Skip to main content
SpringerLink
Log in

Hydra, a candidate for an alternative model in environmental genomics

  • Review Paper
  • Published:
Molecular & Cellular Toxicology Aims and scope Submit manuscript

Abstract

The need for nonmammalian and nonvertebrate experimental systems for toxicology is increasing because of growing concern about animal welfare. Hydra, a genus of freshwater cnidarian, has been used in classical toxicology for more than 40 years and has been recommended as a standard model for ecotoxicology. Functional assays using Hydra homologues of the signal molecules and transcription factors of other metazoans have demonstrated that Hydra shares the common molecular mechanisms for pattern formation with bilaterian animals. The availability of the Hydra genome and mRNA information has meant that it can be used as a model organism in biological sciences. The purpose of this review is to explore recent developments in our understanding of the molecular aspects of axis formation, bud formation, regeneration, and the nervous system in Hydra and to introduce Hydra as an alternative animal model in environmental toxicogenomics for predicting the toxicity of environmental pollutants at the molecular level.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Cowan, T. The Animal Welfare Act: Background and Selected Animal Welfare Legislation. Congressional Research Service 7-5700 (2013).

    Google Scholar 

  2. Galliot, B. Hydra, a fruitful model system for 270 years. Int J Dev Biol 56:411–423 (2012).

    Article  CAS  PubMed  Google Scholar 

  3. Pollino, C. A. & Holdway, D. A. Potential of two Hydra species as standard toxicity test animals. Ecotoxicol Environ Saf 43:309–316 (1999).

    Article  CAS  PubMed  Google Scholar 

  4. Snape, J. R., Maund, S. J., Pickford, D. B. & Hutchinson, T. H. Ecotoxicogenomics: the challenge of integrating genomics into aquatic and terrestrial ecotoxicology. Aquat Toxicol 67:143–154 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Bode, H. R. The head organizer in Hydra. Int J Dev Biol 56:473–478 (2012).

    Article  CAS  PubMed  Google Scholar 

  6. Hobmayer, B. et al. WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407:186–189 (2000).

    Article  CAS  PubMed  Google Scholar 

  7. Chapman, J. A. et al. The dynamic genome of Hydra. Nature 464:592–596 (2010).

    Article  CAS  PubMed  Google Scholar 

  8. Medina, M., Collins, A. G., Silberman, J. D. & Sogin, M. L. Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Natl Acad Sci USA 98:9707–9712 (2001).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Kim, J., Kim, W. & Cunningham, C. W. A new perspective on lower metazoan relationships from 18S rDNA sequences. Mol Biol Evol 16:423–427 (1999).

    Article  CAS  PubMed  Google Scholar 

  10. Wainright, P. O., Hinkle, G., Sogin, M. L. & Stickel, S. K. Monophyletic origins of the metazoa: an evolutionary link with fungi. Science 260:340–342 (1993).

    Article  CAS  PubMed  Google Scholar 

  11. Quinn, B., Gagne, F. & Blaise, C. Hydra, a model system for environmental studies. Int J Dev Biol 56:613–625 (2012).

    Article  CAS  PubMed  Google Scholar 

  12. Lengfeld, T. et al. Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 330:186–199 (2009).

    Article  CAS  PubMed  Google Scholar 

  13. Guder, C. et al. An ancient Wnt-Dickkopf antagonism in Hydra. Development 133:901–911 (2006).

    Article  CAS  PubMed  Google Scholar 

  14. De Robertis, E. M., Larrain, J., Oelgeschlager, M. and Wessely, O. The establishment of Spemann’s organizer and patterning of the vertebrate embryo. Nat Rev Genet 1:171–181 (2000).

    Article  PubMed Central  PubMed  Google Scholar 

  15. Broun, M., Gee, L., Reinhardt, B. & Bode, H. R. Formation of the head organizer in Hydra involves the canonical Wnt pathway. Development 132:2907–2916 (2005).

    Article  CAS  PubMed  Google Scholar 

  16. Nakamura, Y., Tsiairis, C. D., Ozbek, S. & Holstein, T. W. Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer. Proc Natl Acad Sci USA 108:9137–9142 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Johnson, E. M. & Gabel, B. E. An artificial ‘embryo’ for detection of abnormal developmental biology. Fundam Appl Toxicol 3:243–249 (1983).

    Article  CAS  PubMed  Google Scholar 

  18. Quinn, B., Gagne, F. & Blaise, C. Evaluation of the acute, chronic and teratogenic effects of a mixture of eleven pharmaceuticals on the cnidarian, Hydra attenuata. Sci Total Environ 407:1072–1079 (2009).

    Article  CAS  PubMed  Google Scholar 

  19. Johnson, E. M., Gorman, R. M., Gabel, B. E. & George, M. E. The Hydra attenuata system for detection of teratogenic hazards. Teratog Carcinog Mutagen 2:263–276 (1982).

    Article  CAS  PubMed  Google Scholar 

  20. Wilby, O. K. & Tesh, J. M. The Hydra assay as an early screen for teratogenic potential. Toxicol In Vitro 4:582–583 (1990).

    Article  CAS  PubMed  Google Scholar 

  21. Brooun, M. et al. Organizer formation in Hydra is disrupted by thalidomide treatment. Dev Biol 378:51–63 (2013).

    Article  CAS  PubMed  Google Scholar 

  22. Otto, J. J. & Campbell, R. D. Budding in Hydra attenuata: bud stages and fate map. J Exp Zool 200:417–428 (1977).

    Article  CAS  PubMed  Google Scholar 

  23. Mitchell, F. M. & Holdway, D. A. The acute and chromic toxicity of the dispersants Corexit 9527 and 9500, water accommodated fraction (WAF) of crude oil, and dispersant enhanced WAF (DEWAF) to Hydra viridissima (green hydra). Wat Res 34:343–348 (2000).

