Divergence from a dedicated cellular suicide mechanism: exploring the evolution of cell death.

The developmental cell death in the nematode C. elegans is controlled by a simple and dedicated genetic program. This genetic program is evolutionarily conserved in higher organisms, including mammals. However, although mammalian homologs of C. elegans cell death gene products continue to regulate apoptosis, they are no longer dedicated regulators of cell death. On the other hand, multiple cellular noncell death-related mechanisms have been recruited to regulate cell death under different conditions. Such evidence suggests that evolution has led to an extensive integration of mammalian apoptosis machinery with multiple cellular physiological processes.

[1]  S. Korsmeyer,et al.  Cell Death Critical Control Points , 2004, Cell.

[2]  F. Martinon,et al.  The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. , 2002, Molecular cell.

[3]  Junying Yuan,et al.  Cross-Talk between Two Cysteine Protease Families , 2000, The Journal of cell biology.

[4]  H. Horvitz,et al.  C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2 , 1994, Cell.

[5]  Chi Li,et al.  Growth Factor Regulation of Autophagy and Cell Survival in the Absence of Apoptosis , 2005, Cell.

[6]  V. Dixit,et al.  Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf , 2004, Nature.

[7]  D. Goeddel,et al.  Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. , 2000, Immunity.

[8]  J. Puck,et al.  Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency , 2002, Nature.

[9]  M. Fishman,et al.  Prevention of vertebrate neuronal death by the crmA gene. , 1994, Science.

[10]  S. Korsmeyer,et al.  Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[11]  A. Strasser,et al.  Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins , 2002, Cell Death and Differentiation.

[12]  Shai Shaham,et al.  The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme , 1993, Cell.

[13]  Yigong Shi,et al.  Structure of the apoptotic protease-activating factor 1 bound to ADP , 2005, Nature.

[14]  H. Lipkin.  Where is the ?c? , 1978 .

[15]  V. Dixit,et al.  Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis , 2005, The Journal of experimental medicine.

[16]  Xiaodong Wang,et al.  Induction of Apoptotic Program in Cell-Free Extracts: Requirement for dATP and Cytochrome c , 1996, Cell.

[17]  C. Thompson,et al.  Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. , 2004, Molecular cell.

[18]  H. Horvitz,et al.  Genetics of programmed cell death in C. elegans: past, present and future. , 1998, Trends in genetics : TIG.

[19]  Francesco Cecconi,et al.  Apaf1 (CED-4 Homolog) Regulates Programmed Cell Death in Mammalian Development , 1998, Cell.

[20]  Guido Kroemer,et al.  Lysosomes and autophagy in cell death control , 2005, Nature Reviews Cancer.

[21]  Craig B. Thompson,et al.  Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes , 2004, Nature Cell Biology.

[22]  Alexei Degterev,et al.  Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury , 2005, Nature chemical biology.

[23]  Junying Yuan,et al.  Induction of apoptosis in fibroblasts by IL-1β-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3 , 1993, Cell.

[24]  D. Vaux,et al.  Apaf-1 and caspase-9 accelerate apoptosis, but do not determine whether factor-deprived or drug-treated cells die , 2004, The Journal of cell biology.

[25]  J. Beckmann,et al.  Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. , 1998, Immunity.

[26]  Takeshi Tokuhisa,et al.  The role of autophagy during the early neonatal starvation period , 2004, Nature.

[27]  Junying Yuan,et al.  Autophagy in cell death: an innocent convict? , 2005, The Journal of clinical investigation.

[28]  S. Korsmeyer,et al.  A Role for Proapoptotic BID in the DNA-Damage Response , 2005, Cell.

[29]  Maria K. Lehtinen,et al.  Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. , 2002, Molecular cell.

[30]  T. Mak,et al.  Apaf1 Is Required for Mitochondrial Pathways of Apoptosis and Brain Development , 1998, Cell.

[31]  V. Dixit,et al.  Cryopyrin activates the inflammasome in response to toxins and ATP , 2006, Nature.

[32]  S. Rabacchi,et al.  Caspase-2 Mediates Neuronal Cell Death Induced by β-Amyloid , 2000, The Journal of Neuroscience.

[33]  Alexei Degterev,et al.  A decade of caspases , 2003, Oncogene.

[34]  Jeffrey Robbins,et al.  Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death , 2005, Nature.

[35]  Keisuke Kuida,et al.  Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice , 1996, Nature.

[36]  S. R. Datta,et al.  BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis , 2003, Nature.

[37]  L. Nutt,et al.  Metabolic Regulation of Oocyte Cell Death through the CaMKII-Mediated Phosphorylation of Caspase-2 , 2005, Cell.

[38]  P. Hammerman,et al.  Akt-Directed Glucose Metabolism Can Prevent Bax Conformation Change and Promote Growth Factor-Independent Survival , 2003, Molecular and Cellular Biology.

