Afuni, a Novel Transforming Growth Factor-beta Gene is Involved in Arm Regeneration by the Brittle Star Amphiura Filiformis

Overview

Journal Dev Genes Evol

Specialty Biology

Date 2005 Jul 13

PMID 16010544

Citations 11

Authors

R Bannister

I M McGonnell

A Graham

M C Thorndyke

P W Beesley

Affiliations

Soon will be listed here.

Abstract

The bone morphogenetic proteins (BMPs) are a family of the transforming growth factor-beta (TGF-beta) superfamily that perform multiple roles during vertebrate and invertebrate development. Here, we report the molecular cloning of a novel BMP from regenerating arms of the ophiuroid Amphiura filiformis. The theoretically translated amino acid sequence of this novel BMP has high similarity to that of the sea urchin BMP univin. This novel BMP has been named afuni. Whole-mount in situ hybridisation implicates afuni in arm regeneration. Expression occurs in distinct proximal and distal regions of late regenerates (3- and 5-week postablation). These sites are at different stages of regeneration, suggesting multiple roles for this gene in adult arm development. Cellular expression of this gene occurs in migratory cells within the radial water canal (RWC) of regenerating and nonregenerating arms. These migrating coelomocytes suggest a key role for the coelomic RWC as a source of the cellular material for use in arm regeneration by A. filiformis.

Citing Articles

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References

Chen C, Chen C, Hwang S . Identification and characterization of bone morphogenetic protein 2/4 gene from the starfish Archaster typicus. Comp Biochem Physiol B Biochem Mol Biol. 2002; 131(2):143-51. DOI: 10.1016/s1096-4959(01)00486-9. View

Hogan B . Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 1996; 10(13):1580-94. DOI: 10.1101/gad.10.13.1580. View

Carnevali M, Bonasoro F . Microscopic overview of crinoid regeneration. Microsc Res Tech. 2002; 55(6):403-26. DOI: 10.1002/jemt.1187. View

Davidson E, Peterson K, Cameron R . Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science. 1995; 270(5240):1319-25. DOI: 10.1126/science.270.5240.1319. View

Ducy P, Karsenty G . The family of bone morphogenetic proteins. Kidney Int. 2000; 57(6):2207-14. DOI: 10.1046/j.1523-1755.2000.00081.x. View

Peterson K, Cameron R, Davidson E . Set-aside cells in maximal indirect development: evolutionary and developmental significance. Bioessays. 1997; 19(7):623-31. DOI: 10.1002/bies.950190713. View

Graff J . Embryonic patterning: to BMP or not to BMP, that is the question. Cell. 1997; 89(2):171-4. DOI: 10.1016/s0092-8674(00)80196-8. View

Stenzel P, Angerer L, Smith B, Angerer R, Vale W . The univin gene encodes a member of the transforming growth factor-beta superfamily with restricted expression in the sea urchin embryo. Dev Biol. 1994; 166(1):149-58. DOI: 10.1006/dbio.1994.1303. View

Nieto M, Patel K, Wilkinson D . In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol. 1996; 51:219-35. DOI: 10.1016/s0091-679x(08)60630-5. View

10.

Chang C, Hemmati-Brivanlou A . Cell fate determination in embryonic ectoderm. J Neurobiol. 1998; 36(2):128-51. View

11.

Angerer L, Oleksyn D, Logan C, McClay D, Dale L, Angerer R . A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. Development. 2000; 127(5):1105-14. DOI: 10.1242/dev.127.5.1105. View

12.

Harada Y, Shoguchi E, Taguchi S, Okai N, Humphreys T, Tagawa K . Conserved expression pattern of BMP-2/4 in hemichordate acorn worm and echinoderm sea cucumber embryos. Zoolog Sci. 2002; 19(10):1113-21. DOI: 10.2108/zsj.19.1113. View

13.

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

14.

Ponce M, Micol J, Peterson K, Davidson E . Molecular characterization and phylogenetic analysis of SpBMP5-7, a new member of the TGF-beta superfamily expressed in sea urchin embryos. Mol Biol Evol. 1999; 16(5):634-45. DOI: 10.1093/oxfordjournals.molbev.a026146. View

15.

Urist M, Iwata H, Ceccotti P, Dorfman R, Boyd S, McDowell R . Bone morphogenesis in implants of insoluble bone gelatin. Proc Natl Acad Sci U S A. 1973; 70(12):3511-5. PMC: 427270. DOI: 10.1073/pnas.70.12.3511. View

16.

Combet C, Blanchet C, Geourjon C, Deleage G . NPS@: network protein sequence analysis. Trends Biochem Sci. 2000; 25(3):147-50. DOI: 10.1016/s0968-0004(99)01540-6. View

17.

De Robertis E, Sasai Y . A common plan for dorsoventral patterning in Bilateria. Nature. 1996; 380(6569):37-40. DOI: 10.1038/380037a0. View

18.

Reinhardt B, Broun M, Blitz I, Bode H . HyBMP5-8b, a BMP5-8 orthologue, acts during axial patterning and tentacle formation in hydra. Dev Biol. 2004; 267(1):43-59. DOI: 10.1016/j.ydbio.2003.10.031. View

19.

Chitnis A . Control of neurogenesis--lessons from frogs, fish and flies. Curr Opin Neurobiol. 1999; 9(1):18-25. DOI: 10.1016/s0959-4388(99)80003-8. View

20.

OKane S, Ferguson M . Transforming growth factor beta s and wound healing. Int J Biochem Cell Biol. 1997; 29(1):63-78. DOI: 10.1016/s1357-2725(96)00120-3. View