Development Genes and Evolution

, Volume 223, Issue 1–2, pp 53–66 | Cite as

Stem cell dynamics in Cnidaria: are there unifying principles?

  • David A. Gold
  • David K. JacobsEmail author


The study of stem cells in cnidarians has a history spanning hundreds of years, but it has primarily focused on the hydrozoan genus Hydra. While Hydra has a number of self-renewing cell types that act much like stem cells—in particular the interstitial cell line—finding cellular homologues outside of the Hydrozoa has been complicated by the morphological simplicity of stem cells and inconclusive gene expression data. In non-hydrozoan cnidarians, an enigmatic cell type known as the amoebocyte might play a similar role to interstitial cells, but there is little evidence that I-cells and amoebocytes are homologous. Instead, self-renewal and transdifferentiation of epithelial cells was probably more important to ancestral cnidarian development than any undifferentiated cell lineage, and only later in evolution did one or more cell types come under the regulation of a “stem” cell line. Ultimately, this hypothesis and competing ones will need to be tested by expanding genetic and developmental studies on a variety of cnidarian model systems.


Cnidaria Stem cells Interstitial cell Amoebocyte Hydra Aurelia 



D.A.G. would like to thank Robert Steele and Volker Hartenstein for helpful discussion while preparing this manuscript, with additional thanks to Volker Hartenstein for help in translating Weismann’s text. We gratefully thank two anonymous reviewers for valuable advice, and acknowledge funding from an NIH Training Grant in Genomic Analysis and Interpretation T32HG002536 (D.A.G.) and the National Aeronautics and Space Administration Astrobiology Program (D.K.J.).


  1. Afzelius B, Rosen B (1965) Nutritive phagocytosis in animal cells—an electron microscopical study of gastroderm of hydroid Clava squamata Mull. Z Zellforsch Mikrosk Anat 67:24PubMedCrossRefGoogle Scholar
  2. Alié A, Leclère L, Jager M, Dayraud C, Chang P, Le Guyader H, Queinnec E, Manuel M (2011) Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of “germline genes” with stemness. Dev Biol 350:183–197PubMedCrossRefGoogle Scholar
  3. Ambrosone A, Marchesano V, Tino A, Hobmayer B, Tortiglione C (2012) Hymyc1 downregulation promotes stem cell proliferation in Hydra vulgaris. PLoS One 7(1):e30660PubMedCrossRefGoogle Scholar
  4. Barnes R, Harrison F (1990) Introduction. In: Harrison F, Westfall J (eds) Microscopic anatomy of invertebrates. Volume 2: Placozoa, Porifera, Cnidaria, and Ctenophora, 1st edn. Wiley-Liss, New YorkGoogle Scholar
  5. Black RE, Riley GK (1985) Dissociation and reaggregation of cells of Chrysaora quinquecirrha (Cnidaria, Scyphozoa). J Exp Zool 233:369–375PubMedCrossRefGoogle Scholar
  6. Bode HR (2009) Axial patterning in Hydra. Cold Spring Harb Perspect Biol 1:a000463–a000463PubMedCrossRefGoogle Scholar
  7. Bode HR, Heimfeld S, Chow MA, Huang LW (1987) Gland cells arise by differentiation from interstitial cells in Hydra attenuata. Dev Biol 122:577–585PubMedCrossRefGoogle Scholar
  8. Bosch T (2007) Why polyps regenerate and we don't: towards a cellular and molecular framework for Hydra regeneration. Dev Biol 303(2):421–433PubMedCrossRefGoogle Scholar
  9. Bosch TCG (2008) In: Bosch TCG (ed) Stem cells in immortal Hydra. Springer Netherlands, DordrechtCrossRefGoogle Scholar
  10. Bosch TCG (2009) Hydra and the evolution of stem cells. Bioessays 31:478–486PubMedCrossRefGoogle Scholar
