Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T07:47:59.615Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  14 July 2015

Jing Liang ,
Heghush Aleksanyan ,
Stan Metzenberg  and
Steven B. Oppenheimer
Jing Liang
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, California 91330–8303, USA.
Heghush Aleksanyan
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, California 91330–8303, USA.
Stan Metzenberg
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. 18111 Nordhoff Street, Northridge, California 91330–8303, USA. Department of Biology and Center for Cancer and Developmental Biology, California State University, 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. 18111 Nordhoff Street, Northridge, California 91330–8303, USA. Tel: +1 818 677 3336. Fax: +1 818 677-2034. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Archenteron developmentInnate immunityl-rhamnoseRhamnose-binding lectinα-l-RhamnosidaseSea urchin gastrulation
Type
Research Article
Information
Zygote , Volume 24 , Issue 3 , June 2016 , pp. 371 - 377
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Davidson, E.H. (2006). The sea urchin genome, where would it lead us? Science 314, 939–40.Google Scholar
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.Urchin_Genome.prob.2002.>Google Scholar
Ernst, S.G. (1997), A century of sea urchin development. Am. Zool. 37, 250–9.Google Scholar
Ettensohn, C.A. (1984). Primary invagination of the vegetal plate during sea urchin gastrulation. Am. Zool. 24, 571–88.Google Scholar
Ettensohn, C.A. (1990). Cell interactions in the sea urchin embryo studied by fluorescence photoablation. Science 24 8, 1115–9.CrossRefGoogle Scholar
Ettensohn, C.A. & McClay, D.R. (1988). Cell lineage conversion in the sea urchin embryo. Dev. Biol. 125, 396–409.Google Scholar
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.Google Scholar
Hamdoun, A. & Epel, D. (2007) Embryo stability and vulnerability in an always changing world. Proc. Natl. Acad. Sci. USA 104, 1745–50.Google Scholar
Harden, J. (1989). Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation. Dev. Biol. 136, 430–45.Google Scholar
Herbst, C (1900). Ueber dasauseinanderegene im furchungsund gewebe-zellen in kalkfreiem medium. Arch. F. Entwick 9, 424–63.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) . BBA-General Subjects. 1725, 160–13.Google Scholar
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.Google Scholar
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.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.Google Scholar
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, 97–106.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.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, 193–200.Google Scholar
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.CrossRefGoogle Scholar
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/#.Google Scholar
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.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
Rashidi, F., Yaghoobian, J. & Oppenheimer, S.B. (2011). Quantitative drug testing model using living sea urchin embryos. FASEB J. 25, 763–8.Google Scholar
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, 1–6.Google Scholar
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.Google Scholar
Sea Urchin Genome Sequencing Consortium (2006). The genome of the sea urchin. Strongylocentrotus purpuratus Science 314, 941–52.Google Scholar
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.Google Scholar
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.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
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.CrossRefGoogle ScholarPubMed