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Involvement of l(–)-rhamnose in sea urchin gastrulation: a live embryo assay

Published online by Cambridge University Press:  18 October 2013

Tiffany N. Smith
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, California 91330–8303, USA.
Steven B. Oppenheimer*
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge. 1811 Nordhoff Street, Northridge, California 91330–8303, USA.
*
All correspondence to Steven B. Oppenheimer. Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge. 1811 Nordhoff Street, Northridge, California 91330–8303, USA. Tel: +1 818 677 3336. Fax: +1 818 677 2034. e-mail: [email protected]

Summary

The sea urchin embryo is a National Institutes of Health model system that has provided major developments, and is important in human health and disease. To obtain initial insights to identify glycans that mediate cellular interactions, Lytechinus pictus sea urchin embryos were incubated at 24 or 30 h post-fertilization with 0.0009–0.03 M alpha-cyclodextrin, melibiose, l(–)-rhamnose, trehalose, d(+)-xylose or l(–)-xylose in lower-calcium artificial sea water (pH 8.0, 15°C), which speeds the entry of molecules into the interior of the embryos. While α-cyclodextrin killed the embryos, and l(–)-xylose had small effects at one concentration tested, l(–)-rhamnose caused substantially increased numbers of unattached archenterons and exogastrulated embryos at low glycan concentrations after 18–24 h incubation with the sugar. The results were statistically significant compared with the control embryos in the absence of sugar (P < 0.05). The other sugars (melibiose, trehalose, d(+)-xylose) had no statistically significant effects whatsoever at any of the concentrations tested. In total, in the current study, 39,369 embryos were examined. This study is the first demonstration that uses a live embryo assay for a likely role for l(–)-rhamnose in sea urchin gastrula cellular interactions, which have interested investigators for over a century.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

Beck, B.H., Farmer, B.D., Straus, D.L., Li, C. & Peatman, E. (2012). Putative roles for a rhamnose binding lectin in Flavobacterium columnare pathogenesis in channel catfish Ictalurus punctatus. Fish Shellfish Immunol. 33, 1008–15.Google Scholar
Bidwell, J.P. & Spotte, S. (1985). Artificial Seawaters: Formulas and Methods. Boston, USA: Jones and Barlett Publishers, Inc.Google Scholar
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 Sea Urchin Strongylocentrotus purpuratus. Bethesda, MD, USA: National Human Genome Research Institute. Available online at: http://www.genome.gov/Pages/Research/Sequencing/SeqProposals/SeaUrchin_Genome.pdfGoogle Scholar
Ernst, S.G. (1997). A century of sea urchin development. Amer. Zool. 37, 250–9.Google Scholar
Franchi, N., Schiavon, F., Carletto, M., Gasparini, F., Bertoloni, G., Tosatto, S.C.E. & Ballarin, L. (2011). Immune roles of a rhamnose-binding lectin in the colonial ascidian Botryllus schlosseri. Immunology 216, 725–36.Google ScholarPubMed
Herbst, C. (1900). Ueber dasauseinanderegene im furchungsund gewebe-zellen in kalkfreiem medium. Arch. F. Entwick 9, 424–63.CrossRefGoogle Scholar
Hosono, M., Ishikawa, K., Mineki, R., Murayama, K., Numata, C., Ogawa, Y., Takayanagi, Y. & Nitta, K. (1999). Tandem repeat structure of rhamnose-binding lectin from catfish (Silurus asotus) eggs. Biochim. Biophys. Acta: General Subjects 1472, 668–75.Google Scholar
Hosono, M., Sugawara, S., Ogawa, Y., Kohno, T., Takayanagi, M. & Nitta, K. (2005). Purification, characterization, cDNA cloning, and expression of asialofetuin-binding C-type lectin from eggs of shishamo smelt (Osmerus [Spirinchus] lanceolatus). Biochim. Biophys. Acta: General Subjects 1725, 160–73.Google 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
Kim, M., Binnington, B., Sakac, D., Fernandes, K.R., Shi, S.P., Lingwood, C.A. & Branch, D.R. (2011). Comparison of detection methods for cell surface globotriaosylceramide. J. Immunol. Methods 371, 4860.Google Scholar
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, 193200.Google Scholar
Lopez, J.A., Fain, M.G. & Cadavid, L.F. (2011). The evolution of the immune-type gene family Rhamnospondin in cnidarians. Gene 473, 119–24.Google Scholar
Oppenheimer, S.B. & Carroll, E.J. (2004). Introduction to Embryonic Development. Upper Saddle River, NJ, USA: Pearson Education Publisher.Google Scholar
Ozeki, Y., Matsui, T., Suzuki, M. & Titani, K. (1991). Amino acid sequence and molecular characterization of a d-galactoside-specific lectin purified from sea urchin (Anthocidaris crassispina) eggs. Biochemistry 30, 2391–4.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, 159–64.Google Scholar
Schwarz, R.S., Hodes-Villamar, L., Fitzpatrick, K.A., Fain, M.G., Hughes, A.L. & Cadavid, L.F. (2007). A gene family of putative immune recognition molecules in the hydroid Hydractinia. Immunogenetics 59, 233–46.Google Scholar
Shirai, T., Watanabe, Y., Lee, M., Ogawa, T. & Muramoto, K. (2009). Structure of rhamnose-binding lectin CSL3: unique pseudo-tetrameric architecture of a pattern recognition protein. J. Mol. Biol. 391, 390403.Google Scholar
Shrivastava, A., Rhodes, R., Pochiraju, S., Nakane, D. & McBride, M.J. (2012). Flavobacterium johnsoniae RemA is a mobile cell surface lectin involved in gliding. J. Bacteriol. 194, 3678–88.Google Scholar
Singh, S., Karabidian, E., Kandel, A., Metzenberg, S., Carroll, E.J. & Oppenheimer, S.B. (2013). A role for polyglucans in a model sea urchin cellular interaction. Zygote doi:10.1017/S0967199413000038. [Epub ahead of print]Google Scholar
Tateno, H., Saneyoshi, A., Ogawa, T., Muramota, K., Kamiya, H. & Saneyoshi, M. (1998). Isolation and characterization of rhamnose-binding lectins from eggs of steelhead trout (Oncorhynchus mykiss) homologous to low density lipoprotein receptor superfamily. J. Biol. Chem. 273, 19190–7.Google Scholar
Terada, T., Wantanabe, Y., Tateno, H., Naganuma, T., Ogawa, T., Muramoto, K. & Kamiya, H. (2007). Structural characterization of a rhamnose-binding glycoprotein (lectin) from Spanish mackerel (Scomberomorous niphonius) eggs. Biochim. Biophys. Acta: General Subjects 1770, 617–29.Google Scholar
Watanabe, Y., Shiina, N., Shinozaki, F., Yokoyama, H., Kominami, J., Nakamura-Tsuruta, S., Hirabayashi, J., Sugahara, K., Kamiya, H., Matsubara, H., Ogawa, T. & Muramoto, K. (2008). Isolation and characterization of l-rhamnose-binding lectin, which binds to microsporidian Glugea plecoglossi, from ayu (Plecoglossus altivelis) eggs. Dev. Comp. Immunol. 32, 487–99.CrossRefGoogle ScholarPubMed
Watanabe, Y., Abolhassani, M., Tojo, Y., Suda, Y., Miyazawa, K., Igarahsi, Y., Sakuma, K., Ogawa, T. & Muramoto, K. (2009). Evaluation of silica gel-immobilized phosphorylcholine columns for size exclusion chromatography and their application in the analysis of the subunit structures of fish-egg lectins. J. Chromatogr. A 1216, 8563–6.Google Scholar