Skip to main content

Wnt Signaling in Cnidarians

  • Protocol
Book cover Wnt Signaling

Part of the book series: Methods in Molecular Biology ((MIMB,volume 469))

Abstract

Cnidarians are an ancient group of animals at the base of metazoan evolution. They exhibit a simple body plan with only one well-defined body axis and a small number of cell types. Cnidarians are also well known for their enormous regeneration capacity. Recent work in the freshwater polyp Hydra and in the sea anemone Nematostella has identified an unexpectedly high level of genetic complexity of wnt genes. Canonical Wnt signaling acts in pattern formation and regeneration of Hydra and also in gastrulation and early embryogenesis of Nematostella. Vertebrate-specific Wnt-antagonists were also identified from cnidarians and exhibit similar conserved functions. The simple cnidarian body plan and the now available genomes from Hydra and Nematostella, together with new functional approaches, make these animals an attractive model for studying the basic functions of canonical and non-canonical Wnt signaling.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
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 109.99
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

  1. Chen, J. Y., Oliveri, P., Gao, F., et al. (2002) Precambrian animal life: probable developmental and adult cnidarian forms from Southwest China. Dev Biol 248, 182–196.

    Article  PubMed  CAS  Google Scholar 

  2. Conway Morris S. (2000) The Cambrian “explosion”: slow-fuse or megatonnage? Proc Natl Acad Sci USA 97, 4426–4429.

    Article  PubMed  CAS  Google Scholar 

  3. Steele, R. E. (2006) Trembley's polyps go transgenic. Proc Natl Acad Sci USA 103, 6415–6416.

    Article  PubMed  CAS  Google Scholar 

  4. Steele, R. E. (2002) Developmental signaling in Hydra: what does it take to build a “simple” animal? Dev Biol 248, 199–219.

    Article  PubMed  CAS  Google Scholar 

  5. MacWilliams, H. K. (1983) Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of the head activation. Dev Biol 96, 239–257.

    Article  PubMed  CAS  Google Scholar 

  6. MacWilliams, H. K. (1983) Hydra transplantation phenomena and the mechanism of hydra head regeneration. I. Properties of the head inhibition. Dev Biol 96, 217–238.

    Article  PubMed  CAS  Google Scholar 

  7. Bode, M. P., Bode, H. R. (1984) Formation of pattern in regenerating tissue pieces of Hydra attenuata. III. The shaping of the body column. Dev Biol 106, 315–325.

    Article  PubMed  CAS  Google Scholar 

  8. Bode, P. M., Bode, H. R. (1980) Formation of pattern in regenerating tissue pieces of hydra attenuata. I. Head-body proportion regulation. Dev Biol 78, 484–496.

    Article  PubMed  CAS  Google Scholar 

  9. Meinhardt H. (2002) The radial-symmetric hydra and the evolution of the bilateral body plan: an old body became a young brain. Bioessays 24, 185–191.

    Article  PubMed  Google Scholar 

  10. Holstein, T. W., Hobmayer, E., Technau, U. (2003) Cnidarians: an evolutionarily conserved model system for regeneration? Dev Dyn 226, 257–267.

    Article  PubMed  CAS  Google Scholar 

  11. Bode, H. R. (2003) Head regeneration in Hydra. Dev Dyn 226, 225–236.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  13. Technau, U., Cramer von Laue, C., Rentzsch, F., et al. (2000) Parameters of self-organization in Hydra aggregates. Proc Natl Acad Sci USA 97, 12127–12131.

    Article  PubMed  CAS  Google Scholar 

  14. Darling, J. A., Reitzel, A. R., Burton, P. M., et al. (2005) Rising starlet: the starlet sea anemone, Nematostella vectensis. Bioessays 27, 211–221.

    Article  PubMed  CAS  Google Scholar 

  15. Holland, P. (2004) Developmental biology. The ups and downs of a sea anemone. Science 304, 1255–1256.

    Article  PubMed  CAS  Google Scholar 

  16. Fritzenwanker, J. H., Technau, U. (2002) Induction of gametogenesis in the basal cni-darian Nematostella vectensis (Anthozoa). Dev Genes Evol 212, 99–103.

