Skip to main content

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 69))

Abstract

The progress of evolutionary biology has revealed that symbiosis played a basic role in the evolution of complex eukaryotic organisms, including humans. Mitochondria are actually simplified endosymbiotic bacteria currently playing the role of cellular organelles. Mitochondrial domestication occurred at the very beginning of eukaryotic evolution. Mitochondria have two different basic functions: they produce energy using oxidative respiration, and they initiate different forms of apoptotic programmed/regulated cell death. Apoptotic programmed cell death may have different cytological forms. Mechanisms of apoptotic programmed cell death exist even in the unicellular organisms, and they play a basic role in the development of complex multicellular organisms, such as fungi, green plants, and animals. Multicellularity was independently established many times among eukaryotes. There are indications that apoptotic programmed cell death is a trait required for the establishment of multicellularity. Regulated cell death is initiated by many different parallel biochemical pathways. It is generally accepted that apoptosis evolved during mitochondrial domestication. However, there are different hypothetical models of the origin of apoptosis. The phylogenetic studies of my group indicate that apoptosis probably evolved during an evolutionary arms race between host ancestral eukaryotic predators and ancestral prey mitochondria (named protomitochondria). Protomitochondrial prey produced many different toxins as a defense against predators. From these toxins evolved extant apoptotic factors. There are indications that aerobic respiration and apoptosis co-evolved and are functionally linked in extant organisms. Perturbations of apoptosis and oxidative respiration are frequently observed during neoplastic transition. Our group showed that perturbations of apoptosis in yeasts also cause perturbations of oxidative respiration.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abedin M, King N (2010) Diverse evolutionary paths to cell adhesion. Trends Cell Biol 20:734–742

    CAS  PubMed  PubMed Central  Google Scholar 

  • Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X, Akey CW (2002) Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol Cell 9:423–432

    CAS  PubMed  Google Scholar 

  • Akematsu T, Endoh H (2010) Role of apoptosis-inducing factor (AIF) in programmed nuclear death during conjugation in Tetrahymena thermophila. BMC Cell Biol 11:13

    PubMed  PubMed Central  Google Scholar 

  • Aoyagi S, Sugiyama M, Fukuda H (1998) BEN1 and ZEN1 cDNAs encoding S1-type DNases that are associated with programmed cell death in plants. FEBS Lett 429:134–138

    CAS  PubMed  Google Scholar 

  • Arambage S, Grant K, Pardo I, Ranford-Cartwright L, Hurd H (2009) Malaria ookinetes exhibit multiple markers for apoptosis-like programmed cell death in vitro. Parasit Vectors 2:32

    PubMed  PubMed Central  Google Scholar 

  • Arnoult D, Tatischeff I, Estaquier J, Girard M, Sureau F, Tissier JP, Grodet A, Dellinger M, Traincard F, Kahn A, Ameisen JC, Petit PX (2001) On the evolutionary conservation of the cell death pathway: mitochondrial release of an apoptosis-inducing factor during Dictyostelium discoideum cell death. Mol Biol Cell 12:3016–3030

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baehrecke EH (2003) Autophagic programmed cell death in Drosophila. Cell Death Differ 10:940–945

    CAS  PubMed  Google Scholar 

  • Bender CE, Fitzgerald P, Tait SW, Llambi F, GP MS, Tupper DO, Pellettieri J, Sánchez Alvarado A, Salvesen GS, Green DR (2012) Mitochondrial pathway of apoptosis is ancestral in metazoans. Proc Natl Acad Sci U S A 109:4904–4909

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berghe V, 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 15:135–147

    Google Scholar 

  • Bernardi P (2013) The mitochondrial permeability transition pore: a mystery solved? Front Physiol 4:95

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bonora M, Pinton P (2014) The mitochondrial permeability transition pore and cancer: molecular mechanisms involved in cell death. Front Oncol 4:302

    PubMed  PubMed Central  Google Scholar 

  • Büttner S, Habernig L, Broeskamp F, Ruli D, Vögtle FN, Vlachos M, Macchi F, Küttner V, Carmona-Gutierrez D, Eisenberg T, Ring J, Markaki M, Taskin AA, Benke S, Ruckenstuhl C, Braun R, Van den Haute C, Bammens T, van der Perren A, Fröhlich KU, Winderickx J, Kroemer G, Baekelandt V, Tavernarakis N, Kovacs GG, Dengjel J, Meisinger C, Sigrist SJ, Madeo F (2013) Endonuclease G mediates α-synuclein cytotoxicity during Parkinson’s disease. EMBO J 32:3041–3054

