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Molecular Pathways of Different Types of Cell Death: Many Roads to Death

  • Dmitri V. Krysko
  • Agnieszka Kaczmarek
  • Peter Vandenabeele

Abstract

Cell death is a fundamental cellular response that has a crucial role in shaping our bodies during development and in regulating tissue homeostasis by eliminating unwanted cells. Three major morphologies of cell death have been described: apoptosis (type I), cell death associated with autophagy (type II) and necrosis (type III). In mammalian cells, the apoptotic response is mediated by either an intrinsic or an extrinsic pathway, depending on the origin of the death stimuli, and is almost always caspase-dependent. For a long time necrosis has been considered to be an accidental and uncontrolled form of cell death. However, evidence is accumulating that necrotic cell death in some cases can be as well controlled and programmed as caspase-dependent apoptosis. Autophagy is foremost a survival mechanism that is activated in cells subjected to nutrient or obligate growth factor deprivation. When cellular stress continues, cell death may continue by autophagy alone, or else it often becomes associated with features of apoptotic or necrotic cell death, depending on the stimulus and cell type. It is debatable whether autophagic cell death is an alternative way of dying, different from apoptotic and necrotic cell death, or whether failure of autophagy to rescue the cell can lead to cell death by either pathway. The aim of this chapter is to provide a general overview of current knowledge on signalling events that result in apoptosis, necrosis and cell death associated with autophagy.

Apoptosis Necrosis Autophagy Caspases Mitochondria 

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References

  1. Abida WM, Gu W (2008) p53-Dependent and p53-independent activation of autophagy by ARF. Cancer Res 68:352–357PubMedCrossRefGoogle Scholar
  2. Amaravadi RK, Yu D, Lum JJ et al (2007) Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 117:326–336PubMedCrossRefGoogle Scholar
  3. Ambalavanan N, Tyson JE, Kennedy KA et al (2005) Vitamin A supplementation for extremely low birth weight infants: outcome at 18 to 22 months. Pediatrics 115:E249–E254PubMedCrossRefGoogle Scholar
  4. Amchenkova AA, Bakeeva LE, Chentsov YS et al (1988) Coupling membranes as energy-transmitting cables. I. Filamentous mitochondria in fibroblasts and mitochondrial clusters in cardiomyocytes. J Cell Biol 107:481–495PubMedCrossRefGoogle Scholar
  5. Aravind L, Dixit VM, Koonin EV (1999) The domains of death: evolution of the apoptosis machinery. Trends Biochem Sci 24:47–53PubMedCrossRefGoogle Scholar
  6. Baba M, Osumi M, Scott SV et al (1997) Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J Cell Biol 139:1687–1695PubMedCrossRefGoogle Scholar
  7. Baehrecke EH (2005) Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol 6:505–510PubMedCrossRefGoogle Scholar
  8. Barkla DH, Gibson PR (1999) The fate of epithelial cells in the human large intestine. Pathology 31:230–238PubMedCrossRefGoogle Scholar
  9. Bernardi P, Krauskopf A, Basso E et al (2006) The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J 273:2077–2099PubMedCrossRefGoogle Scholar
  10. Bernardi P, Rasola A (2007) Calcium and cell death: the mitochondrial connection. Subcell Biochem 45:481–506PubMedCrossRefGoogle Scholar
  11. Bertrand MJ, Milutinovic S, Dickson KM et al (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 30:689–700PubMedCrossRefGoogle Scholar
  12. Blomgran R, Zheng L, Stendahl O (2007) Cathepsin-cleaved Bid promotes apoptosis in human neutrophils via oxidative stress-induced lysosomal membrane permeabilization. J Leukocyte Biol 81:1213–1223PubMedCrossRefGoogle Scholar
  13. Boone E, Vanden Berghe T, Van Loo G et al (2000) Structure/Function analysis of p55 tumour necrosis factor receptor and fas-associated death domain. Effect on necrosis in L929sA cells. J Biol Chem 275:37596–37603PubMedCrossRefGoogle Scholar
