Skip to main content
SpringerLink
Log in
Book cover

Stem Cells pp 37–57Cite as

Stem Cells in Immortal Hydra

  • Chapter

Hydra’s potential immortality and extensive capacity to regenerate and self-renew is due to the presence of three distinct stem cell lineages: ectodermal and endodermal epithelial stem cells, and interstitial stem cells. Over the last few years, stem cells in Hydra became well-defined in cellular terms of their biology. More recently, efforts using the nearly unlimited potential for tissue manipulation combined with functional transgenesis have shed light on the molecular control mechanisms involved. Here I review those efforts in an attempt to give both a historical perspective and an update on the recent experimental highlights. In particular, I will focus on six aspects of stem cells in Hydra: (i) their continuous transition through the proliferation/differentiation switch; (ii) their rapid responses to signals from the cellular environment; (iii) the emerging importance of Wnt and Notch signaling in controlling stem cell behavior; (iv) the role of chromatin modification in terminal differentiation; (v) the observation of transdifferentiation in some of the stem cell progeny; and (vi) the implications for the evolution of germ cells, ageing and cancer. Together, these findings seem to indicate that Hydra not only provides insights into signalling pathways involved in stem cell differentiation in the Bilaterian ancestor; they also demonstrate that despite morphological and functional differences, and more than 500 million years of phylogenic separation between Hydra and human, common signaling pathways are responsible for stem cell maintenance, lineage determination, and differentiation.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
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

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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. Nat. Cell. Biol. 8(5):532–538.

    Article  PubMed  CAS  Google Scholar 

  • Blackstone NW (2006) Multicellular redox regulation: integrating organismal biology and redox chemistry. Bioessays 28(1):72–77.

    Article  PubMed  CAS  Google Scholar 

  • Blackstone NW (2007) A food’s-eye view of the transition from basal metazoans to bilaterians. Integr. Comp. Biol. 1–10. Doi:10.1093/icb/icm056.

    Google Scholar 

  • Bode HR, Heimfeld S, Chow MA, Huang LW. (1987) Gland cells arise by differentiation from interstitial cells in Hydra attenuata. Dev. Biol. 122(2):577–585.

    Article  PubMed  CAS  Google Scholar 

  • Bosch TCG (2004) Control of asymmetric cell divisions: will cnidarians provide an answer? BioEssays 26(9):929–931.

    Article  PubMed  Google Scholar 

  • Bosch TCG (2007a) Why polyps regenerate and we don’t: towards a cellular and molecular framework for Hydra regeneration. Dev. Biol. 303 (2):421–433.

    Article  PubMed  CAS  Google Scholar 

  • Bosch TCG (2007b) Symmetry breaking in stem cells of the basal metazoan Hydra. Prog. Mol. Subcell. Biol. 45:61–78.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bosch TCG, David CN (1990). Cloned interstitial stem cells grow as contiguous patches in hydra. Dev. Biol. 138: 513–515.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bosch TCG, Fujisawa T (2001) Polyps, peptides and patterning. BioEssays 23(5):420–427.

    Article  PubMed  CAS  Google Scholar 

  • Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, Rando TA (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317(5839):807–810.

    Article  PubMed  CAS  Google Scholar 

  • Brien P (1966) Biologie de la reproduction animale. Masson & Cie, Paris.

    Google Scholar 

  • Broun M, Gee L, Reinhardt B, Bode HR (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132(12):2907–2916.

    Article  PubMed  CAS  Google Scholar 

  • Buss LW (1987) The evolution of individuality. Princeton University Press, Princeton.

    Google Scholar 

  • Buss LW, Green DR (1985) Histoincompatibility in vertebrates: the relict hypothesis. Dev. Comp. Immunol. 9(2):191–201. Review.

    Article  PubMed  CAS  Google Scholar 

  • Campbell RD (1967) Tissue dynamics of steady state growth in Hydra littoralis. I. Patterns of cell division. Dev. Biol. 15(5):487–502.