  11. Bosch TCG, Rollbhler R, Scheider B, David CN (1991) Role of the cellular environment in interstitial stem cell proliferation in Hydra. Roux's Arch Dev Biol 200:269–276CrossRefGoogle Scholar
  12. Bosch TCG, Anton-Erxleben F, Hemmrich G, Khalturin K (2010) The Hydra polyp: nothing but an active stem cell community. Dev Growth Differ 52:15–25PubMedCrossRefGoogle Scholar
  13. Bridge D, Cunningham CW, Schierwater B, DeSalle R, Buss LW (1992) Class–level relationships in the phylum Cnidaria: evidence from mitochondrial genome structure. Proc Natl Acad Sci U S A 89:8750–8753PubMedCrossRefGoogle Scholar
  14. Brusca RC, Brusca GJ (2003) Invertebrates 2nd ed. Sinauer AssociatesGoogle Scholar
  15. Burton PM, Finnerty JR (2009) Conserved and novel gene expression between regeneration and asexual fission in Nematostella vectensis. Roux's Arch Dev Biol 219:79–87Google Scholar
  16. Calder D (1982) Life history of the cannonball jellyfish, Stomolophus meleagris L. Agassiz, 1860 (Scyphozoa, Rhizostomida). Biol Bull 162:149–162CrossRefGoogle Scholar
  17. Campbell R (1987) Organization of the nematocyst battery in the tentacle of Hydra: arrangement of the complex anchoring junctions between nematocytes, epithelial cells, and basement membrane. Cell Tissue Res 249:647–655Google Scholar
  18. Campbell R, Bode H (1983) Terminology for morphology and cell types. In: Lenhoff H (ed) Hydra: Research methods. Plenum, New York, pp 5–14Google Scholar
  19. Campbell R, David CN (1974) Cell cycle kinetics and development of Hydra attenuata. II. Interstitial cells. J Cell Sci 16:349–358PubMedGoogle Scholar
  20. Cartwright P, Halgedahl SL, Hendricks JR, Jarrard RD, Marques AC, Collins AG, Lieberman BS (2007) Exceptionally preserved jellyfishes from the Middle Cambrian. PLoS One 2:e1121PubMedCrossRefGoogle Scholar
  21. Chapman DM (1968) Structure, histochemistry and formation of the podocyst and cuticle of Aurelia aurita. J Mar Biol Assoc 48:187–208CrossRefGoogle Scholar
  22. Chapman DM (1974) Cnidarian histology. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology: Reviews and new perspectives. Academic, New York, pp 1–92Google Scholar
  23. Chapman DM (1978) Microanatomy of the cubopolyp, Tripedalia cystophora (Class Cubozoa). Helgoländer Meeresun 31:128–168CrossRefGoogle Scholar
  24. Chapman DM (1999) Microanatomy of the bell rim of Aurelia aurita (Cnidaria: Scyphozoa). Can J Zool 77:34–46Google Scholar
  25. Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D et al (2010) The dynamic genome of Hydra. Nature 464:592–596PubMedCrossRefGoogle Scholar
  26. Child CM (1951) Physiological dominance in the reconstitution of the scyphistoma of Aurelia. Physiol Zool 24:177–185PubMedGoogle Scholar
  27. Collins AG, Schuchert P, Marques A, Jankowski T, Medina M et al (2006) Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol 55:97–115PubMedCrossRefGoogle Scholar
  28. Curtis S, Cowden R (1974) Some aspects of regeneration in the scyphistoma of Cassiopea (Class Scyphozoa) as revealed by the use of antimetabolites and microspectrophotometry. Am Zool 14:851–866Google Scholar
  29. David CN, Campbell RD (1972) Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. J Cell Sci 11:557–568PubMedGoogle Scholar
  30. David CN, Plotnick I (1980) Distribution of interstitial stem cells in Hydra. Dev Biol 76:175–184PubMedCrossRefGoogle Scholar
  31. Denker E, Manuel M, Leclère L, Le Guyader H, Rabet N (2008) Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). Dev Biol 315:99–113PubMedCrossRefGoogle Scholar
