Developmental cell biology: Developmental apoptosis in C. elegans: a complex CEDnario

Apoptosis, an evolutionarily conserved programme of cellular self-destruction, is essential for the development and survival of most multicellular animals. It is required to ensure functional organ architecture and to maintain tissue homeostasis. During development of the simple nematode Caenorhabditis elegans, apoptosis claims over 10% of the somatic cells that are generated ? these cells were healthy but unnecessary. Exciting insights into the regulation and execution of apoptosis in C. elegans have recently been made. These new findings will undoubtedly influence our perception of developmental apoptosis in more complex species, including humans.

[1]  S. Korsmeyer,et al.  Review Cell Death: Critical Control Points Another Line of Evidence for the Importance of Caspases in Cell Death Came From , 2022 .

[2]  H. Horvitz,et al.  The C. elegans cell death specification gene ces-1 encodes a snail family zinc finger protein. , 1999, Molecular cell.

[3]  M. Gautschi,et al.  Nascent-polypeptide-associated complex , 2002, Cellular and Molecular Life Sciences CMLS.

[4]  H. Steller,et al.  The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis , 2002, Nature Cell Biology.

[5]  Eric H. Baehrecke,et al.  How death shapes life during development , 2002, Nature Reviews Molecular Cell Biology.

[6]  Yigong Shi,et al.  Structural, biochemical, and functional analyses of CED-9 recognition by the proapoptotic proteins EGL-1 and CED-4. , 2004, Molecular cell.

[7]  R. Youle,et al.  Mitochondrial fission in apoptosis , 2005, Nature Reviews Molecular Cell Biology.

[8]  K. Ravichandran,et al.  Cues for apoptotic cell engulfment: eat-me, don't eat-me and come-get-me signals. , 2003, Trends in cell biology.

[9]  D. Vaux,et al.  Two kinds of BIR-containing protein - inhibitors of apoptosis, or required for mitosis. , 2001, Journal of cell science.

[10]  A. M. van der Bliek,et al.  C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. , 1999, Molecular cell.

[11]  Translational Repression of p53 by GLD-1 Regulates DNA Damage-Induced Apoptosis , 2005 .

[12]  Michael O. Hengartner,et al.  C. elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein , 2001, Current Biology.

[13]  H. Horvitz,et al.  Genetic control of programmed cell death in the nematode C. elegans , 1986, Cell.

[14]  W. D. Fairlie,et al.  CED-4 forms a 2 : 2 heterotetrameric complex with CED-9 until specifically displaced by EGL-1 or CED-13 , 2006, Cell Death and Differentiation.

[15]  J. Tilly Commuting the death sentence: how oocytes strive to survive , 2001, Nature Reviews Molecular Cell Biology.

[16]  H. Horvitz,et al.  Two C. elegans genes control the programmed deaths of specific cells in the pharynx. , 1991, Development.

[17]  L. Peso,et al.  Disruption of the CED-9.CED-4 complex by EGL-1 is a critical step for programmed cell death in Caenorhabditis elegans. , 2000, The Journal of biological chemistry.

[18]  S. Nagata DNA degradation in development and programmed cell death. , 2005, Annual review of immunology.

[19]  Huilin Li,et al.  Structure of the CED-4–CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans , 2005, Nature.

[20]  S. Mitani,et al.  C. elegans ced-13 can promote apoptosis and is induced in response to DNA damage , 2005, Cell Death and Differentiation.

[21]  H. Horvitz,et al.  The Caenorhabditis elegans cell-death protein CED-3 is a cysteine protease with substrate specificities similar to those of the human CPP32 protease. , 1996, Genes & development.

[22]  M. Raff,et al.  Programmed Cell Death in Animal Development , 1997, Cell.

[23]  Jay Z. Parrish,et al.  Functional genomic analysis of apoptotic DNA degradation in C. elegans. , 2003, Molecular cell.

[24]  S. Korsmeyer,et al.  Cell Death in Development , 1999, Cell.

[25]  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.

[26]  H. Horvitz,et al.  The survivin-like C. elegans BIR-1 protein acts with the Aurora-like kinase AIR-2 to affect chromosomes and the spindle midzone. , 2000, Molecular cell.

[27]  Tim Crook,et al.  iASPP oncoprotein is a key inhibitor of p53 conserved from worm to human , 2003, Nature Genetics.

[28]  Wouter Houthoofd,et al.  The embryonic cell lineage of the nematode Halicephalobus gingivalis (Nematoda: Cephalobina: Panagrolaimoidea) , 2007 .

[29]  Eric H. Baehrecke,et al.  Autophagy: dual roles in life and death? , 2005, Nature Reviews Molecular Cell Biology.

[30]  J. Sulston,et al.  Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. , 1977, Developmental biology.

[31]  S. Milstein,et al.  A conserved checkpoint pathway mediates DNA damage--induced apoptosis and cell cycle arrest in C. elegans. , 2000, Molecular cell.

[32]  Horvitz,et al.  Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. , 1991, Genetics.

[33]  M. Hengartner Apoptosis Corralling the Corpses , 2001, Cell.

[34]  H. Horvitz,et al.  Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein , 1995, Nature.