    Article  PubMed  CAS  Google Scholar 

  • Clarke MF, Fuller M. (2006) Stem cells and cancer: two faces of eve. Cell 124(6):1111–1115.

    Article  PubMed  CAS  Google Scholar 

  • Collins AG (1998) Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proc Natl Acad Sci U S A. 95(26):15458–15463.

    Article  PubMed  CAS  Google Scholar 

  • David CN, Campbell RD (1972) Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. J Cell Sci. 11(2):557–568.

    PubMed  CAS  Google Scholar 

  • David CN, Challoner D (1974) Distribution of interstitial cells and differentiating nematocytes in nests in Hydra attenuata. Am. Zool. 14:537–542.

    Google Scholar 

  • David CN, Murphy S (1977) Characterization of interstitial stem cells in hydra by cloning. Dev. Biol. 58(2):372–383.

    Article  PubMed  CAS  Google Scholar 

  • David CN, Gierer A (1974) Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. J. Cell. Sci. 16(2):359–375.

    PubMed  CAS  Google Scholar 

  • David CN, Plotnick I (1980) Distribution of interstitial stem cells in Hydra. Dev. Biol. 76(1):175–184.

    Article  PubMed  CAS  Google Scholar 

  • Dübel S, Hoffmeister SA, Schaller HC (1987) Differentiation pathways of ectodermal epithelial cells in hydra. Differentiation 35(3):181–189.

    PubMed  Google Scholar 

  • Duncan AW, Rattis FM, DiMascio LN, Congdon KL, Pazianos G, Zhao C, Yoon K, Cook JM, Willert K, Gaiano N, Reya T. (2005) Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 6(3):314–322.

    Article  PubMed  CAS  Google Scholar 

  • Fujisawa T. (1989) Role of interstitial cell migration in generating position-dependent patterns of nerve cell differentiation in Hydra. Dev Biol. 133(1):77–82.

    Article  PubMed  CAS  Google Scholar 

  • Fujisawa T, David CN, Bosch TCG (1990) Transplantation stimulates interstitial cell migration in hydra. Dev Biol. 138(2):509–512.

    Article  PubMed  CAS  Google Scholar 

  • Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C (2002) A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep. 3(7):688–694.

    Article  PubMed  CAS  Google Scholar 

  • Genikhovich G, Kürn U, Hemmrich G, Bosch TCG (2006) Discovery of genes expressed in Hydra embryogenesis. Dev. Biol. 289(2):466–481.

    Article  PubMed  CAS  Google Scholar 

  • Gierer A, Berking S, Bode H, David CN, Flick K, Hansmann G, Schaller H, Trenkner E (1972) Regeneration of hydra from reaggregated cells. Nat. New Biol. 239(91):98–101.

    PubMed  CAS  Google Scholar 

  • Hager G, David CN. (1997) Pattern of differentiated nerve cells in hydra is determined by precursor migration. Development 124(2):569–576.

    PubMed  CAS  Google Scholar 

  • Heimfeld S, Bode HR. (1984) Interstitial cell migration in Hydra attenuata. I. Quantitative description of cell movements. Dev. Biol. 105(1):1–9.

    Article  PubMed  CAS  Google Scholar 

  • Hobmayer B, Rentzsch F, Kuhn K, Happel CM, von Laue CC, Snyder P, Rothbacher U, Holstein TW (2000) WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407(6801):186–189.

    Article  PubMed  CAS  Google Scholar 

  • James J, Das AV, Rahnenfuhrer J, Ahmad I (2004) Cellular and molecular characterization of early and late retinal stem cells/progenitors: differential regulation of proliferation and context dependent role of Notch signaling. J. Neurobiol. 61(3):359–376.

    Article  PubMed  CAS  Google Scholar 

  • Käsbauer T, Towb P, Alexandrova O, David CN, Dall’armi E, Staudigl A, Stiening B, Bottger A (2007) The Notch signaling pathway in the cnidarian Hydra. Dev. Biol. 303(1):376–390.