    PubMed  PubMed Central  Google Scholar 

  • Carloni S, Buonocore G, Balduini W (2008) Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol Dis 32:329–339

    CAS  PubMed  Google Scholar 

  • Carmona-Gutierrez D, Bauer MA, Zimmermann A, Aguilera A, Austriaco N, Ayscough K, Balzan R, Bar-Nun S, Barrientos A, Belenky P, Blondel M, Braun RJ, Breitenbach M, Burhans WC, Büttner S, Cavalieri D, Chang M, Cooper KF, Côrte-Real M, Costa V, Cullin C, Dawes I, Dengjel J, Dickman MB, Eisenberg T, Fahrenkrog B, Fasel N, Fröhlich KU, Gargouri A, Giannattasio S, Goffrini P, Gourlay CW, Grant CM, Greenwood MT, Guaragnella N, Heger T, Heinisch J, Herker E, Herrmann JM, Hofer S, Jiménez-Ruiz A, Jungwirth H, Kainz K, Kontoyiannis DP, Ludovico P, Manon S, Martegani E, Mazzoni C, Megeney LA, Meisinger C, Nielsen J, Nyström T, Osiewacz HD, Outeiro TF, Park HO, Pendl T, Petranovic D, Picot S, Polčic P, Powers T, Ramsdale M, Rinnerthaler M, Rockenfeller P, Ruckenstuhl C, Schaffrath R, Segovia M, Severin FF, Sharon A, Sigrist SJ, Sommer-Ruck C, Sousa MJ, Thevelein JM, Thevissen K, Titorenko V, Toledano MB, Tuite M, Vögtle FN, Westermann B, Winderickx J, Wissing S, Wölfl S, Zhang ZJ, Zhao RY, Zhou B, Galluzzi L, Kroemer G, Madeo F (2018) Guidelines and recommendations on yeast cell death nomenclature. Microb Cell 5:4–31

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carraro M, Bernardi P (2016) Calcium and reactive oxygen species in regulation of the mitochondrial permeability transition and of programmed cell death in yeast. Cell Calcium 60:102–107

    CAS  PubMed  PubMed Central  Google Scholar 

  • Celiker H, Gore J (2013) Cellular cooperation: insights from microbes. Trends Cell Biol 23:9–15

    CAS  PubMed  Google Scholar 

  • Chen F, Hersh BM, Conradt B, Zhou Z, Riemer D, Gruenbaum Y, Horvitz HR (2000) Translocation of C. elegans CED-4 to nuclear membranes during programmed cell death. Science 287:1485–1489

    CAS  PubMed  Google Scholar 

  • Chinopoulos C (2018) Mitochondrial permeability transition pore: Back to the drawing board. Neurochem Int 117:49–54

    CAS  PubMed  Google Scholar 

  • Chowdhury I, Tharakan B, Bhat GK (2008) Caspases - an update. Comp Biochem Physiol B Biochem Mol Biol 151:10–27

    PubMed  Google Scholar 

  • Curtis MJ, Wolpert TJ (2002) The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death. Plant J 29:295–312

    PubMed  Google Scholar 

  • D’Arcy MS (2019) Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int 43:582–592

    PubMed  Google Scholar 

  • Davila AF, Zamorano P (2013) Mitochondria and the evolutionary roots of cancer. Phys Biol 10:026008

    CAS  PubMed  Google Scholar 

  • Davis MC, Ward JG, Herrick G, Allis CD (1992) Programmed nuclear death: apoptotic-like degradation of specific nuclei in conjugating Tetrahymena. Dev Biol 154:419–432

    CAS  PubMed  Google Scholar 

  • Demetrius LA, Simon DK (2012) An inverse-Warburg effect and the origin of Alzheimer’s disease. Biogerontology 13:583–594

    CAS  PubMed  Google Scholar 

  • Doherty J, Baehrecke EH (2018) Life, death and autophagy. Nat Cell Biol 20:1110–1117

    CAS  PubMed  Google Scholar 

  • Dorstyn L, Kumar S (2006) A cytochrome c-free fly apoptosome. Cell Death Differ 13:1049–1051

