Symmetry Breaking in Stem Cells of the Basal Metazoan Hydra

  • Thomas C. G. Bosch
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 45)


Stem Cell Interstitial Cell Asymmetric Division Asymmetric Cell Division Gastric Region 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akashi K, He X, Chen J, Iwasaki H, Niu C, Steenhard B, Zhang J, Haug J, Li L (2003) Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood 101(2):383–389.PubMedGoogle Scholar
  2. Augustin R, Franke A, Khalturin K, Kiko R, Siebert S, Hemmrich G, Bosch TCG (2006) Dickkopf related genes are components of the positional value gradient in Hydra. Dev Biol (in press).Google Scholar
  3. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG (2006) Chromatin signatures of pluripotent cell lines. Nature Cell Biol 8(5):532–538.PubMedGoogle Scholar
  4. Bashirullah A, Cooperstock RL, Lipshitz HD (1998) RNA localization in development. Ann Rev Biochem 67:335–394.PubMedGoogle Scholar
  5. Bode HR, Heimfeld S, Chow M, Huang LW (1987) Gland cells arise by differentiation from interstitial cells in Hydra attenuata. Dev Biol 122:577–585.PubMedGoogle Scholar
  6. Bosch TCG (2003) Ancient signals: peptides and the interpretation of positional information in ancestral metazoans. Comp Biochem Physiol B Biochem Mol Biol 136(2):185–196.PubMedGoogle Scholar
  7. Bosch TCG (2006) Why polyps regenerate and we don't: towards a cellular and molecular framework for Hydra regeneration. Dev Biol (in press).Google Scholar
  8. Bosch TCG, David CN (1986). Male and female stem cells and sex reversal in Hydra polyps. Proc Natl Acad Sci USA 83:9478–9482.PubMedGoogle Scholar
  9. Bosch TCG, David CN (1987) Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev Biol 121:182–191.Google Scholar
  10. Bosch TCG, David CN (1990) Cloned interstitial stem cells grow as contiguous patches in hydra. Dev Biol 138:513–515.PubMedGoogle Scholar
  11. Bosch TCG, Fujisawa T (2001) Polyps, peptides and patterning. BioEssays 23(5):420–427.PubMedGoogle Scholar
  12. Bosch TCG, Rollbühler R, Scheider B, David CN (1991) Role of the cellular environment in interstitial stem cell proliferation in hydra. Roux's Arch Dev Biol 200:269–276.Google Scholar
  13. Brinkmann M, Oliver D, Thurm U (1996) Mechanoelectric transduction in namatocytes of a hydropolyp (Corynidae). J Comp Phys 178:125–138.Google Scholar
  14. Campbell RD (1985) Sex determination in Hydra: roles of germ cells (interstitial cells) and somatic cells. J Exp Zool 234:451–458.Google Scholar
  15. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298:1039–1043.PubMedGoogle Scholar
  16. Chen D, McKearin D (2003) Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol 13:1786–1791.PubMedGoogle Scholar
  17. Collins AG (1998) Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18 S rRNA molecular evidence. Proc Natl Acad Sci USA 95:15458–15463.PubMedGoogle Scholar
  18. Darmer D, Hauser F, Nothacker HP, Bosch TC, Williamson M, Grimmelikhuijzen CJ (1998) Three different prohormones yield a variety of Hydra-RFamide (Arg-Phe-NH2) neuropeptides in Hydra magnipapillata Biochem J 332(2):403–412.PubMedGoogle Scholar
  19. David CN, Challoner D (1974) Distribution of interstitial cells and differentiating nematocytes in Hydra attenuata. Am Zool 14:537–542.Google Scholar
  20. David CN, Gierer A (1974) Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. J Cell Sci 16:359–375.PubMedGoogle Scholar
  21. David CN, MacWilliams H (1978) Regulation of the self-renewal probability in Hydra stem cell clones. Proc Natl Acad Sci USA 75(2):886–890.PubMedGoogle Scholar
  22. David CN, Murphy S (1977) Characterization of interstitial stem cells in hydra by cloning. Dev Biol 58:372–383.PubMedGoogle Scholar
