[en] Tumor cell adhesion and migration to laminin are important events during invasion and metastatic spread. Galectin-3, a multifunctional member of the galectin family, binds specifically the poly-N-acetyllactosamine residues of laminin and has been implicated in tumor invasion and metastasis. Galectin-3 is multimerized by transglutaminase, an enzyme that catalyzes cross-linking between glutamine and other aminoacid residues. In this study, we examined the consequences of transglutaminase-mediated galectin-3 oligomerization on the interactions between cancer cells and laminin. We first demonstrated that human galectin-3 is cross-linked by guinea pig liver transglutaminase, forms oligomers, and incorporates the marker 5-(biotinamido) pentylamine. Expression of transglutaminase activity in the A375 and A2058 human melanoma cell extracts was revealed by its ability to induce galectin-3 oligomerization and 5-(biotinamido) pentylamine incorporation. Transglutaminase-treated galectin-3 did not affect adhesion or migration of the melanoma cells to laminin but consistently induced a significant increase of the percentage of cell spreading compared to the control (23.5 +/- 2.3%, vs. 10.6 +/- 1.9% at 180 min, p < 0.05), or to untreated galectin-3 or transglutaminase alone. Our study is the first demonstration that human galectin-3 is oligomerized by transglutaminase with, as a consequence, a specific effect of melanoma cell spreading on laminin. This phenomenon could be of significance in the modulation of cancer cell interactions with laminin during tumor invasion and metastasis.
Arumugham, R.G., Hsieh, T.C Y., Tanzer, M.L. and Laine, R. (1986) "Structure of the asparagine-linked sugar chains of laminin." Biochim. Biophys. Acta 883, 112-126.
Bargisian, C., Fellin, F.M., Jain, A. and Martinez, J. (1988) "Dissociation of fibrinogen and fibronectin binding from transglutaminase-mediated cross-linking at the hepatocyte surface." J. Biol Chem. 263, 14015-14022.
Bargisian, C., Stern, A.M. and Martinez, J. (1991) "Tissue (type II) transglutaminase covalently incorporates itself, fibrinogen, or fibronectin into high molecular weight complexes on the extracellular surface of isolated hepatocytes." J. Biol. Chem. 266, 22501-22509.
Barondes, S.H., Castronovo, V., Cooper, D N.W., Cummings, R.D., Drickamer, D., 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 (letter)." Cell 78, 597-598.
Barondes, S.U., Cooper, D N.W., Gitt, M.A. and Leffler, H. (1994b) "Galectins - Structure and function of a large family of animal lectins." J. Biol. Chem. 269, 28807-28810.
Beck, K., Hunter, I and Engel, J. (1990) "Structure and function of laminin: anatomy of a multidomam glycoprotein." FASEB J. 4, 148-160.
Beninati, S , Abbruzzese, A. and Cardinali, M. (1993) "Differences in the post-translational modification of proteins by polyamines between weakly and highly metastatic B16 melanoma cells." Int J. Cancer. 53, 792-797.
Castronovo, V. (1993) "Laminin receptors and laminin-binding proteins during tumor invasion and metastasis." Inv. Metastasis 13, 1-30.
Castronovo, V., Luyten, F., van den Brûle, F. and Sobel, M.E. (1992) "Identification of a 14-kDa laminin binding protein (HLBP14) in human melanoma cells that is identical to the 14-kDa galactoside binding lectin." Arch. Biochem. Biophys. 297, 132-138.
Castronovo, V., Taraboletti, G., Liotta, L.A. and Sobel, M.E. (1989) "Modulation of laminin receptor expression by estrogen and progestins in human breast cancer cell lines." J. Natl. Cancer Inst. 81, 781-788.
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.
Dean, J.W.III., Chandrasekaran, S. and Tanzer, M.L. (1990) "A biological role of the carbohydrate moieties of laminin." J. Biol. Chem. 265, 12553-12562.
Delcros, J.G., Bard, S., Roch, A.M., Quash, G., Poupon, M.F. and Korach, S. (1986) "Transglutaminase activity and putrescine-binding capacity in cloned cell lines with different metastatic potential." FEES Lett. 196, 325-330.
Dennis, J.W , Waller, C A. and Schirrmacher, V. (1984) "Identification of asparagine-linked oligosaccharides involved in tumor cell adhesion to laminin and type IV collagen." J. Cell. Biol 99, 1416-1423.
Folk, J.E. (1980) "Transglutaminases." Ann. Rev. Biochem. 49, 517-531.
Frigeri, L.G. and Liu, F.T. (1992) "Surface expression of functional IgE binding protein, an endogenous lectin, on mast cells and macrophages." J. Immunol. 148, 861-867.
Fujiwara, S., Shinkai, H., Deutzmann, R., Paulsson, M. and Timpl, R (1988) "Structure and distribution of N-linked oligosaccharide chains on various domains of mouse tumor laminin." Biochem. J. 252, 453-461.
Gentile, V., Thomazy, V., Piacentini, M., Fesus, L. and Davies, P.J.A. (1992) "Expression of tissue transglutaminase in Balb-C 3T3 fibroblasts. effects on cellular morphology and adhesion." J Cell. Biol 119, 463-474.
Gu, M., Wang, W., Song, W K., Cooper, D.N.W. and Kaufmen, S.J. (1994) "Selective modulation of the interaction of α7β1 integrin with fibronectin and laminin by L-14 lectin during skeletal muscle differentiation." J. Cell Sci 107, 175-181.