  14. Boya P, Gonzalez-Polo RA, Casares N et al (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25:1025–1040PubMedCrossRefGoogle Scholar
  15. Bursch W, Ellinger A, Gerner C et al (2000) Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann N Y Acad Sci 926:1–12PubMedCrossRefGoogle Scholar
  16. Callus BA, Ekert PG, Heraud JE et al (2008) Cytoplasmic p53 is not required for PUMA-induced apoptosis. Cell Death Differ 15:213–215 author reply 215–216PubMedCrossRefGoogle Scholar
  17. Chan FK, Shisler J, Bixby JG et al (2003) A role for tumour necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J Biol Chem 278:51613–51621PubMedCrossRefGoogle Scholar
  18. Chautan M, Chazal G, Cecconi F et al (1999) Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr Biol 9:967–970PubMedCrossRefGoogle Scholar
  19. Chen G, Goeddel DV (2002) TNF-R1 signalling: a beautiful pathway. Science 296:1634–1635PubMedCrossRefGoogle Scholar
  20. Chipuk JE, Green DR (2006) Dissecting p53-dependent apoptosis. Cell Death Differ 13:994–1002PubMedCrossRefGoogle Scholar
  21. Chipuk JE, Kuwana T, Bouchier-Hayes L et al (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303:1010–1014PubMedCrossRefGoogle Scholar
  22. Chiu R, Novikov L, Mukherjee S et al (2002) A caspase cleavage fragment of p115 induces fragmentation of the Golgi apparatus and apoptosis. J Cell Biol 159:637–648PubMedCrossRefGoogle Scholar
  23. Clarke PG, Clarke S (1995) Historic apoptosis. Nature 378:230PubMedCrossRefGoogle Scholar
  24. Clarke PG, Clarke S (1996) Nineteenth century research on naturally occurring cell death and related phenomena. Anat Embryol (Berl) 193:81–99Google Scholar
  25. Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326(Pt 1) 1–16PubMedGoogle Scholar
  26. Collins TJ, Berridge MJ, Lipp P et al (2002) Mitochondria are morphologically and functionally heterogeneous within cells. Embo J 21:1616–1627PubMedCrossRefGoogle Scholar
  27. Collins TJ, Bootman MD (2003) Mitochondria are morphologically heterogeneous within cells. J Exp Biol 206:1993–2000PubMedCrossRefGoogle Scholar
  28. De Giorgi F, Lartigue L, Ichas F (2000) Electrical coupling and plasticity of the mitochondrial network. Cell Calcium 28:365–370PubMedCrossRefGoogle Scholar
  29. Degterev A, Hitomi J, Germscheid M et al (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem BBiol 4:313–321CrossRefGoogle Scholar
  30. Degterev A, Huang Z, Boyce M et al (2005) Chemical inhibitor of non-apoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1:112–119PubMedCrossRefGoogle Scholar
  31. Deiss LP, Galinka H, Berissi H et al (1996) Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. Embo J 15:3861–3870PubMedGoogle Scholar
  32. Denecker G, Hoste E, Gilbert B et al (2007) Caspase-14 protects against epidermal UVB photodamage and water loss. Nat Cell Biol 9:666–674PubMedCrossRefGoogle Scholar
  33. Denecker G, Ovaere P, Vandenabeele P et al (2008) Caspase-14 reveals its secrets. J Cell Biol 180:451–458PubMedCrossRefGoogle Scholar
  34. Denecker G, Vercammen D, Steemans M et al (2001) Death receptor-induced apoptotic and necrotic cell death: differential role of caspases and mitochondria. Cell Death Differ 8:829–840PubMedCrossRefGoogle Scholar
  35. Dennis SC, Gevers W, Opie LH (1991) Protons in ischemia: where do they come from; where do they go to? J Mol Cell Cardiol 23:1077–1086PubMedCrossRefGoogle Scholar
  36. D’Herde K, De Prest B, Mussche S et al (2000) Ultrastructural localization of cytochrome c in apoptosis demonstrates mitochondrial heterogeneity. Cell Death Differ 7:331–337PubMedCrossRefGoogle Scholar
  37. Di Sano F, Ferraro E, Tufi R et al (2006) Endoplasmic reticulum stress induces apoptosis by an apoptosome-dependent but caspase 12-independent mechanism. J Biol Chem 281:2693–2700PubMedCrossRefGoogle Scholar
  38. Doerfler P, Forbush KA, Perlmutter RM (2000) Caspase enzyme activity is not essential for apoptosis during thymocyte development. J Immunol 164:4071–4079PubMedGoogle Scholar
