Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T10:09:34.865Z Has data issue: false hasContentIssue false
  • English
  • Français

Terminal alpha-d-mannosides are critical during sea urchin gastrulation

Published online by Cambridge University Press:  18 May 2016

Heghush Aleksanyan ,
Jing Liang ,
Stan Metzenberg  and
Steven B. Oppenheimer
Heghush Aleksanyan
Affiliation:
Department of Biology and Center for Cancer and Developmental Biology, California State University, Northridge, California 91330-8303, USA.
Jing Liang
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.
*
All correspondence to: 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. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The sea urchin embryo is a United States National Institutes of Health (NIH) designated model system to study mechanisms that may be involved in human health and disease. In order to examine the importance of high-mannose glycans and polysaccharides in gastrulation, Lytechinus pictus embryos were incubated with Jack bean α-mannosidase (EC 3.2.1.24), an enzyme that cleaves terminal mannose residues that have α1–2-, α1–3-, or α1–6-glycosidic linkages. The enzyme treatment caused a variety of morphological deformations in living embryos, even with α-mannosidase activities as low as 0.06 U/ml. Additionally, formaldehyde-fixed, 48-hour-old L. pictus embryos were microdissected and it was demonstrated that the adhesion of the tip of the archenteron to the roof of the blastocoel in vitro is abrogated by treatment with α-mannosidase. These results suggest that terminal mannose residues are involved in the adhesion between the archenteron and blastocoel roof, perhaps through a lectin-like activity that is not sensitive to fixation.

Keywords

ArchenteronBlastocoel roofGastrulationd-Mannoseα-MannosidaseSea urchin
Type
Research Article
Information
Zygote , Volume 24 , Issue 5 , October 2016 , pp. 775 - 782
Copyright
Copyright © Cambridge University Press 2016 