  23. David CN, Plotnick I (1980) Distribution of interstitial stem cells in Hydra. Dev Biol 76(1):175–184.PubMedGoogle Scholar
  24. David CN, Fujisawa T, Bosch TCG (1991) Interstitial stem cell proliferation in hydra: evidence for strain specific regulatory signals. Dev Biol 148:501–507.PubMedGoogle Scholar
  25. Dellaporta SL, Xu A, Sagasser S, Jakob W, Moreno MA, Buss LW, Schierwater B (2006) Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum. Proc Natl Acad Sci USA 103(23):8751–8756.PubMedGoogle Scholar
  26. Deng W, Lin H (1997) Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev Biol 189(1):79–94.PubMedGoogle Scholar
  27. Dübel S, Hoffmeister SA, Schaller HC (1987) Differentiation pathways of ectodermal epithelial cells in hydra. Differentiation 35(3):181–189.PubMedGoogle Scholar
  28. Dunne J, Javois LC, Huang LW, Bode HR (1985) A subset of cells in the nerve net of Hydra oligactis defined by a monoclonal antibody: its arrangement and development. Dev Biol 109:41–53.PubMedGoogle Scholar
  29. Engel U, Pertz O, Fauser C, Engel J, David CN, Holstein TW (2001) A switch in disulfide linkage during minicollagen assembly in Hydra nematocysts. EMBO J 20(12):3063–3073.PubMedGoogle Scholar
  30. Engel U, Oezbek S, Engel R, Petri B, Lottspeich F, Holstein TW (2002) Nowa, a novel protein with minicollagen Cys-rich domains is involved in nematocyst formation in Hydra. J Cell Sci 115:3923–3934.PubMedGoogle Scholar
  31. Fedders H, Augustin R, Bosch TCG (2004) A Dickkopf-3 related gene is expressed in differentiating nematocytes in the basal metazoan Hydra. Dev Genes Evol 214:72–80.PubMedGoogle Scholar
  32. Fujisawa T (1989) Role of interstitial cell migration in generating position-dependent patterns of nerve cell differentiation in Hydra. Dev Biol 133:77–82.PubMedGoogle Scholar
  33. Genikhovich G, Kürn U, Hemmrich G, Bosch TCG (2006) Discovery of genes expressed in Hydra embryogenesis. Dev Biol 289(2):466–481.PubMedGoogle Scholar
  34. Gierer A, Berking S, Bode H, David CN, Flick K, Hansmann G, Schaller H, Trenkner E (1972) Regeneration of Hydra from reaggregated cells. Nature New Biol 239:98–101.PubMedGoogle Scholar
  35. Grell KG (1971) Trichoplax adhaerens F.E. Schulze und die Entstehung der Metazoen. Naturwiss Rundsch 24:160–161.Google Scholar
  36. Grens A, Mason E, Marsh JL, Bode HR (1995). Evolutionary conservation of a cell fate specification gene: the Hydra achaete scute homolog has proneural activity in Drosophila. Development 121:4027–4035.PubMedGoogle Scholar
  37. Grimes SR (2004) Testis-specific transcriptional control. Gene 343:11–22.PubMedGoogle Scholar
  38. Grimmelikhuijzen CJP, Dockray GJ, Schot LPC (1982a) FMRFamide-like immunoreactivity in the nervous system of hydra. Histochemistry 73:499–508.PubMedGoogle Scholar
  39. Grimmelikhuijzen CJP, Dierickx K, Boer GJ (1982b) Oxytocin/vasopression-like immunoreactivity in the nervous system of Hydra. Neuroscience 7:3191–3199.PubMedGoogle Scholar
  40. Guder C, Pinho S, Nacak T, Hobmayer B, Niehrs C, Holstein TW (2006) An ancient Wnt-Dickkopf antagonism in Hydra. Development 133(5):901–911.PubMedGoogle Scholar
  41. Hager G, David CN (1997) Pattern of differentiated nerve cells in hydra is determined by precursor migration. Development 124:569–576.PubMedGoogle Scholar
  42. Hansen GN, Williamson M, Grimmelikhuijzen CJP (2000) Two-color double-labeling in situ hybridization of whole-mount Hydra using RNA probes for five different Hydra neuropeptide preprohormones: evidence for colocalization. Cell Tissue Res 301:245–253.PubMedGoogle Scholar
  43. Hausmann K, Holstein TW (1985) Sensory receptor with bilateral symmetrical polarity. Naturwissenschaften 72:145–146.Google Scholar