    CAS  PubMed  Google Scholar 

  • Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127

    CAS  PubMed  Google Scholar 

  • Driver JA, Beiser A, Au R, Kreger BE, Splansky GL, Kurth T, Kiel DP, Lu KP, Seshadri S, Wolf PA (2012) Inverse association between cancer and Alzheimer’s disease: results from the Framingham Heart Study. BMJ 344:e1442

    PubMed  PubMed Central  Google Scholar 

  • Durand PM, Choudhury R, Rashidi A, Michod RE (2014) Programmed death in a unicellular organism has species-specific fitness effects. Biol Lett 10:20131088

    PubMed  PubMed Central  Google Scholar 

  • Durand PM, Barreto Filho MM, Michod RE (2019) Cell death in evolutionary transitions in individuality. Yale J Biol Med 92:651–662

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duszenko M, Figarella K, Macleod E, Welburn S (2006) Death of a trypanosome: a selfish altruism. Trends Parasitol 22:536–542

    PubMed  Google Scholar 

  • Eisler H, Fröhlich KU, Heidenreich E (2004) Starvation for an essential amino acid induces apoptosis and oxidative stress in yeast. Exp Cell Res 300:345–353

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Erental A, Sharon I, Engelberg-Kulka H (2012) Two programmed cell death systems in Escherichia coli: an apoptotic-like death is inhibited by the mazEF-mediated death pathway. PLoS Biol 10:e1001281

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fedak H, Palusinska M, Krzyczmonik K, Brzezniak L, Yatusevich R, Pietras Z, Kaczanowski S, Swiezewski S (2016) Control of seed dormancy in Arabidopsis by a cis-acting noncoding antisense transcript. Proc Natl Acad Sci U S A 113:E7846–E7E55

    CAS  PubMed  PubMed Central  Google Scholar 

  • Figarella K, Rawer M, Uzcategui NL, Kubata BK, Lauber K, Madeo F, Wesselborg S, Duszenko M (2005) Prostaglandin D2 induces programmed cell death in Trypanosoma brucei bloodstream form. Cell Death Differ 12:335–346

    CAS  PubMed  Google Scholar 

  • Gannavaram S, Vedvyas C, Debrabant A (2008) Conservation of the pro-apoptotic nuclease activity of endonuclease G in unicellular trypanosomatid parasites. J Cell Sci 121:99–109

    CAS  PubMed  Google Scholar 

  • Golstein P, Kroemer G (2007) Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32:37–43

    CAS  PubMed  Google Scholar 

  • Green DR, Fitzgerald P (2016) Just so stories about the evolution of Apoptosis. Curr Biol 26:R620–R627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Greenhalf W, Stephan C, Chaudhuri B (1996) Role of mitochondria and C-terminal membrane anchor of Bcl-2 in Bax induced growth arrest and mortality in Saccharomyces cerevisiae. FEBS Lett 380:169–175

    CAS  PubMed  Google Scholar 

  • Guttenberg N, Goldenfeld N (2008) Cascade of complexity in evolving predator-prey dynamics. Phys Rev Lett 100:058102

    PubMed  Google Scholar 

  • Hamilton WD (1964a) The genetical evolution of social behaviour. I. J Theor Biol 7:1–16

    CAS  PubMed  Google Scholar 

  • Hamilton WD (1964b) The genetical evolution of social behaviour. II. J Theor Biol 7:17–52

    CAS  PubMed  Google Scholar 

  • Hedgecock EM, Sulston JE, Thomson JN (1983) Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. Science 220:1277–1279

    CAS  PubMed  Google Scholar 

  • Hengartner MO, Horvitz HR (1994) C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76:665–676

    CAS  PubMed  Google Scholar 

  • Hope EA, Amorosi CJ, Miller AW, Dang K, Heil CS, Dunham MJ (2017) Experimental evolution reveals favored adaptive routes to cell aggregation in yeast. Genetics 206:1153–1167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hurd H, Grant K, Arambage S (2006) Apoptosis-like death as a feature of malaria infection in mosquitoes. Parasitology 132:S33–S47

    CAS  PubMed  Google Scholar 

  • Ibáñez K, Boullosa C, Tabarés-Seisdedos R, Baudot A, Valencia A (2014) Molecular evidence for the inverse comorbidity between central nervous system disorders and cancers detected by transcriptomic meta-analyses. PLoS Genet 10:e1004173

    PubMed  PubMed Central  Google Scholar 

  • Ito J, Fukuda H (2002) ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 14:3201–3211

