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Apoptosis in pre-Bilaterians: Hydra as a model

  • Unusual Model Systems for Cell Death Research
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Abstract

Hydra is a member of the ancient metazoan phylum Cnidaria and is an especially well investigated model organism for questions of the evolutionary origin of metazoan processes. Apoptosis in Hydra is important for the regulation of cellular homeostasis under different conditions of nutrient supply. The molecular mechanisms leading to apoptosis in Hydra are surprisingly extensive and comparable to those in mammals. Genome wide sequence analysis has revealed the presence of large caspase and Bcl-2 families, the apoptotic protease activating factor (APAF-1), inhibitors of apoptotic proteases (IAPs) and components of a putative death receptor pathway. Regulation of apoptosis in Hydra may involve BH-3 only proteins and survival pathways, possibly including insulin signalling.

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References

  1. Böttger A, David CN (2003) Evolution of Cell death: caspase mediated mechanisms in early metazoans; noncaspase mechanisms in single celled eukaryotes. In: Grimm S (ed) Genetics of apoptosis. BIOS Scientific Publishers Ltd, Oxford, pp 145–153

    Google Scholar 

  2. Gierer A, Berking S, Bode H et al (1972) Regeneration of hydra from reaggregated cells. Nat New Biol 239:98–101

    Article  CAS  PubMed  Google Scholar 

  3. Fowler SJ, Jose S, Zhang X, Deutzmann R, Sarras MP Jr, Boot-Handford RP (2000) Characterization of hydra type IV collagen. Type IV collagen is essential for head regeneration and its expression is up-regulated upon exposure to glucose. J Biol Chem 275:39589–39599

    Article  CAS  PubMed  Google Scholar 

  4. Sarras MP Jr, Yan L, Grens A et al (1994) Cloning and biological function of laminin in Hydra vulgaris. Dev Biol 164:312–324

    Article  CAS  PubMed  Google Scholar 

  5. Zhang X, Boot-Handford RP, Huxley-Jones J et al (2007) The collagens of hydra provide insight into the evolution of metazoan extracellular matrices. J Biol Chem 282:6792–6802

    Article  CAS  PubMed  Google Scholar 

  6. Alexopoulos H, Bottger A, Fischer S et al (2004) Evolution of gap junctions: the missing link? Curr Biol 14:R879–R880

    Article  CAS  PubMed  Google Scholar 

  7. Filshie BK, Flower NE (1977) Junctional structures in hydra. J Cell Sci 23:151–172

    CAS  PubMed  Google Scholar 

  8. Hand AR, Gobel S (1972) The structural organization of the septate and gap junctions of Hydra. J Cell Biol 52:397–408

    Article  CAS  PubMed  Google Scholar 

  9. Campbell RD (1967) Tissue dynamics of steady state growth in Hydra littoralis. II. Patterns of tissue movement. J Morphol 121:19–28

    Article  CAS  PubMed  Google Scholar 

  10. David CN, Gierer A (1974) Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. J Cell Sci 16:359–375

    CAS  PubMed  Google Scholar 

  11. David CN, Campbell RD (1972) Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. J Cell Sci 11:557–568

    CAS  PubMed  Google Scholar 

  12. Bode HR (1996) The interstitial cell lineage of hydra: a stem cell system that arose early in evolution. J Cell Sci 109:1155–1164

    CAS  PubMed  Google Scholar 

  13. David CN, Murphy S (1977) Characterization of interstitial stem cells in hydra by cloning. Dev Biol 58:372–383

    Article  CAS  PubMed  Google Scholar 

  14. Bosch TCG, David CN (1987) Stem cells of Hydra magnipapillata can differentiate into somatic and germ line cells. Dev Biol 121:182–191

    Article  Google Scholar 

  15. Otto JJ, Campbell RD (1977) Tissue economics of hydra: regulation of cell cycle, animal size and development by controlled feeding rates. J Cell Sci 28:117–132

    CAS  PubMed  Google Scholar 

  16. Bosch TC, David CN (1984) Growth regulation in Hydra: relationship between epithelial cell cycle length and growth rate. Dev Biol 104:161–171

    Article  CAS  PubMed  Google Scholar 

  17. Cikala M, Wilm B, Hobmayer E, Böttger A, David CN (1999) Identification of caspases and apoptosis in the simple metazoan Hydra. Curr Biol 9:959–962

    Article  CAS  PubMed  Google Scholar 

  18. Böttger A, Alexandrova O (2007) Programmed cell death in Hydra. Semin Cancer Biol 17:134–146

    Article  PubMed  Google Scholar 

  19. Abrams JM, White K, Fessler LI, Steller H (1993) Programmed cell death during Drosophila embryogenesis. Development 117:29–43

    CAS  PubMed  Google Scholar 

  20. Mpoke SS, Wolfe J (1997) Differential staining of apoptotic nuclei in living cells: application to macronuclear elimination in Tetrahymena. J Histochem Cytochem 45:675–683