  39. Egner A, Jakobs S, Hell SW (2002) Fast 100-nm resolution three-dimensional microscope reveals structural plasticity of mitochondria in live yeast. Proc Natl Acad Sci USA 99:3370–3375PubMedCrossRefGoogle Scholar
  40. Escuin D, Kline ER, Giannakakou P (2005) Both microtubule-stabilizing and microtubule-destabilizing drugs inhibit hypoxia-inducible factor-1alpha accumulation and activity by disrupting microtubule function. Cancer Res 65:9021–9028PubMedCrossRefGoogle Scholar
  41. Feng Z, Zhang H, Levine AJ et al (2005) The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA 102:8204–8209PubMedCrossRefGoogle Scholar
  42. Ferri KF, Kroemer G (2001) Organelle-specific initiation of cell death pathways. Nat Cell Biol 3:E255–E263PubMedCrossRefGoogle Scholar
  43. Festjens N, Kalai M, Smet J et al (2006a) Butylated hydroxyanisole is more than a reactive oxygen species scavenger. Cell Death Differ 13:66–169CrossRefGoogle Scholar
  44. Festjens N, van Gurp M, van Loo G et al (2004) Bcl-2 family members as sentinels of cellular integrity and role of mitochondrial intermembrane space proteins in apoptotic cell death. Acta Haematol 111:7–27PubMedCrossRefGoogle Scholar
  45. Festjens N, Vanden Berghe T, Cornelis S et al (2007) RIP1, a kinase on the crossroads of a cell’s decision to live or die. Cell Death Differ 14:400–410PubMedCrossRefGoogle Scholar
  46. Festjens N, Vanden Berghe T, Vandenabeele P (2006b) Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757:1371–1387CrossRefGoogle Scholar
  47. Foghsgaard L, Wissing D, Mauch D et al (2001) Cathepsin B acts as a dominant execution protease in tumour cell apoptosis induced by tumour necrosis factor. J Cell Biol 153:999–1010PubMedCrossRefGoogle Scholar
  48. Francois M, Le Cabec V, Dupont MA et al (2000) Induction of necrosis in human neutrophils by Shigella flexneri requires type III secretion, IpaB and IpaC invasins, and actin polymerization. Infect Immun 68:1289–1296PubMedCrossRefGoogle Scholar
  49. Goldstein JC, Munoz-Pinedo C, Ricci JE et al (2005) Cytochrome c is released in a single step during apoptosis. Cell Death Differ 12:453–462PubMedCrossRefGoogle Scholar
  50. Goldstein JC, Waterhouse NJ, Juin P et al (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2:156–162PubMedCrossRefGoogle Scholar
  51. Gonzalez-Polo RA, Boya P, Pauleau AL et al (2005) The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J Cell Sci 118:3091–3102PubMedCrossRefGoogle Scholar
  52. Goossens V, De Vos K, Vercammen D et al (1999) Redox regulation of TNF signalling. Biofactors 10:145–156PubMedCrossRefGoogle Scholar
  53. Groenendyk J, Michalak M (2005) Endoplasmic reticulum quality control and apoptosis. Acta Biochim Pol 52:381–395PubMedGoogle Scholar
  54. Groth-Pedersen L, Ostenfeld MS, Hoyer-Hansen M et al (2007) Vincristine induces dramatic lysosomal changes and sensitizes cancer cells to lysosome-destabilizing siramesine. Cancer Res 67:2217–2225PubMedCrossRefGoogle Scholar
  55. Harding TM, Morano KA, Scott SV et al (1995) Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 131:591–602PubMedCrossRefGoogle Scholar
  56. Harper N, Hughes M, MacFarlane M et al (2003) Fas-associated death domain protein and caspase- 8 are not recruited to the tumour necrosis factor receptor 1 signalling complex during tumour necrosis factor-induced apoptosis. J Biol Chem 278:25534–25541PubMedCrossRefGoogle Scholar
  57. Hicks SW, Machamer CE (2005) Golgi structure in stress sensing and apoptosis. Biochim Biophys Acta 1744:406–414PubMedCrossRefGoogle Scholar
  58. Hippert MM, O’Toole PS, Thorburn A (2006) Autophagy in cancer: good, bad, or both? Cancer Res 66:9349–9351PubMedCrossRefGoogle Scholar
  59. Hofmann K (1999) The modular nature of apoptotic signalling proteins. Cell Mol Life Sci 55:1113–1128PubMedCrossRefGoogle Scholar
  60. Holler N, Zaru R, Micheau O et al (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 1:489–495PubMedCrossRefGoogle Scholar
  61. Horvitz HR (1999) Genetic control of programmed cell death in the nematode Caenorhabditis elegans. Cancer Res 59:1701S–1706SPubMedGoogle Scholar