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jansson B, Jankovic J (1985) Low cancer rates among patients with Parkinson’s disease. Ann Neurol 17:505–509

    CAS  PubMed  Google Scholar 

  • Kaczanowski S (2016) Apoptosis: its origin, history, maintenance and the medical implications for cancer and aging. Phys Biol 13:031001

    PubMed  Google Scholar 

  • Kaczanowski S, Sajid M, Reece SE (2011) Evolution of apoptosis-like programmed cell death in unicellular protozoan parasites. Parasit Vectors 4:44

    PubMed  PubMed Central  Google Scholar 

  • Kaczanowski S, Klim J, Zielenkiewicz U (2018) An apoptotic and endosymbiotic explanation of the Warburg and the inverse Warburg hypotheses. Int J Mol Sci 19:3100

    PubMed Central  Google Scholar 

  • Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klim J, Gładki A, Kucharczyk R, Zielenkiewicz U, Kaczanowski S (2018) Ancestral State Reconstruction of the Apoptosis Machinery in the Common Ancestor of Eukaryotes. G3 (Bethesda) 8:2121–2134

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kroemer G (1997) Mitochondrial implication in apoptosis: towards an endosymbiont hypothesis of apoptosis evolution. Cell Death Differ 4:443–456

    CAS  PubMed  Google Scholar 

  • Kutschera U (2009) Symbiogenesis, natural selection, and the dynamic earth. Theory Biosci 128:191–203

    CAS  PubMed  Google Scholar 

  • LaFerla FM, Tinkle BT, Bieberich CJ, Haudenschild CC, Jay G (1995) The Alzheimer’s A beta peptide induces neurodegeneration and apoptotic cell death in transgenic mice. Nat Genet 9:21–30

    CAS  PubMed  Google Scholar 

  • Li L, Luo X, Wang X (2001) Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412:95–99

    CAS  PubMed  Google Scholar 

  • Li W, Sun L, Liang Q, Wang J, Mo W, Zhou B (2006) Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol Biol Cell 17:1802–1811

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu ML, Yao MC (2012) Role of ATG8 and autophagy in programmed nuclear degradation in Tetrahymena thermophila. Eukaryot Cell 11:494–506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lyon C, Evans C, Bill B, Otsuka A, Aguilera R (2000) The C. elegans apoptotic nuclease NUC-1 is related in sequence and activity to mammalian DNase II. Gene 252:147–154

    CAS  PubMed  Google Scholar 

  • Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M, Kroemer G (1996) Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 184:1155–1160

    CAS  PubMed  Google Scholar 

  • Margulis L (1993) Symbiosis in cell evolution. Freeman, New York

    Google Scholar 

  • Mariño G, Niso-Santano M, Baehrecke EH, Kroemer G (2014) Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol 15:81–94

    PubMed  PubMed Central  Google Scholar 

  • Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (2005) The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity. J Biol Chem 280:30735–30740

    CAS  PubMed  Google Scholar 

  • Meslin B, Beavogui AH, Fasel N, Picot S (2011) Plasmodium falciparum metacaspase PfMCA-1 triggers a z-VAD-fmk inhibitable protease to promote cell death. PLoS One 6:e23867

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meurette O, Rebillard A, Huc L, Le Moigne G, Merino D, Micheau O, Lagadic-Gossmann D, Dimanche-Boitrel MT (2007) TRAIL induces receptor-interacting protein 1-dependent and caspase-dependent necrosis-like cell death under acidic extracellular conditions. Cancer Res 67:218–226

    CAS  PubMed  Google Scholar 

  • Minina EA, Filonova LH, Fukada K, Savenkov EI, Gogvadze V, Clapham D, Sanchez-Vera V, Suarez MF, Zhivotovsky B, Daniel G, Smertenko A, Bozhkov PV (2013) Autophagy and metacaspase determine the mode of cell death in plants. J Cell Biol 203:917–927

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minina EA, Bozhkov PV, Hofius D (2014) Autophagy as initiator or executioner of cell death. Trends Plant Sci 19:692–697

    CAS  PubMed  Google Scholar 

  • Mochizuki H, Goto K, Mori H, Mizuno Y (1996) Histochemical detection of apoptosis in Parkinson’s disease. J Neurol Sci 137:120–123

    CAS  PubMed  Google Scholar 

  • Moore RB, Oborník M, Janouskovec J, Chrudimský T, Vancová M, Green DH, Wright SW, Davies NW, Bolch CJ, Heimann K, Slapeta J, Hoegh-Guldberg O, Logsdon JM, Carter DA (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–963