    CAS  PubMed  Google Scholar 

  21. Bosch TCG, David CN (1986) Immunocompetence in Hydra: epithelial cells recognize self-nonself and react against it. J Exp Zool 238:225–234

    Article  Google Scholar 

  22. Kuznetsov SG, Bosch TC (2003) Self/nonself recognition in Cnidaria: contact to allogeneic tissue does not result in elimination of nonself cells in Hydra vulgaris. Zoology (Jena) 106:109–116

    CAS  Google Scholar 

  23. Fujisawa T, David CN (1984) Loss of differentiating nematocytes induced by regeneration and wound healing in Hydra. J Cell Sci 68:243–255

    CAS  PubMed  Google Scholar 

  24. Yaross MS, Bode HR (1978) Regulation of interstitial cell differentiation in Hydra attenuata. IV. Nerve cell commitment in head regeneration is position-dependent. J Cell Sci 34:27–38

    CAS  PubMed  Google Scholar 

  25. Yaross MS, Bode HR (1978) Regulation of interstitial cell differentiation in Hydra attenuata. V. Inability of regenerating head to support nematocyte differentiation. J Cell Sci 34:39–52

    CAS  PubMed  Google Scholar 

  26. Chera S, Ghila L, Dobretz K et al (2009) Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev Cell 17:279–289

    Article  CAS  PubMed  Google Scholar 

  27. Campbell RD (1976) Elimination by Hydra interstitial and nerve cells by means of colchicine. J Cell Sci 21:1–13

    CAS  PubMed  Google Scholar 

  28. Fujisawa T, Sugiyama T (1978) Genetic analysis of developmental mechanisms in Hydra. IV. Characterization of a nematocyst-deficient strain. J Cell Sci 30:175–185

    CAS  PubMed  Google Scholar 

  29. Marcum BA, Campbell RD (1978) Development of Hydra lacking nerve and interstitial cells. J Cell Sci 29:17–33

    CAS  PubMed  Google Scholar 

  30. Aizenshtadt TB (1978) Oogenesis in Hydra. III. The growth and fusion of the oocytes. Ontogenez 9:115–123

    CAS  PubMed  Google Scholar 

  31. Alexandrova O, Schade M, Böttger A, David CN (2005) Oogenesis in Hydra: nurse cells transfer cytoplasm directly to the growing oocyte. Dev Biol 281:91–101

    Article  CAS  PubMed  Google Scholar 

  32. Technau U, Miller MA, Bridge D, Steele RE (2003) Arrested apoptosis of nurse cells during Hydra oogenesis and embryogenesis. Dev Biol 260:191–206

    Article  CAS  PubMed  Google Scholar 

  33. Carrington PE, Sandu C, Wei Y et al (2006) The structure of FADD and its mode of interaction with procaspase-8. Mol Cell 22:599–610

    Article  CAS  PubMed  Google Scholar 

  34. Festjens N, Cornelis S, Lamkanfi M, Vandenabeele P (2006) Caspase-containing complexes in the regulation of cell death and inflammation. Biol Chem 387:1005–1016

    Article  CAS  PubMed  Google Scholar 

  35. Chowdhury I, Tharakan B, Bhat GK (2006) Current concepts in apoptosis: the physiological suicide program revisited. Cell Mol Biol Lett 11:506–525

    Article  CAS  PubMed  Google Scholar 

  36. Dempsey PW, Doyle SE, He JQ, Cheng G (2003) The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev 14:193–209

    Article  CAS  PubMed  Google Scholar 

  37. Giam M, Huang DC, Bouillet P (2008) BH3-only proteins and their roles in programmed cell death. Oncogene 27(Suppl 1):S128–S136

    Article  CAS  PubMed  Google Scholar 

  38. Vaux DL, Silke J (2005) IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 6:287–297

    Article  CAS  PubMed  Google Scholar 

  39. Aouacheria A, Brunet F, Gouy M (2005) Phylogenomics of life-or-death switches in multicellular animals: Bcl-2, BH3-Only, and BNip families of apoptotic regulators. Mol Biol Evol 22:2395–2416

    Article  CAS  PubMed  Google Scholar 

  40. Wiens M, Diehl-Seifert B, Muller WE (2001) Sponge Bcl-2 homologous protein (BHP2-GC) confers distinct stress resistance to human HEK-293 cells. Cell Death Differ 8:887–898

    Article  CAS  PubMed  Google Scholar 

  41. Wiens M, Krasko A, Muller CI, Muller WE (2000) Molecular evolution of apoptotic pathways: cloning of key domains from sponges (Bcl-2 homology domains and death domains) and their phylogenetic relationships. J Mol Evol 50:520–531

    CAS  PubMed  Google Scholar 

  42. Wang C, Youle RJ (2009) The role of mitochondria in apoptosis. Annu Rev Genet

  43. Geng X, Shi Y, Nakagawa A et al (2008) Inhibition of CED-3 zymogen activation and apoptosis in Caenorhabditis elegans by caspase homolog CSP-3. Nat Struct Mol Biol 15:1094–1101

