Skip to main content
SpringerLink
Log in

Cnidarian Interstitial Cells: The Dawn of Stem Cell Research

  • Chapter
  • First Online:
Stem Cells in Marine Organisms

Abstract

The first stem cells described in the biological literature were those of hydroid cnidarians; their detection by Weismann in 1883 gave rise to his germ line and “germ plasm” theory (with “germ plasm” meaning what is called genome today). Somatic cells preserving properties of eggs (called Stammzellen, i.e. stem cells, by him) were considered by him to be the cellular source of regeneration and reproduction. Weismann’s studies have been the foundation of modern cnidarian stem cell research. In the latter, hydroid stem cells have been referred to as interstitial cells (shortly i-cells), and have mostly been studied in two cnidarian genera: the freshwater polyp Hydra and the colonial marine hydroid Hydractinia. In these animals, i-cells constitute a complex system of multipotent (in Hydra) or totipotent (in Hydractinia) stem cells and their derivatives. I-cells’ potencies have been investigated by specific elimination of stem cells and reintroduction of i-cells from donors. The complement of stem cells confers potential immortality to the genetic individual. Cnidarians’ cells in general have an unmatched capability of re- and transdifferentiation. Isolated, fully differentiated striated muscle cells of hydroid medusae may resume features of multipotent stem cells and give rise to almost all cell types including germ cells. Reverse development of adult stages back into juveniles is a further manifestation of cnidarian developmental plasticity. Typical i-cells have not been described in other cnidarian groups. In these taxa the source of new nematocytes nerve and germ cells may be differentiated cells that preserve plasticity. Following a historical perspective we review recent advances in hydroid i-cell research, and discuss the potential of invertebrate stem cell work.

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

Access this chapter

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 EPUB and 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

Institutional subscriptions

References

  • Alder H, Schmid V (1987) Cell cycles and in vitro transdifferentiation and regeneration of isolated, striated muscle of jellyfish. Dev Biol 124:358–369

    Article  CAS  Google Scholar 

  • Alexandrova O, Schade M, Bottger A, David CN (2005) Oogenesis in Hydra: nurse cells transfer cytoplasm directly to the growing oocyte. Dev Biol 28:91–101

    Article  CAS  Google Scholar 

  • Aochi M, Kato KI (1980) The polyp reconstitution in ectoderm and-or endoderm isolated from Arelia aurita. Dev Growth Diff 22:717

    Google Scholar 

  • Berking S (1979) Control of nerve cell formation from multipotent stem cells in Hydra. J Cell Sci 4:193–205

    Google Scholar 

  • Berking S (1980) Commitment of stem cells to nerve cells and migration of nerve cell precursors in preparatory bud development in Hydra. J Embryol Exp Morphol 60:373–387

    CAS  Google Scholar 

  • 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  Google Scholar 

  • Bode HR, Berking S, David CN, Gierer A, Schaller H, Trenkner E (1973) Quantitative analysis of cell types during growth and morphogenesis in Hydra. Wilhelm Roux’ Arch 171:269–285

    Article  Google Scholar 

  • Bode HR, David CN (1978) Regulation of a multipotent stem cell, the interstitial cell of hydra. Progr Biophys Molec Biol 33:189–206

    Article  CAS  Google Scholar 

  • Bode HR, Flick KM, Smith GS (1976) Regulation of interstitial cell differentiation in Hydra attenuata. I. Homeostatic control of interstitial cell population size. J Cell Sci 20:29–46

    CAS  Google Scholar 

  • Bode HR, Gee LW, Cow MA (1990) Neuron differentiation in hydra involves dividing intermediates. Dev Biol 139:231–334

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bode HR, Smith GS (1977) Regulation of interstitial cell differentiation in Hydra attenuata. II. Correlation of the axial position of interstitial cells with nematocyte differentiation. Wilhelm Roux’ Arch 181:203–213

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bosch TCG (2007a) Symmetry breaking in stem cells of the basal metazoan Hydra. In: Macieira-Coelho (ed) Asymmetric cell division series, Progr Mol Subcell Biol. Springer, Heidelberg, pp 61–78

    Chapter  Google Scholar 

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

    Article  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  CAS  Google Scholar 

  • Bosch TCG, David CN (1986) Male and female stem cells and sex reversal in Hydrapolyps. Proc Natl Acad Sci USA 83:9478–9482