  62. Hoyer-Hansen M, Jaattela M (2008) Autophagy—an emerging target for cancer therapy. Autophagy 4Google Scholar
  63. Inbal B, Bialik S, Sabanay I et al (2002) DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J Cell Biol 157:455–468PubMedCrossRefGoogle Scholar
  64. Jaattela M, Tschopp J (2003) Caspase-independent cell death in T lymphocytes. Nat Immunol 4:416–423PubMedCrossRefGoogle Scholar
  65. Jiang X, Wang X (2000) Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to Apaf-1. J Biol Chem 275:31199–31203PubMedCrossRefGoogle Scholar
  66. Juhasz G, Csikos G, Sinka R et al (2003) The Drosophila homolog of Aut1 is essential for autophagy and development. FEBS Lett 543:154–158PubMedCrossRefGoogle Scholar
  67. Kalai M, Lamkanfi M, Denecker G et al (2003) Regulation of the expression and processing of caspase-12. J Cell Biol 162:457–467PubMedCrossRefGoogle Scholar
  68. Kalai M, Van Loo G, Vanden Berghe T et al (2002) Tipping the balance between necrosis and apoptosis in human and murine cells treated with interferon and dsRNA. Cell Death Differ 9:981–994PubMedCrossRefGoogle Scholar
  69. Kang SJ, Wang S, Kuida K et al (2002) Distinct downstream pathways of caspase-11 in regulating apoptosis and cytokine maturation during septic shock response. Cell Death Differ 9:1115–1125PubMedCrossRefGoogle Scholar
  70. Kelekar A (2005) Autophagy. Ann N Y Acad Sci 1066:259–271PubMedCrossRefGoogle Scholar
  71. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257PubMedGoogle Scholar
  72. Khwaja A, Tatton L (1999) Resistance to the cytotoxic effects of tumour necrosis factor alpha can be overcome by inhibition of a FADD/caspase-dependent signalling pathway. J Biol Chem 274:36817–36823PubMedCrossRefGoogle Scholar
  73. Kim YS, Morgan MJ, Choksi S et al (2007) TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol Cell 26:675–687PubMedCrossRefGoogle Scholar
  74. Kischkel FC, Hellbardt S, Behrmann I et al (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)- associated proteins form a death-inducing signalling complex (DISC) with the receptor. Embo J 14:5579–5588PubMedGoogle Scholar
  75. Klionsky DJ (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8:931–937PubMedCrossRefGoogle Scholar
  76. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290:1717–1721PubMedCrossRefGoogle Scholar
  77. Koneri K, Goi T, Hirono Y et al (2007) Beclin 1 gene inhibits tumour growth in colon cancer cell lines. Anticancer Res 27:1453–1457PubMedGoogle Scholar
  78. Korsmeyer SJ, Wei MC, Saito M et al (2000) Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 7:1166–1173PubMedCrossRefGoogle Scholar
  79. Koterski JF, Nahvi M, Venkatesan MM et al (2005) Virulent Shigella flexneri causes damage to mitochondria and triggers necrosis in infected human monocyte-derived macrophages. Infect Immun 73:504–513PubMedCrossRefGoogle Scholar
  80. Kroemer G, El-Deiry WS, Golstein P et al (2005) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 12 Suppl 2:1463–1467PubMedCrossRefGoogle Scholar
  81. Krysko DV, Roels F, Leybaert L et al (2001) Mitochondrial transmembrane potential changes support the concept of mitochondrial heterogeneity during apoptosis. J Histochem Cytochem 49:1277–1284PubMedGoogle Scholar
  82. Krysko DV, Vanden Berghe T, D’Herde K et al (2008) Apoptosis and necrosis: Detection, discrimination and phagocytosis. Methods 44:205–221PubMedCrossRefGoogle Scholar
  83. Krysko DV, Vandenabeele P, D’Herde K (2007) Cell death at a glance. In: CR Kettleworth (ed) “Cell apoptosis research advances” pp. 1–21 Nova Science publishers, IncGoogle Scholar
  84. Kuma A, Hatano M, Matsui M et al (2004) The role of autophagy during the early neonatal starvation period. Nature 432:1032–1036PubMedCrossRefGoogle Scholar
  85. Kunstle G, Hentze H, Germann PG et al (1999) Concanavalin A hepatotoxicity in mice: tumour necrosis factor-mediated organ failure independent of caspase-3-like protease activation. Hepatology 30:1241–1251PubMedCrossRefGoogle Scholar
