[en] Development of complex organisms requires specific temporospatial differentiation and expression of the correct phenotype through activation of a variety of genes. Galectins are mammalian lectins able to interact with various extracellular matrix glycoconjugates and have been implicated in several biological events including cell attachment, differentiation, apoptosis, embryogenesis, and cancer invasion and metastasis. In this study, we have examined the expression of galectin-1 and galectin-3 during human first trimester embryogenesis using immunohistochemistry and Western blotting. Variable amounts of galectin-1 and galectin-3 were detected in all tissue protein extracts. Galectin-1 expression was demonstrated in the connective tissue and derived tissues such as smooth and striated muscle cells, and in some epithelia, such as in the basal layers of the skin after 14 weeks and in the epithelial cells of the gonads. Galectin-3 was detected mainly in epithelia, such as the skin, epithelial lining of the digestive and respiratory tract, and urothelium and excretory tubes of the kidney, but also in the myocardial cells, in the peripheral and preossifying hypertrophic chondrocytes, and in the notochord and in the liver. Our study constitutes the first demonstration of galectin-1 and galectin-3 during human embryogenesis. The differential expression of these two lectins suggests that they could participate in the complex processes of tissue differentiation.
Disciplines :
Biochemistry, biophysics & molecular biology Anatomy (cytology, histology, embryology...) & physiology Human health sciences: Multidisciplinary, general & others
Author, co-author :
van den Brûle, Frédéric; Université de Liège - ULiège > Laboratoire de recherche sur les métastases
Fernandez, Pedro L.; Hospital Clinic and Medical School, Barcelona, Spain > Department of Anatomical Pathology
Buicu, Crina; Université de Liège - ULiège > Laboratoire de recherche sur les métastases
Liu, Fu-Tong; La Jolla Institute for Allergy and Immunology, San Diego, CA, USA > L
Jackers, Pascale ; Université de Liège - ULiège > Laboratoire de recherche sur les métastases
Lambotte, René; Université de Liège - ULiège > Department of Obstetrics and Gynecology
Castronovo, Vincenzo ; Université de Liège - ULiège > Laboratoire de recherche sur les métastases
Language :
English
Title :
Differential expression of galectin-1 and galectin-3 during first trimester human embryogenesis.
Publication date :
August 1997
Journal title :
Developmental Dynamics
ISSN :
1058-8388
eISSN :
1097-0177
Publisher :
Wiley Liss, Inc., New York, United States - New York
Volume :
209
Issue :
4
Pages :
399-405
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
BIOMED 1 (No. BMH-1-CT92-0520)
Funders :
Association Sportive contre le Cancer Télévie [BE]
Agrwal, N., Wang, J.L., and Voss, P.G. (1989) Carbohydrate-binding protein 35: Levels of transcription and mRNA accumulation in quiescent and proliferating cells. J. Biol. Chem. 264:17236-17242.
Akimoto, Y., Hirabayashi, J., Kasai, K.-I., and Hirano, H. (1995) Expression of the endogenous 14-kDa β-galactoside-binding lectin galectin in normal human skin. Cell. Tissue Res. 280:1-10.
Allen, H.J., Sucato, D., Gottstine, S., Kisailus, E., Nava, H., Petrelli, N., Castillo, N., and Wilson, D. (1991) Localization of endogenous β-galactoside-binding lectin in human cells and tissues. Tumor Biol. 12:52-60.
Aubin, J.E., Liu, F., Malaval, L., and Gupta, A.K. (1995) Osteoblast and chondroblast differentiation. Bone 17:77S-83S.
Bao, Q., and Hughes, R.C. (1995) Galectin-3 expression and effects on cyst enlargement and tubulogenesis in kidney epithelial MDCK cells cultured in three-dimensional matrices in vitro. J. Cell. Sci. 108:2791-2800.
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.I., Leffler, H., Liu, F.T., Lotan, R., Mercurio, A.M., Monsigny, M., Pillai, S., Poirier, F., Raz, A., Rigby, P.W.J., Rini, J.M., and Wang, J.L. (1994a) Galectins: A family of animal β-galactoside- binding lectins. Cell 76:597-598.