    Article  PubMed  CAS  Google Scholar 

  • Khalturin K, Anton-Erxleben F, Milde S, Plötz C, Wittlieb J, Hemmrich G, Bosch TCG (2007) Transgenic stem cells in Hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation. Dev. Biol. 309(1):32–44.

    Article  PubMed  CAS  Google Scholar 

  • 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(13):1592–1605.

    Article  PubMed  CAS  Google Scholar 

  • 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(24):2190–2195.

    Article  PubMed  CAS  Google Scholar 

  • Kuzmichev A, Jenuwein T, Tempst P, Reinberg D (2004) Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol. Cell. 14(2):183–193.

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, Malide D, Rovira II, Schimel D, Kuo CJ, Gutkind JS, Hwang PM, Finkel T (2007) Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317(5839):803–806.

    Article  PubMed  CAS  Google Scholar 

  • Martinez DE (1998) Mortality patterns suggest lack of senescence in hydra. Exp. Gerontol. 33(3):217–225.

    Article  PubMed  CAS  Google Scholar 

  • Martinez DE (2002) Senescence and rejuvenation in asexual metazoans. In: Hughes RB, editor. Reproductive biology of the invertebrates. XI progress in asexual reproduction. New York: Wiley, pp. 115–140.

    Google Scholar 

  • Metcalf D. (2007) Concise review: hematopoietic stem cells and tissue stem cells: current concepts and unanswered questions. Stem Cells 25(10):2390–2395.

    Article  PubMed  Google Scholar 

  • Miller DJ, Ball EE, Technau U (2005) Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet. 21(10):536–539.

    Article  PubMed  CAS  Google Scholar 

  • Miller DJ, Hemmrich G, Ball EE, Hayward DC, Khalturin K, Funayama N, Agata K, Bosch TCG (2007) The innate immune repertoire in cnidaria–ancestral complexity and stochastic gene loss. Genome Biol. 8(4):R59.

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki K, Sano H, Kobayashi S, Nishimiya-Fujisawa C, Fujisawa T (2000) Expression and evolutionary conservation of nanos-related genes in Hydra. Dev. Genes Evol. 210(12):591–602.

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki K, Nishimiya-Fujisawa C, Fujisawa T (2001) Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Dev. Genes Evol. 211(6):299–308.

    Article  PubMed  CAS  Google Scholar 

  • Nencioni A, Grunebach F, Patrone F, Ballestrero A, Brossart P (2006) The proteasome and its inhibitors in immune regulation and immune disorders. Crit. Rev. Immunol. 26(6):487–498.

    PubMed  CAS  Google Scholar 

  • Nüchter T, Benoit M, Engel U, Ozbek S, Holstein TW (2006) Nanosecond-scale kinetics of nematocyst discharge. Curr. Biol. 16(9):R316–R318.

    Article  PubMed  CAS  Google Scholar 

  • Peters L, Meister G. (2007) Argonaute proteins: mediators of RNA silencing. Mol. Cell. 26(5):611–623.

    Article  PubMed  CAS  Google Scholar 

  • Philippe H, Lartillot N, Brinkmann H (2005) Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol. Biol. Evol. 22(5):1246–1253.

    Article  PubMed  CAS  Google Scholar 

  • Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300(5616):131–135.

    Article  PubMed  CAS  Google Scholar 

  • Raz E (2000) The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1(3):1017.

    Article  Google Scholar 

  • Rebscher N, Zelada-Gonzalez F, Banisch TU, Raible F, Arendt D (2007) Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. Dev Biol. 306(2):599–611.

    Article  PubMed  CAS  Google Scholar 

  • Reya T, Clevers H. (2005) Wnt signalling in stem cells and cancer. Nature 434(7035):843–850.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt T, David CN (1986) Gland cells in Hydra: cell cycle kinetics and development. J Cell Sci. 85:197–215.

    PubMed  CAS  Google Scholar 

  • Seto AG, Kingston RE, Lau NC (2007) The coming of age for Piwi proteins. Mol. Cell. 26(5):603–609.