  32. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749PubMedCrossRefGoogle Scholar
  33. Eckelbarger KJ, Larson RL (1988) Ovarian morphology and oogenesis in Aurelia aurita (Scyphozoa: Semaeostomae): ultra-structural evidence of heterosynthetic yolk formation in a primitive metazoan. Mar Biol 100:103–115CrossRefGoogle Scholar
  34. Erwin D (2008) Wonderful Ediacarans, wonderful cnidarians? Evol Dev 10:263–264PubMedCrossRefGoogle Scholar
  35. Erwin D, LaFlamme M, Tweedt S, Sperling E, Pisani D, Peterson K (2011) The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334:1091PubMedCrossRefGoogle Scholar
  36. Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884PubMedCrossRefGoogle Scholar
  37. 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 7:201–215PubMedCrossRefGoogle Scholar
  38. Fautin DG (1991) Developmental pathways of anthozoans. Hydrobiologia 216:143–149CrossRefGoogle Scholar
  39. Feng B, Ng J, Heng J (2009) Molecules that promote or enhance reprogramming of somatic cells to induced pluripotent stem cells. Cell Stem Cell 4:301–312PubMedCrossRefGoogle Scholar
  40. Fischer AB, Hofmann DK (2004) Budding, bud morphogenesis, and regeneration in Carybdea marsupialis Linnaeus, 1758 (Cnidaria: Cubozoa). Hydrobiologia 530–531:331–337CrossRefGoogle Scholar
  41. Frank U, Plickert G, Müller W (2009) Cnidarian interstitial cells: the dawn of stem cell research. In: Rinkevich B, Matranga V (Eds), Stem cells in marine organisms, 978-90-481-2766-5, SpringerGoogle Scholar
  42. Galliot B, Quiquand M, Ghila L, de Rosa R, Miljkovic-Licina M, Chera S (2009) Origins of neurogenesis, a cnidarian view. Dev Biol 332:2–24PubMedCrossRefGoogle Scholar
  43. Gauthier G (1963) Cytological studies on gastroderm of Hydra. J Exp Zool 152:13CrossRefGoogle Scholar
  44. Gierer A, Berking S, Bode H, David C, Flick K (1972) Regeneration of Hydra from reaggregated cells. Nat New Biol 239:98–101PubMedCrossRefGoogle Scholar
  45. Glenner H, Hansen AJ, Sørensen MV, Ronquist F, Huelsenbeck JP, Willerslev E (2004) Bayesian inference of the metazoan phylogeny. Curr Biol 14:1644–1649PubMedCrossRefGoogle Scholar
  46. Haeckel E (1879) Evolution of man. Appleton, New YorkGoogle Scholar
  47. Hahn CW (1905) Dimorphism and regeneration in Metridium. J Exp Zool 2:225–235CrossRefGoogle Scholar
  48. Hamner WM, Jenssen RM (1974) Growth, degrowth, and irreversible cell differentiation in Aurelia aurita. Integr Comp Biol 14:833–849CrossRefGoogle Scholar
  49. Hand C, Uhlinger K (1995) Asexual reproduction by transverse fission and some anomalies in the sea anemone Nematostella vectensis. Invertebr Biol 114:9–18CrossRefGoogle Scholar
  50. Hargitt CW (1904) Regeneration in Rhizostoma pulmo. J Exp Zool 1:73–94CrossRefGoogle Scholar
  51. Hartl M, Mitterstiller AM, Valovka T, Breuker K, Hobmayer B, Bister K (2010) Stem cell-specific activation of an ancestral myc protooncogene with conserved basic functions in the early metazoan Hydra. Proc Natl Acad Sci U S A 107:4051–4056PubMedCrossRefGoogle Scholar
  52. Heng JCD, Feng B, Han J, Jiang J, Kraus P, Ng JH, Orlov YL, Huss M, Yang L, Lufkin T et al (2010) The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 6:167–174PubMedCrossRefGoogle Scholar
  53. Henry LA, Hart M (2005) Regeneration from injury and resource allocation in sponges and corals—a review. Int Rev Hydrobiol 90:125–158CrossRefGoogle Scholar
  54. Holstein T (1990) Cell cycle length, cell size, and proliferation rate in Hydra stem cells. Dev Biol 142:392–400PubMedCrossRefGoogle Scholar
