, Chiang HC, Choksi S, Liu J, Ward Y, Wu LG, Liu ZG (2014). Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol 16(1): 55-65.
66. Murphy JM, Czabotar PE, Hildebrand JM, Lucet IS, Zhang JG, Alva-rez-Diaz S, Lewis R, Lalaoui N, Metcalf D, Webb AI, Young SN, Varghe- se LN, Tannahill GM, Hatchell EC, Majewski IJ, Okamoto T, Dobson RC, Hilton DJ, Babon JJ, Nicola NA, Strasser A, Silke J, Alexander WS (2013). The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39(3): 443-453.
67. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J (2009). RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325(5938): 332-336.
68. Wang Z, Jiang H, Chen S, Du F, Wang X (2012). The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 148(1-2): 228-243.
69. Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X, Wang X (2012). Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148(1-2): 213-227.
70. Tait SW, Oberst A, Quarato G, Milasta S, Haller M, Wang R, Karvela M, Ichim G, Yatim N, Albert ML, Kidd G, Wakefield R, Frase S, Krautwald S, Linkermann A, Green DR (2013). Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep 5(4): 878-885.
71. Moriwaki K, Farias Luz N, Balaji S, De Rosa MJ, O'Donnell CL, Gough PJ, Bertin J, Welsh RM, Chan FK (2016). The Mitochondrial Phosphatase PGAM5 Is Dispensable for Necroptosis but Promotes Inflammasome Activation in Macrophages. J Immunol 196(1): 407-415.
72. Karch J, Kanisicak O, Brody MJ, Sargent MA, Michael DM, Molkentin JD (2015). Necroptosis Interfaces with MOMP and the MPTP in Mediating Cell Death. PLoS One 10(6): e0130520.
73. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD (2005). Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434(7033): 658-662.
74. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T, Tsujimoto Y (2005). Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434(7033): 652-658.
75. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ (2005). Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci U S A 102(34): 12005-12010.
76. Bonora M, Bononi A, De Marchi E, Giorgi C, Lebiedzinska M, Marchi S, Patergnani S, Rimessi A, Suski JM, Wojtala A, Wieckowski MR, Kroemer G, Galluzzi L, Pinton P (2013). Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition. Cell Cycle 12(4): 674-683.
77. 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.
78. 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.
79. Skouta R, Dixon SJ, Wang J, Dunn DE, Orman M, Shimada K, Rosenberg PA, Lo DC, Weinberg JM, Linkermann A, Stockwell BR (2014). Ferrostatins inhibit oxidative lipid damage and cell death in diverse disease models. J Am Chem Soc 136(12): 4551-4556.
80. Dixon SJ, Stockwell BR (2014). The role of iron and reactive oxygen species in cell death. Nat Chem Biol 10(1): 9-17.
81. Andrabi SA, Dawson TM, Dawson VL (2008). Mitochondrial and nuclear cross talk in cell death: parthanatos. Ann N Y Acad Sci 1147:233-241.
82. Cimadamore F, Curchoe CL, Alderson N, Scott F, Salvesen G, Ter-skikh AV (2009). Nicotinamide rescues human embryonic stem cell-derived neuroectoderm from parthanatic cell death. Stem Cells 27(8): 1772-1781.
83. Wang Y, Kim NS, Haince JF, Kang HC, David KK, Andrabi SA, Poirier GG, Dawson VL, Dawson TM (2011). Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci Signal 4(167): ra20.
84. Menger L, Vacchelli E, Adjemian S, Martins I, Ma Y, Shen S, Yama-zaki T, Sukkurwala AQ, Michaud M, Mignot G, Schlemmer F, Sulpice E, Locher C, Gidrol X, Ghiringhelli F, Modjtahedi N, Galluzzi L, Andre F, Zitvogel L, Kepp O, Kroemer G (2012). Cardiac glycosides exert anticancer effects by inducing immunogenic cell death. Sci Transl Med 4(143): 143ra199.
85. Zitvogel L, Kepp O, Galluzzi L, Kroemer G (2012). Inflammasomes in carcinogenesis and anticancer immune responses. Nat Immunol 13(4): 343-351.
86. Bergsbaken T, Fink SL, Cookson BT (2009). Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7(2): 99-109.
87. Kepp O, Galluzzi L, Zitvogel L, Kroemer G (2010). Pyroptosis-a cell death modality of its kind? Eur J Immunol 40(3): 627-630.
88. Gurung P, Lukens JR, Kanneganti TD (2015). Mitochondria: diversity in the regulation of the NLRP3 inflammasome. Trends Mol Med 21(3): 193-201.
89. Jesenberger V, Procyk KJ, Yuan J, Reipert S, Baccarini M (2000). Salmonella-induced caspase-2 activation in macrophages: a novel mechanism in pathogen-mediated apoptosis. J Exp Med 192(7): 1035-1046.
90. Cervantes J, Nagata T, Uchijima M, Shibata K, Koide Y (2008). Intra-cytosolic Listeria monocytogenes induces cell death through caspase-1 activation in murine macrophages. Cell Microbiol 10(1): 41-52.
91. Fink SL, Cookson BT (2006). Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8(11): 1812-1825.
92. Buttner S, Eisenberg T, Herker E, Carmona-Gutierrez D, Kroemer G, Madeo F (2006). Why yeast cells can undergo apoptosis: death in times of peace, love, and war. J Cell Biol 175(4): 521-525.
93. Carmona-Gutierrez D, Kroemer G, Madeo F (2012). When death was young: an ancestral apoptotic network in bacteria. Mol Cell 46(5): 552-554.
94. Dwyer DJ, Camacho DM, Kohanski MA, Callura JM, Collins JJ (2012). Antibiotic-induced bacterial cell death exhibits physiological and biochemical hallmarks of apoptosis. Mol Cell 46(5): 561-572.
95. Eisenberg T, Buttner S, Kroemer G, Madeo F (2007). The mitochondrial pathway in yeast apoptosis. Apoptosis 12(5): 1011-1023.
96. Carmona-Gutierrez D, Eisenberg T, Buttner S, Meisinger C, Kroemer G, Madeo F (2010). Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ 17(5): 763-773.
97. Madeo F, Carmona-Gutierrez D, Ring J, Buttner S, Eisenberg T, Kroemer G (2009). Caspase-dependent and caspase-independent cell death pathways in yeast. Biochem Biophys Res Commun 382(2): 227-231.
98. Yuan J, Horvitz HR (2004). A first insight into the molecular mechanisms of apoptosis. Cell 116(2 Suppl): S53-56, 51 p following S59.
99. Steller H (2008). Regulation of apoptosis in Drosophila. Cell Death Differ 15(7): 1132-1138.