  44. Hayakawa E, Fujisawa C, Fujisawa T (2004) Involvement of Hydra achaete-scute gene CnASH in the differentiation pathway of sensory neurons in the tentacles. Dev Genes Evol 214(10):486–492.PubMedGoogle Scholar
  45. Heimfeld S, Bode HR (1984) Interstitial cell migration in Hydra attenuata: I. Quantitative description of cell movements. Dev Biol 105:1–9.PubMedGoogle Scholar
  46. Hobmayer E, Holstein TW, David CN (1990a) Tentacle morphogenesis in hydra I: the role of head activator. Development 109:887–895.Google Scholar
  47. Hobmayer E, Holstein TW, David CN (1990b) Tentacle morphogenesis in hydra II: formation of a complex between a sensory nerve cell and a battery cell. Development 109:897–901.Google Scholar
  48. Holstein T (1981) The morphogenesis of nematocytes in Hydra and Forskália: an ultrastructural study. J Ultrastruct Res 75:276–290.PubMedGoogle Scholar
  49. Holstein TW, David CN (1990) Cell cycle length, cell size, and proliferation rate in hydra stem cells. Dev Biol 142:392–400.PubMedGoogle Scholar
  50. Holstein TW, Benoit M, von Herder G, Wanner G, David CN, Gaub EH (1994) Fibrous mini-collagens in Hydra nematocytes. Science 223:402–404.Google Scholar
  51. Kirmizis A, Bartley SM, Kuzmichev A, Margueron R, Reinberg D, Green R, Farnham PJ (2004) Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev 18:1592–1605.PubMedGoogle Scholar
  52. Koch AW, Holstein TW, Mala C, Kurz E, Engel J, David CN (1998) Spinalin, a new glycine- and histidine-rich protein in spines of Hydra nematocysts. J Cell Sci 111(11):1545–1554.PubMedGoogle Scholar
  53. Koizumi O, Heimfeld S, Bode HR (1988) Plasticity in the nervous system of adult hydra. II. Conversion of ganglion cells of the body column into epidermal sensory cells of the hypostome. Dev Biol 129:358–371.PubMedGoogle Scholar
  54. Kortschak RD, Samuel G, Saint R, Miller DJ (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol 13:2190–2195.PubMedGoogle Scholar
  55. Krupnik VE, Sharp JD, Jiang C, Robison K, Chickering TW, Amaravadi L, Brown DE, Guyot D, Mays G, Leiby K, Chang B, Duong T, Goodearl AD, Gearing DP, Sokol SY, McCarthy SA (1999) Functional and structural diversity of the human Dickkopf gene family Gene 238(2):301–313.Google Scholar
  56. Kurz E, Holstein TW, Petri BM, Engel J, David CN (1991) Mini-collagens in Hydra nematocytes. J Cell Biol 115:1159–1169.PubMedGoogle Scholar
  57. Kuzmichev A, Junewein T, Tempst P, Reinberg D (2004) Different Ezh2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol Cell 14:183–193.PubMedGoogle Scholar
  58. Kuznetsov S, Lyanguzowa M, Bosch TCG (2001) Role of epithelial cells and programmed cell death in Hydra spermatogenesis. Zoology 104(1):25–31.PubMedGoogle Scholar
  59. Leatherman JL, Jongens TA (2003) Transcriptional silencing and translational control: key features of early germline development. BioEssays 25(4):326–335.PubMedGoogle Scholar
  60. Leys SP, Ereskovsky AV (2006) Embryogenesis and larval differentiation in sponges. Can J Zool 84:262–287.Google Scholar
  61. Lin H, Schagat T (1997) Neuroblasts: a model for the asymmetric division of stem cells. Trends Genet 13:33–39.PubMedGoogle Scholar
  62. Lindgens D, Holstein TW, Technau U (2004) Hyzic, the Hydra homolog of the zic/odd-paired gene, is involved in the early specification of the sensory nemtaocytes. Development 131(1):191–201.PubMedGoogle Scholar
  63. Littlefield CL (1984) The interstitial cells control the sexual phenotype of heterosexual chimeras of hydra. Dev Biol 102:426–432.PubMedGoogle Scholar
  64. Littlefield CL (1985) Germ cells in Hydra oligactis males. I. Isolation of a subpopulation of interstitial cells that is developmentally restricted to sperm production. Dev Biol 112(1):185–193.PubMedGoogle Scholar