  55. Holstein T, Hobmayer E, David C (1991) Pattern of epithelial cell cycling in Hydra. Dev Biol 148:602–611PubMedCrossRefGoogle Scholar
  56. Hou XG, Stanley G, Zhao J, Ma XY (2005) Cambrian anemones with preserved soft tissue from the Chengjiang biota, China. Lethaia 38:193–203CrossRefGoogle Scholar
  57. Houliston E, Momose T, Manuel M (2010) Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends Genet 26:159–167PubMedCrossRefGoogle Scholar
  58. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, Chen S, Muhlestein W, Melton DA (2008) Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 26:1269–1275PubMedCrossRefGoogle Scholar
  59. Hutton D, Smith V (1996) Antibacterial properties of isolated amoebocytes from the sea anemone Actinia equina. Biol Bull 191:441–451CrossRefGoogle Scholar
  60. Ivester M (1977) Nematocyst differentiation in the Anthozoon Renilla reniformis (Pallas). Trans Am Microsc Soc 96:238–247CrossRefGoogle Scholar
  61. Jacobs DK, Gates RD (2003) Developmental genes and the reconstruction of metazoan evolution—implications of evolutionary loss, limits on inference of ancestry and type 2 errors. Integr Comp Biol 43:619–646CrossRefGoogle Scholar
  62. Jacobs DK, Nakanishi N, Yuan D, Camara A, Nichols SA, Hartenstein V (2007) Evolution of sensory structures in basal metazoa. Integr Comp Biol 47:712–723PubMedCrossRefGoogle Scholar
  63. Jacobs DK, Gold DA, Nakanishi N, Yuan D, Camara A, Nichols SA, Hartenstein V (2010) Basal metazoan sensory evolution. In: Desalle R, Scheirwater R (Eds) Key transitions in animal evolution. CRCGoogle Scholar
  64. Jager M, Queinnec E, Le Guyader H, Manuel M (2011) Multiple Sox genes are expressed in stem cells or in differentiating neuro-sensory cells in the hydrozoan Clytia hemisphaerica. EvoDevo 2:12PubMedCrossRefGoogle Scholar
  65. 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 309:32–44PubMedCrossRefGoogle Scholar
  66. Kim J, Kim W, Cunningham CW (1999) A new perspective on lower metazoan relationships from 18S rDNA sequences. Mol Biol Evol 16:423–427PubMedCrossRefGoogle Scholar
  67. Kim JB, Sebastiano V, Wu G, Araúzo-Bravo MJ, Sasse P, Gentile L, Ko K, Ruau D, Ehrich M, van den Boom D et al (2009) Oct4-induced pluripotency in adult neural stem cells. Cell 136:411–419PubMedCrossRefGoogle Scholar
  68. King N, Westbrook MJ, Young SL, Kuo A, Abedin M et al (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–788PubMedCrossRefGoogle Scholar
  69. Koizumi O, Bode HR (1986) Plasticity in the nervous system of adult hydra. I. The position-dependent expression of FMRFamide-like immunoreactivity. Dev Biol 116:407–421PubMedCrossRefGoogle Scholar
  70. Koizumi O, Bode HR (1991) Plasticity in the nervous system of adult hydra. III. Conversion of neurons to expression of a vasopressin-like immunoreactivity depends on axial location. J Neurosci 11:2011–2020PubMedGoogle Scholar
  71. 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 129:358–371PubMedCrossRefGoogle Scholar
  72. Künzel T, Heiermann R, Frank U, Müller W, Tilmann W, Bause M, Nonn A, Helling M, Schwarz RS, Plickert G (2010) Migration and differentiation potential of stem cells in the cnidarian Hydractinia analysed in eGFP-transgenic animals and chimeras. Dev Biol 348:120–129PubMedCrossRefGoogle Scholar
  73. Kussarow A, Pang K, Sturm C, Hrouda M, Lentfer J et al (2005) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433:156–160CrossRefGoogle Scholar
  74. Larkman AU (1983) An ultrastructural study of oocyte growth within the endoderm and entry into the mesoglea in Actinia fragacea (Cnidaria, Anthozoa). J Morphol 178:155–177PubMedCrossRefGoogle Scholar
