The Origin and Evolution of Programmed Cell Death

Abstract

Programmed cell death and apoptosis have been assumed to emerge with multicellularity, and to depend on specific ‘death genes’ whose sole effects are execution or repression of cell death. In 1996, I proposed the ‘original sin’ hypothesis, postulating that the origin of self‐destruction is as ancient as the origin of the first cells, and predicting that there are no specific ‘death genes’. Rather, an ancestral and unavoidable capacity of effectors of cell survival – of cell metabolism, differentiation, cycling – to induce cell death favoured their continuous selection during evolution for both their ‘pro‐life’ and ‘pro‐death’ activities. Diversification of these effectors was accelerated by their recruitment into host/parasite interactions and symbioses, including the one that gave birth to eukaryote cells. The main prediction of the ‘original sin’ hypothesis is supported by recent findings showing that effectors of cell death indeed have previously undetected roles in cell survival.

Key concepts

  • Programmed cell death (PCD) is an evolutionary conserved, regulated process of cell suicide crucial in the development and homeostasis of multicellular animals and plants.

  • Various forms of PCD have also been discovered in unicellular organisms, including bacteria, favouring the survival in adverse environments of a part of the colony at the expense of the premature dismissal of another.

  • Because PCD appears as an ‘altruistic’ cell response, the evolutionary origin of PCD has been equated with that of ‘altruistic’ cell behaviour.

  • The ‘original sin’ hypothesis postulates that the origin of PCD is as ancient as the origin of the first cell, resulting from an unavoidable capacity of most molecular effectors of cell survival (metabolism, differentiation and cell cycle) to induce stochastic self‐destruction, when their activity is not regulated by other cell survival effectors acting as partial antagonists.

  • The ‘original sin’ hypothesis predicts that there are no specific ‘death genes’; rather, the ancestral capacity of most effectors of cell survival to also induce cell suicide allowed their continuous selection during evolution for both their ‘pro‐life’ and ‘pro‐death’ activities.

  • Some of the pleiotropic ‘pro‐life’ and ‘pro‐death’ effectors diversified and propagated in bacteria as toxin/antidote ‘addiction modules’, achieving a form of enforced symbiosis, because their dismissal results in the self‐destruction of the cell in which they reside.

  • Host/parasite conflicts, lateral gene transfers and enforced symbioses – between bacteria and their ‘addiction modules’ of plasmid origin, and later between eukaryote cells and their mitochondria endosymbionts of bacterial origin – played a crucial role in the subsequent diversification and propagation of PCD.

  • The seminal studies of the genetic control of PCD in the nematode Caenorhabditis elegans implied that executioners and repressors of PCD had no other possible effect than execution or repression of cell death; however, a series of recent findings indicates that executioners and repressors of PCD exert other previously undetected vital effects in both multicellular and unicellular organisms.

Keywords: evolution; programmed cell death; apoptosis; unicellular organisms; bacteria; ageing

References

Aizenman E, Engelberg‐Kulka H and Glaser G (1996) An E. coli chromosomal “addiction module” regulated by guanosine [corrected] 3′,5′‐bispyrophosphate: a model for programmed bacterial cell death. Proceedings of the National Academy of Sciences of the USA 93: 6059–6063.

Ameisen JC (1996) The origin of programmed cell death. Science 272: 1278–1279.

Ameisen JC (1998) The evolutionary origin and role of programmed cell death in single celled organisms: a new view of executioners, mitochondria, host‐pathogen interactions, and the role of death in the process of natural selection. In: Lockshin R, Zakeri Z and Tilly J (eds) When Cells Die, pp. 3–56. New York: Wiley‐Liss, Inc.

Ameisen JC (1999) La Sculpture du Vivant. Le suicide cellulaire ou la mort créatrice. Paris, Editions du Seuil, (Points Seuil, 2003).

Ameisen JC (2002) On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death and Differentiation 9: 367–393.

Ameisen JC (2004) Looking for death at the core of life in the light of evolution. Cell Death and Differentiation 11: 4–10.