  86. Kurz T, Terman A, Gustafsson B et al (2008) Lysosomes in iron metabolism, ageing and apoptosis. Histochem Cell Biol 129:389–406PubMedCrossRefGoogle Scholar
  87. Lakhani SA, Masud A, Kuida K et al (2006) Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 311:847–851PubMedCrossRefGoogle Scholar
  88. Lamkanfi M, Declercq W, Kalai M et al (2002) Alice in caspase land. A phylogenetic analysis of caspases from worm to man. Cell Death Differ 9:358–361PubMedCrossRefGoogle Scholar
  89. Lamkanfi M, D’Hondt K, Vande Walle L et al (2005) A novel caspase-2 complex containing TRAF2 and RIP1. J Biol Chem 280:6923–6932PubMedCrossRefGoogle Scholar
  90. Lamkanfi M, Festjens N, Declercq W et al (2007) Caspases in cell survival, proliferation and differentiation. Cell Death Differ 14:44–55PubMedCrossRefGoogle Scholar
  91. Lamkanfi M, Kalai M, Vandenabeele P (2004) Caspase-12: an overview. Cell Death Differ 11:365–368PubMedCrossRefGoogle Scholar
  92. Laster SM, Wood JG, Gooding LR (1988) Tumour necrosis factor can induce both apoptic and necrotic forms of cell lysis. J Immunol 141:2629–2634PubMedGoogle Scholar
  93. Lee CY, Baehrecke EH (2001) Steroid regulation of autophagic programmed cell death during development. Development 128:1443–1455PubMedGoogle Scholar
  94. Lee CY, Clough EA, Yellon P et al (2003) Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Curr Biol 13:350–357PubMedCrossRefGoogle Scholar
  95. Lefranc F, Facchini V, Kiss R (2007) Proautophagic drugs: a novel means to combat apoptosisresistant cancers, with a special emphasis on glioblastomas. Oncologist 12:1395–1403PubMedCrossRefGoogle Scholar
  96. Lesnefsky EJ, Gudz TI, Moghaddas S et al (2001) Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site. J Mol Cell Cardiol 33:37–47PubMedCrossRefGoogle Scholar
  97. Levine B (2006) Unraveling the role of autophagy in cancer. Autophagy 2:65–66PubMedGoogle Scholar
  98. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132:27–42PubMedCrossRefGoogle Scholar
  99. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115:2679–2688PubMedCrossRefGoogle Scholar
  100. Li P, Nijhawan D, Budihardjo I et al (1997) Cytochrome c and dATP-dependent formation of Apaf- 1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–489PubMedCrossRefGoogle Scholar
  101. Lim SY, Davidson SM, Mocanu MM et al (2007) The cardioprotective effect of necrostatin requires the cyclophilin-D component of the mitochondrial permeability transition pore. Cardiovasc Drugs Ther 21:467–469PubMedCrossRefGoogle Scholar
  102. Lleo A, Invernizzi P, Selmi C et al (2007) Autophagy: highlighting a novel player in the autoimmunity scenario. J Autoimmun 29:61–68PubMedCrossRefGoogle Scholar
  103. Lockshin RA, William CM (1965) Programmed Cell Death. 3. Neural Control of the Breakdown of the Intersegmental Muscles of Silkmoths. J Insect Physiol 11:601–610PubMedCrossRefGoogle Scholar
  104. Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36:2405–2419PubMedCrossRefGoogle Scholar
  105. Lum JJ, Bauer DE, Kong M et al (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120:237–248PubMedCrossRefGoogle Scholar
  106. Luo X, Budihardjo I, Zou H et al (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481–490PubMedCrossRefGoogle Scholar
  107. Ma Y, Temkin V, Liu H et al (2005) NF-kappaB protects macrophages from lipopolysaccharide- induced cell death: the role of caspase 8 and receptor-interacting protein. J Biol Chem 280:41827–41834PubMedCrossRefGoogle Scholar
  108. Maag RS, Mancini M, Rosen A et al (2005) Caspase-resistant Golgin-160 disrupts apoptosis induced by secretory pathway stress and ligation of death receptors. Mol Biol Cell 16:3019–3027PubMedCrossRefGoogle Scholar
  109. Maiuri MC, Zalckvar E, Kimchi A et al (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8:741–752PubMedCrossRefGoogle Scholar
  110. Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146:3–15PubMedGoogle Scholar
  111. Malhotra JD, Kaufman RJ (2007) The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 18:716–731PubMedCrossRefGoogle Scholar