[39]  Y. Lerenthal,et al.  Proapoptotic BID Is an ATM Effector in the DNA-Damage Response , 2005, Cell.

[40]  K Sudo,et al.  Ex vivo whole-embryo culture of caspase-8-deficient embryos normalize their aberrant phenotypes in the developing neural tube and heart , 2002, Cell Death and Differentiation.

[41]  Keisuke Kuida,et al.  Reduced Apoptosis and Cytochrome c–Mediated Caspase Activation in Mice Lacking Caspase 9 , 1998, Cell.

[42]  S. Srinivasula,et al.  Cytochrome c and dATP-Dependent Formation of Apaf-1/Caspase-9 Complex Initiates an Apoptotic Protease Cascade , 1997, Cell.

[43]  G. Poirier,et al.  PARP-1, a determinant of cell survival in response to DNA damage. , 2003, Experimental hematology.

[44]  Kevin A. Roth,et al.  Apaf1-dependent programmed cell death is required for inner ear morphogenesis and growth , 2004, Development.

[45]  Jean-Claude Martinou,et al.  Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia , 1994, Neuron.

[46]  J. Koh,et al.  Protection by Pyruvate against Transient Forebrain Ischemia in Rats , 2001, The Journal of Neuroscience.

[47]  S. Korsmeyer,et al.  Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. , 2000, Science.

[48]  Stefan J Riedl,et al.  A structure of the human apoptosome at 12.8 A resolution provides insights into this cell death platform. , 2005, Structure.

[49]  D. Brdiczka,et al.  Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases. , 1998, Biochimica et biophysica acta.

[50]  E. Baehrecke,et al.  Steroid regulation of autophagic programmed cell death during development. , 2001, Development.

[51]  Xiaodong Wang,et al.  Bid, a Bcl2 Interacting Protein, Mediates Cytochrome c Release from Mitochondria in Response to Activation of Cell Surface Death Receptors , 1998, Cell.

[52]  M. Moskowitz,et al.  Dual Role of Caspase-11 in Mediating Activation of Caspase-1 and Caspase-3 under Pathological Conditions , 2000, The Journal of cell biology.

[53]  Keisuke Kuida,et al.  Caspases 3 and 7: Key Mediators of Mitochondrial Events of Apoptosis , 2006, Science.

[54]  Yigong Shi,et al.  2:1 Stoichiometry of the CED4–CED9 Complex and the Tetrameric CED-4: Insights into the Regulation of CED-3 Activation , 2006, Cell cycle.

[55]  S. Rabacchi,et al.  Caspase-2 mediates neuronal cell death induced by beta-amyloid. , 2000, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  Denis Bouchard,et al.  Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. , 2003, Genes & development.

[57]  Philippe Dessen,et al.  Inhibition of Macroautophagy Triggers Apoptosis , 2005, Molecular and Cellular Biology.

[58]  F. Martinon,et al.  Gout-associated uric acid crystals activate the NALP3 inflammasome , 2006, Nature.

[59]  J. Tschopp,et al.  Induction of TNF Receptor I-Mediated Apoptosis via Two Sequential Signaling Complexes , 2003, Cell.

[60]  David L. Vaux,et al.  Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells , 1988, Nature.

[61]  P. Reddy.  Interleukin-18: recent advances , 2004, Current opinion in hematology.

[62]  Junying Yuan,et al.  Salmonella-Induced Caspase-2 Activation in Macrophages , 2000, The Journal of experimental medicine.

[63]  M. Mattson,et al.  “Apoptotic” biochemical cascades in synaptic compartments: Roles in adaptive plasticity and neurodegenerative disorders , 1999, Journal of neuroscience research.

[64]  Ajjai Alva,et al.  Regulation of an ATG7-beclin 1 Program of Autophagic Cell Death by Caspase-8 , 2004, Science.

[65]  Martin Raff,et al.  Cell suicide for beginners , 1998, Nature.

[66]  Junying Yuan,et al.  Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β , 2000, Nature.

[67]  T. Taniguchi,et al.  Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. , 2000, Science.

[68]  C. Koch,et al.  G6PD deficient cells and the bioreduction of disulfides: effects of DHEA, GSH depletion and phenylarsine oxide. , 2000, Biochemical and biophysical research communications.

[69]  E. Kandel,et al.  Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. , 2001, Genes & development.

[70]  Y. Lazebnik,et al.  Deficiency in caspase-9 or caspase-3 induces compensatory caspase activation , 2000, Nature Medicine.

[71]  D. Vaux,et al.  CrmA expression in T lymphocytes of transgenic mice inhibits CD95 (Fas/APO‐1)‐transduced apoptosis, but does not cause lymphadenopathy or autoimmune disease. , 1996, The EMBO journal.

[72]  Masashi Narita,et al.  Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC , 1999, Nature.

[73]  S. Korsmeyer,et al.  VDAC2 Inhibits BAK Activation and Mitochondrial Apoptosis , 2003, Science.