Ameisen JC and Capron A (1991) Cell dysfunction and depletion in AIDS: the programmed cell death hypothesis. Immunology Today 12: 102–105.

Ameisen JC, Idziorek T, Billaut‐Mulot O et al. (1995) Apoptosis in a unicellular eukaryote (Trypanosoma cruzi): implications for the evolutionary origin and role of programmed cell death in the control of cell proliferation, differentiation and survival. Cell Death and Differentiation 2: 285–300.

Amitai S, Kolodkin‐Gal I, Hananya‐Meltabashi M, Sacher A and Engelberg‐Kulka H (2009) E. coli MazF leads to the simultaneous selective synthesis of both “death proteins” and “survival proteins”. PLoS Genetics 5(3): e1000390; Epub March 13.

Bjedov I, Tenaillon O, Gérard B et al. (2003) Stress‐induced mutagenesis in bacteria. Science 300: 1404–1409.

Christensen ST, Wheatley DN, Rasmussen MI and Rasmussen L (1995) Mechanisms controlling death, survival and proliferation in a model unicellular eukaryote Tetrahymena thermophila. Cell Death and Differentiation 2: 301–308.

Clem RJ, Fechheimer M and Miller LK (1991) Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254: 1388–1390.

Cornillon S, Foa C, Davoust J et al. (1994) Programmed cell death in Dictyostelium. Journal of Cell Science 107: 2691–2704.

Darwin C (1859) On the origin of species by means of natural selection. London: John Murray. The Complete work of Charles Darwin online: http://darwin‐online.org.uk/.

Delivani P, Adrain C, Taylor RC, Duriez PJ and Martin SJ (2006) Role for CED‐9 and Egl‐1 as regulators of mitochondrial fission and fusion dynamics. Molecular Cell 21: 761–773.

Derry WB, Putzke AP and Rothman JH (2001) Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294: 591–595.

Ellis HM and Horvitz HR (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44: 817–829.

Ellis RE, Yuan J and Horvitz HR (1991) Mechanisms and functions of cell death. Annual Review of Cell Biology 7: 663–698.

Engelberg‐Kulka H, Amitai S, Kolodkin‐Gal I and Hazan R (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genetics 2(10): e135.

Evan GA (1994) Old cells never die, they just apoptose. Trends in Cell Biology 4: 191–192.

Galluzzi L, Joza N, Tasdemir E et al. (2008) No death without life: vital functions of apoptotic effectors. Cell Death and Differentiation 15: 1113–1123.

Glucksman A (1951) Cell deaths in normal vertebrate ontogeny. Biological Reviews of the Cambridge Philosophical Society 26: 59–86.

González‐Pastor JE, Hobbs EC and Losick R (2003) Cannibalism by sporulating bacteria. Science 301: 510–513.

Greenberg JT (1996) Programmed cell death: a way of life for plants. Proceedings of the National Academy of Sciences of the USA 93: 12094–12097.

Hayes F (2003) Toxins‐antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301: 1496–1499.

Horvitz HR (1999) Genetic control of programmed cell death in the nematode Caenorhabditis elegans. Cancer Research 59(suppl.): 1701–1706.

Jazwinski SM (1996) Longevity, genes, and aging. Science 273: 54–59.

Jones RG, Bui T, White C et al. (2007) The proapoptotic factors Bax and Bak regulate T cell proliferation through control of endoplasmic reticulum Ca(2+) homeostasis. Immunity 27: 268–280.

Kaiser D (1996) Bacteria also vote. Science 272: 1598–1599.

Karbowski M, Norris KL, Cleland MM, Jeong SY and Youle RJ (2006) Role of Bax and Bak in mitochondrial morphogenesis. Nature 443: 658–662.

Kolodkin‐Gal I, Hazan R, Gaathon A, Carmeli S and Engelberg‐Kulka H (2007) A linear pentapeptide is a quorum‐sensing factor required for mazEF‐mediated cell death in E. coli. Science 318: 652–655.

Liu WH, Lin YL, Wang JP et al. (2006) Restriction of vaccinia virus replication by a ced‐3 and ced‐4‐dependent pathway in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the USA 103: 4174–4179.