  75. Larkman AU (1984a) An ultrastructural study of the establishment of the testicular cysts during spermatogenesis in the sea anemone Actinia fragacea (Cnidaria: Anthozoa). Gamete Res 9:303–327CrossRefGoogle Scholar
  76. Larkman AU (1984b) The fine structure of granular amoebocytes from the gonads of the sea anemone Actinia fragacea (Cnidaria: Anthozoa). Protoplasma 122:203–221CrossRefGoogle Scholar
  77. Leclère L, Jager M, Barreau C, Chang P, Le Guyader H, Manuel M, Houliston E (2012) Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia. Dev Biol 364:236–248PubMedCrossRefGoogle Scholar
  78. Lee P, Pang K, Matus D, Martindale M (2006) A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol 17:157–167PubMedCrossRefGoogle Scholar
  79. Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Ozbek S, Bode H, Holstein TW (2009) Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 330:186–199PubMedCrossRefGoogle Scholar
  80. Lentz T (1965) The fine structure of differentiating interstitial cells in Hydra. Z Zellforsch Mikrosk Anat 67:547–560PubMedCrossRefGoogle Scholar
  81. Lesh-Laurie G, Suchy P (1991) Cnidaria: Scyphozoa and Cubozoa. In: Harrison F, Westfall J (eds) Microscopic anatomy of invertebrates. Volume 2: Placozoa, Porifera, Cnidaria, and Ctenophora. Wiley-Liss, New YorkGoogle Scholar
  82. 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 216–217:91–97CrossRefGoogle Scholar
  83. 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 112:185–193PubMedCrossRefGoogle Scholar
  84. Littlefield CL, Bode HR (1986) Germ cells in Hydra oligactis males. II. Evidence for a subpopulation of interstitial stem cells whose differentiation is limited to sperm production. Dev Biol 116:381–386PubMedCrossRefGoogle Scholar
  85. Loh Y, Wu Q, Chew J, Vega V, Zhang W (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38:431–440PubMedCrossRefGoogle Scholar
  86. Magie CR, Pang K, Martindale MQ (2005) Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 215:618–630PubMedCrossRefGoogle Scholar
  87. Marcum BA, Campbell RD (1978) Development of Hydra lacking nerve and interstitial cells. J Cell Sci 29:17–33PubMedGoogle Scholar
  88. Marlow HQ, Srivastava M, Matus DQ, Rokhsar D, Martindale MQ (2009) Anatomy and development of the nervous system of Nematostella vectensis, an Anthozoan Cnidarian. Dev Neurobiol 69:235–254PubMedCrossRefGoogle Scholar
  89. Martin VJ (1988) Development of nerve cells in hydrozoan planulae: I. Differentiation of ganglionic cells. Biol Bull 174:319–329CrossRefGoogle Scholar
  90. Martin V, Chia F (1982) Fine structure of a scyphozoan planula, Cassiopeia xamachana. Biol Bull 163:320–328CrossRefGoogle Scholar
  91. Martin VJ, Thomas MB (1981a) Elimination of the interstitial cells in the planula larva of the marine hydrozoan Pennaria tiarella. J Exp Zool 217:303–323CrossRefGoogle Scholar
  92. Martin V, Thomas M (1981b) The origin of the nervous system in Pennaria tiarella, as revealed by treatment with colchicine. Biol Bull 160:303–310CrossRefGoogle Scholar
  93. Matus D, Magie C, Pang K, Martindale M (2008) The Hedgehog gene family of the cnidarian, Nematostella vectensis, and implications for understanding metazoan Hedgehog pathway evolution. Dev Biol 313:501–518PubMedCrossRefGoogle Scholar
  94. McNeil PL (1981) Mechanisms of nutritive endocytosis. I. Phagocytic versatility and cellular recognition in Chlorohydra digestive cells, a scanning electron microscope study. J Cell Sci 49:311–339PubMedGoogle Scholar