  112. Mancini M, Machamer CE, Roy S et al (2000) Caspase-2 is localized at the Golgi complex and cleaves golgin-160 during apoptosis. J Cell Biol 149:603–612PubMedCrossRefGoogle Scholar
  113. Martin DN, Baehrecke EH (2004) Caspases function in autophagic programmed cell death in Drosophila. Development 131:275–284PubMedCrossRefGoogle Scholar
  114. Mathew R, White E (2007) Why sick cells produce tumours: the protective role of autophagy. Autophagy 3:502–505PubMedGoogle Scholar
  115. Matsumura H, Shimizu Y, Ohsawa Y et al (2000) Necrotic death pathway in Fas receptor signalling. J Cell Biol 151, 1247–1256PubMedCrossRefGoogle Scholar
  116. Mattson MP, Magnus T (2006) Ageing and neuronal vulnerability. Nat Rev Neurosci 7:278–294PubMedCrossRefGoogle Scholar
  117. Mayer A, Neupert W, Lill R (1995) Translocation of apocytochrome c across the outer membrane of mitochondria. J Biol Chem 270:12390–12397PubMedCrossRefGoogle Scholar
  118. Meier P, Vousden KH (2007) Lucifer’s labyrinth--ten years of path finding in cell death. Mol Cell 28:746–754PubMedCrossRefGoogle Scholar
  119. Melendez A, Talloczy Z, Seaman M et al (2003) Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301:1387–1391PubMedCrossRefGoogle Scholar
  120. Melino G, Knight RA, Nicotera P (2005) How many ways to die? How many different models of cell death? Cell Death Differ 12 Suppl 2:1457–1462PubMedCrossRefGoogle Scholar
  121. Mellen MA, de la Rosa EJ, Boya P (2008) The autophagic machinery is necessary for removal of cell corpses from the developing retinal neuroepithelium. Cell Death DifferGoogle Scholar
  122. Mellen MA, de la Rosa EJ, Boya P (2008) The autophagic machinery is necessary for removal of cell corpses from the developing retinal neuroepithelium. Cell Death Differ Mills KR, Reginato M, Debnath J et al (2004) Tumour necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc Natl Acad Sci U S A 101:3438–3443PubMedCrossRefGoogle Scholar
  123. Mukherjee S, Chiu R, Leung SM et al (2007) Fragmentation of the Golgi apparatus: an early apoptotic event independent of the cytoskeleton. Traffic 8:369–378PubMedCrossRefGoogle Scholar
  124. Nagata S (1999) Fas ligand-induced apoptosis. Annu Rev Genet 33:29–55PubMedCrossRefGoogle Scholar
  125. Nakagawa T, Zhu H, Morishima N et al (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98–103PubMedCrossRefGoogle Scholar
  126. Nakamura K, Bossy-Wetzel E, Burns K et al (2000) Changes in endoplasmic reticulum luminal environment affect cell sensitivity to apoptosis. J Cell Biol 150:731–740PubMedCrossRefGoogle Scholar
  127. Nguyen TM, Subramanian IV, Kelekar A et al (2007) Kringle 5 of human plasminogen, an angiogenesis inhibitor, induces both autophagy and apoptotic death in endothelial cells. Blood 109:4793–4802PubMedCrossRefGoogle Scholar
  128. Noda T, Ohsumi Y (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273:3963–3966PubMedCrossRefGoogle Scholar
  129. Obeng EA, Boise LH (2005) Caspase-12 and caspase-4 are not required for caspase-dependent endoplasmic reticulum stress-induced apoptosis. J Biol Chem 280:29578–29587PubMedCrossRefGoogle Scholar
  130. Okada H, Mak TW (2004) Pathways of apoptotic and non-apoptotic death in tumour cells. Nat Rev Cancer 4:592–603PubMedCrossRefGoogle Scholar
  131. Pattingre S, Tassa A, Qu X et al (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927–939PubMedCrossRefGoogle Scholar
  132. Pegoraro L, Palumbo A, Erikson J et al (1984) A 14;18 and an 8;14 chromosome translocation in a cell line derived from an acute B-cell leukemia. Proc Natl Acad Sci U S A 81:7166–7170PubMedCrossRefGoogle Scholar
  133. Peter ME, Krammer PH (2003) The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 10:26–35PubMedCrossRefGoogle Scholar
  134. Petiot A, Pattingre S, Arico S et al (2002) Diversity of signalling controls of macroautophagy in mammalian cells. Cell Struct Funct 27:431–441PubMedCrossRefGoogle Scholar
  135. Petrovski G, Zahuczky G, Katona K et al (2007a) Clearance of dying autophagic cells of different origin by professional and non-professional phagocytes. Cell Death DifferGoogle Scholar
