Expression of Galectins in Cancer: A Critical Review

[en] A large body of literature has examined and described galectin expression in cancer. Discrepancies have been observed in the reported data, which hampered clear understanding of the expression profiles. This relates to the use of different types of methods that evaluate either global or specific gene expression in heterogeneous cancer tissue samples, type of antibodies used in immunohistochemistry and procedures of comparison of gene expression. In this manuscript, we review the main data concerning expression of galectins in human cancer. Only galectin-1 and galectin-3, the most abundant and examined galectins, will be examined here.

Disciplines :

Oncology
Biochemistry, biophysics & molecular biology

Author, co-author :

van den Brule, Frédéric; Université de Liège - ULiège > Laboratoire de Recherche sur les métastases

Califice, Stéphane; Université de Liège - ULiège > Laboratoire de Recherche sur les Métastases

Castronovo, Vincenzo ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie générale et cellulaire - GIGA-R : Labo de recherche sur les métastases

Language :

English

Title :

Expression of Galectins in Cancer: A Critical Review

Publication date :

2004

Journal title :

Glycoconjugate Journal

ISSN :

0282-0080

eISSN :

1573-4986

Publisher :

Kluwer Academic Publishers, Netherlands

Volume :

Issue :

7-9

Pages :

537-42

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Fonds Léon Fredericq [BE]

Available on ORBi :

since 28 September 2009

Statistics

Number of views

62 (2 by ULiège)

Number of downloads

1 (0 by ULiège)