  95. McNeil PL (1984) Mechanisms of nutritive endocytosis. III. A freeze-fracture study of phagocytosis by digestive cells of Chlorohydra. Tissue Cell 16:519–533PubMedCrossRefGoogle Scholar
  96. McNeil PL, Hohman TC, Muscatine L (1981) Mechanisms of nutritive endocytosis. II. The effect of charged agents on phagocytic recognition by digestive cells. J Cell Sci 52:243–269PubMedGoogle Scholar
  97. Medina M, Collins AG, Silberman JD, Sogin ML (2001) Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Natl Acad Sci U S A 98:9707–9712PubMedCrossRefGoogle Scholar
  98. Meszaros A, Bigger C (1999) Qualitative and quantitative study of wound healing processes in the coelenterate, Plexaurella fusifera: spatial, temporal, and environmental (light attenuation) influences. J Invertebr Pathol 73:321–331PubMedCrossRefGoogle Scholar
  99. Millane RC, Kanska J, Duffy DJ, Seoighe C, Cunningham S, Plickert G, Frank U (2011) Induced stem cell neoplasia in a cnidarian by ectopic expression of a POU domain transcription factor. Development 138:2429–2439PubMedCrossRefGoogle Scholar
  100. Minasian LL Jr (1980) The distribution of proliferating cells in an anthozoan polyp, Haliplanella luciae (Actiniaria: Acontiaria), as indicated by 3H-thymidine incorporation. In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. New York, Elsevier North-HollandGoogle Scholar
  101. Mochizuki K, Nishimiya-Fujisawa C, Fujisawa T (2001) Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Roux's Arch Dev Biol 211:299–308Google Scholar
  102. Müller WA (1996) Pattern formation in the immortal Hydra. Trends Genet 12:91–96PubMedCrossRefGoogle Scholar
  103. Müller W, Teo R (2004) Totipotent migratory stem cells in a hydroid. Dev Biol 275:215–224PubMedCrossRefGoogle Scholar
  104. Mydlarz LD, Holthouse SF, Peters EC, Harvell CD (2008) Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. PLoS One 3:e1811PubMedCrossRefGoogle Scholar
  105. Nakanishi N, Yuan D, Jacobs DK, Hartenstein V (2008) Early development, pattern, and reorganization of the planula nervous system in Aurelia (Cnidaria, Scyphozoa). Dev Genes Evol 218:511–524PubMedCrossRefGoogle Scholar
  106. Nakanishi N, Renfer E, Technau U, Rentzsch F (2012) Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 139:347–357PubMedCrossRefGoogle Scholar
  107. Neumann R (1977) Polyp morphogenesis in a scyphozoan: evidence for a head inhibitor from the presumptive foot end in vegetative buds of Cassiopeia andromeda. Roux's Arch Dev Biol 183:79–83CrossRefGoogle Scholar
  108. Ng HH, Surani MA (2011) The transcriptional and signalling networks of pluripotency. Nature 13:490–496Google Scholar
  109. 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 157:1–9PubMedCrossRefGoogle Scholar
  110. Nordström K, Wallén R, Seymour J, Nilsson D (2003) A simple visual system without neurons in jellyfish larvae. Proc Biol Sci 270:2349–2354PubMedCrossRefGoogle Scholar
  111. Olano CT, Bigger CH (2000) Phagocytic activities of the gorgonian coral Swiftia exserta. J Invertebr Pathol 76:176–184PubMedCrossRefGoogle Scholar
  112. Palmer CV, Traylor-Knowles NG, Willis BL, Bythell JC (2011) Corals use similar immune cells and wound-healing processes as those of higher organisms. PLoS One 6:e23992PubMedCrossRefGoogle Scholar
  113. Patterson M (1979) Cellular reaction to injury in the anthozoan Anthopleura elegantissima. J Invertebr Pathol 33:189–196CrossRefGoogle Scholar
  114. Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Queinnec E et al (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706–712PubMedCrossRefGoogle Scholar
