Galectin-3 as a multifunctional protein

• Autorzy: Krzeslak A , Lipinska A.
• Języki publikacji: EN

Abstrakty

EN

Galectin-3 is a 31 kDa member of a growing family of b-galactosidebinding animal lectins. This protein is expressed in a variety of tissues and cell types and is mainly found in the cytoplasm, although, depending on cell type and proliferative state, a significant amount of this lectin can also be detected in the nucleus, on the cell surface or in the extracellular environment. Galectin-3 is secreted from cells by a novel and incompletely understood mechanism that is independent of the classical secretory pathway through the endoplasmic reticulum/Golgi network. Galectin-3 exhibits pleiotropic biological function, playing a key role in many physiological and pathological processes.

Słowa kluczowe

EN

P-type lectin; lectin; galectin; carbohydrate-binding protein; oligosaccharide; cancer progression; C-type lectin; non-classical secretion; multifunctional protein; cell adhesion; ligand; pentraxin; protein; apoptosis

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2004
• Tom: 09
• Numer: 2
• Opis fizyczny: p.305-328,fig.,ref.

Twórcy

autor

Krzeslak A

• University of Lodz, Banacha 12-16, 90-237 Lodz, Poland

autor

Lipinska A.

Bibliografia

• 1. Barondes, S.H., Cooper, D.N.W., Gitt, M.A. and Leffler, H. Galectins. Structure and function of a large family of animal lectins. J. Biol. Chem.. 269(1994)20807-20810.
• 2. Drickamer, K. and Taylor, M.E. Biology of animal lectins. Annu. Rev. Cell Biol. 9 (1993) 237-264.
• 3. Kasai, K. and Hirabayashi, J. Galectins: a family of animal lectins that decipher glycocodes. J. Biochem. 119 (1996) 1-8.
• 4. Hughes, R.C. The galectin family of mammalian carbohydrate-binding molecules. Biochem. Soc. Transact. 25 (1997) 1194-1198.
• 5. Hughes, R.C. Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim. Biophys. Acta 1473 (1999) 172-185.
• 6. Hughes, R.C. Galectins as modulators of cell adhesion. Biochimie 83 (2001) 667-676.
• 7. Rabinovich, G.A., Riera, C.M., Landa, C.A. and Sotomayor, C.E. Galectins: a key intersection between glycobiology and immunology. Brazil. J. Med. Biol. Res. 32 (1999) 383-393.
• 8. Rabinovich, G.A., Baum, L.G., Tinari, N., Paganelli, R., Natoli, C., Liu, FT. and Iacobelli, S. Galectins and their ligands: amplifiers, silencers or tuners of the inflamatory response? Trends Immunol. 23 (2002) 313-320.
• 9. Liu, F.-T., Patterson, R.J. and Wang, J.L. Intracellular functions of galectins. Biochim. Biophys. Acta 1572 (2002) 263-273.
• 10. Perillo, N.L., Marcus, M.E. and Baum, L.G. Galectins: versatile modulators of cell adhesion, cell proliferation, and cell death. J. Mol. Med. 76 (1998) 402-412.
• 11. Wada, J. and Makino, H. Galectins, galactoside-binding mammalian lectins: clinical application of multi-functional proteins. Acta Med. Okayama 55 (2001) 11-17.
• 12. Danguy, A., Camby, I. and Kiss, R. Galectins and cancer. Biochim. Biophys. Acta 1572 (2002) 285-293.
• 13. Moutsatsos, I.K., Wade, M., Schindler, M. and Wang, J.L. Endogenous lectins from cultured cells: nuclear localization of carbohydrate-binding protein 35 in proliferating 3T3 fibroblasts. Proc. Natl. Acad. Sci. USA 84 (1987)6452-6456.
• 14. Hirabayashi, J. and Kasai, K. The family of metazoan metal-independent beta-galactoside-binding lectins: structure, function and molecular evolution. Glycobiology 4 (1993) 297-304.