Hsu, D.K., Zuberi, R.I. and Liu, F.T. (1992) "Biochemical and biophysical characterization of human recombinant IgE-binding protein, an S-type animal lectin." J. Biol. Chem. 267, 14167-14174.
Hughes, R C. (1994) "Mac-2: a versatile galactose-binding protein of mammalian tissues." Glycobiology 4, 5-12.
Ichinose, A., Bottenus, R E. and Davie, E.W. (1990) "Structure of transglutaminases." J. Biol. Chem 265, 13411-13414.
Inohara, H., Akaham, S., Koths, K. and Raz, A (1996) "Interactions between galectin-3 and Mac-2-binding protein mediate cell-cell adhesion." Cancer Res. 56, 4530-4534.
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.
Kuwabara, I. and Liu, F.T. (1996) "Galectin-3 promotes adhesion of human neutrophils to laminin." J Immunol. 156, 3939-3944
Lee, K.N., Maxwell, M.D., Patterson, M.K J., Birckbichler, P.J. and Conway, E. (1992) "Identification of transglutaminase substrates in HT29 colon cancer cells: use of 5-(biotinamido) pentylamine as a transglutaminase-specific probe." Biochim. Biophys. Acta. 1136, 12-16
Levi, G. and Teichberg, V.I. (1981) "Isolation and physicochemical characterization of electrolectin, a β-D-galactoside binding lectin from the electric organ of Electrophorus Electricus." J. Biol Chem. 256, 5735-5740.
Lorand, L. and Conrad, S. (1984) "Transglutaminases." Mol. Cell Biochem. 58, 9-35.
Mahanthappa, N.K., Cooper, D.N.W., Barondes, S.H. and Schwarting, G.A. (1994) "Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism." Development 120, 1373-1384.
Martinez, J., Rich, E and Bargisian, C (1989) "Transglutaminase-mediated cross-linking of fibrinogen by human umbilical vein endothelial cells." J Biol Chem. 264, 20502-20508.
Mehul, B., Bawumia, S. and Hughes, R.C. (1995) "Cross-linking of galectin-3, a galactose-binding protein of mammalian cells, by tissue-type transglutaminase." FEBS Lett. 360, 160-164.
Mehul, B., Bawumia, S., Martin, S.R. and Hughes, R.C. (1994) "Structure of a baby hamster kidney carbohydrate-binding protein CBP30, an S-type animal lectin." J. Biol. Chem. 269, 18250-18258.
Moutsatsos, I.K., Davis, J.M. and Wang, J.L. (1986) "Endogenous lectins from cultured cells subcellular localization of carbohydrate-binding protein 35 in 3T3 fibroblasts." J. Cell. Biol. 102, 477-483.
Ochieng, J., Gerold, M. and Raz, A. (1992) "Dichotomy in the laminin-binding properties of soluble and membrane-bound human galactoside-binding protein." Biochem. Biophys. Res. Comm. 186, 1674-1680.
Raz, A., Avivi, A., Pazerini, G. and Carmi, P. (1987) "Cloning and expression of cDNA for two endogenous UV-2237 fibrosarcoma lectin genes." Exp. Cell. Res. 173, 109-116.
Raz, A., Carmi, P., Raz, T., Hogan, V., Mohamed, A. and Wolman, S R. (1991) "Molecular cloning and chromosomal mapping of a human galactoside-binding protein." Cancer Res 51, 2173-2178
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.
Roff, C.F , Rosevear, P.R., Wang, J.L. and Barker, R (1983) "Identification of carbohydrate-binding proteins from mouse and human fibroblasts." Biochem. J. 211, 625-629.
Roff, C.F and Wang, J L. (1983) "Endogenous lectins from cultured cells: isolation and characterization of carbohydrate-binding proteins from 3T3 fibroblasts." J. Biol. Chem. 258, 10657-10663.
Sato, S. and Hughes, R.C. (1992) "Binding specificity of a baby hamster kidney lectin for H type I and II chains, polylacto samine glycans, and appropriately glycosylated forms of laminm and fibronectin." J. Biol. Chem. 267, 6983-6990.
Todaro, G.J., Fryling, C. and DeLarco, J.E. (1980) "Transforming growth factors produced by certain human tumor cells, polypeptides that interact with epidermal growth factor receptors." Proc. Natl. Acad. Sci. USA 77, 5258-5262.
Upchurch, H.F., Conway, E., Patterson, M.K.J. and Maxwell, M.D. (1991) "Localization of cellular transglutaminase on the extracellular matrix after wounding: characteristics of the matrix bound enzyme." J. Cell Physiol. 149, 375-382.
van den Brûle, F.A., Buicu, C., Baldet, M., Sobel, M.E , Cooper, D.N.W., Marshal, P. and Castronovo, V. (1995a) "Galectin-1 modulates human melanoma cell adhesion to laminin." Biochem. Biophys. Res. Comm. 209, 760-767.
van den Brûle, F A , Buicu, C., Sobel, M.E. and Castronovo, V. (1995b) "Galectin-3, a laminin binding protein, fails to modulate adhesion of human melanoma cells to laminm." Neoplasma 42, 215-219.
van den Brûle, F.A., Fernandez, P L., Buicu, C., Liu, F.-T., Jackers, P. Lambotte, R. and Castronovo, V. (1997) "Differential expression of galectin-1 and galectin-3 during first trimester human embryogenesis." Dev. Dynamics 209, 399-405.
Woo, H.J., Shaw, L.M., Messier, J.M. and Mercurio, A.M. (1990) "The major non-integrin laminin binding protein of macrophages is identical to carbohydrate binding protein 35 (Mac-2)." J. Biol. Chem. 265, 7097-7099.
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.