  115. Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alié A, Morgenstern B, Manuel M et al (2010) Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27:1983–1987PubMedCrossRefGoogle Scholar
  116. Piraino S, De Vito D, Schmich J, Bouillon J, Boero F (2004) Reverse development in Cnidaria. Can J Zool 82:1748–1754CrossRefGoogle Scholar
  117. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV et al (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94PubMedCrossRefGoogle Scholar
  118. Reber-Müller S, Streitwolf-Engel R, Yanze N, Schmid V, Stierwald M, Erb M, Seipel K (2006) BMP2/4 and BMP5-8 in jellyfish development and transdifferentiation. Int J Dev Biol 50:377–384PubMedCrossRefGoogle Scholar
  119. Rebscher N, Volk C, Teo R, Plickert G (2008) The germ plasm component Vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata. Dev Dyn 237:1736–1745PubMedCrossRefGoogle Scholar
  120. Reitzel AM, Burton PM, Krone C, Finnerty JR (2007) Comparison of developmental trajectories in the starlet sea anemone Nematostella vectensis: embryogenesis, regeneration, and two forms of asexual fission. Invertebr Biol 126:99–112CrossRefGoogle Scholar
  121. Renfer E, Amon-Hassenzahl A, Steinmetz PR, Technau U (2010) A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc Natl Acad Sci U S A 107:104–108PubMedCrossRefGoogle Scholar
  122. Resch AM, Palakodeti D, Lu YC, Horowitz M, Graveley BR (2012) Transcriptome analysis reveals strain-specific and conserved stemness genes in Schmidtea mediterranea. PLoS One 7:e34447PubMedCrossRefGoogle Scholar
  123. Reyes-Bermudez A, Miller D (2009) In vitro culture of cells derived from larvae of the staghorn coral Acropora millepora. Coral Reefs 28:859–864CrossRefGoogle Scholar
  124. Rinkevich B (1996) Do reproduction and regeneration in damaged corals compete for energy allocation? Mar Ecol Prog Ser 143:297–302CrossRefGoogle Scholar
  125. Ryan JF, Baxevanis AD (2007) Hox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla. Biol Direct 2:37PubMedCrossRefGoogle Scholar
  126. Sánchez Alvarado A (2000) Regeneration in the metazoans: why does it happen? Bioessays 22:578–590PubMedCrossRefGoogle Scholar
  127. Schmid V, Alder H (1984) Isolated, mononucleated, striated muscle can undergo pluripotent transdifferentiation and form a complex regenerate. Cell 38:801–809PubMedCrossRefGoogle Scholar
  128. Schmid V, Reber-Muller S (1995) Transdifferentiation of isolated striated muscle of jellyfish: the initiation process. Semin Cell Biol 6:109–116PubMedCrossRefGoogle Scholar
  129. Schmid V, Stidwill R, Bally A, Marcum B, Tardent P (1981) Heat dissociation and maceration of marine Cnidaria. Roux's Arch Dev Biol 190:143–149CrossRefGoogle Scholar
  130. Schmid V, Wydler M, Alder H (1982) Transdifferentiation and regeneration in vitro. Dev Biol 92:476–488PubMedCrossRefGoogle Scholar
  131. Seipel K, Yanze N, Schmid V (2004) The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int J Dev Biol 48:1–7PubMedCrossRefGoogle Scholar
  132. Shimizu H, Sawada Y, Sugiyama T (1993) Minimum tissue size required for hydra regeneration. Dev Biol 155:287–296PubMedCrossRefGoogle Scholar
  133. Shinzato C, Iguchi A, Hayward DC, Technau U, Ball EE, Miller DJ (2008) Sox genes in the coral Acropora millepora: divergent expression patterns reflect differences in developmental mechanisms within the Anthozoa. BMC Evol Biol 8:311PubMedCrossRefGoogle Scholar
  134. Singer I (1971) Tentacular and oral-disc regeneration in sea anemone, Aiptasia diaphana.3. Autoradiographic analysis of patterns of tritiated thymidine uptake. J Embryol Exp Morpholog 26:253–270Google Scholar