    Article  CAS  PubMed  Google Scholar 

  44. Silke J, Vaux DL (2001) Two kinds of BIR-containing protein—inhibitors of apoptosis, or required for mitosis. J Cell Sci 114:1821–1827

    CAS  PubMed  Google Scholar 

  45. Lin N, Zhang C, Pang J, Zhou L (2009) By design or by chance: cell death during Drosophila embryogenesis. Apoptosis 14:935–942

    Article  PubMed  Google Scholar 

  46. Igaki T, Kanda H, Yamamoto-Goto Y et al (2002) Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J 21:3009–3018

    Article  CAS  PubMed  Google Scholar 

  47. Kanda H, Igaki T, Kanuka H, Yagi T, Miura M (2002) Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling. J Biol Chem 277:28372–28375

    Article  CAS  PubMed  Google Scholar 

  48. Kauppila S, Maaty WS, Chen P et al (2003) Eiger and its receptor, Wengen, comprise a TNF-like system in Drosophila. Oncogene 22:4860–4867

    Article  CAS  PubMed  Google Scholar 

  49. Taylor RC, Cullen SP, Martin SJ (2008) Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 9:231–241

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  51. Dunn SR, Phillips WS, Spatafora JW, Green DR, Weis VM (2006) Highly conserved caspase and Bcl-2 homologues from the sea anemone Aiptasia pallida: lower metazoans as models for the study of apoptosis evolution. J Mol Evol 63:95–107

    Article  CAS  PubMed  Google Scholar 

  52. Zmasek CM, Zhang Q, Ye Y, Godzik A (2007) Surprising complexity of the ancestral apoptosis network. Genome Biol 8:R226

    Article  PubMed  Google Scholar 

  53. Lasi M (2009) Das komplexe Netzwerk Apoptose regulierender Proteine in Hydra. Dissertation, Ludwig-Maximilians-University Munich

  54. Yu X, Acehan D, Menetret JF et al (2005) A structure of the human apoptosome at 12.8. A resolution provides insights into this cell death platform. Structure 13:1725–1735

    Article  CAS  PubMed  Google Scholar 

  55. 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

    Article  CAS  PubMed  Google Scholar 

  56. Shaham S (1998) Identification of multiple Caenorhabditis elegans caspases and their potential roles in proteolytic cascades. J Biol Chem 273:35109–35117

    Article  CAS  PubMed  Google Scholar 

  57. Müller-Taubenberger A, Vos MJ, Böttger A et al. (2006) Monomeric red fluorescent protein variants used for imaging studies in different species. Eur J Cell Biol

  58. Conradt B, Horvitz HR (1998) The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93:519–529

    Article  CAS  PubMed  Google Scholar 

  59. Schumacher B, Schertel C, Wittenburg N et al (2005) C. elegans ced-13 can promote apoptosis and is induced in response to DNA damage. Cell Death Differ 12:153–161

    Article  CAS  PubMed  Google Scholar 

  60. Edgar BA (2006) How flies get their size: genetics meets physiology. Nat Rev Genet 7:907–916

    Article  CAS  PubMed  Google Scholar 

  61. Burgering BM, Kops GJ (2002) Cell cycle and death control: long live Forkheads. Trends Biochem Sci 27:352–360

    Article  CAS  PubMed  Google Scholar 

  62. Puig O, Tjian R (2006) Nutrient availability and growth: regulation of insulin signaling by dFOXO/FOXO1. Cell Cycle 5:503–505

    CAS  PubMed  Google Scholar 

  63. Steele R, Lieu P, Shenk M, Sarras M (1996) Response to insulin and the expression pattern of a gene encoding an insulin receptor homologue suggests a role for an insulin-like molecule in regulating growth and patterning in Hydra. Dev Genes Evol 206:247–259

    Article  CAS  Google Scholar 

  64. Herold M, Cikala M, MacWilliams H, David CN, Böttger A (2002) Cloning and characterisation of PKB and PRK homologs from Hydra and the evolution of the protein kinase family. Dev Genes Evol 212:513–519

    Article  CAS  PubMed  Google Scholar 

  65. David CN, Schmidt N, Schade M, Pauly B, Alexandrova O, Böttger A (2005) Hydra and the evolution of apoptotis. Integr Comp Biol 45:631–638

    Article  CAS  Google Scholar 

  66. Böttger A, Alexandrova O, Cikala M, Schade M, Herold M, David CN (2002) GFP expression in Hydra: lessons from the particle gun. Dev Genes Evol 212:302–305

    Article  PubMed  Google Scholar 

  67. Wittlieb J, Khalturin K, Lohmann JU, Anton-Erxleben F, Bosch TC (2006) Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc Natl Acad Sci USA 103:6208–6211

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Angelika Böttger.

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Lasi, M., David, C.N. & Böttger, A. Apoptosis in pre-Bilaterians: Hydra as a model. Apoptosis 15, 269–278 (2010). https://doi.org/10.1007/s10495-009-0442-7

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