    Article  PubMed  Google Scholar 

  17. Kraus, Y., Technau, U. (2006) Gastrulation in the sea anemone Nematostella vectensis occurs by invagination and immigration: an ultrastructural study. Dev Genes Evol 216, 119–132.

    Article  PubMed  Google Scholar 

  18. Fritzenwanker, J. H., Genikhovich, G., Kraus, Y., et al. (2007) Early development and axis specification in the sea anemone Nematostella vectensis. Dev Biol 310, 264–279.

    Article  PubMed  CAS  Google Scholar 

  19. Lee, P. N., Kumburegama, S., Marlow, H. Q., et al. (2007) Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vect-ensis, is mediated by Dishevelled. Dev Biol 310, 169–186.

    Article  PubMed  CAS  Google Scholar 

  20. Putnam, N. H., Srivastava, M., Hellsten, U., et al. (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86–94.

    Article  PubMed  CAS  Google Scholar 

  21. Technau, U., Rudd, S., Maxwell, P., et al. (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidar-ians. Trends Genet 21, 633–639.

    Article  PubMed  CAS  Google Scholar 

  22. Miller, D. J., Ball, E. E., Technau, U. (2005) Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet 21, 536–539.

    Article  PubMed  CAS  Google Scholar 

  23. Martindale, M. Q., Pan, K., Finnerty, J. R. (2004) Investigating the origins of triplob-lasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nema-tostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131, 2463–2474.

    Article  PubMed  CAS  Google Scholar 

  24. Finnerty, J. R., Pang, K., Burton, P., et al. (2004) Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 304, 1335–1337.

    Article  PubMed  CAS  Google Scholar 

  25. Scholz, C. B., Technau, U. (2003) The ancestral role of Brachyury: expression of NemBra1 in the basal cnidarian Nematostella vectensis (Anthozoa). Dev Genes Evol 212, 563–570.

    PubMed  CAS  Google Scholar 

  26. Technau, U., Scholz, C. B. (2003) Origin and evolution of endoderm and mesoderm. Int J Dev Biol 47, 531–539.

    PubMed  Google Scholar 

  27. Magie, C. R., Pang, K., Martindale, M. Q. (2005) Genomic inventory and expression of Sox and Fox genes in the cnidarian Nema-tostella vectensis. Dev Genes Evol 215, 618–630.

    Article  PubMed  CAS  Google Scholar 

  28. Torras, R., Yanze, N., Schmid, V., et al. (2004) Nanos expression at the embryonic posterior pole and the medusa phase in the hydrozoan Podocoryne carnea. Evol Dev 6, 362–371.

    Article  PubMed  CAS  Google Scholar 

  29. Extavour, C. G., Pang, K., Matus, D. Q., et al. (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  PubMed  CAS  Google Scholar 

  30. Matus, D. Q., Thomsen, G. H., Mar tindale, M. Q. (2006) Dorso/ventral genes are asymmetrically expressed and involved in germ-layer demarcation during cnidarian gastrulation. Curr Biol 16, 499–505.

    Article  PubMed  CAS  Google Scholar 

  31. Technau, U., Bode, H. R. (1999) HyBra1, a Brachyury homologue, acts during head formation in Hydra. Development 126, 999–1010.

    PubMed  CAS  Google Scholar 

  32. Spring, J., Yanze, N., Middel, A. M., et al. (2000) The mesoderm specification factor twist in the life cycle of jellyfish. Dev Biol 228, 363–375.

    Article  PubMed  CAS  Google Scholar 

  33. Spring, J., Yanze, N., Josch, C., et al. (2002) Conservation of Brachyury, Mef2, and Snail in the myogenic lineage of jellyfish: a connection to the mesoderm of bilateria. Dev Biol 244, 372–384.

    Article  PubMed  CAS  Google Scholar 

  34. Fritzenwanker, J. H., Saina, M., Technau, U. (2004) Analysis of forkhead and snail expression reveals epithelial-mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev Biol 275, 389–402.

