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Immunohistochemical localisation of a galectin from Bufo arenarum ovary

Published online by Cambridge University Press:  15 January 2010

María T. Elola ,
Marcelo O. Cabada ,
Gustavo A. Barisone  and
Nilda E. Fink
María T. Elola
Affiliation:
Universidad Nacional de La Plata and Universidad Nacional de Rosario, Argentina
Marcelo O. Cabada
Affiliation:
Universidad Nacional de La Plata and Universidad Nacional de Rosario, Argentina
Gustavo A. Barisone
Affiliation:
Universidad Nacional de La Plata and Universidad Nacional de Rosario, Argentina
Nilda E. Fink*
Affiliation:
Universidad Nacional de La Plata and Universidad Nacional de Rosario, Argentina
*
N.E. Fink, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Calle 47 y 115, 1900 La Plata, Argentina. Telephone: (54 21) 210784 ext. 40. Fax: (54 21) 231150. e-mail: fink@biol.unlp.edu.ar.
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Summary

Galectins are a group of soluble animal lectins that exhibit specificity for β-galactosides and conserve sequence homology in the carbohydrate-recognition domain. The galectin from Bufo arenarum ovary showed a strong cross-reaction with the lectin of 14.5 kDa purified from embryos at early blastula stage. In this paper, we studied the immunohistochemical localisation of the galectin of 14.5 kDa from ovary of the toad B. arenarum in adult ovary sections. We also analysed the immunohistochemical localisation of the embryonic lectin during early development using the antiserum anti-ovary galectin. In the ovary, oocytes in the previtellogenic stage showed strong reactivity in the nucleus and the cortex but not in the cytoplasm. Oocytes in the stage of primary vitellogenesis exhibited a similar pattern in the nuclear and cortical areas but showed immunostaining in the cytoplasm. Intense nuclear staining was detected in oocytes in the stage of late vitellogenesis and in mature oocytes, which also presented strong reactions in the yolk platelets that completely covered the cytoplasm. In blastula embryos the staining was found in the blastomeres, the yolk platelets and the blastocoele. Each lectin localisation is discussed in relation to potential biological roles in the corresponding tissues.

Keywords

Bufo arenarumGalectinImmunohistochemistryOvaryToad
Type
Research Article
Information
Zygote , Volume 6 , Issue 1 , February 1998 , pp. 1 - 9
Copyright
Copyright © Cambridge University Press 1998