• 15. Jia, S. and Wang, J.L. Carbohydrate binding protein 35. Complementary DNA sequence reveals homology with proteins of the heterogeneous nuclear RNP. J. Biol. Chem. 263 (1988) 6009-6011.
• 16. Wang, J.L., Laing, J.G. and Anderson, R.L. Lectins in the cell nucleus. Glycobiology 3 (1991) 243-252.
• 17. Hughes, R.C. Mac-2: a versatile galactose-binding protein of mammalian tissues. Glycobiology 4 (1994) 5-12.
• 18. Birdsall, B., Feeney, J., Burdett, I.D.J., Bawumia, S., Barboni, E.A.M. and Hughes, R.C. NMR solution studies of hamster galectin-3 and electron microscopic visualization of surface-adsorbed complexes: evidence for interactions between the N- and C-terminal domains. Biochemistry 40 (2001)4859-4866.
• 19. Huflejt, M.E., Turck, C.W., Lindstedt, R., Barondes, S.H. and Leffler, H. L-29, a soluble lactose-binding lectin, is phosphorylated on serine 6 and serine 12 in vivo and by casein kinase I. J. Biol. Chem. 268 (1993) 2671226718.
• 20. Mazurek, N., Conklin, J., Byrd, J.C., Raz, A. and Bresalier, R.S. Phosphorylation of the ß-galactoside-binding protein galectin-3 modulates binding to its ligands. J. Biol. Chem.. 275 (2000) 36311-36315.
• 21. Menon, R.P. and Hughes, R.C. Determinants in the N-terminal domains of galectin-3 for secretion by a novel pathway circumventing the endoplasmic reticulum-Golgi complex. Eur. J. Biochem. 264 (1999) 569-576.
• 22. Liao, D.I., Kapadia, G., Ahmed, H., Vasta, G.R. and Herzberg, O. Structure of S-lectin, a developmentally regulated vertebrate ß-galactoside-binding protein. Proc. Natl. Acad. Sci. USA 91 (1994) 1428-1432.
• 23. Lobsanov, Y.D., Gitt, M.A., Leffler, H., Barondes, S.H. and Rini, J.M. X-ray crystal structure of the human dimeric s-Lac lectin, L-14-II, in complex with lactose at 2.9 Á resolution. J. Biol. Chem.. 268 (1993) 27034-27038.
• 24. Seetharaman, J., Kanigsberg A., Slaaby, R., Leffler, H., Barondes, S.H. and Rini, J.M. X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-Á resolution. J. Biol. Chem.. 273 (1998) 1304713052.
• 25. Hirabayashi, J., Hashidate, T., Arata, Y., Nishi, N., Nakamura, T., Hirashima, M., Urashima, T., Oka, T., Futai, M., Muller, W.E.G., Yagi, F.
• and Kasai, K. Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim. Biophys. Acta 1572 (2002) 232-254.
• 26. Sato, S., Burdett, I. and Hughes, R.C. Secretion of the baby hamster kidney 30-kDa galactose-binding lectin from polarized and nonpolarized cells: a pathway independent of the endoplasmic reticulum-Golgi complex. Exp. Cell Res. 207 (1993) 8-18.
• 27. Sato, S. and Hughes, R.C. Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J. Biol. Chem.. 269 (1994)4424-4430.
• 28. Nickel, W. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur. J. Biochem. 270 (2003) 2109-2119.
• 29. Mehul, B. and Hughes, R.C. Plasma membrane targeting, vesicular budding and release of galectin 3 from the cytoplasm of mammalian cells during secretion. J. Cell Sci. 110 (1997) 1169-1178.
• 30. Gong, HC., Honjo, Y., Nangia-Makker, P., Hogan, V., Mazurak, N., Bresalier, R.S. and Raz, A. The NH2 terminus of galectin-3 governs cellular compartmentalization and functions in cancer cells. Cancer Res. 59 (1999) 6239-6245.
• 31. Zlatkine, P., Mehul, B. and Magee, A.I. Retargeting of cytosolic proteins to the plasma membrane by the Lck protein tyrosine kinase dual acylation motif. J. Cell Sci. 110 (1997) 673-679.