  65. Littlefield CL (1991) Cell lineages in Hydra: isolation and characterization of an interstitial stem cell restricted to egg production in Hydra oligactis. Dev Biol 143:378–388.Google Scholar
  66. Littlefield CL (1994) Cell-cell interactions and the control of sex determination in hydra. Semin Dev Biol 5:13–20.Google Scholar
  67. Mariscal RN (1974) Nematocysts. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology: reviews and new perspectives. Academic Press, New York, pp 129–178.Google Scholar
  68. Metschnikoff E (1883) Untersuchungen über die intracelluläre Verdauung bei Wirbellosen Tieren. Arb Zool Inst Wien 5:141–168.Google Scholar
  69. Moore KA, Lemischka IR (2006) Stem cells and their niches. Science 311:1880–1885.PubMedGoogle Scholar
  70. Morrison SJ, Shah NM, Anderson DJ (1997) Regulatory mechanisms in stem cell biology. Cell 88:287–298.PubMedGoogle Scholar
  71. Müller WEG (2001) How was metazoan threshold crossed? The hypothetical Urmetazoa. Comp Biochem Physiol (A) 129:433–460.Google Scholar
  72. Müller WA, Teo R, Frank U (2004) Totipotent migratory stem cells in a hydroid. Dev Biol 275:215–224.PubMedGoogle Scholar
  73. Ng J, Hart CM, Morgan K, Simon JA (2000) A Drosophila ESC-E(Z) protein complex is distinct from other Polycomb group complexes and contains covalently modified ESC. Mol Cell Biol 20:3069–3078.PubMedGoogle Scholar
  74. Nishimiya-Fujisawa C, Sugiyama T (1993) Genetic analysis of developmental mechanisms in Hydra. XX. Cloning of interstitial stem cells restricted to the sperm differentiation pathway in Hydra magnipapillata. Dev Biol 157:1–9.PubMedGoogle Scholar
  75. Nishimiya-Fujisawa C, Sugiyama T (1995) Genetic analysis of developmental mechanisms in hydra. XXII. Two types of female germ stem cells are present in a male strain of Hydra magnipapillata. Dev Biol 172:324–336.PubMedGoogle Scholar
  76. Okamoto I, Otte AP, Allis CD, Reinberg D, Heard E (2004) Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303:644–649.PubMedGoogle Scholar
  77. Ozbek S, Pokidysheva E, Schwager M, Schulthess T, Tariq N, Barth D, Milbradt AG, Moroder L, Engel J, Holstein TW (2004) The glycoprotein NOWA and minicollagens are part of a disulfide-linked polymer that forms the cnidarian nematocyst wall. J Biol Chem 279(50):52016–52023.PubMedGoogle Scholar
  78. Pires-DaSilva A, Sommer RJ (2003) Evolution of signalling pathways. Natl Rev Genetics 4:39–49.Google Scholar
  79. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, dela Cruz CC, Otte AP, Panning B, Zhang Y (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300:131–135.PubMedGoogle Scholar
  80. Rideout WM, Eggan K, Jaenisch R (2001) Nuclear cloning and epigenetic reprogramming of the genome. Science 293:1093–1098.PubMedGoogle Scholar
  81. Ruppert EE, Barnes RD (1994) Invertebrate zoology, 6th edn. Saunders College Publishing, Fort Worth.Google Scholar
  82. Sasai Y (2001) Regulation of neural determination by evolutionarily conserved signals: anti-BMP factors and what next? Curr Opin Neurobiol 11(1):22–26.PubMedGoogle Scholar
  83. Schierwater B, Kuhn K (1998) Homology of Hox genes and the zootype concept in early metazoan evolution. Mol Phylogenet Evol 9:375–381.PubMedGoogle Scholar
  84. Schmidt T, David CN (1986) Gland cells in Hydra: cell cycle kinetics and development. J Cell Sci 85:197–215.PubMedGoogle Scholar
  85. Schofield R (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4(1/2):7–25.PubMedGoogle Scholar
  86. Seydoux G (1996) Mechanisms of translational control in early development. Curr Opin Genet Dev 6(5):555–561.PubMedGoogle Scholar
  87. Shimizu H, Bode HR (1995) Nematocyte differentiation in hydra: commitment to nematocyte type occurs at the beginning of the pathway. Dev Biol 169:136–150.PubMedGoogle Scholar