  135. Steele RE, David CN, Technau U (2011) A genomic view of 500 million years of cnidarian evolution. Trends Genet 27:7–13PubMedCrossRefGoogle Scholar
  136. Steinberg S (1963) Regeneration of whole polyps from ectodermal fragments of scyphistoma larvae of Aurelia aurita. Biol Bull 124:337–343CrossRefGoogle Scholar
  137. Stockard C (1908) III. Studies of tissue growth. An experimental study of the rate of regeneration in Cassiopea xamachana (Bigelow). Publication 103, Carnegie Institution of Washington. 61-102Google Scholar
  138. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676PubMedCrossRefGoogle Scholar
  139. Technau U, Steele RE (2011) Evolutionary crossroads in developmental biology: Cnidaria. Development 138:1447–1458PubMedCrossRefGoogle Scholar
  140. Thomas M, Edwards N (1991) Cnidaria: Hydrozoa. In: Harrison F, Westfall J (eds) Microscopic anatomy of invertebrates. Volume 2: Placozoa, Porifera, Cnidaria, and Ctenophora. Wiley-Liss, New YorkGoogle Scholar
  141. Trevino M, Stefanik DJ, Rodriguez R, Harmon S, Burton PM (2011) Induction of canonical Wnt signaling by alsterpaullone is sufficient for oral tissue fate during regeneration and embryogenesis in Nematostella vectensis. Dev Dyn 240:2673–2679PubMedCrossRefGoogle Scholar
  142. Tucker RP, Shibata B, Blankenship TN (2011) Ultrastructure of the mesoglea of the sea anemone Nematostella vectensis (Edwardsiidae). Invertebr Biol 130:11–24CrossRefGoogle Scholar
  143. Vagelli A (2007) New observations on the asexual reproduction of Aurelia aurita (Cnidaria, Scyphozoa) with comments on its life cycle and adaptive significance. Invertebr Zool 4:111–127Google Scholar
  144. Van Lieshout JS, Martin VJ (1992) Development of planuloid buds of Cassiopea xamachana (Cnidaria: Scyphozoa). Trans Am Microsc Soc 111:89–110CrossRefGoogle Scholar
  145. Vargas-Ángel B, Peters E (2007) Cellular reactions to sedimentation and temperature stress in the Caribbean coral Montastraea cavernosa. J Invertebr Pathol 95:140–145PubMedCrossRefGoogle Scholar
  146. Watanabe H, Hoang VT, Mättner R, Holstein TW (2009) Immortality and the base of multicellular life: lessons from cnidarian stem cells. Semin Cell Dev Biol 20:1114–1125PubMedCrossRefGoogle Scholar
  147. West DL (1978) The epitheliomuscular cell of hydra: its fine structure, three-dimensional architecture and relation to morphogenesis. Tissue Cell 10:629–646PubMedCrossRefGoogle Scholar
  148. Westfall JA (1966) The differentiation of nematocysts and associated structures in the cnidaria. Z Zellforsch Mikrosk Anat 75:381–403PubMedCrossRefGoogle Scholar
  149. Wheeler BM, Heimberg AM, Moy VN, Sperling EA, Holstein TW, Heber S, Peterson KJ (2009) The deep evolution of metazoan microRNAs. Evol Dev 11:50–68PubMedCrossRefGoogle Scholar
  150. Wood R (1959) Intercellular attachment in the epithelium of Hydra as revealed by electron microscopy. J Biophys Biochem Cytol 6:343–352PubMedCrossRefGoogle Scholar
  151. Work TM, Aeby GS (2010) Wound repair in Montipora capitata. J Invertebr Pathol 105:116–119PubMedCrossRefGoogle Scholar
  152. 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 385:64–70PubMedCrossRefGoogle Scholar
  153. Yuan D, Nakanishi N, Jacobs DK, Hartenstein V (2008) Embryonic development and metamorphosis of the scyphozoan Aurelia. Dev Genes Evol 218:525–539PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California, Los AngelesLos AngelesUSA

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