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References

Ahmed, H., Pohl, J., Fink, N.E., Strobel, F. & Vasta, G.R. (1996). The primary structure and carbohydrate specificity of a β-galactosyl-binding lectin from toad (Bufo arenarum Hensel) ovary reveal closer similarities to the mammalian galectin-1 than to the galectin from the clawed frog Xenopus laevis. J. Biol. Chem. 271, 33083–94.CrossRefGoogle Scholar
Akimoto, Y., Kawakami, H., Oda, Y., Obinata, A., Endo, H., Kasai, K. & Hirano, H. (1992). Changes in expression of the endogenous ß-galactoside-binding 14-kDa lectin of chick embryonic skin during epidermal differentiation. Exp. Cell Res. 199, 297–304.CrossRefGoogle Scholar
Akimoto, Y., Obinata, A., Hirabayashi, J., Sakakura, Y., Endo, H., Kasai, K. & Hirano, H. (1993). Secretion of endogenous 16-kDa ß-galactoside-binding lectin from vitamin A-pretreated chick embryonic cultured skin. Exp. Cell Res. 205, 251–60.CrossRefGoogle Scholar
Akimoto, Y., Hirabayashi, J., Kasai, K. & Hirano, H. (1995a). Expression of the endogenous 14-kDa ß-galactoside-binding lectin galectin in normal human skin. Cell Tissue Res. 280, 1–10.CrossRefGoogle Scholar
Akimoto, Y., Obinata, A., Hirabayashi, J., Sakakura, Y., Endo, H., Kasai, K. & Hirano, H. (1995b). Changes in expression of two endogenous ß-galactoside-binding isolectins in the dermis of chick embryonic skin during development in ovo and in vitro. Cell Tissue Res. 279, 3–12.CrossRefGoogle Scholar
Allen, H.J., Sucato, D., Woynarowska, B., Gottstine, S., Sharma, A. & Bernacki, R.J. (1990). Role of galaptin in ovarian carcinoma adhesion to extracellular matrix in vitro. J. Cell Biochem. 43, 43–57.CrossRefGoogle ScholarPubMed
Armant, D.R., Carson, D.D., Decker, G.L., Welply, J.K. & Lennarz, W.J. (1986). Characterization of yolk platelets isolated from developing embryos of Arbacia punctulata. Dev. Biol. 113, 342–55.CrossRefGoogle ScholarPubMed
Avellana-Adalid, V., Rebel, G., Caron, M., Cornillot, J.-D., Bladier, D. & Joubert-Caron, R. (1994). Changes in S-type lectin localization in neuroblastoma cells (N1E115) upon differentiation. Glycoconjugate J. 11, 286–91.CrossRefGoogle ScholarPubMed
Barondes, S.H., Castronovo, V., Cooper, D.N.W., Cummings, R.D., Drickamer, K., Feizi, T., Gitt, M.A., Hirabayashi, J., Hughes, C., Kasai, K., Leffler, H., Liu, F.-T., Lotan, R., Mercurio, A.M., Monsigny, M., Pillai, S., Poirer, F., Raz, A., Rigby, P.W.J., Rini, J.M. & Wang, J.L. (1994a). Galectins: a family of animal ß-galactoside-binding lectins. Cell 76, 597–8.CrossRefGoogle Scholar
Barondes, S.H., Cooper, D.N.W., Girt, M.A. & Leffler, H. (1994b). Galectins: structure and function of a large family of animal lectins. J. Biol. Chem. 269, 20807–10.Google ScholarPubMed
Bols, N.C., Roberson, M.M., Haywood-Reid, P.L., Cerra, R.F. & Barondes, S.H. (1986). Secretion of a cytoplasmic lectin from Xenopus laevis skin. J. Cell Biol. 102, 492–9.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 72, 248–54.CrossRefGoogle ScholarPubMed
Cerra, R.F., Haywood-Reid, P.L. & Barondes, S.H. (1984). Endogenous mammalian lectin localized extracellularly in lung elastic fibers, J. Cell Biol. 98, 1580–9.CrossRefGoogle ScholarPubMed
Cervello, M. & Matranga, V. (1989). Evidence for precursor-product relationship between vitellogenin and toposome, a glycoprotein complex mediating cell adhesion. Cell Differ. Dev. 26, 67–76.CrossRefGoogle ScholarPubMed
Cho, M. & Cummings, R.D. (1995). Galectin-1, a ß-galactoside-binding lectin in Chinese hamster ovary cells, J. Biol. Chem. 270, 5207–12.CrossRefGoogle Scholar
Cooper, D.N.W. & Barondes, S.H. (1990). Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism, J. Cell Biol. 110, 1681–91.CrossRefGoogle ScholarPubMed
Cooper, D.N.W., Massa, S.M. & Barondes, S.H. (1991). Endogenous muscle lectin inhibits myoblast adhesion to laminin. J. Cell Biol. 115, 1437–48.CrossRefGoogle ScholarPubMed