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

Bidwell, J.P. & Spotte, S. (1985). Artificial Seawaters, Formulas and Methods. Boston: Jones & Bartlett Publishers, Inc.; p. 256.Google Scholar
Brückner, K., Perez, L., Clausen, H. & Cohen, S. (2000). Glycosyltransferase activity of Fringe modulates Notch–Delta interactions. Nature 406, 411–5.CrossRefGoogle ScholarPubMed
Chisholm, A.D. (2006). Gastrulation: Wnts signal constriction. Curr. Biol. 16, R874–6.Google Scholar
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.Google Scholar
de Leoz, M.L., Young, L.J., An, H.J., Kronewitter, S.R., Kim, J., Miyamoto, S., Borowsky, A.D., Chew, H.K. & Lebrilla, C.B. (2011). High-mannose glycans are elevated during breast cancer progression. Mol. Cell. Proteomics 10 (1), M110.002717. doi: 10.1074/mcp.M110.002717.Google Scholar
Gustafson, T. & Wolpert, L. (1963). The cellular basis of morphogenesis and sea urchin development. Int. Rev. Cytol. 15, 139–214.Google Scholar
Hardin, J. (1988). The role of secondary mesenchyme cells during sea urchin gastrulation studied by laser ablation. Dev. Biol. 103, 317–24.Google Scholar
Hardin, J. & McClay, D.R. (1990). Target recognition by the archenteron during sea urchin gastrulation. Dev. Biol. 142, 86–102.Google Scholar
Hörstadius, S. (1935). Uber die Determination im Verlaufe der Eiachse bei Seeigeln. [Determination during the egg axis in sea urchins.] Pubb. Staz. Zool. Napoli 14, 251–479.Google Scholar
Idoni, B., Ghazarian, H., Metzenberg, S., Hutchins-Carroll, V., Oppenheimer, S.B. & Carroll, E.J. Jr. (2010). Use of specific glycosidases to probe cellular interactions in the sea urchin embryo. Exp. Cell Res. 316, 2004–211.Google Scholar
Juliano, C.E., Voronina, E., Stack, C., Aldrich, M., Cameron, A.R. & Wessel, G.M. (2006). Germ line determinants are not localized early in sea urchin development, but do accumulate in the small micromere lineage. Dev. Biol. 300, 406–15.Google Scholar
Kabakoff, B. & Lennarz, W.J. (1990). Inhibition of glycoprotein processing blocks assembly of spicules during development of the sea urchin embryo. J. Cell Biol. 111, 391–400.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
Kominami, T. & Takata, H. (2004). Gastrulation in the sea urchin embryo: a model system for analyzing the morphogenesis of a monolayered epithelium. Dev. Growth Differ. 46, 309–26.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
Latham, V.H., Tully, M.J. & Oppenheimer, S.B. (1999). A putative role for carbohydrates in sea urchin gastrulation. Acta Histochem. 100, 193–200.Google Scholar
Li, Y.T. (1967). Studies on the glycosidases in Jack bean meal. J. Biol. Chem. 242, 5474–80.Google Scholar
Liang, J., Aleksanyan, H., Metzenberg, S. & Oppenheimer, S.B. (2015). Involvement of l(–)-rhamnose in sea urchin gastrulation. Part II: α-l-Rhamnosidase. Zygote 14, 1–7. [Epub ahead of print]Google Scholar
Marek, K.W., Vijay, I.K. & Marth, J.D. (1999). A recessive deletion in the GlcNAc-1-phosphotransferase gene results in peri-implantation embryonic lethality. Glycobiology 9, 1263–71.Google Scholar
Metzler, M., Gertz, A., Sarkar, M., Schachter, H., Schrader, J.W. & Marth, J.D. (1994). Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J. 13, 2056–65.Google Scholar
Miller, J., Fraser, S.E. & McClay, D. (1995). Dynamics of thin filopodia during sea urchin gastrulation. Development 121, 2501–11.Google Scholar
Navarro, V.M., Walker, S.L., Badali, O., Abundis, M.I., Ngo, L.L., Weerasinghe, G., Barajas, M., Zem, G. & Oppenheimer, S.B. (2002). Analysis of surface properties of fixed and live cells using derivatized agarose beads. Acta Histochem. 104, 99–106.Google Scholar
Nocente-McGrath, C., Brenner, C.A. & Ernst, SG. (1989). Endo16, a lineage-specific protein of the sea urchin embryo, is first expressed just prior to gastrulation. Dev. Biol. 136, 264–72.Google Scholar
Ransick, A. & Davidson, E.H. (1995). Micromeres are required for normal vegetal plate specification in sea urchin embryos. Development 121, 3215–22.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, 159–64.Google Scholar
Romano, L.A. & Wray, G.A. (2006). Endo16 is required for gastrulation in the sea urchin Lytechinus variegatus . Dev. Growth Differ. 48, 487–97.Google Scholar
Schneider, E.G., Nguyen, H.T. & Lennarz, W.J. (1978). The effect of tunicamycin, an inhibitor of protein glycosylation, on embryonic development in the sea urchin. J. Biol. Chem. 253, 2348–55.Google Scholar
Sethi, A.J., Angerer, R.C. & Angerer, L.M. (2009). Gene regulatory network interactions in sea urchin endomesoderm induction. PLoS Biol. 7, e1000029.Google Scholar
Sherwood, D.R. & McClay, D.R. (1999). LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development 126, 1703–13.Google Scholar
Singh, S., Karabidian, E., Kandel, A., Metzenberg, S., Carroll, E.J. Jr & Oppenheimer, S.B. (2014). A role for polyglucans in a model sea urchin embryo cellular interaction. Zygote 22, 419–29.Google Scholar
Soltysik-Española, M., Klinzing, D.C., Pfarr, K., Burke, R.D. & Ernst, S.G. (1994). Endo16, a large multidomain protein found on the surface and ECM of endodermal cells during sea urchin gastrulation, binds calcium. Dev. Biol. 165, 73–85.Google Scholar
Yajima, M. & Wessel, G.M. (2011). Small micromeres contribute to the germline in the sea urchin. Development 138, 237–43.Google Scholar
Yamamoto, H., Awada, C., Hanaki, H., Sakane, H., Tsujimoto, I., Takahashi, Y., Takao, T. & Kikuchi, A. (2013). The apical and basolateral secretion of Wnt11 and Wnt3a in polarized epithelial cells is regulated by different mechanisms. J. Cell Sci. 126, 2931–43.Google Scholar