    Article  Google Scholar 

  • Bosch TCG, David CN (1987) Stem cells of Hydra magnipapillatacan differentiate somatic and germ cell lines. 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  CAS  Google Scholar 

  • Bosch TCG, Rollbühler R, Scheider B, David CN (1991) Role of the cellular environment in interstitial stem cell proliferation in hydra. Dev Genes Evol 200:269–276

    Google Scholar 

  • Brien P, Reniers-Decoen M (1950) La significance des cellules interstitielles des hydres d’eau douce et le problème de la résèrve embryonaire. Bulletin Biol France Belgique 89:285–325

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bunting M (1894) The origin of sex cells in Hydractiniaand Podocoryneand the development of Hydractinia. J Morphol 9:203–236

    Article  Google Scholar 

  • Burnett AL, Davis LE, Ruffin FE (1966) A histological and ultrastructural study of germinal differentiation of interstitial cells arising from gland cells in Hydra viridis. J Morphol 120:1–8

    Article  CAS  Google Scholar 

  • Burnett AL, Lowell R, Cyrlin M (1973) Regeneration of a complete hydra from a single differentiated somatic cell type. In: Burnett AL (ed) Biology of Hydra. Academic Press, New York, pp 225–270

    Google Scholar 

  • Buss LW (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Natl Acad Sci USA 79:5337–5341

    Article  CAS  Google Scholar 

  • Buss LW (1983) Evolution, development, and the units of selection. Proc Natl Acad Sci USA 80:1387–1391

    Article  CAS  Google Scholar 

  • Buss LW (1999) Slime molds, ascidians, and the utility of evolutionary theory. Proc Natl Acad Sci USA 96:8801–8803

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Campbell RD (1979) Development of hydra lacking interstitial and nerve cells (“epithelial hydra”). In: Subtelny S, Konigsberg IR (eds) Determinants of Spatial Organization. 37th Symp Soc Dev Biol. Academic Press, New York, pp 267–293

    Google Scholar 

  • Campbell RD, David CN (1974) Cell cycle kinetics and development of Hydra attenuata. II. Interstitial cells. J Cell Sci 16:349–358

    CAS  Google Scholar 

  • David CN, Bosch TCG, Hobmeyer B, Holstein T, Schmidt T (1987) Interstitial stem cells in hydra. In: Loomis WF (ed) Genetic control of development. Alan R Liss, New York, p 389

    Google Scholar 

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

    CAS  Google Scholar 

  • David CN, Fujisawa T, Bosch TC (1991) Interstitial stem cell proliferation in hydra: evidence for strain-specific regulatory signals. Dev Biol 148:501–507

    Article  CAS  Google Scholar 

  • David CN, Gierer A (1974) Cell cycle kinetics and development of Hydra attenuata. J Cell Sci 16:359–376

    CAS  Google Scholar 

  • David CN, MacWilliams H (1978) Regulation of the self-renewal probability in hydra stem cell clones. Proc Natl Acad Sci USA 75:886–890

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Davis LE (1970) Cell division during dedifferentiation and redifferentiation in regenerating isolated gastrodermis of Hydra. Exp Cell Res 60:127–132

    Article  CAS  Google Scholar 

  • Davis LE (1973) Ultrastructural changes during dedifferentiation and redifferentiation in regenerating, isolated gastrodermis. In: Burnett AL (ed) Biology of Hydra. Academic Press, New York, pp 171–219

    Google Scholar 

  • Diehl FA (1973) The developmental significance of interstitial cells during regeneration and budding. In: Burnett AL (ed) Biology of Hydra. Academic Press, New York, pp 109–141

    Google Scholar 

  • Diehl FA, Burnett AL (1964) The role of interstitial cells in the maintenance of hydra. I. Specific destruction of interstitial cells in normal, asexual, non-budding animals. J Exp Zool 155:253–260

    Article  CAS  Google Scholar 

  • Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884

    Article  CAS  Google Scholar 

  • Extavour CG, Pang K, Matus DQ, Martindale MQ (2005) Vasa and nanos expression patterns in a sea anemone and the evolution of bilaterian germ cell specification mechanisms. Evol Dev 7:201–215