  136. Petrovski G, Zahuczky G, Majai G et al (2007b) Phagocytosis of cells dying through autophagy evokes a pro-inflammatory response in macrophages. Autophagy 3:509–511Google Scholar
  137. Qu X, Yu J, Bhagat G et al (2003) Promotion of tumourigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112:1809–1820PubMedGoogle Scholar
  138. Qu X, Zou Z, Sun Q et al (2007) Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 128:931–946PubMedCrossRefGoogle Scholar
  139. Rai NK, Tripathi K, Sharma D et al (2005) Apoptosis: a basic physiologic process in wound healing. Int J Low Extrem Wounds 4:138–144PubMedCrossRefGoogle Scholar
  140. Riley T, Sontag E, Chen P et al (2008) Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9:402–412PubMedCrossRefGoogle Scholar
  141. Rizzuto R, Pinton P, Carrington W et al (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280:1763–1766PubMedCrossRefGoogle Scholar
  142. Roach HI, Clarke NM (2000) Physiological cell death of chondrocytes in vivo is not confined to apoptosis. New observations on the mammalian growth plate. J Bone Joint Surg Br 82:601–613PubMedCrossRefGoogle Scholar
  143. Rodriguez J, Lazebnik Y (1999) Caspase-9 and APAF-1 form an active holoenzyme. Genes Dev 13:3179–3184PubMedCrossRefGoogle Scholar
  144. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529PubMedCrossRefGoogle Scholar
  145. Saelens X, Festjens N, Vande Walle L et al (2004) Toxic proteins released from mitochondria in cell death. Oncogene 23:2861–2874PubMedCrossRefGoogle Scholar
  146. Saleh A, Srinivasula SM, Acharya S et al (1999) Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J Biol Chem 274:17941–17945PubMedCrossRefGoogle Scholar
  147. Saleh M, Mathison JC, Wolinski MK et al (2006) Enhanced bacterial clearance and sepsis resistance in caspase-12-deficient mice. Nature 440:1064–1068PubMedCrossRefGoogle Scholar
  148. Saleh M, Vaillancourt JP, Graham RK et al (2004) Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms. Nature 429:75–79PubMedCrossRefGoogle Scholar
  149. Scaffidi C, Fulda S, Srinivasan A et al (1998) Two CD95 (APO-1/Fas) signalling pathways. EMBO J 17:1675–1687PubMedCrossRefGoogle Scholar
  150. Schweichel JU, Merker HJ (1973) The morphology of various types of cell death in prenatal tissues. Teratology 7:253–266CrossRefGoogle Scholar
  151. Sheikh MS, Fornace AJ Jr (2000) Death and decoy receptors and p53-mediated apoptosis. Leukemia 14:1509–1513PubMedCrossRefGoogle Scholar
  152. Shimizu S, Kanaseki T, Mizushima N et al (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6:1221–1228PubMedCrossRefGoogle Scholar
  153. Smith CC, Davidson SM, Lim SY et al (2007) Necrostatin: a potentially novel cardioprotective agent? Cardiovasc Drugs Ther 21:227–233PubMedCrossRefGoogle Scholar
  154. Smith KG, Strasser A, Vaux DL (1996) CrmA expression in T lymphocytes of transgenic mice inhibits CD95 (Fas/APO-1)-transduced apoptosis, but does not cause lymphadenopathy or autoimmune disease. Embo J 15:5167–5176PubMedGoogle Scholar
  155. Stanger BZ, Leder P, Lee TH et al (1995) RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell 81:513–523PubMedCrossRefGoogle Scholar
  156. Tasdemir E, Maiuri MC, Galluzzi L et al (2008) Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 10:676–687PubMedCrossRefGoogle Scholar
  157. Thumm M, Egner R, Koch B et al (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett 349:275–280PubMedCrossRefGoogle Scholar
  158. Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169–174PubMedCrossRefGoogle Scholar
  159. Tsukamoto S, Kuma A, Murakami M et al (2008) Autophagy Is Essential for Preimplantation Development of Mouse Embryos. Science 321:117–120PubMedCrossRefGoogle Scholar
  160. Twiddy D, Brown DG, Adrain C et al (2004) Pro-apoptotic proteins released from the mitochondria regulate the protein composition and caspase-processing activity of the native Apaf-1/caspase- 9 apoptosome complex. J Biol Chem 279:19665–19682PubMedCrossRefGoogle Scholar