  88. Spradling A, Drummond-Barbosa D, Kai T (2001) Stem cells find their niche. Nature 414:98–104.PubMedGoogle Scholar
  89. Sproull F, David CN (1979) Stem cell growth and differentiation in Hydra attenuate. II. Regulation of nerve and nematocyte differentiation in multiclone aggregates. J Cell Sci 38:171–179.PubMedGoogle Scholar
  90. Sugiyama T, Sugimoto N (1985) Genetic analysis of developmental mechanisms in hydra. XI. Mechanism of sex reversal by heterosexual parabiosis. Dev Biol 110:413–421.PubMedGoogle Scholar
  91. Szczepanek S, Cikala M, David CN (2002) Poly-gamma-glutamate synthesis during formation of nematocyst capsules in Hydra. J Cell Sci 115(4):745–751.PubMedGoogle Scholar
  92. Takahashi T, Muneoka Y, Lohmann J, deHaro LM, Solleder G, Bosch TCG, David CN, Bode HR, Koizumi O, Shimizu H, Hatta M, Fujisawa T, Sugiyama T (1997) Systematic isolation of peptide signal molecules regulating development in hydra: Lwamide and PW families. Proc Natl Acad Sci USA 94:1241–1246.PubMedGoogle Scholar
  93. Takahashi T, Koizumi O, Ariura Y, Romanovitch A, Bosch TCG, Kobayakawa Y, Mohri S, Bode HR, Yum S, Hatta M, Fujisawa T (2000) A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra. Development 127:997–1005.PubMedGoogle Scholar
  94. Tardent P (1974) Gametogenesis in the genus hydra. Am Zool 14:447–456.Google Scholar
  95. Tardent P (1995) The cnidarian cnidocyte, a high-tech cellular weaponry. BioEssays 17:351–362.Google Scholar
  96. Technau U, Holstein TW (1996) Phenotypic maturation of neurons and continuous precursor migration in the formation of the peduncle nerve net in Hydra. Dev Biol 177:599–615.PubMedGoogle Scholar
  97. Technau U, Rudd S, Maxwell P, Gordon P, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Holstein TW, Ball EE, Miller DJ (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians Trends Genet 21(12):633–639.Google Scholar
  98. Teragawa CK, Bode HR (1990) Special and temporal patterns of interstitial cell migration in Hydra vulgaris. Dev Biol 138:63–81.PubMedGoogle Scholar
  99. Teragawa CK, Bode HR (1995) Migrating interstitial cells differentiate into neurons in hydra. Dev Biol 171:286–293.PubMedGoogle Scholar
  100. Valk-Lingbeek ME, Bruggeman SW, van Lohuizen M (2004) Stem cells and cancer; the polycomb connection. Cell 118(4):409–418.PubMedGoogle Scholar
  101. Wang J, Mager J, Scneider E, Magnuson T (2002) The mouse PcG gene eed is required for Hox gene repression and extraembryonic development. Mamm Genome 13:493–503.PubMedGoogle Scholar
  102. Wittlieb J, Khalturin K, Lohmann J, Anton-Erxleben F, Bosch TCG (2006) Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc Natl Acad Sci USA 103:6208–6211.PubMedGoogle Scholar
  103. Wolpert LJ (1988) Stem cells: a problem in asymmetry. J Cell Sci Suppl 10:1–9.PubMedGoogle Scholar
  104. Xie T, Spradling AC (2000) A niche maintaining germ line stem cells in the Drosophila ovary. Science 290:328–330.PubMedGoogle Scholar
  105. Yamashita YM, Fuller MT, Jones DL (2005) Signaling in stem cell niches: lessons from the Drosophila germline. J Cell Sci 118:665–672.PubMedGoogle Scholar
  106. Yaross MS, HR Bode (1978) Regulation of interstitial cell differentiation in Hydra attenuata. III Effects of i-cell and nerve cell densities. J Cell Sci 34:1–25.PubMedGoogle Scholar
  107. Yum S, Takahashi T, Koizumi O, Ariura Y, Kobayakawa Y, Mohri S, Fujisawa T (1988) A novel neuropeptide, Hym-176, induces contraction of the ectodermal muscle in Hydra. Biochem Biophys Res Comm 248:584–590.Google Scholar

Copyright information

© Springer Berlin Heidelberg 2007

Authors and Affiliations

  • Thomas C. G. Bosch
    • 1
  1. 1.Zoological InstituteChristian-Albrechts-University KielKielGermany

Personalised recommendations