[74]  S. Akira,et al.  Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3 , 2006, Nature.

[75]  W. Zong,et al.  Alkylating DNA damage stimulates a regulated form of necrotic cell death. , 2004, Genes & development.

[76]  G. Núñez,et al.  Cell death and immunity: NODs: intracellular proteins involved in inflammation and apoptosis , 2003, Nature Reviews Immunology.

[77]  M. Moskowitz,et al.  Defects in regulation of apoptosis in caspase-2-deficient mice. , 1998, Genes & development.

[78]  A. Strasser,et al.  Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. , 1999, Science.

[79]  S. Snyder,et al.  Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[80]  José Luis de la Pompa,et al.  Differential Requirement for Caspase 9 in Apoptotic Pathways In Vivo , 1998, Cell.

[81]  S. Korsmeyer,et al.  Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis , 1999, Nature.

[82]  X. Liu,et al.  An APAF-1·Cytochrome c Multimeric Complex Is a Functional Apoptosome That Activates Procaspase-9* , 1999, The Journal of Biological Chemistry.

[83]  S. Lipton,et al.  Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[84]  M. Paskind,et al.  Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. , 1995, Cell.

[85]  M. Kelliher,et al.  The distinct roles of TRAF2 and RIP in IKK activation by TNF-R1: TRAF2 recruits IKK to TNF-R1 while RIP mediates IKK activation. , 2000, Immunity.

[86]  Stefan Grimm,et al.  The Death Domain Kinase RIP Mediates the TNF-Induced NF-κB Signal , 1998 .

[87]  K. Vousden,et al.  PUMA, a novel proapoptotic gene, is induced by p53. , 2001, Molecular cell.

[88]  S Falkow,et al.  The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[89]  Andreas Villunger,et al.  Bmf: A Proapoptotic BH3-Only Protein Regulated by Interaction with the Myosin V Actin Motor Complex, Activated by Anoikis , 2001, Science.

[90]  H. Horvitz,et al.  Activation of C. elegans cell death protein CED-9 by an ammo-acid substitution in a domain conserved in Bcl-2 , 1994, Nature.

[91]  F. Ausubel,et al.  Programmed cell death mediated by ced-3 and ced-4 protects Caenorhabditis elegans from Salmonella typhimurium-mediated killing , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[92]  Keisuke Kuida,et al.  Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome , 2002, Nature.

[93]  C. Janeway,et al.  Innate immune recognition. , 2002, Annual review of immunology.

[94]  M. Tohyama,et al.  Molecular Cloning of a Novel Polypeptide, DP5, Induced during Programmed Neuronal Death* , 1997, The Journal of Biological Chemistry.

[95]  V. Shoshan-Barmatz,et al.  In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death. , 2004, The Biochemical journal.

[96]  T. Kang,et al.  Caspase-8 Serves Both Apoptotic and Nonapoptotic Roles1 , 2004, The Journal of Immunology.

[97]  D. Goeddel,et al.  FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. , 1998, Science.

[98]  N. Olson,et al.  Caspase Activity Is Required for Stimulated B Lymphocytes to Enter the Cell Cycle1 , 2003, The Journal of Immunology.

[99]  S. R. Datta,et al.  Akt Phosphorylation of BAD Couples Survival Signals to the Cell-Intrinsic Death Machinery , 1997, Cell.

[100]  Junying Yuan,et al.  Murine Caspase-11, an ICE-Interacting Protease, Is Essential for the Activation of ICE , 1998, Cell.

[101]  Junying Yuan,et al.  Cleavage of BID by Caspase 8 Mediates the Mitochondrial Damage in the Fas Pathway of Apoptosis , 1998, Cell.

[102]  T. Mak,et al.  Caspase-3 regulates cell cycle in B cells: a consequence of substrate specificity , 2003, Nature Immunology.

[103]  Xuejun Jiang,et al.  Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. , 2002, Molecular cell.

[104]  G. Dorn,et al.  Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death , 2022 .

[105]  M. Su,et al.  Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. , 1995, Science.

[106]  T. Cotter,et al.  Direct oxidative modifications of signalling proteins in mammalian cells and their effects on apoptosis , 2005, Redox report : communications in free radical research.

[107]  F. Cecconi,et al.  Physiological and pathological roles of Apaf1 and the apoptosome , 2003, Journal of cellular and molecular medicine.

[108]  M. Zeng,et al.  Fas-induced caspase denitrosylation. , 1999, Science.

[109]  P. Leder,et al.  The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. , 1998, Immunity.

[110]  Ruedi Aebersold,et al.  Molecular characterization of mitochondrial apoptosis-inducing factor , 1999, Nature.

[111]  M. Zoratti,et al.  The mitochondrial permeability transition. , 1995, Biochimica et biophysica acta.

[112]  K. O. Elliston,et al.  A novel heterodimeric cysteine protease is required for interleukin-1βprocessing in monocytes , 1992, Nature.