• 32. Woo, H.-J., Shaw, L.M., Messier, J.M. and Mercurio, A.M. The major non-integrin laminin binding protein of macrophages is identical to carbohydrate binding pro-tein 35 (Mac-2). J. Biol. Chem. 265 (1990) 7097-7099.
• 33. Rosenberg, I., Cherayil, B.J., Isselbacher, K.J. and Pillai, S. Mac-2-binding glycoproteins. Putative ligands for a cytosolic ß-galactoside lectin. J. Biol. Chem. 266 (1991) 18731-18736.
• 34. Koths, K., Taylor, E., Halenbeck, R., Casipit, C. and Wang, A. Cloning and characterization of a human Mac-2-binding protein, a new member of the superfamily defined by the macrophage scavenger receptor cysteine-rich domain. J. Biol. Chem. 268 (1993) 14245-14249.
• 35. Sato, S. and Hughes, R.C. Binding specificity of a baby hamster kidney lectin for H type I and II chains, polylactosamine glycans, and appropriately glycosylated forms of laminin and fibronectin. J. Biol. Chem. 267 (1992) 6983-6990.
• 36. Probstmeier, R., Montag, D. and Schachner, M. Galectin-3, a ß-galactoside-binding animal lectin, binds to neural recognition molecules. J. Neurochem. 64 (1995) 2465-2472.
• 37. Ochieng, J. and Warfield, P. Galectin-3 binding potentials of mouse tumor RHS and human placental laminins. Biochem. Biophys. Res. Commun. 217 (1995)402-406.
• 38. Dong, S. and Hughes, R.C. Macrophage surface glycoproteins binding to galectin-3 (Mac-2-antigen). Glycoconj. J. 14 (1997) 267-274.
• 39. Ochieng, J., Leite-Browning, M.L. and Warfield, P. Regulation of cellular adhesion to extracellular matrix proteins by galectin-3. Biochem. Biophys. Res. Commun. 246 (1998) 788-791.
• 40. Kuwabara, I. and Liu, F.T. Galectin-3 promotes adhesion of human neutrophils to laminin. J. Immunol. 156 (1996) 3939-3944.
• 41. Sarafian, V., Jadot, M., Foidart, J.M., Letesson, J.J., Van den Brule, F., Castronovo, V., Wattiaux, R. and Coninck, S.W. Expression of Lamp-1 and Lamp-2 and their interactions with galectin-3 in human tumor cells. Int. J. Cancer 75 (1998) 105-111.
• 42. Gonen, T., Grey, A.C., Jacobs, M.D., Donaldson, P.J. and Kistler, J. MP20, the second most abundant lens membrane protein and member of the tetraspanin superfamily, joins the list of ligands of galectin-3. BMC Cell Biol. 2 (2001) 17.
• 43. Goletz, S., Hanisch, F.-G. and Karsten, U. Novel aGalNAc containing glycans on cytokeratins are recognized in vitro by galectins with type II carbohydrate recognition domains. J. Cell Sci. 110 (1997) 1585-1596.
• 44. Seve, A.-P., Felin, M., Doyennette-Moyne, M.-A., Sahraoui, T., Aubery, M. and Hubert, J. Evidence for a lactose-mediated association between two nuclear carbohydrate-binding proteins. Glycobiology 3 (1993) 23-30.
• 45. Menon, R.P., Strom, M. and Hughes, R.C. Interaction of a novel cysteine and histidine-rich cytoplasmic protein with galectin-3 in a carbohydrate-independent manner. FEBS Lett. 470 (2000) 227-231.
• 46. Park, J.W., Voss, P.G., Grabski, S., Wang, J.L. and Patterson, R.J. Association of galectin-1 and galectin-3 with Gemin4 in complexes containing the SMN protein. Nucl. Acids Res. 27 (2001) 3595-3602.
• 47. Akahani, S., Nangia-Makker, P., Inohara, H., Kim, H.-R.C. and Raz, A. Galectin-3: a novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res. 57 (1997) 5272-5276.