Barondes, S.H., Cooper, D.N., Gitt, M.A., and Leffler, H. (1994b) Galectins. Structure and function of a large family of animal lectins. J. Biol. Chem. 269:20807-20810.
Brassart, D., Kolodziejczik, E., Granato, D., Woltz, A., Pavillard, M., Perotti, F., Frigeri, L.G., Liu, F.T., Borel, Y., and Neeser, J.R. (1992) An intestinal galactose-specific lectin mediates the binding of murine IgE to mouse intestinal epithelial cells. Eur. J. Biochem. 203:393-399.
Castronovo, V., Campo, E., van den Brûle, F.A., Claysmith, A.P., Cioce, V., Liu, F.T., Fernandez, P.L., and Sobel, M.E. (1992) Inverse modulation of steady-state messenger RNA levels of two non- integrin laminin-binding proteins in human colon carcinoma. J. Natl. Cancer Inst. 84:1161-1169.
Castronovo, V., van den Brûle, F.A., Jackers, P., Clausse, N., Liu, F.-T., Gillet, C., and Sobel, M.E. (1996) Decreased expression of galectin-3 is associated with progression of breast cancer. J. Pathol. 179:43-48.
Catt, J.W., Harrison, F.L., and Carleton, J.S. (1987) Distribution of an endogenous β-galactoside-specific lectin during foetal and neonatal rabbit development. J. Cell. Sci. 87:623-633.
Cooper, D.N., and 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. 110:1681-1691.
Cooper, D.N., Massa, S.M., and Barondes, S.H. (1991) Endogenous muscle lectin inhibits myoblast adhesion to laminin. J. Cell. Biol. 115:1437-1448.
Cowles, E.A., Agrwal, N., Anderson, R.L., and Wang, J.L. (1990) Carbohydrate-binding protein 35: Isoelectric points of the polypeptide and a phosphorylated derivative. J. Biol. Chem. 265:17706- 17712.
Dagher, S.F., Wang, J.L., and Patterson, R.J. (1995) Identification of galectin-3 as a factor in pre-mRNA splicing. Proc. Natl. Acad. Sci. USA 92:1213-1217.
Fenderson, B.A., Eddy, E.M., and Hakomori, S.-I. (1990) Glycoconjugate expression during embryogenesis and its biological significance. BioEssays 12:173-179.
Fowlis, D., Colnot, C., Ripoche, M.-A., and Poirier, F. (1995) Galectin-3 is expressed in the notochord, developing bones, and skin of the postimplantation mouse embryo. Dev. Dyn. 203:241-251.
Frigeri, L.G., and Liu, F.T. (1992) Surface expression of functional IgE binding protein, an endogenous lectin, on mast cells and macro- phages. J. Immunol. 148:861-867.
Frunchnak, Y.N., Martha, G.N., McFadden, K.D., and Milos, N.C. (1993) Alterations of heart development in Xenopus laevis by galactoside-binding lectin or its sugar hapten inhibitor. Anat. Embryol. 187:299-316.
Graham, C., and Karnovsky M.J. (1966) The early stages of absorption of horseradish peroxidase in the proximal tubules of mouse kidneys: Ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem. 14:291.
Hsu, S.M., Raine, L., and Fanger, H. (1981) Use of avidin-biotin- peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29:577-580.
Hynes, M.A., Gitt, M., Barondes, S.H., Jessel, T.M., and Buck, L.B. (1990) Selective expression of an endogenous lactose-binding lectin gene in subsets of central and peripheral neurons. J. Neurosci. 10:1004-1013.
Inohara, H., and Raz, A. (1995) Functional evidence that cell surface galectin-3 mediates homotypic cell adhesion. Cancer Res. 55:3267- 3271.
Jia, S., and Wang, J.L. (1988) Carbohydrate binding protein 35. Complementary DNA sequence reveals homology with proteins of the heterogenous nuclear RNP. J. Biol. Chem. 263:6009-6011.