More statistics

Scopus citations^®

173

Scopus citations^®
without self-citations

172

OpenCitations

126

Bibliography

Castronovo V, van den Brûle FA, Jackers P, Clausse N, Liu FT, Gillet C, Sobel ME, Decreased expression of galectin-3 is associated with progression of human breast cancer, J Pathol 179, 43-8 (1996).
van den Brûle FA, Buicu C, Berchuck A, Bast RC, Deprez M, Liu FT, Cooper DN, Pieters C, Sobel ME, Castronovo V, Expression of the 67-kD laminin receptor, galectin-1, and galectin-3 in advanced human uterine adenocarcinoma, Hum Pathol 27, 1185-91 (1996).
Sanjuan X, Fernandez PL, Castells A, Castronovo V, van den Brule F, Liu FT, Cardesa A, Campo E, Differential expression of galectin 3 and galectin 1 in colorectal cancer progression, Gastroenterology 113, 1906-15 (1997).
van den Brûle FA, Waltregny D, Liu FT, Castronovo V, Alteration of the cytoplasmic/nuclear expression pattern of galectin-3 correlates with prostate carcinoma progression, Int J Cancer 89, 361-7 (2000).
van den Brûle FA, Waltregny D, Castronovo V, Increased expression of galectin-1 in carcinoma-associated stroma predicts poor outcome in prostate carcinoma patients, J Pathol 193, 80-7 (2001).
Gabius HJ, Brehler R, Schauer A, Cramer F, Localization of endogenous lectins in human breast, benign breast lesions and mammary carcinomas, Virchows Arch (Cell Pathol) 52, 107-15 (1986).
Irimura T, Matsushita Y, Sutton RC, Carralero D, Ohannesian DW, Cleary KR, Ota DM, Nicolson GL, Lotan R, Increased content of an endogenous lactose-binding lectin in human colorectal carcinoma progressed to metastatic stages, Cancer Res 51, 387-93 (1991).
Lotan R, Matsushita Y, Ohannesian D, Carralero D, Ota DM, Cleary KR, Nicolson GL, Irimura T, Lactose-binding lectin expression in human colorectal carcinomas. Relation to tumor progression, Carbohydr Res 213, 47-57 (1991).
Gillenwater A, Xu XC, el-Naggar AK, Clayman GL, Lotan R, Expression of galectins in head and neck squamous cell carcinoma, Head Neck 18, 422-32 (1996).
Allen HJ, Sucato D, Woynarowska B, Gottstine S, Sharma A, Bernacki RJ, Role of galaptin in ovarian carcinoma adhesion to extracellular matrix in vitro, J Cell Biochem 43, 43-57 (1990).
Allen HJ, Sucato D, Gottstine S, Kisailus E, Nava H, Petrelli N, Castillo N, Wilson D, Localization of endogenous beta-galactoside-binding lectin in human cells and tissues, Tumor Biol 12, 52-60 (1991).
Cindolo L, Benvenuto G, Salvatore P, Pero R, Salvatore G, Mirone V, Prezioso D, Altieri V, Bruni CB, Chiariotti L, Galectin-1 and galectin-3 expression in human bladder transitional-cell carcinomas, Int J Cancer 84, 39-43 (1999).
Yamaoka K, Mishima K, Nagashima Y, Asai A, Sanai Y, Kirino T, Expression of galectin-1 mRNA correlates with the malignant potential of human gliomas and expression of antisense galectin-1 inhibits the growth of 9 glioma cells, J Neurosci Res 59, 722-30 (2000).
Chiariotti L, Berlingieri MT, De Rosa P, Battaglia C, Berger N, Bruni CB, Fusco A, Increased expression of the negative growth factor, galactoside-binding protein, gene in transformed thyroid cells and in human thyroid carcinomas, Oncogene 7, 2507-11 (1992).
Chiariotti L, Berlingieri MT, Battaglia C, Benvenuto G, Martelli ML, Salvatore P, Chiappetta G, Bruni CB, Fusco A, Expression of galectin-1 in normal human thyroid gland and in differentiated and poorly differentiated thyroid tumors, Int J Cancer 64, 171-5 (1995).
Xu XC, el-Naggar AK, Lotan R, Differential expression of galectin-1 and galectin-3 in thyroid tumors. Potential diagnostic implications, Am J Pathol 147, 815-22 (1995).
Rorive S, Belot N, Decaestecker C, Lefranc F, Gordower L, Micik S, Maurage CA, Kaltner H, Ruchoux MM, Danguy A, Gabius HJ, Salmon I, Kiss R, Camby I, Galectin-1 is highly expressed in human gliomas with relevance for modulation of invasion of tumor astrocytes into the brain parenchyma, Glia 33, 241-55 (2001).