• 48. Rousseau, C., Muriel, M.-P., Musset, M., Botti, J. and Seve, A.-P. Glycosylated nuclear lectin CBP70 also associated with endoplasmic reticulum and the Golgi apparatus: does the "classic pathway" of glycosylation also apply to nuclear glycoproteins? J. Cell. Biochem. 78 (2000)638-649.
• 49. Bawumia S., Barboni, E.A.M., Menon, R.P. and Hughes, R.C. Specificity of interactions of galectin-3 with Chrp, a cysteine- and histidine-rich cytoplasmic protein. Biochimie 85 (2003) 189-194.
• 50. Vito, P., Pellegrini, L., Guiet, C. and D'Adamio, L. Cloning of AIP1, a novel protein that associates with the apoptosis-linked gene ALG-2 in a Ca2+-dependent reaction. J. Biol. Chem. 274 (1999) 1533-1540.
• 51. Ohannesian, D.W., Lotan, D., Thoman, P., Jessup, J.M., Fukuda, M., Gabius, H.J. and Lotan, R. Carcinoembryonic antigen and other glycoconjugates act as ligands for galectin-3 in human colon carcinoma cells. Cancer Res. 55 (1995) 2191-2199.
• 52. Yang, R.-Y., Hsu, D.K. and Liu, F.-T. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc. Natl. Acad. Sci. USA 93 (1996) 67376742.
• 53. Vlassara, H., Li, Y.M., Imani, F., Wojciechowicz, D., Yang, Z., Liu, F.T., and Cerami, A. Identification of galectin 3 as a high affinity binding protein for advanced glycation end products (AGE): a new member of the AGE-receptor complex. Mol. Med. 1 (1995) 634-646.
• 54. Pricci, F., Leto, G., Amadio, L., Iacobini, C., Romeo, G., Cordone, S., Gradini, R., Barsotti, P., Liu, F.T., Di Mario, U., and Pugliese, G. Role of galectin 3 as a receptor for advanced glycosylation end products. Kidney Int. 58 (2000) S31-S39.
• 55. Zhu, W., Sano, H., Nagai, R., Fukuhara, K., Miyazaki, A., and Horiuchi, S. The role of galectin-3 in endocytosis of advanced glycation end products and modified low density lipoproteins. Biochem. Biophys. Res. Commun. 280 (2001) 1183-1188.
• 56. Matarrese, P., Tinari, N., Semeraro, M.L., Natoli, C., Iacobelli, S. and Malorni, W. Galectin-3 overexpression protects from cell damage and death by influencing mitochondrial homeostasis. FEBS Lett. 473 (2000) 311-315.
• 57. Matarrese, P., Fusco, O., Tinari, N., Natoli, C., Liu F.-T., Semeraro, M.L., Malorni, W. and Iacobelli, S. Galectin-3 overexpression protects from apoptosis by improving cell adhesion properties. Int. J. Cancer 85. (2000) 545-554.
• 58. Moon, B.-K., Lee, Y.J., Battle, P., Jessup, J.M., Raz, A. and Kim, H.-R.C. Galectin-3 protects human breast carcinoma cells against nitric oxide-induced apoptosis. Implication of galectin-3 function during metastasis. Am. J. Pathol. 159 (2001) 1055-1060.
• 59. Hanada M., Aimé-Sempé C., Sato, T. and Reed, J.C. Structure-function analysis of Bcl-2 protein. J. Biol. Chem.. 270 (1995) 11962-11969.
• 60. Nagata, S. Apoptosis. Fibrinolysis & Proteolysis 14 (2000) 82-86.
• 61. Zörnig, M., Hueber, A.-O., Baum, W. and Evan, G. Apoptosis regulators and their role in tumorigenesis. Biochim. Biophys. Acta 1551 (2001) F1-F37.
• 62. Yu, F., Finley, R.L., Jr., Raz, A. and Kim, H.-R.C. Galectin-3 translocates to the perinuclear membranes and inhibits cytochrome c release from the mitochondria. A role for synexin in galectin-3 translocation. J. Biol. Chem.. 277 (2002) 15819-15827.
• 63. Kim, H.-R.C., Lin, H.-M., Biliran, H. and Raz, A. Cell cycle arrest and inhibition of anoikis by galectin-3 in human breast epithelial cells. Cancer Res. 59 (1999) 4148-4154.
• 64. Lin, H.-M., Moon, B.-K., Yu, F. and Kim, H.-R.C. Galectin-3 mediates genistein--induced G2/M arrest and inhibits apoptosis. Carcinogenesis 21 (2000)1941-1945.
• 65. Wang, L., Inohara, H., Pienta, K.J. and Raz, A. Galectin-3 is a nuclear matrix protein which binds RNA. Biochem. Biophys. Res. Commun. 217 (1995) 292-303.
• 66. Dagher, S.F., Wang, J.L. and Patterson, R.J. Identification of galectin-3 as a factor in pre-mRNA splicing. Proc. Natl. Acad. Sci. USA 92 (1995) 1213-1217.
• 67. Lin, H.-M., Pestell, R.G., Raz, A. and Kim, H.-R.C. Galectin-3 enhances cyclin Di promoter activity through SP1 and a cAMP-responsive element in human breast epithelial cells. Oncogene 21 (2002) 8001-8010.
• 68. Yoshii, T., Fukumori, T., Honjo, Y., Inohara, H., Kim, H.-R.C. and Raz, A. Galectin-3 phosphorylation is required for its anti-apoptotic function and cell cycle arrest. J. Biol. Chem. 277 (2002) 6852-6857.
• 69. Xu, X.-C., El-Naggar, A.K. and Lotan, R. Differential expression of galectin-1 and galectin-3 in thyroid tumors. Potential diagnostic implications. Am. J. Pathol. 147 (1995) 815-822.
• 70. Fernandez, P.L., Merino, M.J., Gómez M., Campo, E., Medina, T., Castronovo, V., Sanjuán, X., Cardesa, A., Liu, F.-T. and Sobel, M.E. Galectin-3 and laminin expression in neoplastic and non-neoplastic thyroid tissue. J. Pathol. 181 (1997) 80-86.
• 71. Orlandi, F., Saggiorato, E., Pivano, G., Puligheddu, B., Termine, A., Cappia, S., De Giuli, P. and Angeli, A. Galectin-3 is a presurgical marker of human thyroid carcinoma. Cancer Res. 58 (1998) 3015-3020.
• 72. Inohara, H., Honjo, Y., Yoshii, T., Akahani, S., Yoshida, J., Hattori, K., Okamoto, S., Sawada, T., Raz, A. and Kubo, T. Expression of galectin-3 in fine-needle aspirates as a diagnostic marker differentiating benign from malignant thyroid neoplasms. Cancer 85 (1999) 2475-2484.
• 73. Cvejic, D., Savin, S., Golubovic, S., Paunovic, I., Tatic, S. and Havelka, M. Galectin-3 and carcinoembryonic antigen expression in medullary thyroid carcinoma: possible relation to tumour progression. Histopathology 37 (2000)530-535.
• 74. Kawachi, K., Matsushita, Y., Yonezawa, S., Nakano, S., Shirao, K., Natsugoe, S., Sueyoshi, K., Aikou, T. and Sato, E. Galectin-3 expression in various thyroid neoplasms and its possible role in metastasis formation. Human Pathol. 31 (2000) 428-433.
• 75. Yoshii, T., Inohara, H., Takenaka, Y., Honjo, Y., Akahani, S., Nomura, T., Raz, A. and Kubo, T. Galectin-3 maintains the transformed phenotype of thyroid papillary carcinoma cells. Int. J. Oncol. 18 (2001) 787-792.
• 76. Saggiorato, E., Cappia, S., De Gliuli, P., Mussa, A., Pancani, G., Caraci, P., Angeli, A. and Orlandi, F. Galectin-3 as a presurgical immuno-cytodiagnostic marker of minimally invasive follicular thyroid carcinoma. J. Clin. Endocrinol. Metab. 86 (2001) 5152-5158.
• 77. Coli, A., Bigotti, G., Zuchetti, F., Negro, F. and Massi, G. Galectin-3, a marker of well-differentiated thyroid carcinoma, is expressed in thyroid nodules with cytological atypia. Histopathology 40 (2002) 80-87.
• 78. Faggiano, A., Talbot, M., Lacroix, L., Bidart, J.M., Baudin, E., Schlumberger, M. and Caillou, B. Differential expression of galectin-3 in medullary thyroid carcinoma and C-cell hyperplasia. Clin. Endocrinol. 57 (2002)813-819.
• 79. Herrmann, M.E., LiVolsi, V.A., Pasha, T.L., Roberts, S.A., Wojcik, E.M. and Baloch, Z.W. Immunohistochemical expression of galectin-3 in benign and malignant thyroid lesions. Arch. Pathol. Lab. Med. 126 (2002) 710713.
• 80. Takenaka, Y., Inohara, H., Yoshii, T., Oshima, K., Nakahara, S., Akahani, S., Honjo, Y., Yamamoto, Y., Raz, A. and Kubo, T. Malignant transformation of thyroid follicular cells by galectin-3. Cancer Lett. 195 (2003) 111-119.
• 81. Berberat, P.O., Friess, H., Wang, L., Zhu, Z., Bley, T., Frigeri, L., Zimmermann, A., and Büchler, M.W. Comparative analysis of galectins in primary tumors and tumor metastasis in human pancreatic cancer. J. Histochem. Cytochem. 49 (2001) 539-549.
• 82. Hsu, D.K., Dowling, C.A., Jeng, K.-C.G., Chen, J.-T., Yang, R.-Y. and Liu, F.-T. Galectin-3 expression is induced in cirrhotic liver and hepatocellular carcinoma. Int. J. Cancer 81 (1999) 519-526.
• 83. Castronovo, V., Campo, E., van den Brůle, F.A., Claysmith, A.P., Cioce, V., Liu, F.-T., Fernandez, P.L. and Sobel, M.E. Inverse modulation of steady-state messenger RNA levels of two non-integrin laminin-binding proteins in human colon carcinoma. J. Natl. Cancer Inst. 84 (1992) 11611169.
• 84. Lotz, M.M., Andrews, C.W. Jr., Korzelius, C.A., Lee, E.C., Steele, G.D. Jr., Clarke, A. and Mercurio, A.M. 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 (1993) 3466-3470.
• 85. Irimura, T., Matsushita, Y., Sutton, R.C., Carralero, D., Ohannesian, D.W., Cleary, K.R., Ota, D.M., Nicolson, G.L. and Lotan, R. Increased content of a endogenous lactose-binding lectin in human colorectal carcinoma progressed to metastatic stages. Cancer Res. 51 (1991) 387-393.
• 86. Schoeppner, H.L., Raz, A., Ho, S.B. and Bresalier, R.S. Expression of an endogenous galactose-binding lectin correlates with neoplastic progression in the colon. Cancer 75 (1995) 2818-2826.
• 87. Sanjuán, X., Fernandez, P.L., Castells, A., Castronovo, V., van der Brule, F., Liu, F.-T., Cardesa, A. and Campo, E. Differential expression of galectin 3 and galectin 1 in colorectal cancer progression. Gastroenterology 113 (1997) 1906-1915.
• 88. Nagy, N., Legendre, H., Engels, O., André, S., Kaltner, H., Wasano, K., Zick, Y., Pector, J.-C., Decaestecker, C., Gabius, H.-J., Salmon, I. and Kiss, R. Refined prognostic evaluation in colon carcinoma using immunohistochemical galectin finger-printing. Cancer 97 (2003) 18491858.
• 89. Bresalier, R.S., Mazurek, N., Sternberg, L.R., Byrd, J.C., Yunker, C.K., Nangia--Makker, P. and Raz, A. Metastasis of human colon cancer is altered by modifying expression of the ß-galactoside-binding protein galectin 3. Gastroenterology 115 (1998) 287-296.
• 90. Dudas, S.P., Yunker, C.K., Sternberg, L.R., Byrd, J.C. and Bresalier, R.S. Expression of human intestinal mucin is modulated by the ß-galactoside binding protein galectin-3 in colon cancer. Gastroenterology 123 (2002) 817-826.
• 91. Castronovo, V., Van Den Brůle, F.A., Jackers, P., Clusse, N., Liu, F.T., Gillet, C. and Sobel, M.E. Decreased expression of galectin-3 is associated with progression of human breast cancer. J. Pathol. 179 (1996) 43-48.
• 92. Idikio, H. Galectin-3 expression in human breast carcinoma: correlation with cancer histologic grade. Int. J. Oncol. 12 (1998) 1287-1290.
• 93. Honjo, Y., Nangia-Makker, P., Inohara, H. and Raz, A. Down-regulation of galectin-3 suppresses tumorigenecity of human breast carcinoma cells. Clin. Cancer Res. 7 (2001) 661-668.
• 94. Song, Y.K., Billiar, T.R. and Lee, Y.J. Role of galectin-3 in breast cancer metastasis. Involvement of nitric oxide. Am. J. Pathol. 160 (2002) 10691075.
• 95. Ellerhorst, J., Troncoso, P., Xu, X.C., Lee, J. and Lotan, R. Galectin-1 and galectin-3 expression in human prostate tissue and prostate cancer. Urol. Res. 27 (1999)362-367.
• 96. Pacis, R A., Pilat, M.J., Pienta, K.J., Wojno, K., Raz, A., Hogan, V. and Cooper, C.R. Decreased galectin-3 expression in prostate cancer. Prostate 44 (2000) 118-123.
• 97. Van den Brůle, F.A., Waltregny, D., Liu, F.-T. and Castronovo, V. Alteration of the cytoplasmic/nuclear expression pattern of galectin-3 correlates with prostate carcinoma progression. Int. J. Cancer 89 (2000) 361-367.
• 98. Choufani, G., Nagy, N., Saussez, S., Marchant, H., Bisschop, P., Burchert, M., Danguy, A., Louryan, S., Salmon, I., Gabius, H.-J., Kiss, R. and Hassid, S. The levels of expression of galectin-1, galectin-3, and the Thomsen-Friedenreich antigen and their binding sites decrease as clinical aggressiveness increases in head and neck cancers. Cancer 86 (1999) 2353-2363.
• 99. Delorge, S., Saussez, S., Pelc, P., Devroede, B., Marchant, H., Burchert, M., Zeng, F.Y., Danguy, A., Salmon, I., Gabius, H.J., Kiss, R. and Hassid, S. Correlation of galectin-3/galectin-3-binding sites with low differentiatio status in head and neck squamous cell carcinomas. Otolaryngol. Head Neck Surg. 122 (2000) 834-841.
• 100. Lefranc, F., Chevalier, C., Vinchon, M., Dhellemmes, P., Schüring, M.-P., Kaltner, H., Brotchi, J., Ruchoux, M.-M., Gabius, H.-J., Salmon, I. and Kiss, R. Characterization of the levels of expression of retinoic acid receptors, galectin-3, macrophage migration inhibiting factor, and p53 in 51 adamantinomatous craniopharyngiomas. J. Neurosurg. 98 (2003) 145153.
• 101. Sheikholeslam-Zadeh, R., Decaestecker, C., Delbrouck, C., Danguy, A., Salmon, I., Zick, Y., Kaltner, H., Hassid, S., Gabius, H.-J., Kiss, R. and Choufani, G. The levels of expression of galectin-3, but not of galectin-1 and galectin-8, correlate with apoptosis in human cholesteatomas. Laryngoscope 111 (2001) 1042-1047.
• 102. Honjo, Y., Inohara, H., Akahani, S., Yoshii, T., Takenaka, Y., Yoshida, J., Hattori, K., Tomiyama, Y., Raz, A. and Kubo, T. Expression of cytoplasmic galectin-3 as a prognostic marker in tongue carcinoma. Clin. Cancer Res. 6 (2000) 4635-4640.
• 103. Bresalier, R.S., Yan, P.-S., Byrd, J.C., Lotan, R. and Raz, A. Expression of the endogenous galactose-binding protein galectin-3 correlates with the malignant potential of tumors in the central nervous system. Cancer 80 (1997) 776-787.
• 104. Gordower, L., Decaestecker, C., Kacem, Y., Lemmers, A., Gusman, J., Burchert, M., Danguy, A., Gabius, H., Salmon, I., Kiss, R. and Camby, I. Galectin-3 and galectin-3-binding site expression in human adult astrocytic tumours and related angiogenesis. Neuropathol. Appl. Neurobiol. 25 (1999) 319-330.
• 105. Camby, I., Belot, N., Rorive, S., Lefranc, F., Maurage, C.-A., Lahm, H., Kaltner, H., Hadari, Y., Ruchoux, M.-M., Brotchi, J., Zick, Y., Salmon, I., Gabius, H.-J. and Kiss, R. Galectins are differentially expressed in supratentorial pilocytic astrocytomas, astrocytomas, anaplastic astrocytomas and glioblastomas, and significantly modulate tumor astrocytes migration. Brain Pathol. 11 (2001) 12-26.