    CAS  PubMed  Google Scholar 

  • Mpoke S, Wolfe J (1996) DNA digestion and chromatin condensation during nuclear death in Tetrahymena. Exp Cell Res 225:357–365

    CAS  PubMed  Google Scholar 

  • O’Connor C (2010) Essentials of cell biology. https://www.nature.com/scitable/ebooks/essentials-of-cell-biology-14749010/118237915/

  • Oda K, Kawasaki N, Fukuyama M, Ikeda S (2007) Ectopic expression of mitochondria endonuclease Pnu1p from Schizosaccharomyces pombe induces cell death of the yeast. J Biochem Mol Biol 40:1095–1099

    CAS  PubMed  Google Scholar 

  • Osada E, Akematsu T, Asano T, Endoh H (2014) A novel mitochondrial nuclease-associated protein: a major executor of the programmed nuclear death in Tetrahymena thermophila. Biol Cell 106:97–109

    CAS  PubMed  Google Scholar 

  • Parfrey LW, Lahr DJ (2013) Multicellularity arose several times in the evolution of eukaryotes. Bioessays 35:339–347. https://doi.org/10.1002/bies.201100187

    Article  CAS  PubMed  Google Scholar 

  • Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petit P, Susin S, Zamzami N, Mignotte B, Kroemer G (1996) Mitochondria and programmed cell death: back to the future. FEBS Lett 396:7–13

    CAS  PubMed  Google Scholar 

  • Qi S, Pang Y, Hu Q, Liu Q, Li H, Zhou Y, He T, Liang Q, Liu Y, Yuan X, Luo G, Wang J, Yan N, Shi Y (2010) Crystal structure of the Caenorhabditis elegans apoptosome reveals an octameric assembly of CED-4. Cell 141:446–457

    CAS  PubMed  Google Scholar 

  • Ratcliff WC, Denison RF, Borrello M, Travisano M (2012) Experimental evolution of multicellularity. Proc Natl Acad Sci U S A 109:1595–1600

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rico E, Alzate JF, Arias AA, Moreno D, Clos J, Gago F, Moreno I, Domínguez M, Jiménez-Ruiz A (2009) Leishmania infantum expresses a mitochondrial nuclease homologous to EndoG that migrates to the nucleus in response to an apoptotic stimulus. Mol Biochem Parasitol 163:28–38

    CAS  PubMed  Google Scholar 

  • Robertson AM, Thomson J (1982) Morphology of programmed cell death in the ventral nerve cord of Caenorhabditis elegans larvae. Development 67:89–100

    Google Scholar 

  • Roisin-Bouffay C, Luciani MF, Klein G, Levraud JP, Adam M, Golstein P (2004) Developmental cell death in dictyostelium does not require paracaspase. J Biol Chem 279:11489–11494

    CAS  PubMed  Google Scholar 

  • Rokas A (2008) The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu Rev Genet 42:235–251

    CAS  PubMed  Google Scholar 

  • Rubinsztein DC, Mariño G, Kroemer G (2011) Autophagy and aging. Cell 146:682–695

    CAS  PubMed  Google Scholar 

  • Rust A, Leese C, Binz T, Davletov B (2016) Botulinum neurotoxin type C protease induces apoptosis in differentiated human neuroblastoma cells. Oncotarget 7:33220–33228

    PubMed  PubMed Central  Google Scholar 

  • Sakahira H, Enari M, Nagata S (1998) Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391:96–99

    CAS  PubMed  Google Scholar 

  • Schweichel JU, Merker HJ (1973) The morphology of various types of cell death in prenatal tissues. Teratology 7:253–266

    CAS  PubMed  Google Scholar 

  • Seipp S, Schmich J, Leitz T (2001) Apoptosis--a death-inducing mechanism tightly linked with morphogenesis in Hydractina echinata (Cnidaria, Hydrozoa). Development 128:4891–4898

    CAS  PubMed  Google Scholar 

  • Seipp S, Wittig K, Stiening B, Böttger A, Leitz T (2006) Metamorphosis of Hydractinia echinata (Cnidaria) is caspase-dependent. Int J Dev Biol 50:63–70

    CAS  PubMed  Google Scholar 

  • Silva RD, Sotoca R, Johansson B, Ludovico P, Sansonetty F, Silva MT, Peinado JM, Côrte-Real M (2005) Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Mol Microbiol 58:824–834