Choufani G, Nagy N, Saussez S, Marchant H, Bisschop P, Burchert M, Danguy A, Louryan S, Salmon I, Gabius HJ, Kiss R, 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, 2353-63 (1999).
Berberat PO, Friess H, Wang L, Zhu Z, Bley T, Frigeri L, Zimmermann A, Buchler MW, Comparative analysis of galectins in primary tumors and tumor metastasis in human pancreatic cancer, J Histochem Cytochem 49, 539-49 (2001).
Shimonishi T, Miyazaki K, Kono N, Sabit H, Tuneyama K, Harada K, Hirabayashi J, Kasai K, Nakanuma Y, Expression of endogenous galectin-1 and galectin-3 in intrahepatic cholangiocarcinoma, Hum Pathol 32, 302-10 (2001).
Ellerhorst J, Troncoso P, Xu XC, Lee J, Lotan R, Galectin-1 and galectin-3 expression in human prostate tissue and prostate cancer, Urol Res 27, 362-7 (1999).
van den Brûle F, Clausse N, Waltregny D, Garnier F, Castronovo V, Increased frequency of galectin-1 expression in prostatic tumor-associated capillary endothelial cells: Possible induction by prostate carcinoma cells, Angiogenesis 3, 317-25 (1999).
Perillo NL, Pace KE, Seilhamer JJ, Baum LG, Apoptosis of T cells mediated by galectin-1, Nature 378, 736-9 (1995).
Raz A, Avivi A, Pazerini G, Carmi P, Cloning and expression of cDNA for two endogenous UV-2237 fibrosarcoma lectin genes, Exp Cell Res 173, 109-16 (1987).
Raz A, Meromsky L, Zvibel I, Lotan R, Transformation-related changes in the expression of endogenous cell lectins, Int J Cancer 39, 353-60 (1987).
Raz A, Carmi P, Pazerini G, Expression of two different endogenous galactoside-binding lectins sharing sequence homology, Cancer Res 48, 645-9 (1988).
Lotan R, Ito H, Yasui W, Yokozaki H, Lotan D, Tahara E, Expression of a 31-kDa lactoside-binding lectin in normal human gastric mucosa and in primary and metastatic gastric carcinomas, Int J Cancer 56, 474-80 (1994).
Ho MK, Springer TA, Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies, J Immunol 128, 1221-8 (1982).
Cvejic D, Savin S, Paunovic I, Tatic S, Havelka M, Sinadinovic J, Immunohistochemical localization of galectin-3 in malignant and benign human thyroid tissue, Anticancer Res 18, 2637-42 (1998).
Orlandi F, Saggiorato E, Pivano G, Puligheddu B, Termine A, Cappia S, De Giuli P, Angeli A, Galectin-3 is a presurgical marker of human thyroid carcinoma, Cancer Res 58, 3015-20 (1998).
Gasbarri A, Martegani MP, Del Prete F, Lucante T, Natali PG, Bartolazzi A, Galectin-3 and CD44v6 isoforms in the preoperative evaluation of thyroid nodules, J Clin Oncol 17, 3494-502 (1999).
Inohara H, Honjo Y, Yoshii T, Akahani S, Yoshida J, Hattori K, Okamoto S, Sawada T, Raz A, Kubo T, Expression of galectin-3 in fine-needle aspirates as a diagnostic marker differentiating benign from malignant thyroid neoplasms, Cancer 85, 2475-84 (1999).
Cvejic D, Savin S, Golubovic S, Paunovic I, Tatic S, Havelka M, Galectin-3 and carcinoembryonic antigen expression in medullary thyroid carcinoma: Possible relation to tumour progression, Histopathology 37, 530-5 (2000).
Bartolazzi A, Gasbarri A, Papotti M, Bussolati G, Lucante T, Khan A, Inohara H, Marandino F, Orlandi F, Nardi F, Vecchione A, Tecce R, Larsson O, Application of an immunodiagnostic method for improving preoperative diagnosis of nodular thyroid lesions, Lancet 357, 1644-50 (2001).
Saggiorato E, Cappia S, De Giuli P, Mussa A, Pancani G, Caraci P, Angeli A, Orlandi F, Galectin-3 as a presurgical immunocytodiagnostic marker of minimally invasive follicular thyroid carcinoma, J Clin Endocrinol Metab 86, 5152-8515 (2001).
Bresalier RS, Yan P-S, Byrd JC, Lotan R, 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, 776-87 (1997).
Schaffert C, Pour PM, Chaney WG, Localization of galectin-3 in normal and diseased pancreatic tissue, Int J Pancreatol 23, 1-9 (1998).
Baldus SE, Zirbes TK, Weingarten M, Fromm S, Glossmann J, Hanisch FG, Monig SP, Schroder W, Flucke U, Thiele J, Holscher AH, Dienes HP, Increased galectin-3 expression in gastric cancer: Correlations with histopathological subtypes, galactosylated antigens and tumor cell proliferation, Tumour Biol 21, 258-66 (2000).