Dagher, S.F., Wang, J.L. & Patterson, R.J. (1995). Identification of galectin-3 as a factor in pre-mRNA splicing. Proc. Natl. Acad. Sci. USA 92, 1213–17.CrossRefGoogle ScholarPubMed
Del Conte, E. & Sirlin, J.L. (1951). Serie tipo de los primeros estadios embrionarios en Bufo arenarum. Acta Zool. Lilloana 12, 495–9.Google Scholar
Didier, E., Didier, P., Bayle, D. & Chevalier, M. (1988). Lectin activity and distribution of chicken lactose lectin I in the extracellular matrix of the chick developing kidney. Cell Differ. 24, 83–96.CrossRefGoogle ScholarPubMed
Elola, M.T. & Fink, N.E. (1996). Purification and partial biochemical characterization of an S-type lectin from blastula embryos of Bufo arenarum. Comp. Biochem. Physiol. 115, 175–82.CrossRefGoogle ScholarPubMed
Elola, M.T., Fink de Cabutti, N.E. & Herkovits, J. (1987). A developmentally regulated lectin in Bufo arenarum embryos. Brazilian J. Med. Biol. Res. 20, 749–53.Google ScholarPubMed
Elola, M.T., Fink de Cabutti, N.E. & Herkovits, J. (1988). Con A-, PHA- and WGA-binding in Bufo arenarum embryos. Morphol. Embryol. 34, 119–23.Google ScholarPubMed
Fink de Cabutti, N.E., Caron, M., Joubert, R., Elola, M.T., Bladier, D. & Herkovits, J. (1987). Purification and some characteristics of a ß-galactoside binding soluble lectin from amphibian ovary. FEBS Lett. 223, 330–4.CrossRefGoogle Scholar
Foddy, L., Stamatoglou, S.C. & Hughes, R.C. (1990). An endogenous carbohydrate-binding protein of baby hamster kidney (BHK21 C13) cells, J. Cell Sci. 97, 139–48.Google ScholarPubMed
Fowlis, D., Colnot, C., Ripoche, M.-A. & Poirier, F. (1995). Galectin-3 is expressed in the notochord, developing bones, and skin of the postimplantation mouse embryo. Dev. Dynam. 203, 241–51.CrossRefGoogle ScholarPubMed
Gu, M., Wang, W., Song, W.K., Cooper, D.N.W. & Kaufman, S.J. (1994). Selective modulation of the interaction of α7ß1 integrin with fibronectin and laminin by L-14 lectin during skeletal muscle differentiation, J. Cell Sci. 107, 175–81.Google Scholar
Hamburger, V. (1960). In A Manual of Experimental Embryology, p. 35. Chicago: University of Chicago Press.Google Scholar
Harlow, E. & Lane, D. (1988). In Antibodies: A Laboratory Manual, p. 594. New York: Cold Spring Harbor Laboratory.Google Scholar
Harrison, F.L. & Wilson, T.J.G. (1992). The 14kDa ß-galactoside binding lectin in myoblast and myotubes cultures: localization by confocal microscopy, J. Cell Sci. 101, 635–46.CrossRefGoogle Scholar
Hirabayashi, J. & Kasai, K. (1993). The family of metazoan metal-independent ß-galactoside-binding lectins: structure, function and molecular evolution. Glycobiology 3, 297–304.CrossRefGoogle Scholar
Hubert, J., Seve, A.P., Facy, P. & Monsigny, M. (1989). Are nuclear lectins and nuclear glycoproteins involved in the modulation of nuclear functions? Cell Differ. Dev. 27, 69–81.CrossRefGoogle ScholarPubMed
Inohara, H. & Raz, A. (1995). Functional evidence that cell surface galectin-3 mediates homotypic cell adhesion. Cancer Res. 55, 3267–71.Google ScholarPubMed
Irimura, T., Matsushita, Y., Sutton, R.C., Carralero, D., Ohannesian, D.W., Cleary, K.R., Ota, D.M., Nicolson, G.L. & Lotan, R. (1991). Increased content of an endogenous lactose-binding lectin in human colorectal carcinoma progressed to metastaric stages. Cancer Res. 51, 387–93.Google ScholarPubMed
Kasai, K. & Hirabayashi, J. (1996). Galectins: a family of animal lectins that decipher glycocodes. J. Biochem. 119, 1–8.CrossRefGoogle ScholarPubMed
Lotan, R., Lotan, D. & Raz, A. (1985). Inhibition of tumor cell colony formation in culture by a monoclonal antibody to endogenous lectins. Cancer Res. 4, 5,4349–53.Google Scholar
Lotz, M.M., Andrews, C.W. Jr, Korzelius, C.A., Lee, E.C., Steele, G.D., Clarke, A. & Mercurio, A.M. (1993). Decreased expression of Mac-2 (carbohydrate binding protein 35) and loss of its nuclear localization are associated with the neoplastic progression of colon carcinoma. Proc. Nati. Acad. Sci. USA 90, 3466–70.CrossRefGoogle ScholarPubMed