    CAS  PubMed  Google Scholar 

  • Soares EV (2011) Flocculation in Saccharomyces cerevisiae: a review. J Appl Microbiol 110:1–18

    CAS  PubMed  Google Scholar 

  • Steller H (1995) Mechanisms and genes of cellular suicide. Science 267:1445–1449

    CAS  PubMed  Google Scholar 

  • Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56:110–156

    CAS  PubMed  Google Scholar 

  • Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119

    CAS  PubMed  Google Scholar 

  • Sundström J, Vaculova A, Smertenko A, Savenkov E, Golovko A, Minina E, Tiwari B, Rodriguez-Nieto S, Zamyatnin AJ, Välineva T, Saarikettu J, Frilander M, Suarez M, Zavialov A, Ståhl U, Hussey P, Silvennoinen O, Sundberg E, Zhivotovsky B, Bozhkov P (2009) Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat Cell Biol 11:1347–1354

    PubMed  Google Scholar 

  • Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441–446

    CAS  PubMed  Google Scholar 

  • Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R (2001) A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 8:613–621

    CAS  PubMed  Google Scholar 

  • Tamm I, Wang Y, Sausville E, Scudiero DA, Vigna N, Oltersdorf T, Reed JC (1998) IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res 58:5315–5320

    CAS  PubMed  Google Scholar 

  • Tovar J, León-Avila G, Sánchez LB, Sutak R, Tachezy J, van der Giezen M, Hernández M, Müller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172–176

    CAS  PubMed  Google Scholar 

  • Valen LV (1973) A new evolutionary law. Evol Theory 1:1–30

    Google Scholar 

  • Van Durme M, Nowack MK (2016) Mechanisms of developmentally controlled cell death in plants. Curr Opin Plant Biol 29:29–37

    PubMed  Google Scholar 

  • Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A, Levine A (1999) Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO(2) limitation and oxidative stress. Curr Biol 9:1061–1064

    CAS  PubMed  Google Scholar 

  • Walker JE, Carroll J, He J (2020) Reply to Bernardi: the mitochondrial permeability transition pore and the ATP synthase. Proc Natl Acad Sci U S A 117:2745–2746

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walter D, Wissing S, Madeo F, Fahrenkrog B (2006) The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2. J Cell Sci 119:1843–1851

    CAS  PubMed  Google Scholar 

  • Wang X, Yang C, Chai J, Shi Y, Xue D (2002) Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298:1587–1592

    CAS  PubMed  Google Scholar 

  • Warburg O (1956) On the origin of cancer cells. Science 123:309–314

    CAS  PubMed  Google Scholar 

  • Welburn S, Dale C, Ellis D, Beecroft R, Pearson T (1996) Apoptosis in procyclic Trypanosoma brucei rhodesiense in vitro. Cell Death Differ 3:229–236

    CAS  PubMed  Google Scholar 

  • Whittingham WF, Raper KB (1960) Non-viability of stalk cells in dictyostelium. Proc Natl Acad Sci U S A 46:642–649

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Q, Lin T, Zhang Y, Zheng J, Bonanno JA (2005) Molecular cloning and characterization of a human AIF-like gene with ability to induce apoptosis. J Biol Chem 280:19673–19681

    CAS  PubMed  Google Scholar 

  • Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75:641–652

    CAS  PubMed  Google Scholar 

  • Zhang J, Zhang Y, Li J, Xing S, Li C, Li Y, Dang C, Fan Y, Yu J, Pei Z, Zeng J (2012) Autophagosomes accumulation is associated with β-amyloid deposits and secondary damage in the thalamus after focal cortical infarction in hypertensive rats. J Neurochem 120:564–573

    CAS  PubMed  Google Scholar 

  • Zou H, Li Y, Liu X, Wang X (1999) An APAF-1. cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274:11549–11556

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by the National Science Centre of Poland NCN grant number 2017/27/B/NZ8/02502.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Szymon Kaczanowski .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kaczanowski, S. (2020). Symbiotic Origin of Apoptosis. In: Kloc, M. (eds) Symbiosis: Cellular, Molecular, Medical and Evolutionary Aspects. Results and Problems in Cell Differentiation, vol 69. Springer, Cham. https://doi.org/10.1007/978-3-030-51849-3_10

Download citation

Publish with us

Policies and ethics