Lee, E.G., Woo, H.J., Korzelius, C.A., Steele, G.D.J., and Mercurio, A.M. (1991) Carbohydrate-binding protein 35 is the major cell- surface laminin-binding protein in colon carcinoma. Arch. Surg. 126:1498-1502.
Lotan, R., Ito, H., Yasui, W., Yokozaki, H., Lotan, D., and Tahara, E. (1994) Expression of a 31-kDa lactoside-binding lectin in normal human gastric mucosa and in primary and metastatic gastric carcinomas. Int. J. Cancer 56:474-480.
Lotz, M., Andrews, C.J., Korzelius, C., Lee, E., Steele, G.J., Clarcke, A., and Mercurio, A. (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. Natl. Acad. Sci. USA 90:3466-3470.
Mahanthappa, N.K., Cooper, D.N.W., Barondes, S.H., and Schwarting, G.A. (1994) Rat olfactory neurons can utilier the endogenous lectin, L-14, in a novel adhesion mechanism. Development 120:1373-1384.
Marschal, P., Cannon, V., Barondes, S.H., and 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.
Oda, Y., Leffler, H., Sakakura, Y., Kasai, K.I., and Barondes, S.H. (1991) Human breast carcinoma cDNA encoding a galactoside- binding lectin homologous to mouse Mac-2 antigen. Gene 99:279- 283.
Perillo, N.L., Pace, K.E., Seilhamer, J.J., and Baum, L.G. (1995) Apoptosis of T cells mediated by galectin-1. Nature 378:736-739.
Poirier, F., Timmons, P.M., Chan, C.T.J., Guénet, J.L., and Rigby, P.W.J. (1992) Expression of the L14 lectin during mouse embryogenesis suggests multiple roles during pre- and post-implantation development. Development 115:143-155.
Rastan, S., Thorpe, S.J., Scudder, P., Brown, S., Gooi, H.C., and Feizi, T. (1985) Cell interactions in preimplantation embryos: evidence for involvement of saccharides of the poly-N-acetyllactosamine series. J. Embryol. exp. Morph. 87:115-128.
Raz, A., Pazerini, G., and Carmi, P. (1989) Identification of the metastasis-associated, galactoside-binding lectin as a chimeric gene product with homology to an IgE-binding protein. Cancer Res. 49:3489-3493.
Southan, C., Aitken, A., Childs, R.A., Abbott, W.M., and Feizi, T. (1987) Amino acid sequence of β-galactoside-binding bovine heart lectin. FEBS Lett. 214:301-304.
Tracey, B.M., Feizi, T., Abbott, W.M., Carruthers, R.A., Green, B.N., and Lawson, A.M. (1992) Subunit molecular mass assignment of 14,654 Da to the soluble β-galactoside-binding lectin from bovine heart muscle and demonstration of intramolecular disulfide bonding associated with oxidative inactivation. J. Biol. Chem. 267:10342- 10347.
van den Brûle, F.A., Buicu, C., Baldet, M., Sobel, M.E., Cooper, D.N.W., Marschal, P., and Castronovo, V. (1995) Galectin-1 modulates human melanoma cell adhesion to laminin. Biochem. Biophys. Res. Comm. 209:760-767.
van den Brûle, F.A., Buicu, C., Berchuck, A., Bast, R.C., Deprez, E., Liu, F.-T., Cooper, D.N.W, Pieters, C., Sobel, M.E., and Castronovo, V. (1996) Expression of the 67 kD laminin receptor, galectin-1 and galectin-3 in advanced human uterine carcinoma. Hum. Pathol. 27:1185-1191.
Wang, J.L., Laing, J.G., and Anderson, R.L. (1991) Lectins in the cell nucleus. Glycobiology 1:243-252.
Wasano, K., Hirakawa, Y., and Yamamoto, T. (1990) Immunohistochemical localization of 14 kDa β-galactoside-binding lectin in various organs of rat. Cell. Tissue Res. 259:43-49.
Zhou, Q., and Cummings, R.D. (1993) L-14 lectin recognition of laminin and its promotion of in vitro cell adhesion. Arch. Biochem. Biophys. 300:6-17.