    Article  PubMed  CAS  Google Scholar 

  35. Hayward, D. C., Miller, D. J., Ball, E. E. (2004) Snail expression during embryonic development of the coral Acropora: blurring the diploblast/triploblast divide? Dev Genes Evol 214, 257–260.

    Article  PubMed  Google Scholar 

  36. Guder, C., Philipp, I., Lengfeld, T., et al. (2006) The Wnt code: cnidarians signal the way. Oncogene 25, 7450–7460.

    Article  PubMed  CAS  Google Scholar 

  37. Wittlieb, J., Khalturin, K., Lohmann, J. U., et al. (2006) Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc Natl Acad Sci USA 103, 6208–6211.

    Article  PubMed  CAS  Google Scholar 

  38. King, N., Hittinger, C. T., Carroll, S. B. (2003) Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301, 361–363.

    Article  PubMed  CAS  Google Scholar 

  39. Hobmayer, B., Rentzsch, F., Kuhn, K., et al. (2000) WNT signaling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407, 186–189.

    Article  PubMed  CAS  Google Scholar 

  40. Hobmayer, E., Hatta, M., Fischer, R., et al. (1996) Identification of a Hydra homologue of the beta-catenin/plakoglobin/armadillo gene family. Gene 172, 155–159.

    Article  PubMed  CAS  Google Scholar 

  41. Minobe, S., Fei, K., Yan, L., et al. (2000) Identification and characterization of the epithelial polarity receptor “Frizzled” in Hydra vulgaris. Dev Genes Evol 210, 258–262.

    Article  PubMed  CAS  Google Scholar 

  42. Kusserow, A., Pang, K., Sturm, C., et al. (2005) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433, 156–160.

    Article  PubMed  CAS  Google Scholar 

  43. Lee, P. N., Pang, K., Matus, D. Q., et al. (2006) A WNT of things to come: Evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol 17, 157–167.

    Article  PubMed  Google Scholar 

  44. Guder, C., Pinho, S., Nacak, T. G., et al. (2006) An ancient Wnt-Dickkopf antagonism in Hydra. Development 133, 901–911.

    Article  PubMed  CAS  Google Scholar 

  45. Sullivan, J. C., Ryan, J. F., Mullikin, J. C., et al. (2007) Conserved and novel Wnt clusters in the basal eumetazoan Nematostella vectensis. Dev Genes Evol 217, 235–239.

    Article  PubMed  CAS  Google Scholar 

  46. Spitz, F., Duboule, D. (2005) Developmental biology: reproduction in clusters. Nature 434, 715–716.

    Article  PubMed  CAS  Google Scholar 

  47. Spitz, F., Gonzalez, F., Duboule, D. (2003) A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 113, 405–417.

    Article  PubMed  CAS  Google Scholar 

  48. Philipp, I., Holstein, T. W., Hobmayer, B. (2005) HvJNK, a Hydra member of the c-Jun NH2-terminal kinase gene family, is expressed during nematocyte differentiation. Gene Expr Patterns 5, 397–402.

    Article  PubMed  CAS  Google Scholar 

  49. Rentzsch, F., Hobmayer, B., Holstein, T. W. (2005) Glycogen synthase kinase 3 has a proapoptotic function in Hydra gametogen-esis. Dev Biol 278, 1–12.

    Article  PubMed  CAS  Google Scholar 

  50. Strutt, H., Price, M. A., Strutt, D. (2006) Planar polarity is positively regulated by casein kinase Iepsilon in Drosophila. Curr Biol 16, 1329–1336.

    Article  PubMed  CAS  Google Scholar 

  51. Price, M. A. (2006) CKI, there's more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev 20, 399–410.

    Article  PubMed  CAS  Google Scholar 

  52. Kawano, Y., Kypta, R. (2003) Secreted antagonists of the Wnt signaling pathway. J Cell Sci 116, 2627–2634.

    Article  PubMed  CAS  Google Scholar 

  53. Davidson, G., Mao, B., del Barco Barrantes, I., Niehrs, C (2002) Kremen proteins interact with Dickkopf1 to regulate anteropos-terior CNS patterning. Development 129, 5587–5596.

