Skip to main content

Coelomic expression of a novel bone morphogenetic protein in regenerating arms of the brittle star Amphiura filiformis

Development Genes and Evolution volume 218, Article number: 33 (2008) Cite this article

Abstract

The bone morphogenetic proteins (BMPs) are a family of signalling molecules involved in numerous developmental processes including cell fate determination in embryonic ectoderm of vertebrate and invertebrate species. Recently, published evidence has indicated that BMPs are involved in echinoderm adult tissue regeneration. We have cloned a novel member of the BMP2/4 subfamily from the ophiuroid echinoderm Amphiura filiformis, which we have named afBMP2/4. Whole-mount in-situ hybridisation performed on non-regenerating brittle star arms revealed that expression of afBMP2/4 is localised to the radial water canal (RWC) and that this expression is upregulated at segmental intervals along the arm. This observed expression pattern suggests a putative active role for this echinoderm BMP transcript in somatic growth and maintenance of the brittle star arm. Expression of this factor has also been observed in regenerating arms 2 weeks post-ablation, implicating the RWC as a source of cells for ophiuroid arm regeneration.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  • Angerer LM, Oleksyn DW, Logan CY, McClay DR, Dale L, Angerer RC (2000) A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. Development 127:1105–1114

    CAS  PubMed  Google Scholar 

  • Bannister R, McGonnell IM, Graham A, Thorndyke MC, Beesley PW (2005) Afuni, a novel transforming growth factor-β gene is involved in arm regeneration by the brittle star Amphiura filiformis. Dev Genes Evol 215:393–401

    Article  CAS  PubMed  Google Scholar 

  • Candia Carnevali MD, Bonasoro F (2001) Microscopic overview of crinoid regeneration. Microsc Res Tech 55:403–426

    Article  CAS  PubMed  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  CAS  PubMed  Google Scholar 

  • Davidson EH, Peterson KJ, Cameron RA (1995) Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270:1319–1325

    Article  CAS  PubMed  Google Scholar 

  • De Robertis EM, Sasai Y (1996) A common plan for dorsoventral patterning in Bilateria. Nature 380:37–40

    Article  PubMed  Google Scholar 

  • Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559

    Article  CAS  PubMed  Google Scholar 

  • Lapraz F, Rottinger E, Duboc V, Range R, Duloquin L, Walton K, Wu SY, Bradham C, Loza MA, Hibino T, Wilson K, Poustka A, McClay D, Angerer L, Gache C, Lepage T (2006) RTK and TGF-beta signaling pathways genes in the sea urchin genome. Dev Biol 300:132–152

    Article  CAS  PubMed  Google Scholar 

  • Patruno M, McGonnell IM, Graham A, Beesley PW, Candia Carnevali MD, Thorndyke MC (2003) Anbmp2/4 is a new member of the transforming growth factor-β superfamily isolated from a crinoid and involved in regeneration. Proc R Soc Lond B 270:1341–1347

    Article  CAS  Google Scholar 

  • Ponce MR, Micol JL, Peterson KJ, Davidson EH (1999) Molecular characterization and phylogenetic analysis of SpBMP5–7, a new member of the TGF-β superfamily expressed in sea urchin embryos. Mol Biol Evol 16:634–645

    CAS  PubMed  Google Scholar 

  • Sköld M, Rosenberg R (1996) Arm regeneration frequency in eight species of ophiuroidea (Echinodermata) from European sea areas. J Sea Res 35:353–362

    Article  Google Scholar 

  • Stenzel P, Angerer LM, Smith BJ, Angerer RC, Vale WW (1994) The univin gene encodes a member of the transforming growth factor-β superfamily with restricted expression in the sea urchin embryo. Dev Biol 166:149–158

    Article  CAS  PubMed  Google Scholar 

  • Stern CD (2005) Neural induction: old problem, new findings, yet more questions. Development 132:2007–2021

    Article  CAS  PubMed  Google Scholar 

  • Thorndyke MC, Patruno M, Moss C, Beesley PW, Mallefet J (2001) Cellular and molecular bases of arm regeneration in brittlestars. In: Barker M (ed) Echinoderms 2000. Swets & Zeitlinger, Lisse, pp 193–199

    Google Scholar 

  • Wilson L, Maden M (2005) The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev Biol 282:1–13

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the staff at Kristineberg marine research Station for support during this work. R.B and M. C. T also acknowledge the support of the EU Transnational Access to Infrastructures programme, and VR (Sweden) as well as the Network of Excellence “Marine Genomics Europe” (GOCE-04-505403) for work conducted at Kristineberg marine research Station. We would also like to thank Patricia Goggin at the Electron Microscopy Unit, Royal Holloway, University of London, for assistance with preparation of resin sections. This work was funded by a NERC studentship.

Author information

Author notes

  1. Richard Bannister

    Present address: Institute for the Environment, Brunel University, Uxbridge, Middlesex, UB8 3PH, UK

Affiliations

  1. School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

    Richard Bannister & Philip W. Beesley

  2. Department of Veterinary Basic Sciences, Royal Veterinary College, Royal College Street, London, NW1 0TU, UK

    Imelda M. McGonnell

  3. MRC Centre for Developmental Neurobiology, Kings College London, London, SE1 1UL, UK

    Anthony Graham

  4. Kristineberg Marine Research Station, Royal Swedish Academy of Sciences, 450 34, Fiskebäckskil, Sweden

    Michael C. Thorndyke

Authors
  1. Richard Bannister
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Imelda M. McGonnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anthony Graham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael C. Thorndyke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Philip W. Beesley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philip W. Beesley.

Additional information

Communicated by M.Q. Martindale

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bannister, R., McGonnell, I.M., Graham, A. et al. Coelomic expression of a novel bone morphogenetic protein in regenerating arms of the brittle star Amphiura filiformis . Dev Genes Evol 218, 33 (2008). https://doi.org/10.1007/s00427-007-0193-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00427-007-0193-9

Keywords

  • Amphiura filiformis
  • Bone morphogenetic protein
  • Coelom
  • Echinoderm
  • Regeneration