    Article  PubMed  CAS  Google Scholar 

  • Siebert S, Anton-Erxleben F, Bosch TCG (2008) Cell type complexity in the basal metazoan Hydra is maintained by both stem cell based mechanisms and transdifferentiation. Dev. Biol. 313(1):13–24.

    Article  PubMed  CAS  Google Scholar 

  • Shimizu H, Bode HR (1995) Nematocyte differentiation in hydra: commitment to nematocyte type occurs at the beginning of the pathway. Dev Biol. 169(1):136–150.

    Article  PubMed  CAS  Google Scholar 

  • Spivakov M, Fisher AG (2007) Epigenetic signatures of stem-cell identity. Nat. Rev. Genet. 8(4):263–271.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Koizumi O, Ariura Y, Romanovitch A, Bosch TC, 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(5):997–1005.

    PubMed  CAS  Google Scholar 

  • Tardent P (1995) The cnidarian cnidocyte, a high-tech cellular weaponry. BioEssays 17:351–362.

    Article  Google Scholar 

  • Tardent P (1974) Gametogenesis in the Genus Hydra. Amer. Zool. 14:447–456.

    Google Scholar 

  • 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(2):599–615.

    Article  PubMed  CAS  Google Scholar 

  • Technau U, Rudd S, Maxwell P, Gordon PM, 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.

    Article  PubMed  CAS  Google Scholar 

  • Teragawa CK, Bode HR (1990) Spatial and temporal patterns of interstitial cell migration in Hydra vulgaris. Dev. Biol. 138(1):63–81.

    Article  PubMed  CAS  Google Scholar 

  • Teragawa CK, Bode HR (1995) Migrating interstitial cells differentiate into neurons in hydra. Dev Biol. 171(2):286–293.

    Article  PubMed  CAS  Google Scholar 

  • Till JE, McCulloch EA (1963) Early repair processes in marrow cells irradiated and proliferating in vivo. Radiat. Res. 18:96–105.

    Article  PubMed  CAS  Google Scholar 

  • Till JE, McCulloch EA (1961) A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat. Res. 14:213–222.

    Article  PubMed  CAS  Google Scholar 

  • Trowbridge JJ, Xenocostas A, Moon RT, Bhatia M (2006) Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation. Nat. Med. 12(1):89–98.

    Article  PubMed  CAS  Google Scholar 

  • Valk-Lingbeek ME, Bruggeman SW, van Lohuizen M (2004) Stem cells and cancer; the polycomb connection. Cell 118(4):409–418.

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Lehmann R (1991) Nanos is the localized posterior determinant in Drosophila. Cell 66(4):637–647. Erratum in Cell 1992, 68(6):1177.

    Article  PubMed  CAS  Google Scholar 

  • Weismann A (1883) Die Entstehung der Sexualzellen bei Hydramedusen. Fischer, Jena.

    Google Scholar 

  • Weismann A (1892) Das Keimplasma. Eine Theorie der Vererbung. Fischer, Jena.

    Google Scholar 

  • 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. U S A 103:6208–6211.

    Article  PubMed  CAS  Google Scholar 

  • Yoshida K, Fujisawa T, Hwang JS, Ikeo K, Gojobori T (2006) Degeneration after sexual differentiation in hydra and its relevance to the evolution of aging. Gene 385:64–70.

    Article  PubMed  CAS  Google Scholar 

  • Zacharias H, Anokhin B, Khalturin K, Bosch TCG (2004) Genome sizes and chromosomes in the basal metazoan Hydra. Zoology, 107:219–227.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zoological Institute, Christian-Albrechts-University, Olshausenstrasse 40, 24098, Kiel, Germany

    Thomas C. G. Bosch

Authors
  1. Thomas C. G. Bosch
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Christian-Albrechts-University, Olshausenstrasse 40, 24098, Kiel, Germany

    Thomas C. G. Bosch

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science + Business Media B.V

About this chapter

Cite this chapter

Bosch, T.C.G. (2008). Stem Cells in Immortal Hydra . In: Bosch, T.C.G. (eds) Stem Cells. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8274-0_3

Download citation

Publish with us

Policies and ethics

Search

Navigation