    Article  PubMed  CAS  Google Scholar 

  54. Mao, B., Niehrs, C. (2003) Kremen2 modulates Dickkopf2 activity during Wnt/LRP6 signaling. Gene 302, 179–183.

    Article  PubMed  CAS  Google Scholar 

  55. Jones, S. E., Jomar y, C. (2002) Secr eted Frizz led-related proteins: searching for relationships and patterns. Bioessays 24, 811–820.

    Article  PubMed  CAS  Google Scholar 

  56. Fedders, H., Augustin, R., Bosch, T. C. (2004) A Dickkopf-3-related gene is expressed in differentiating nematocytes in the basal meta-zoan Hydra. Dev Genes Evol 214, 72–80.

    Article  PubMed  CAS  Google Scholar 

  57. Augustin, R., Franke, A., Khalturin, K., et al. (2006) Dickkopf related genes are components of the positional value gradient in Hydra. Dev Biol 296, 262–270.

    Article  Google Scholar 

  58. Wikramanayake, A. H., Hong, M., Lee, P. N., et al. (2003) An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation. Nature 426, 446–450.

    Article  PubMed  CAS  Google Scholar 

  59. Momose, T., Houliston, E. (2007) Two oppositely localised frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol 5, e70.

    Article  PubMed  Google Scholar 

  60. Momose, T., Schmid, V. (2006) Animal pole determinants define oral-aboral axis polarity and endodermal cell-fate in hydrozoan jellyfish Podocoryne carnea. Dev Biol 292, 371–380.

    Article  PubMed  CAS  Google Scholar 

  61. Browne, E. N. (1909) The production of new hydranths in hydra by the insertion of small grafts. J Exp Zool 7, 1–37.

    Article  Google Scholar 

  62. Broun, M., Bode, H. R. (2002) Characterization of the head organizer in hydra. Development 129, 875–884.

    PubMed  CAS  Google Scholar 

  63. Broun, M., Gee, L., Reinhardt, B., et al. (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132, 2907–2916.

    Article  PubMed  CAS  Google Scholar 

  64. Cramer von Laue, C. (2003) Analysis of the dual function of beta-Catenin in Wnt signaling and in Cadherin-mediated cel l adhesion of Hydra, Darmstadt University of Technology, Darmstadt.

    Google Scholar 

  65. Muller, W., Frank, U., Teo, R., et al. (2007) Wnt signaling in hydroid development: ectopic heads and giant buds induced by GSK-3beta inhibitors. Int J Dev Biol 51, 211–220.

    Article  PubMed  Google Scholar 

  66. Plickert, G., Jacoby, V., Frank, U., et al. (2006). Wnt signaling in hydroid development: Formation of the primary body axis in embryogenesis and its subsequent patterning. Dev Biol 298, 368–378.

    Article  PubMed  CAS  Google Scholar 

  67. Lie, D. C., Colamarino, S. A., Song, H. J., et al. (2005) Wnt signaling regulates adult hippocampal neurogenesis. Nature 437, 1370–1375.

    Article  PubMed  CAS  Google Scholar 

  68. Onai, T., Sasa, N., Matsui, M., et al. (2004) Xenopus XsalF: anterior neuroectoder-mal specification by attenuating cellular responsiveness to Wnt signaling. Dev Cell 7, 95–106.

    Article  PubMed  CAS  Google Scholar 

  69. Teo, R., Mohrlen, F., Plickert, G., et al. (2006). An evolutionary conserved role of Wnt signaling in stem cell fate decision. Dev Biol 289, 91–99.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by funding from the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG).

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Holstein, T.W. (2008). Wnt Signaling in Cnidarians. In: Vincan, E. (eds) Wnt Signaling. Methods in Molecular Biology, vol 469. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-60327-469-5

Download citation

  • DOI: https://doi.org/10.1007/978-1-60327-469-5

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-60327-468-5

  • Online ISBN: 978-1-60327-469-2

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics