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Exogenous hyalin and sea urchin gastrulation. Part III: Biological activity of hyalin isolated from Lytechinus pictus embryos

Published online by Cambridge University Press:  01 November 2008

Azalia Contreras ,
John Vitale ,
Virginia Hutchins-Carroll ,
Edward J. Carroll Jr  and
Steven B. Oppenheimer
Azalia Contreras
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, 18111 Nordhoff Street, Northridge, CA 91330–8303, USA.
John Vitale
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, 18111 Nordhoff Street, Northridge, CA 91330–8303, USA.
Virginia Hutchins-Carroll
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, 18111 Nordhoff Street, Northridge, CA 91330–8303, USA.
Edward J. Carroll Jr
Affiliation:
Department of Chemistry and Biochemistry, California State University, Northridge, 18111 Nordhoff Street, Northridge, CA 91330–8262, USA.
Steven B. Oppenheimer*
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, Northridge, CA 91330–8303, USA. Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, 18111 Nordhoff Street, Northridge, CA 91330–8303, USA.
*
All correspondence to: Dr Steven B. Oppenheimer. Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, Northridge, CA 91330–8303, USA. Tel: +1 818 677 3336. Fax: +1 818 677 2034. e-mail: [email protected]
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Summary

Hyalin is a large glycoprotein, consisting of the hyalin repeat domain and non-repeated regions, and is the major component of the hyaline layer in the early sea urchin embryo of Strongylocentrotus purpuratus. The hyalin repeat domain has been identified in proteins from organisms as diverse as bacteria, sea urchins, worms, flies, mice and humans. While the specific function of hyalin and the hyalin repeat domain is incompletely understood, many studies suggest that it has a functional role in adhesive interactions. In part I of this series, we showed that hyalin isolated from the sea urchin S. purpuratus blocked archenteron elongation and attachment to the blastocoel roof occurring during gastrulation in S. purpuratus embryos, (Razinia et al., 2007). The cellular interactions that occur in the sea urchin, recognized by the U.S. National Institutes of Health as a model system, may provide insights into adhesive interactions that occur in human health and disease. In part II of this series, we showed that S. purpuratus hyalin heterospecifically blocked archenteron–ectoderm interaction in Lytechinus pictus embryos (Alvarez et al., 2007). In the current study, we have isolated hyalin from the sea urchin L. pictus and demonstrated that L. pictus hyalin homospecifically blocks archenteron–ectoderm interaction, suggesting a general role for this glycoprotein in mediating a specific set of adhesive interactions. We also found one major difference in hyalin activity in the two sea urchin species involving hyalin influence on gastrulation invagination.

Keywords

Archenteron attachmentHyalinLytechinus pictus sea urchin embryo
Type
Research Article
Information
Zygote , Volume 16 , Issue 4 , November 2008 , pp. 355 - 361
Copyright
Copyright © Cambridge University Press 2008

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References

Adelson, D.L. & Humphreys, T. (1988). Sea urchin morphogenesis and cell-hyalin adhesion are perturbed by a monoclonal antibody specific for hyalin. Dev. Biol. 104, 319–402.Google ScholarPubMed
Alvarez, M., Nnoli, J., CarrollE., Jr. E., Jr., Hutchins-Carroll, V. & Razinia, Z. & Oppenheimer, S.B. (2007). Exogenous hyalin and sea urchin gastrulation. Part II, Hyalin, an interspecies cell adhesion molecule. Zygote 16, 73–8.CrossRefGoogle Scholar
Bidwell, J.P. & Spotte, S. (1985). Artificial Seawaters, Formulas and Methods, p. 256. Boston: Jones and Barlett Publishers, Inc.Google Scholar
Callebout, I., Gilges, D., Vignon, I. & Mornon, J.P. (2000). HYR, an extracellular module involved in cellular adhesion and related to the immunoglobulin-like fold. Protein Sci. 9, 1382–90.CrossRefGoogle Scholar
Citkowitz, E. (1971). The hyaline layer, its isolation and role in echinoderm development. Dev. Biol. 24, 348–62.CrossRefGoogle ScholarPubMed
Coyle-Thompson, C. & Oppenheimer, S.B. (2005). A novel approach to study adhesion mechanisms by isolation of the interacting system. Acta Histochem. 107, 243–51.CrossRefGoogle ScholarPubMed
Davidson, E.H. (2006). The sea urchin genome, where will it lead us? Science 314, 939–40.CrossRefGoogle ScholarPubMed
Davidson, E.H. & Cameron, R.A. (2002). Arguments for sequencing the genome of the sea urchin Strongylocentrotus purpuratus. www.genome.gov/pages/research/sequencing/SegProposals/Sea>Urchin_Genome.prob. 2002.Urchin_Genome.prob.+2002.>Google Scholar
Edelman, G.M. (1987). CAMs and Igs, cell adhesion and the evolutionary origins of immunity. Immunol. Rev. 100, 9–43.CrossRefGoogle ScholarPubMed
Fink, R.D. & McClay, D.R. (1985). Three cell recognition changes accompany the ingression of sea urchin primary mesenchyme. Cells Dev. Biol. 107, 66–75.Google ScholarPubMed
Gray, J., Justice, R., Nagel, G.M. & Carroll, E.J. (1986). Resolution and characterization of a major protein of the sea urchin hyaline layer. J. Biol. Chem. 261, 9282–8.CrossRefGoogle Scholar
Herbst, C. (1900). Ueber das auseinanderegene im furchungs-und gewebe-zellen in kalkfreiem medium. Arch. F. Entwick 9, 424–63.CrossRefGoogle Scholar
Hoodbhoy, T., CarrollE.J., Jr. E.J., Jr. & Talbot, P. (2000). Relationship between p62 and p66, two proteins of the mammalian cortical granule envelope and hyalin, the major component of the echinoderm hyaline layer, in hamsters. Biol. Reprod. 62, 979–87.CrossRefGoogle Scholar
Hylander, B.L. & Summers, R.G. (1982). An ultrastructural immunocytochemical location of hyalin in the sea urchin egg. Dev. Biol. 93, 368–80.CrossRefGoogle Scholar
Itza, E.M. & Mozingo, N.M. (2005). Septate junctions mediate the barrier to paracellular permeability in sea urchin embryos. Zygote 13, 255–64.CrossRefGoogle ScholarPubMed
Jaffe, L.A. & Terasaki, M. (2004). Quantitative microinjection of oocytes, eggs and embryos. Cell Biol. 74, 219–42.Google ScholarPubMed
Justice, R.W. (1989). Calcium-insoluble proteins of the hyaline layer of the sea urchin, Strongylocentrotus purpuratus. Ph.D. thesis, University of California, Riverside, CA.Google Scholar
Justice, R.W. & Carroll, E.J. Jr. (1989). Antigenically distinct hyaline proteins localize to different regions of the sea urchin cortical granule and hyaline layer. J. Cell Biol. 109, 127a.Google Scholar
Justice, R.W., Nagel, G.M., Gottschling, C.F., Damis, M.F. & Carroll, E.J. Jr. (1992). A 9.6S protein is the third calcium-insoluble component of the sea urchin hyaline layer. Arch. Biochem. Biophys. 294, 297–305.CrossRefGoogle Scholar
Justice, R.W., Gottschling, C.F., Carroll, E.J. Jr. & Nagel, G.M. (1988). A calcium-insoluble 6.4 S protein derived from sea urchin cortical granule exudate. Arch. Biochem. Biophys. 265, 136–45.CrossRefGoogle ScholarPubMed
Khurrum, M., Hernandez, A., Eskalaei, M., Badali, O., Coyle-Thompson, C. & Oppenheimer, S.B. (2004). Carbohydrate involvement in cellular interactions in sea urchin gastrulation. Acta Histochem. 106, 97–106.CrossRefGoogle ScholarPubMed
Latham, V.H., Martinez, A.L., Cazares, L., Hamburger, H., Tully, M.J. & Oppenheimer, S.B. (1998). Accessing the embryo interior without microinjection. Acta Histochem. 100, 193–200.CrossRefGoogle ScholarPubMed
McClay, D.R. (1986). Embryo dissociation, cell isolation and cell reassociation. In Methods in Cell Biology (ed. Schroeder, T.E.), pp. 309–23. San Diego: Academic Press.Google Scholar
Merrill, C.R.D., Goldman, M.L. & Van Keuren, . (1984). Gel protein stains, silver stain. Methods in Enzymology vol. 104 part C, pp. 441–7. New York: Academic Press.Google Scholar
Razinia, Z., CarrollE.J., Jr. E.J., Jr. & Oppenheimer, S.B. (2007). Microplate assay for quantifying developmental morphologies, effects of exogenous hyalin on sea urchin gastrulation. Zygote, 15, 1–6.CrossRefGoogle ScholarPubMed
Sajadi, S., Rojas, P. & Oppenheimer, S. B. (2007). Cyclodextrin, a probe for studying adhesive interactions. Acta Histochem. 109, 338–42.CrossRefGoogle ScholarPubMed
Schuel, H. (1978). Secretory functions of egg cortical granules in fertilization and development, a critical review. Gamete Research 1, 299–382.CrossRefGoogle Scholar
Shapiro, B.M., Somers, C.E. & Weidman, P.J. (1989). Extracellular remodeling during fertilization. In The Cell Biology of Fertilization, (eds. Schatten, H. and Schatten, G.), pp. 251–76. San Diego: Academic Press, Inc.CrossRefGoogle Scholar
Stephens, RE. & Kane, RE. (1970). Some properties of hyalin, The calcium-insoluble protein of the hyaline layer of the sea urchin egg. J. Cell Biol. 44, 611–7.CrossRefGoogle ScholarPubMed
Vater, C.A. & Jackson, R.C. (1989). Purification and characterization of a cortical secretory vesicle membrane fraction. Dev. Biol. 135, 111–23.CrossRefGoogle ScholarPubMed
Warburg, O. & Christian, W. (1941). Isolierung und Kristallisation des garnugsferments enolase. Biochem Z. 310, 384–421.Google Scholar
Wessel, G.M., Berg, L., Adelson, D.L., Cannon, G., & McClay, D.R. (1998). A molecular analysis of hyalin, a substrate for cell adhesion in the hyaline layer of the sea urchin embryo. Dev. Biol. 193, 115–26.CrossRefGoogle ScholarPubMed
Whittaker, C.A., Bergeron, K.F., Whittle, V., Brandhorst, B.P., Burke, R.D. & Hynes, R.O. (2006). The echinoderm adhesome. Dev. Biol. 300, 252–66.CrossRefGoogle ScholarPubMed