[35]  Jay Z. Parrish,et al.  Mitochondrial endonuclease G is important for apoptosis in C. elegans , 2001, Nature.

[36]  David L. Vaux,et al.  IAPs, RINGs and ubiquitylation , 2005, Nature Reviews Molecular Cell Biology.

[37]  A. Fraser,et al.  Genome-wide RNAi identifies p53-dependent and -independent regulators of germ cell apoptosis in C. elegans , 2004, Cell Death and Differentiation.

[38]  D. Vaux,et al.  Solution structure of a baculoviral inhibitor of apoptosis (IAP) repeat , 1999, Nature Structural Biology.

[39]  S H Kaufmann,et al.  Mammalian caspases: structure, activation, substrates, and functions during apoptosis. , 1999, Annual review of biochemistry.

[40]  B. Martinac,et al.  Mechanisms of AIF-Mediated Apoptotic DNA Degradation in Caenorhabditis elegans , 2002 .

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

[42]  S. Seshagiri,et al.  Caenorhabditis elegans CED-4 stimulates CED-3 processing and CED-3-induced , 1997, Current Biology.

[43]  Y. Kohara,et al.  cgh-1, a conserved predicted RNA helicase required for gametogenesis and protection from physiological germline apoptosis in C. elegans. , 2001, Development.

[44]  G. Núñez,et al.  Interaction and Regulation of the Caenorhabditis elegans Death Protease CED-3 by CED-4 and CED-9* , 1997, The Journal of Biological Chemistry.

[45]  Pascal Meier,et al.  Apoptosis in development , 2000, Nature.

[46]  S. Cohen,et al.  Connecting proliferation and apoptosis in development and disease , 2004, Nature Reviews Molecular Cell Biology.

[47]  T. Vellai,et al.  Inactivation of the Autophagy Gene bec-1 Triggers Apoptotic Cell Death in C. elegans , 2005, Current Biology.

[48]  M. Thellmann,et al.  The Snail-like CES-1 protein of C. elegans can block the expression of theBH3-only cell-death activator gene egl-1 by antagonizing the function of bHLH proteins , 2003, Development.

[49]  A. Labrousse,et al.  elegans Dynamin-Related Protein DRP-1 Controls Severing of the Mitochondrial Outer , 1999 .

[50]  A. Look,et al.  Slug Antagonizes p53-Mediated Apoptosis of Hematopoietic Progenitors by Repressing puma , 2005, Cell.

[51]  J. Sulston,et al.  The embryonic cell lineage of the nematode Caenorhabditis elegans. , 1983, Developmental biology.

[52]  M. Hengartner,et al.  Caenorhabditis elegans gene ced-9 protects cells from programmed cell death , 1992, Nature.

[53]  C. Kurz,et al.  Caenorhabditis elegans: an emerging genetic model for the study of innate immunity , 2003, Nature Reviews Genetics.

[54]  A. Bergmann,et al.  Regulators of IAP function: coming to grips with the grim reaper. , 2003, Current opinion in cell biology.

[55]  F. Ausubel,et al.  Caenorhabditis elegans-Based Screen Identifies Salmonella Virulence Factors Required for Conserved Host-Pathogen Interactions , 2004, Current Biology.

[56]  H. Horvitz,et al.  The TRA-1A Sex Determination Protein of C. elegans Regulates Sexually Dimorphic Cell Deaths by Repressing the egl-1 Cell Death Activator Gene , 1999, Cell.

[57]  H. Horvitz,et al.  The Caenorhabditis elegans cell death gene ced-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. , 1992, Development.

[58]  J. Tilly,et al.  Current concepts in Bcl-2 family member regulation of female germ cell development and survival. , 2004, Biochimica et biophysica acta.

[59]  W. B. Derry,et al.  Caenorhabditis elegans p53: Role in Apoptosis, Meiosis, and Stress Resistance , 2001, Science.

[60]  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.

[61]  Suzanne Cory,et al.  The Bcl-2 family: roles in cell survival and oncogenesis , 2003, Oncogene.

[62]  M. Spector,et al.  eor-1 and eor-2 are required for cell-specific apoptotic death in C. elegans. , 2004, Developmental biology.

[63]  G. Núñez,et al.  WD-40 Repeat Region Regulates Apaf-1 Self-association and Procaspase-9 Activation* , 1998, The Journal of Biological Chemistry.

[64]  M. Vidal,et al.  Caenorhabditis elegans HUS-1 Is a DNA Damage Checkpoint Protein Required for Genome Stability and EGL-1-Mediated Apoptosis , 2002, Current Biology.

[65]  H. Steller,et al.  Genetic control of programmed cell death in Drosophila. , 1994, Science.

[66]  F. Ausubel,et al.  Caenorhabditis elegans Innate Immune Response Triggered by Salmonella enterica Requires Intact LPS and Is Mediated by a MAPK Signaling Pathway , 2003, Current Biology.

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

[68]  Y. Lazebnik,et al.  Caspase-9 and APAF-1 form an active holoenzyme. , 1999, Genes & development.

[69]  C. Thummel,et al.  A balance between the diap1 death inhibitor and reaper and hid death inducers controls steroid-triggered cell death in Drosophila. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[70]  D. Hirsh,et al.  The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. , 1979, Developmental biology.

[71]  A. Wyllie Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation , 1980, Nature.

[72]  A. Wyllie,et al.  Cell death: the significance of apoptosis. , 1980, International review of cytology.

[73]  R. Youle,et al.  Dynamics of mitochondrial morphology in healthy cells and during apoptosis , 2003, Cell Death and Differentiation.

[74]  J. Hodgkin,et al.  MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans , 2000, Nature.

[75]  A. Fraser,et al.  CED-4 induces chromatin condensation in Schizosaccharomyces pombe and is inhibited by direct physical association with CED-9 , 1997, Current Biology.

[76]  J. Rothman,et al.  Suppression of CED-3-independent apoptosis by mitochondrial βNAC in Caenorhabditis elegans , 2003, Nature.

[77]  H. Horvitz,et al.  Developing Caenorhabditis elegans neurons may contain both cell-death protective and killer activities. , 1996, Genes & development.

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

[79]  A. Fraser,et al.  Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis , 1999, Current Biology.

[80]  M. Hengartner,et al.  Tales of cannibalism, suicide, and murder: Programmed cell death in C. elegans. , 2005, Current topics in developmental biology.

[81]  O. Hobert,et al.  Caenorhabditis elegans ABL-1 antagonizes p53-mediated germline apoptosis after ionizing irradiation , 2004, Nature Genetics.

[82]  S. Srinivasula,et al.  Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. , 1998, Molecular cell.

[83]  P. Boag,et al.  A conserved RNA-protein complex component involved in physiological germline apoptosis regulation in C. elegans , 2005, Development.

[84]  Yigong Shi,et al.  Molecular mechanisms of caspase regulation during apoptosis , 2004, Nature Reviews Molecular Cell Biology.

[85]  N. Rooijen,et al.  Microglia Promote the Death of Developing Purkinje Cells , 2004, Neuron.

[86]  L. del Peso,et al.  Caenorhabditis elegans EGL-1 Disrupts the Interaction of CED-9 with CED-4 and Promotes CED-3 Activation* , 1998, The Journal of Biological Chemistry.

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

[88]  A. Wyllie,et al.  Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics , 1972, British Journal of Cancer.

[89]  H. Horvitz,et al.  The engulfment process of programmed cell death in caenorhabditis elegans. , 2004, Annual review of cell and developmental biology.

[90]  M. Hengartner,et al.  Translational Repression of C. elegans p53 by GLD-1 Regulates DNA Damage-Induced Apoptosis , 2005, Cell.

[91]  J. Sulston,et al.  Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. , 1983, Science.

[92]  A. Look,et al.  E2A-HLF usurps control of evolutionarily conserved survival pathways , 2001, Oncogene.

[93]  H. Horvitz,et al.  A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons , 1988, Nature.

[94]  K. Hofmann,et al.  The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis , 2001, Current Biology.

[95]  H. Horvitz,et al.  Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. , 1999, Development.

[96]  H. Horvitz,et al.  Transcriptional regulator of programmed cell death encoded by Caenorhabditis elegans gene ces-2 , 1996, Nature.

[97]  G. Núñez,et al.  Interaction and Regulation of Subcellular Localization of CED-4 by CED-9 , 1997, Science.

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

[99]  S. Korsmeyer,et al.  The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. , 2000, Molecular cell.

[100]  M. Nieto,et al.  The snail superfamily of zinc-finger transcription factors , 2002, Nature Reviews Molecular Cell Biology.

[101]  H. Horvitz,et al.  Translocation of C. elegans CED-4 to nuclear membranes during programmed cell death. , 2000, Science.

[102]  M. Yamamoto,et al.  Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. , 2000, Development.

[103]  H. Horvitz,et al.  Phagocytosis promotes programmed cell death in C. elegans , 2001, Nature.

[104]  Michael O. Hengartner,et al.  Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans , 2005, Nature.

[105]  R. Schnabel,et al.  Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans , 2001, Nature.

[106]  D. Baltimore,et al.  Essential role of CED-4 oligomerization in CED-3 activation and apoptosis. , 1998, Science.

[107]  H. Horvitz,et al.  The C. elegans Protein EGL-1 Is Required for Programmed Cell Death and Interacts with the Bcl-2–like Protein CED-9 , 1998, Cell.

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

[109]  M. Vidal,et al.  BRCA1/BARD1 Orthologs Required for DNA Repair in Caenorhabditis elegans , 2004, Current Biology.

[110]  S. Goff Genetic Control of Programmed Cell Death in the Nematode Caenorhabditis elegans 1 , 2007 .

[111]  R. Jagasia,et al.  DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death in C. elegans , 2005, Nature.

[112]  M. Spector,et al.  Interaction between the C. elegans cell-death regulators CED-9 and CED-4 , 1997, Nature.

[113]  J. Parrish,et al.  Demonstration of the in vivo interaction of key cell death regulators by structure-based design of second-site suppressors. , 2000, Proceedings of the National Academy of Sciences of the United States of America.