  161. Twiddy D, Cohen GM, Macfarlane M et al (2006) Caspase-7 is directly activated by the approximately 700-kDa apoptosome complex and is released as a stable XIAP-caspase-7 approximately 200-kDa complex. J Biol Chem 281:3876–3888PubMedCrossRefGoogle Scholar
  162. van Loo G, van Gurp M, Depuydt B et al (2002) The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ 9:20–26PubMedCrossRefGoogle Scholar
  163. Vande Walle L, Lamkanfi M, Vandenabeele P (2008) The mitochondrial serine protease HtrA2/ Omi: an overview. Cell Death Differ 15:453–460CrossRefGoogle Scholar
  164. Vanden Berghe T, Declercq W, Vandenabeele P (2007) NADPH oxidases: new players in TNFinduced necrotic cell death. Mol Cell 26:769–771CrossRefGoogle Scholar
  165. Vanden Berghe T, van Loo G, Saelens X et al (2004) Differential signalling to apoptotic and necrotic cell death by Fas-associated death domain protein FADD. J Biol Chem 279:7925–7933CrossRefGoogle Scholar
  166. Vanlangenakker N, Berghe TV, Krysko DV et al (2008) Molecular mechanisms and pathophysiology of necrotic cell death. Curr Mol Med 8:207–220PubMedCrossRefGoogle Scholar
  167. Vercammen D, Beyaert R, Denecker G et al (1998a) Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumour necrosis factor. J Exp Med 187:1477–1485Google Scholar
  168. Vercammen D, Brouckaert G, Denecker G et al (1998b) Dual signalling of the Fas receptor: initiation of both apoptotic and necrotic cell death pathways. J Exp Med 188:919–930CrossRefGoogle Scholar
  169. Vousden KH (2005) Apoptosis. p53 and PUMA: a deadly duo. Science 309:1685–1686PubMedCrossRefGoogle Scholar
  170. Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15:2922–2933PubMedGoogle Scholar
  171. Wei Y, Pattingre S, Sinha S et al (2008) JNK1-mediated phosphorylation of Bcl-2 regulates starvation- induced autophagy. Mol Cell 30:678–688PubMedCrossRefGoogle Scholar
  172. White E (2008) Autophagic cell death unraveled: Pharmacological inhibition of apoptosis and autophagy enables necrosis. Autophagy 4:399–401PubMedGoogle Scholar
  173. Williams A, Jahreiss L, Sarkar S et al (2006) Aggregate-prone proteins are cleared from the cytosol by autophagy: therapeutic implications. Curr Top Dev Biol 76:89–101PubMedCrossRefGoogle Scholar
  174. Willingham SB, Bergstralh DT, O’Connor W et al (2007) Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2:147–159PubMedCrossRefGoogle Scholar
  175. Yanagisawa H, Miyashita T, Nakano Y et al (2003) HSpin1, a transmembrane protein interacting with Bcl-2/Bcl-xL, induces a caspase-independent autophagic cell death. Cell Death Differ 10:798–807PubMedCrossRefGoogle Scholar
  176. Yang X, Chang HY, Baltimore D (1998) Essential role of CED-4 oligomerization in CED-3 activation and apoptosis. Science 281:1355–1357PubMedCrossRefGoogle Scholar
  177. Yorimitsu T, Klionsky DJ (2005) Autophagy: molecular machinery for self-eating. Cell Death Differ 12 Suppl 2:1542–1552PubMedCrossRefGoogle Scholar
  178. You Z, Savitz SI, Yang J et al (2008) Necrostatin-1 reduces histopathology and improves functional outcome after controlled cortical impact in mice. J Cereb Blood Flow MetabGoogle Scholar
  179. Yu L, Alva A, Su H et al (2004) Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304:1500–1502PubMedCrossRefGoogle Scholar
  180. Zeng X, Yan T, Schupp JE et al (2007) DNA mismatch repair initiates 6-thioguanine--induced autophagy through p53 activation in human tumour cells. Clin Cancer Res 13:1315–1321PubMedCrossRefGoogle Scholar
  181. Zou H, Li Y, Liu X et al (1999) An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274:11549–11556PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Dmitri V. Krysko
    • 1
  • Agnieszka Kaczmarek
    • 1
  • Peter Vandenabeele
    • 2
  1. 1.Molecular Signaling and Cell Death Unit Department for Molecular Biomedical Research VIBVIB & Ghent UniversityGhentBelgium
  2. 2.Department of Molecular Biology Ghent UniversityVIB & Ghent UniversityGhentBelgium

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