    Article  CAS  Google Scholar 

  24. Bielen, H. et al. Divergent functions of two ancient Hydra Brachyury paralogues suggest specific roles for their C-terminal domains in tissue fate induction. Development 134:4187–4197 (2007).

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  26. Fujisawa, T. Hydra regeneration and epitheliopeptides. Dev Dyn 226:182–189 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. Lohmann, J. U. & Bosch, T. C. The novel peptide HEADY specifies apical fate in a simple radially symmetric metazoan. Genes Dev 14:2771–2777 (2000).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Takahashi, T. et al. Hym-301, a novel peptide, regulates the number of tentacles formed in Hydra. Development 132:2225–2234 (2005).

    Article  CAS  PubMed  Google Scholar 

  29. Hoffmeister, S. A. Isolation and characterization of two new morphogenetically active peptides from Hydra vulgaris. Development 122:1941–1948 (1996).

    CAS  PubMed  Google Scholar 

  30. Grens, A. et al. The novel signal peptides, pedibin and Hym-346, lower positional value thereby enhancing foot formation in Hydra. Development 126:517–524 (1999).

    CAS  PubMed  Google Scholar 

  31. Hoffmeister-Ullerich, S. A. The foot formation stimulating peptide pedibin is also involved in patterning of the head in Hydra. Mech Dev 106:37–45 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Harafuji, N. et al. Enhancement of foot formation in Hydra by a novel epitheliopeptide, Hym-323. Development 128:437–446 (2001).

    CAS  PubMed  Google Scholar 

  33. Amimoto, Y., Kodama, R. & Kobayakawa, Y. Foot formation in Hydra: a novel gene, anklet, is involved in basal disk formation. Mech Dev 123:352–361 (2006).

    Article  CAS  PubMed  Google Scholar 

  34. Cardenas, M. et al. Selective protein kinase inhibitors block head-specific differentiation in Hydra. Cell Signal 12:649–658 (2000).

    Article  CAS  PubMed  Google Scholar 

  35. Takahashi, T. et al. Systematic isolation of peptide signal molecules regulating development in Hydra: LWa-mide and PW families. Proc Natl Acad Sci USA 94:1241–1246 (1997).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Fujisawa, T. Hydra peptide project 1993–2007. Dev Growth Differ 50 Suppl 1:S257–268 (2008).

    Article  Google Scholar 

  37. Yum, S. et al. A novel neuropeptide, Hym-176, induces contraction of the ectodermal muscle in Hydra. Biochem Biophys Res Commun 248:584–590 (1998).

    Article  CAS  PubMed  Google Scholar 

  38. Yum, S., Takahashi, T., Hatta, M. & Fujisawa, T. The structure and expression of a preprohormone of a neuropeptide, Hym-176 in Hydra magnipapillata. FEBS Lett 439:31–34 (1998).

    Article  CAS  PubMed  Google Scholar 

  39. Takahashi, T. et al. A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra. Development 127:997–1005 (2000).

    CAS  PubMed  Google Scholar 

  40. Woo, S. et al. Toxaphene affects the levels of mRNA transcripts that encode antioxidant enzymes in Hydra. Comp Biochem Physiol C Toxicol Pharmacol 156:37–41 (2012).

    Article  CAS  PubMed  Google Scholar 

  41. Takahashi, T. et al. Identification of a new member of the GLWamide peptide family: physiological activity and cellular localization in cnidarian polyps. Comp Biochem Physiol B Biochem Mol Biol 135:309–324 (2003).

    Article  PubMed  Google Scholar 

  42. Hayakawa, E., Takahashi, T., Nishimiya-Fujisawa, C. & Fujisawa, T. A novel neuropeptide (FRamide) family identified by a peptidomic approach in Hydra magnipapillata. FEBS J 274:5438–5448 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. Takahashi, T. & Hamaue, N. Molecular characterization of Hydra acetylcholinesterase and its catalytic activity. FEBS Lett 584:511–516 (2010).

    Article  CAS  PubMed  Google Scholar 

  44. Dash, B. et al. Molecular characterization of two superoxide dismutases from Hydra vulgaris. Gene 387:93–108 (2007).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Dash, B. et al. Molecular characterization of phospholipid hydroperoxide glutathione peroxidases from Hydra vulgaris. Gene 381:1–12 (2006).

    Article  CAS  PubMed  Google Scholar 

  46. Dash, B. & Phillips, T. D. Molecular characterization of a catalase from Hydra vulgaris. Gene 501:144–152 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Ankley, G. T. et al. Toxicogenomics in regulatory ecotoxicology. Environ Sci Technol 40:4055–4065 (2006).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. South Sea Environment Research Division, Korea Institute of Ocean Science and Technology, Geoje, 656-830, Korea

    Seungshic Yum, Seonock Woo, Aekyung Lee, Hyokyoung Won & Junghee Kim

  2. Faculty of Marine Environmental Chemistry and Biology, University of Science and Technology, Geoje, 656-830, Korea

    Seungshic Yum & Seonock Woo

Authors
  1. Seungshic Yum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Seonock Woo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aekyung Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hyokyoung Won
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junghee Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seungshic Yum.

Additional information

These authors contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yum, S., Woo, S., Lee, A. et al. Hydra, a candidate for an alternative model in environmental genomics. Mol. Cell. Toxicol. 10, 339–346 (2014). https://doi.org/10.1007/s13273-014-0038-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13273-014-0038-3

Keywords

Search

Navigation