    Article  CAS  Google Scholar 

  • Fedders H, Augustin R, Bosch TC (2004) A Dickkopf-3-related gene is expressed in differentiating nematocytes in the basal metazoan Hydra. Dev Genes Evol 214:72–80

    Article  CAS  Google Scholar 

  • Frank U, Leitz T, Müller WA (2001) The hydroid Hydractinia: a versatile, informative cnidarian representative. Bioessays 23:963–971

    Article  CAS  Google Scholar 

  • Fujisawa T (1988) Inhibition of stenotele commitment by an endogenous factor in Hydra. J Cell Sci 91, 361–366

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fujisawa T, Nishima C, Sugiyama T (1986) Nematocyte differentiation in hydra. Curr Top Dev Biol 20:281–290

    Article  CAS  Google Scholar 

  • Fujisawa T, Sugiyama T (1980) Nematocyte differentiation from interstitial cells newly introduced into interstitial cell-deficient hydra. In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 319–324

    Google Scholar 

  • Galliot B, Miljkovic-Licina M, de Rosa R, Chera S (2006) Hydra, a niche for cell and developmental plasticity. Sem Cell Dev Biol 17:492–502

    Article  CAS  Google Scholar 

  • Galliot B, Schmid V (2002) Cnidarians as a model system for understanding evolution and regeneration. Int J Dev Biol 46:39–48

    Google Scholar 

  • 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(1):4027–4035

    CAS  Google Scholar 

  • Guduric-Fuchs J, Möhrlen F, Frohme M, Frank U (2004) A fragile X mental retardation-like gene in a cnidarian. Gene 343:231–238

    Article  CAS  Google Scholar 

  • Hauenschild C (1954) Genetische und entwicklungsphysiologische Untersuchungen über Intersexualität und Gewebeverträglichkeit bei dem Hydroidpolypen Hydractinia echinata. Wilhelm Roux’ Archiv Entwicklungsmech Org 147:132–138

    Google Scholar 

  • Hauenschild C (1956) Experimentelle Untersuchungen über die Entstehung asexueller Klone bei der Hydromeduse Eleutheria dichotoma. Zeitschrift Naturforschung 11b:394–402

    Google Scholar 

  • Hauenschild C (1957) Ergänzende Mitteilung über die asexuellen Medusenklone bei Eleutheria dichotoma. Zeitschrift Naturforschung 12b:412–413

    Google Scholar 

  • Hayakawa E, Fujisawa C, Fujisawa T (2004) Involvement of Hydra achaete-scutegene CnASHin the differentiation pathway of sensory neurons in the tentacles. Dev Genes Evol 214:486–492

    CAS  Google Scholar 

  • Haynes J, Burnett AL (1963) Dedifferentiation and redifferentiation in Hydra viridis. Science 142:1481–1483

    Article  CAS  Google Scholar 

  • Hellstern S, Stetefeld J, Fauser C, Lustig A, Engel J, Holstein TW, Ozbek S (2006) Structure/function analysis of spinalin, a spine protein of Hydranematocysts. FEBS J 273:3230–3237

    Article  CAS  Google Scholar 

  • Herrmann K, Berking S (1987) The length of S-phase and G2-phase of epithelial cells is regulated during growth and morphgenesis in Hydra attenuata. Development 99:33–39

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hoffmann U, Kroiher M (2001) A possible role for the cnidarian homologue of serum response factor in decision making by undifferentiated cells. Dev Biol 236:304–315

    Article  CAS  Google Scholar 

  • Hofmann DK, Neumann R, Henne K (1978) Strobilation, budding and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda(Cnidaria: Scyphozoa). Marine Biol 47:161–176

    Article  Google Scholar 

  • Holstein TW, David CN (1990a) Cell cycle length, cell size and proliferation rate in Hydrastem cells. Dev Biol 142:392–400

    Article  CAS  Google Scholar 

  • Holstein TW, David CN (1990b) Putative intermediates in the nerve cell differentiation pathway in Hydrahave properties of multipotent stem cells. Dev Biol 142:401–405

    Article  CAS  Google Scholar 

  • Holstein TW, Hobmayer E, David CN (1991) Pattern of epithelial cell cycling in hydra. Dev Biol 148:602–611

    Article  CAS  Google Scholar 

  • Holstein TW, Hobmayer E, Technau U (2003) Cnidarians: an evolutionary conserved model system for regeneration. Dev Dyn 226:257–267

    Article  CAS  Google Scholar 

  • Howard MK, Burke LC, Mailhos C, Pizzey A, Gilbert CS, Lawson WD, Collins MK, Thomas NS, Latchman DS (1993) Cell cycle arrest of proliferating neuronal cells by serum deprivation can result in either apoptosis or differentiation. J Neurochem 60:1783–91

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Khalturin k, Anton-Erxleben F, Mildel S (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  CAS  Google Scholar 

  • Koizumi O, Bode HR (1991) Plasticity of the nervous system of adult hydra. III. Conversion of neurons to expression of a vasopressin-like immunoreactivity depends on axial location. J Neurosci 11:2011–2020

    CAS  Google Scholar 

  • Koizumi O, Heimfeld S, Bode HR (1988) Plasticity of the nervous system of adult hydra. II. Conversion of ganglionic cells of the body column into epidermal sensory cells of the hypostome. Dev Biol 129:358–371

    Article  CAS  Google Scholar 

  • Kroiher M, Plickert G, Müller WA (1990) Pattern of cell proliferation in embryogenesis and planula development of Hydractinia echinatapredicts the postmetamorphic body pattern. Roux’s Archiv Dev Biol 199:156–163

    Article  Google Scholar 

  • Kükenthal W (1923) Octocorallia. In: Krumbach T (ed) Handbuch der Zoologie I. Walter de Gruyter, Leipzig, pp 695, 776

    Google Scholar 

  • Lentz TL (1965) The fine structure of differentiating interstitial cells in hydra. Zeitschrift Zellforschung mikroskop Anatomie 67:547–560

    Article  CAS  Google Scholar 

  • Lentz TL (1966) The cell biology of hydra. North-Holland Publ, Amsterdam

    Google Scholar 

  • Lesh-Laurie GE, Hujer A, Suchy P (1991) Polyp regeneration from isolated tentacles of Aurelia scyphistomae: a role for gating mechanisms and cell division. Hydrobiologia 216–217:91–97

    Article  Google Scholar 

  • 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 nematocytes. Development 131:191–201

    Article  CAS  Google Scholar 

  • Littlefield CL (1991) Cell lineages in Hydra: Isolation and characterization of an interstitial stem cell restricted to egg production in Hydra oligactis. Dev Biol 143:378–88

    Article  Google Scholar 

  • Littlefield CL, Bode HR (1986) Germ cells in Hydra oligactismales. II Evidence for a subpopulation of interstitial stem cells whose differentiation is limited to sperm production. Dev Biol 116:381–386

    Article  CAS  Google Scholar 

  • Lowell RD, Burnett AL (1969) Regeneration of complete hydra from isolated epidermal transplants. Biol Bull 137:312–320

    Article  Google Scholar 

  • Macklin M (1968) Reversal of cell layers in hydra: a critical re-appraisal. Biol Bull 134:465–472

    Article  Google Scholar 

  • Mali B, Soza-Ried J, Frohme M, Frank U (2006) Structural but not functional conservation of an immune molecule: a tachylectin-like gene in Hydractinia. Dev Comp Immunol 30:275–281

    Article  CAS  Google Scholar 

  • Marcum BA, Campbell RD (1978) Developmental roles of epithelial and interstitial cell lineages in hydra: analysis of chimeras. J Cell Sci 32:233–247

    CAS  Google Scholar 

  • Martin VJ, Archer WE (1986) Migration of interstitial cells and their derivatives in a hydrozoan planula. Dev Biol 116:486–496

    Article  Google Scholar 

  • Martin VJ, Archer WE (1997) Stages of larval development and stem cell population changes during metamorphosis of a hydrozoan planula. Biol Bull 192:41–52

    Article  Google Scholar 

  • Miljkovic M, Mazet F, Galliot B (2002) Cnidarian and bilaterian promoters can direct GFP expression in transfected hydra. Dev Biol 246:377–90

    Article  CAS  Google Scholar 

  • Miljkovic-Licina M, Chera S, Ghila L, Galliot B (2007) Head regeneration in wild-type hydra requires de novo neurogenesis. Development 134:1191–1201

    Article  CAS  Google Scholar 

  • Minasian LL, Mariscal RN (1980) Tissue-specific differentiation of cnidoblasts in a sea anemone (Haliplanella luciae). Am Zool 20:803

    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 211:299–308

    Article  CAS  Google Scholar 

  • Müller WA (1964) Experimentelle Untersuchungen über Stockentwicklung und Sexualchimären bei Hydractinia echinata. Roux’ Arch. Entwicklungsmechanik 155:181–268

    Article  Google Scholar 

  • Müller WA (1966) Elimination der I-Zellen und Hemmung der Planulametamorphose durch alkylierende Cytostatika. Naturwissenschaften 7:184–185

    Article  Google Scholar 

  • Müller WA (1967) Differenzierungspotenzen und Geschlechtsstabilität der I-Zellen von Hydractinia echinata. Roux Arch Entwicklungsmech 159:412–432

    Article  Google Scholar 

  • Müller WA (2002) Autoaggressive, multi-headed and other mutant phenotypes in Hydractinia echinata(Cnidaria: Hydrozoa). Int J Dev Biol 46:1023–1033

    Google Scholar 

  • Müller WA, Frank U, Teo R, Mokady O, Guette C, Plickert G (2007) Wnt signaling in hydroid development: Ectopic heads and giant buds induced by GSK-3beta inhibitors. Int J Dev Biol 51:211–220

    Article  CAS  Google Scholar 

  • Müller WA, Leitz T (2002) Metamorphosis in the Cnidaria. Can J Zool 80:755–1771

    Article  Google Scholar 

  • Müller WA, Plickert G, Berking S (1986) Regeneration in Hydrozoa: distal versus proximal transformation in Hydractinia. Roux’s Arch Dev Biol 195:513–518

    Article  Google Scholar 

  • Müller WA, Teo R, Frank U (2004a) Totipotent migratory stem cells in a hydroid. Dev Biol 275:215–224

    Article  CAS  Google Scholar 

  • Müller WA, Teo R, Möhrlen F (2004b) Patterning a multi-headed mutant in Hydractinia: enhancement of head formation and its phenotypic normalization. Int J Dev Biol 48:9–15

    Article  Google Scholar 

  • Neumann R, Schmahl G, Hofmann DK (1980) Bud formation and control of polyp morphogenesis in Cassiopea andromeda (Scyphozoa). In: Tardent P, Tardent R (eds) Developmental and Cellular Biology of Coelenterates. Elsevier, Amsterdam

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448:313–318

    Article  CAS  Google Scholar 

  • Plickert G, Jacoby V, Frank U, Müller WA, Mokady O (2006) Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning. Dev Biol 298:368–378

    Article  CAS  Google Scholar 

  • Plickert G, Kroiher M (1988) Proliferation kinetics and cell lineages can be studied in whole mounts and macerates by means of BrdU/anti-BrdU technique. Development 103:791–794

    CAS  Google Scholar 

  • Plickert G, Kroiher M, Munck A (1988) Cell proliferation and early differentiation during embryonic development and metamorphosis of Hydractinia echinata. Development 103:795–803

    CAS  Google Scholar 

  • Plickert G, Schetter E, Verhey van Wijk N, Schlossherr J, Steinbüchl M, Gajewski M (2003) The role of α-amidated neuropeptides in hydroid development – LWamides and metamorphosis in Hydractinia echinata. Int J Dev Biol 47:439–450

    CAS  Google Scholar 

  • Rebscher N, Volk C, Teo R (2008) Vasa protein is a component of the germ plasm in the cnidarian Hydractinia echinata. Dev Dyn 237(6):1736–45

    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 306:599–611

    Article  CAS  Google Scholar 

  • Sacks PG, Davis LE (1979) Production of nerveless Hydra attenuataby hydroxyurea treatments. J Cell Sci 37:189–203

    CAS  Google Scholar 

  • Schmich J, Kraus Y, De Vito D, Graziussi D, Boero F, Piraino S (2007) Induction of reverse development in two marine Hydrozoans. Int J Dev Biol 51(1):45–56

    Article  Google Scholar 

  • Schmich J, Trepel S, Leitz T (1998) The role of GLWamides in metamorphosis of Hydractinia echinata. Dev Genes Evol 208:267–273

    Article  CAS  Google Scholar 

  • Schmid V, Baader C, Bucciarelli A, Reber-Muller S (1993) Mechanochemical interactions between striated muscle cells of jellyfish and grafted extracellular matrix can induce and inhibit DNA replication and transdifferentiation in vitro. Dev Biol 155:483–496

    Article  CAS  Google Scholar 

  • Schmid V, Wydler M, Alder H (1982) Transdifferentiation and regeneration in vitro. Dev Biol 92:76–488

    Article  Google Scholar 

  • Schmid V, Plickert G (1990) The proportion altering factor (PAF) and the in vitro transdifferentiation of isolated striated muscle of jellyfish into nerve cells. Differentiation 44:95–102

    Article  CAS  Google Scholar 

  • Schmid V, Reber-Müller S (1995) Transdifferentiation of isolated striated muscle of jellyfish in vitro: the initiation process. Sem Cell Biol 6:109–116

    Article  CAS  Google Scholar 

  • Schwarz RS, Hodes-Villamar L, Fitzpatrick KA, Fain MG, Hughes AL, Cadavid LF (2007) A gene family of putative immune recognition molecules in the hydroid Hydractinia. Immunogenetics 59:233–246

    Article  CAS  Google Scholar 

  • Seipel K, Yanze N, Schmid V (2004a) The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int J Dev Biol 48:1–7

    Article  CAS  Google Scholar 

  • Seipel K, Yanze N, Schmid V (2004b) Developmental and evolutionary aspects of the basic helix-loop-helix transcription factors Atonal-like 1 and Achaete-scute homolog 2 in the jellyfish. Dev Biol 269:331–345

    Article  CAS  Google Scholar 

  • Shigeta M, Shibukawa Y, Ihara H, Miyoshi E, Taniguchi N, Gu J (2006) beta1,4-N-Acetylglucosaminyltransferase III potentiates beta1 integrin-mediated neuritogenesis induced by serum deprivation in Neuro2a cells. Glycobiology 16:564–571

    Article  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 169:136–150

    Article  CAS  Google Scholar 

  • Shukalyuk AI, Golovnina KA, Baiborodin SI, Gunbin KV, Blinov AG, Isaeva VV (2006) vasa-related genes and their expression in stem cells of colonial parasitic rhizocephalan barnacle Polyascus polygenea(Arthropoda: Crustacea: Cirripedia: Rhizocephala). Cell Biol Int 31:97–108

    Article  CAS  Google Scholar 

  • Strelin GS (1928) Röntgenologische Untersuchungen an Hydren. Wilhelm Roux’ Archiv Entwicklungsmechanik Organismen 115:27–51

    Article  Google Scholar 

  • Sugiyama T, Fujisawa T (1979) Genetic analysis of developmental mechanisms in hydra. VI. Cellular composition of chimera hydra. J Cell Sci 35:1–15

    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 127:997–1005

    CAS  Google Scholar 

  • Teo R, Möhrlen F, Plickert G, Müller WA, Frank U (2006) An evolutionary conserved role of Wnt signaling in stem cell fate decision. Dev Biol 289:91–99

    Article  CAS  Google Scholar 

  • Terada H, Sugiyama T, Shigenaka Y (1988) Genetic analysis of developmental mechanisms in hydra. XVIII. Mechanism for elimination of the interstitial cell lineage in the mutant strain Sf-1. Dev Biol 126:263–269

    Article  CAS  Google Scholar 

  • Teragawa CK, Bode HR (1991) A head signal influences apical migration of interstitial cells in Hydra vulgaris. Dev Biol 147:293–302

    Article  CAS  Google Scholar 

  • Thieme C, Hofmann DK (2003) Control of head morphogenesis in an invertebrate asexually produced larva-like bud (Cassiopea andromeda; Cnidaria: Scyphozoa). Dev Genes Evol 213:127–133

    Google Scholar 

  • Torras R, Gonzalez-Crespo S (2005) Posterior expression of nanos orthologs during embryonic and larval development of the anthozoan Nematostella vectensis. Int J Dev Biol 49:895–899

    Article  CAS  Google Scholar 

  • Van de Vyver G (1964) Etude histologique du development d’Hydractinia echinata (Flem) Cahiers de Biologie Marine V:295–310

    Google Scholar 

  • Van de Vyver G (1967) Etude de development embyryonnaire des hydraires athecates (gymnoblastiques) a gonophores. Archives de Biologie (Liege) 78:451–518

    Google Scholar 

  • Wanek N, Marcum BA, Campbell RD (1980) Histological structure of epithelial hydra and evidence for the complete absence of interstitial and nerve cells. J Exp Zool 212:1–12

    Article  Google Scholar 

  • Wang YP, Wang ZF, Zhang YC, Tian Q, Wang JZ (2004) Effect of amyloid peptides on serum withdrawal-induced cell differentiation and cell viability. Cell Res 14:467–72

    Article  CAS  Google Scholar 

  • Weis VM, Keene DR, Buss LW (1985) Biology of hydractiniid hydroids. 4. Ultrastructure of the planula of Hydractinia echinata. Biol Bull 168:403–418

    Article  Google Scholar 

  • Weismann A (1883) Die Entstehung der Sexualzellen bei Hydromedusen. Gustav Fischer-Verlag, Jena

    Google Scholar 

  • Weismann A (1885) Die Continuität des Keimplasmas als Grundlage einer Theorie der Vererbung. Gustav Fischer-Verlag, Jena

    Google Scholar 

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

    Google Scholar 

  • Weismann A (1892b) Essays on heredity and kinded biological problems (trans. Poulton EB et al). Clarendon Press, Oxford

    Google Scholar 

  • Weismann A (1904) Keimplasmatheorie, Regeneration. In: Vorträge über Deszendenztheorie, 2nd edn. Gustav Fischer-Verlag, Jena

    Google Scholar 

  • Werner B, Hentschel J (1983) Apogamous life cycle of Stephanoscyphus planulophorus. Mar Biol 74:301–304

    Article  Google Scholar 

  • Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448:318–325

    Article  CAS  Google Scholar 

  • 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  Google Scholar 

  • Yanze N, Groger H, Muller P, Schmid V (1999) Reversible inactivation of cell-type-specific regulatory and structural genes in migrating isolated striated muscle cells of jellyfish. Dev Biol 213:194–201

    Article  Google Scholar 

  • Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920

    Article  CAS  Google Scholar 

  • Zeretzke S, Berking S (2002) In the multiheaded strain (mh-1) of Hydra magnipapillatathe ectodermal epithelial cells are responsible for the formation of additional heads and the endodermal epithelial cells for the reduced ability to regenerate a foot. Dev Growth Differ 44:85–93

    Article  CAS  Google Scholar 

  • Zhang E, Li X, Zhang S, Chen L, Zheng X (2005) Cell cycle synchronization of embryonic stem cells: effect of serum deprivation on the differentiation of embryonic bodies in vitro. Biochem Biophys Res Comm 333:1171–1177

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Peter Schuchert (Muséum d’histoire naturelle, Geneva) and Klaus Sander (University of Freiburg) for providing us with copies of Weissmann’s 1883 work, which had been considered lost for decades. UF is supported by SFI (Science Foundation Ireland), by a Beufort Marine Biodiscovery Grant, and by the Irish Higher Education Authority’s PRTLI Cycle 4 Award.

Author information

Authors and Affiliations

  1. School of Natural Sciences and Martin Ryan Marine Science Institute National University of Ireland, Galway, Ireland

    Uri Frank

  2. Institute of Zoology, University of Cologne, Weyertal 119, 50931, Cologne, Germany

    Günter Plickert

  3. Heidelberg Institute of Zoology, Dept. of Mol.Dev, Biology & Physiology University of Heidelberg, Im Neuenheimer Feld 230, 69120, Heidelberg, Germany

    Werner A. Müller

Authors
  1. Uri Frank
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Günter Plickert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Werner A. Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Uri Frank .

Editor information

Editors and Affiliations

  1. Limnological Research, Israel Oceanographic & , Haifa, 31 080, Israel

    Baruch Rinkevich

  2. Istituto di Biomedicina e Immunologia, CNR Palermo, Via La Malfa 153, Palermo, 90146, Italy

    Valeria Matranga

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Frank, U., Plickert, G., Müller, W.A. (2009). Cnidarian Interstitial Cells: The Dawn of Stem Cell Research. In: Rinkevich, B., Matranga, V. (eds) Stem Cells in Marine Organisms. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2767-2_3

Download citation

Publish with us

Policies and ethics

Search

Navigation