Mahanthappa, N.K., Cooper, D.N.W., Barondes, S.H. & Schwarting, G.A. (1994). Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 120, 1373–84.CrossRefGoogle Scholar
Marschal, P., Herrmann, J., Leffler, H., Barondes, S.H. & Cooper, D.N.W. (1992). Sequence and specificity of a soluble lactose-binding lectin from Xenopus laevis skin. J. Biol. Chem. 267, 12942–9.Google ScholarPubMed
Marschal, P., Cannon, V., Barondes, S.H. & Cooper, D.N.W. (1994). Xenopus laevis L-14 lectin is expressed in a typical pattern in the adult, but is absent from embryonic tissues. Glycobiology 4, 297–305.CrossRefGoogle Scholar
Moutsatsos, I.K., Davis, J.M. & Wang, J.L. (1986). Endogenous lectins from cultured cells: subcellular localization of carbohydrate-binding protein 35 in 3T3 fibroblasts. J. Cell Biol. 102, 477–83.CrossRefGoogle ScholarPubMed
Moutsatsos, I.K., Wade, M., Schindler, M. & Wang, J.L. (1987). Endogenous lectins from cultured cells: nuclear localization of carbohydrate-binding protein 35 in proliferating 3T3 fibroblasts. Proc. Nati Acad. Sci. USA 84, 6452–6.CrossRefGoogle ScholarPubMed
Muramoto, K. & Kamiya, H. (1992). The amino-acid sequence of a lectin from conger eel, Conger myriaster, skin mucus. Biochim. Biophys. Acta 1116, 129–36.Google ScholarPubMed
Ohannesian, D.W., Lotan, D. & Lotan, R. (1994). Concomitant increases in galectin-1 and its glycoconjugate ligands (carcinoembryonic antigen, Lamp-1, and Lamp-2) in cultured human colon carcinoma cells by sodium butyrate. Cancer Res. 54, 5992–6000.Google ScholarPubMed
Ohyama, Y. & Kasai, K. (1988). Isolation and characterization of the chick 14K ß-galactoside-binding lectin gene. J. Biochem. 104, 173–7.Google Scholar
Ozeki, Y, Matsui, T., Nitta, K., Kawauchi, H., Takayanagi, Y & Titani, K. (1991). Purification and characterization of a ß-galactoside binding lectin from frog (Rana catesbeiana) eggs. Biochem. Biophys. Res. Commun. 178, 407–13.Google Scholar
Paroutaud, P., Levi, G., Teichberg, V.I. & Strasberg, A.D. (1987). Extensive amino acid sequence homologies between animal lectins. Proc. Nati. Acad. Sci. USA 84, 6345–8.CrossRefGoogle ScholarPubMed
Poirier, F., Timmons, P.M., Chan, C.-T.J., Guénet, J.-L. & Rigby, P.W.J. (1992). Expression of the L14 lectin during mouse embryogenesis suggests multiple roles during preand post-implantation development. Development 115, 143–55.CrossRefGoogle Scholar
Sakakura, Y., Hirabayashi, J., Oda, Y., Ohyama, Y & Kasai, K. (1990). Structure of chicken 16-kDa ß-galactoside-binding lectin: complete amino acid sequence, cloning of cDNA, and production of recombinant lectin. J. Biol. Chem. 265, 21573–9.Google Scholar
Sánchez Riera, A.M., Sánchez, S.S. & Cabada, M.O. (1988). RNA metabolism in the follicle cells of Bufo arenarum oocytes. II. Autoradiographic studies. Micr. Electr. Biol. Cell. 12, 163–76.Google ScholarPubMed
Sanders, E.J., Zalik, S.E., Schneider, W.J. & Ledsham, Y.M. (1990). The endogenous lectins of the chick blastoderm are present in association with an apolipoprotein in distinct organelles and in the extracellular matrix. Rouxs Arch. Dea. Biol. 199, 295–306.CrossRefGoogle ScholarPubMed
Sato, S. & Hughes, R.C. (1994). Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages, J. Biol. Chem. 269, 4424–30.CrossRefGoogle ScholarPubMed
Valdez Toledo, C.L. & Pisanó, A. (1980). Studies of oogenesis in Bufo arenarum. Reproducción 4, 315–30.Google ScholarPubMed
Wang, J.L., Werner, E.A., Laing, J.G. & Patterson, R.J. (1992). Nuclear and cytoplasmic localization of a lectin-ribonu-cleoprotein complex. Biochem. Soc. Trans. 20, 269–74.CrossRefGoogle ScholarPubMed
Zalik, S.E., Schneider, W.J. & Ledsham, I.M. (1990). The gastrulating chick blastoderm contains 16 kDa and 14-kDa galactose-binding lectins possibly associated with an apolipoprotein. Cell Differ. Dev. 29, 217–31.CrossRefGoogle ScholarPubMed