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Involvement of l(–)-rhamnose in sea urchin gastrulation. Part II: α-l-Rhamnosidase

  • Jing Liang (a1), Heghush Aleksanyan (a1), Stan Metzenberg (a1) and Steven B. Oppenheimer (a2) (a1)

Summary

The sea urchin embryo is recognized as a model system to reveal developmental mechanisms involved in human health and disease. In Part I of this series, six carbohydrates were tested for their effects on gastrulation in embryos of the sea urchin Lytechinus pictus. Only l-rhamnose caused dramatic increases in the numbers of unattached archenterons and exogastrulated archenterons in living, swimming embryos. It was found that at 30 h post-fertilization the l-rhamnose had an unusual inverse dose-dependent effect, with low concentrations (1–3 mM) interfering with development and higher concentrations (30 mM) having little to no effect on normal development. In this study, embryos were examined for inhibition of archenteron development after treatment with α-l-rhamnosidase, an endoglycosidase that removes terminal l-rhamnose sugars from glycans. It was observed that the enzyme had profound effects on gastrulation, an effect that could be suppressed by addition of l-rhamnose as a competitive inhibitor. The involvement of l-rhamnose-containing glycans in sea urchin gastrulation was unexpected, since there are no characterized biosynthetic pathways for rhamnose utilization in animals. It is possible there exists a novel l-rhamnose-containing glycan in sea urchins, or that the enzyme and sugar interfere with the function of rhamnose-binding lectins, which are components of the innate immune system in many vertebrate and invertebrate species.

Copyright

Corresponding author

All correspondence to Steven B. Oppenheimer, Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge. 18111 Nordhoff Street, Northridge, California 91330–8303, USA. Tel: +1 818 677 3336. Fax: +1 818 677-2034. Email: steven.oppenheimer@csun.edu

References

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Davidson, E.H. (2006). The sea urchin genome, where would it lead us? Science 314, 939–40.
Davidson, E.H. & Cameron, R.A. (2002). Arguments for sequencing the genome of sea urchin Strongylocentrotus purpuratus. www.genome.gov/pages/research/sequencing/SegProposals/Sea>Urchin_Genome.prob.2002.
Ernst, S.G. (1997), A century of sea urchin development. Am. Zool. 37, 250–9.
Ettensohn, C.A. (1984). Primary invagination of the vegetal plate during sea urchin gastrulation. Am. Zool. 24, 571–88.
Ettensohn, C.A. (1990). Cell interactions in the sea urchin embryo studied by fluorescence photoablation. Science 24 8, 1115–9.
Ettensohn, C.A. & McClay, D.R. (1988). Cell lineage conversion in the sea urchin embryo. Dev. Biol. 125, 396409.
Faury, G., Ruszova, E., Molinari, J., Mariko, B., Raveaud, S., Velelny, V., Robert, L (2008). The alpha-l-rhamnose recognizing lectin site of human dermal fibroblasts functions as a signal transducer: modulation of Ca++ fluxes and gene expression. Biochim. Biophys. Acta 1780, 1388–94.
Hamdoun, A. & Epel, D. (2007) Embryo stability and vulnerability in an always changing world. Proc. Natl. Acad. Sci. USA 104, 1745–50.
Harden, J. (1989). Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation. Dev. Biol. 136, 430–45.
Herbst, C (1900). Ueber dasauseinanderegene im furchungsund gewebe-zellen in kalkfreiem medium. Arch. F. Entwick 9, 424–63.
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) . BBA-General Subjects. 1725, 160–13.
Idoni, B., Ghazarian, H., Metzenberg, S., Carroll, V.H., Oppenheimer, S.B. & Carroll, E.H. Jr. (2010). Use of specific glycosidases to probe cellular interactions in the sea urchin embryo. Exp. Cell Res. 316, 2204–11.
Ingersoll, E.P. & Ettensohn, C.A. (1994). An N-linked carbohydrate-containing extracellular matrix determinant plays a key role in sea urchin gastrulation. Dev. Biol. 163, 351–66.
Itza, E.M. & Mozingo, N.M. (2005). Septate junctions mediate the barrier to paracellular permeability in sea urchin embryos. Zygote 13, 255–64.
Khurrum, M., Hernandez, A., Esklaei, M., Badali, O., Coyle-Thompson, C. & Oppenheimer, S.B. (2004). Carbohydrate involvement in cellular interactions in sea urchin gastrulation. Acta Histochem.106, 97106.
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.
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.
McFall-Ngai, M., Hadfield, M.G., Bosch, T.C.G. et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110, 3229–36.
Ogawa, T., Watanabe, M., Naganuma, T., and Muramoto, K. (2011) Diversified carbohydrate-binding lectins from marine resources. J. Amino Acids 2011, 838914. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3269628/#.
Ohta, T., Ido, A., Kusano, K., Miura, C., Miura, T. (2014) A novel polysaccharide in insects activates the innate immune system in mouse macrophage RAW264 cells. PLoS One 9, e114823.
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.
Rashidi, F., Yaghoobian, J. & Oppenheimer, S.B. (2011). Quantitative drug testing model using living sea urchin embryos. FASEB J. 25, 763–8.
Razinia, Z., Carroll, E.J. Jr & Oppenheimer, S.B. (2007). Microplate assay for quantifying developmental morphologies, effects of exogenous hyalin on sea urchin gastrulation. Zygote 15, 16.
Sakai, H., Edo, K., Nakagawa, H., Shinohara, M., Nishiitsutsuji, R. & Ohura, K. (2013) Isolation and partial characterization of a l-rhamnose-binding lectin from the globiferous pedicellariae of the toxopneustid sea urchin, Toxopneustes pileolus. International Aquatic Research 5, 12 http://www.intaquares.com/content/pdf/2008-6970-5-12.pdf.
Sea Urchin Genome Sequencing Consortium (2006). The genome of the sea urchin. Strongylocentrotus purpuratus Science 314, 941–52.
Singh, S., Karabidian, E., Kandel, A., Metzenberg, S., Carroll, E.J. & Oppenheimer, S.B. (2014). A role for polyglucans in a model sea urchin cellular interaction. Zygote 22, 419–29 doi:10.1017/S0967199413000038.
Smith, T.N. & Oppenheimer, S.B. (2013). Involvement of l(–)-rhamnose in sea urchin gastrulation: a live embryo assay. Zygote 23, 222–8 doi:10.1017/S0967199413000452.
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.
Watanabe, Y., Tateno, H., Nakamura-Tsuruta, S., Kominami, J., Hirabayashi, J., Nakamura, O., Watanabe, T., Kamiya, H., Naganuma, T., Ogawa, T., Naudé, R.J. & Muramoto, K. (2009). The function of rhamnose-binding lectin in innate immunity by restricted binding to Gb3. Dev. Comp. Immunol. 33, 187–97.

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