Lockshin RA and Zakeri Z (2001) Timeline. Programmed cell death and apoptosis: origins of the theory. Nature Reviews. Molecular Cell Biology 2: 545–550.

Losick R and Stragier P (1992) Crisscross regulation of cell‐type‐specific gene expression during development in B. subtilis. Nature 355: 601–604.

Madeo F, Fröhlich E, Ligr M et al. (1999) Oxygen stress: a regulator of apoptosis in yeast. Journal of Cell Biology 145: 757–767.

Meier P, Finch A and Evan G (2000) Apoptosis in development. Nature 407: 796–801.

Nathan C (2008) Metchnikoff's legacy in 2008. Nature Immunology 9: 695–698.

Oberst A, Bender C and Green DR (2008) Living with death: the evolution of the mitochondrial pathway of apoptosis in animals. Cell Death and Differentiation 15: 1139–1146.

Pedersen K, Zavialov AV, Pavlov MY et al. (2003) The bacterial toxin RelE displays codon‐specific cleavage of mRNAs in the ribosomal A site. Cell 112: 131–140.

Raff MC (1992) Social controls on cell survival and cell death. Nature 356: 397–400.

Rainey PB and Rainey K (2003) Evolution of cooperation and conflict in experimental bacterial populations. Nature 425: 72–74.

Shcheprova Z, Baldi S, Frei SB, Gonnet G and Barral Y (2008) A mechanism for asymmetric segregation of age during yeast budding. Nature 454: 728–734.

Sheldrake AR (1974) The ageing, growth and death of cells. Nature 250: 381–385.

Sheridan C, Delivani P, Cullen SP and Martin SJ (2008) Bax‐ or Bak‐induced mitochondrial fission can be uncoupled from cytochrome c release. Molecular Cell 31: 570–585.

Stewart EJ, Madden R, Paul G and Taddei F (2005) Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biology 3: e45. Epub February 1.

Van Valen L (1973) A new evolutionary law. Evolutionary Theory 1: 1–30.

Vardi A, Berman‐Frank I, Rozenberg T et al. (1999) Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO(2) limitation and oxidative stress. Current Biology 9: 1061–1064.

Vaux DL (1993) Towards an understanding of the molecular mechanisms of physiological cell death. Proceedings of the National Academy of Sciences of the USA 90: 786–789.

Vaux DL, Haeker G and Strasser A (1994) An evolutionary perspective on apoptosis. Cell 76: 777–779.

Velicer GJ, Kroos L and Lenski RE (2000) Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404: 598–601.

Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11: 398–411.

Yarmolinsky MB (1995) Programmed cell death in bacterial populations. Science 267: 836–837.

Zermati Y, Mouhamad S, Stergiou L et al. (2007) Nonapoptotic role for Apaf‐1 in the DNA damage checkpoint. Molecular Cell 28: 624–637.

Further Reading

Albert B, Johnson A, Lewis J et al. (2007) Molecular Biology of the Cell. New York: Garland Science.

Doolittle WF and Bapteste E (2007) Pattern pluralism and the tree of life hypothesis. Proceedings of the National Academy of Sciences of the USA 104: 2043–2049.

Gould SJ (2002) The Stucture of Evolutionary Theory. Cambridge, MA: The Belknap Press of Harvard University Press.

Kaufmann S (1993) The Origins of Order. Self‐organization and Selection in Evolution. New York: Oxford University Press.

Kirschner M, Gerhart J and Mitchison T (2000) Molecular ‘vitalism’. Cell 100: 79–88.

Koonin EV and Aravind L (2002) Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death and Differentiation 9: 394–404.

Lewin B (2007) Genes IX. Boston: Jones and Bartlett Publishers.

Margulis L and Sagan D (1997) Microcosmos. Four Billion Years of Microbial Evolution. Berkeley: University of California Press. (First published by Summit Books 1986).

Maynard Smith J and Szathmary E (1997) The Major Transitions in Evolution. New York: Oxford University Press. (First published 1995).

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Ameisen, Jean Claude(Dec 2009) The Origin and Evolution of Programmed Cell Death. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021988]