Young AN, Amin MB, Moreno CS, Lim SD, Cohen C, Petros JA, Marshall FF, Neish AS, Expression profiling of renal epithelial neoplasms: A method for tumor classification and discovery of diagnostic molecular markers, Am J Pathol 158, 1639-51 (2001).
Schoeppner HL, Raz A, Ho SB, Bresalier RS, Expression of an endogenous galactose-binding lectin correlates with neoplastic progression in the colon, Cancer 75, 2818-26 (1995).
Nakamura M, Inufusa H, Adachi T, Aga M, Kurimoto M, Nakatani Y, Wakano T, Nakajima A, Hida JI, Miyake M, Shindo K, Yasutomi M, Involvement of galectin-3 expression in colorectal cancer progression and metastasis, Int J Oncol 15, 143-8 (1999).
Hsu DK, Dowling CA, Jeng K-CG, Chen J-T, Yang R-Y, Liu F-T, Galectin-3 expression is induced in cirrhotic liver and hepatocellular carcinoma, Int J Cancer 81, 519-26 (1999).
Frigeri LG, Liu FT, Surface expression of functional IgE binding protein, an endogenous lectin, on mast cells and macrophages, J Immunol 148, 861-7 (1992).
Castronovo V, Campo E, van den Brûle FA, Claysmith AP, Cioce V, Liu FT, Fernandez PL, Sobel ME, Inverse modulation of steady-state messenger RNA levels of two non-integrin laminin-binding proteins in human colon carcinoma, J Natl Cancer Inst 84, 1161-9 (1992).
van den Brûle FA, Berchuck A, Bast RC, Liu FT, Gillet C, Sobel ME, Castronovo V, Differential expression of the 67-kD laminin receptor and 31-kD human laminin-binding protein inhuman ovarian carcinomas, Eur J Cancer 30A, 1096-9 (1994).
Castronovo V, Liu FT, van den Brûle FA, Decreased expression of galectin-3 in basal cell carcinoma of the skin, Int J Oncology 15, 67-70 (1999).
Konstantinov KN, Shames B, Izuno G, Liu FT, Expression of epsilon BP, a beta-galactoside-binding soluble lectin, in normal and neoplastic epidermis, Exp Dermatol 3, 9-16 (1994).
Pacis RA, Pilat MJ, Pienta KJ, Wojno K, Raz A, Hogan V, Cooper CR, Decreased galectin-3 expression in prostate cancer, Prostate 44, 118-23 (2000).
Lotz MM, Andrews CWJ, Korzelius CA, Lee EC, Steele GDJ, Clarcke A, Mercurio AM, 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, 3466-70 (1993).
Xu XC, Sola Gallego JJ, Lotan R, El-Naggar AK, Differential expression of galectin-1 and galectin-3 in benign and malignant salivary gland neoplasms, Int J Oncol 17, 271-6 (2000).
Fernandez PL, Merino MJ, Gomez M, Campo E, Medina T, Castronovo V, Sanjuan X, Cardesa A, Liu FT, Sobel ME, Galectin-3 and laminin expression in neoplastic and non-neoplastic thyroid tissue, J Pathol 181, 80-6 (1997).
Gordower L, Decaestecker C, Kacem Y, Lemmers A, Gusman J, Burchert M, Danguy A, Gabius H, Salmon I, Kiss R, Camby I, Galectin-3 and galectin-3-binding site expression in human adult astrocytic tumours and related angiogenesis, Neuropathol Appl Neurobiol 25, 319-30 (1999).
Gaffney RL, Carney JA, Sebo TJ, Erickson LA, Volante M, Papotti M, Lloyd RV, Galectin-3 expression in hyalinizing trabecular tumors of the thyroid gland, Am J Surg Pathol 27, 494-8 (2003).
Faggiano A, Talbot M, Lacroix L, Bidart JM, Baudin E, Schlumberger M, Caillou B, Differential expression of galectin-3 in medullary thyroid carcinoma and C-cell hyperplasia, Clin Endocrinol (Oxf) 57, 813-9 (2002).
Niedobitek C, Niedobitek F, Lindenberg G, Bachler B, Neudeck H, Zuschneid W, Hopfenmuller W, [Expression of galectin-3 in thyroid gland and follicular cell tumors of the thyroid. A critical study of its possible role in preoperative differential diagnosis], Pathologe 22, 205-13 (2001).
Kawachi K, Matsushita Y, Yonezawa S, Nakano S, Shirao K, Natsugoe S, Sueyoshi K, Aikou T, Sato E, Galectin-3 expression in various thyroid neoplasms and its possible role in metastasis formation, Hum Pathol 31, 428-33 (2000).
Medeiros-Neto G, Nascimento MC, Bisi H, Alves VA, Longatto-Filho A, Kanamura CT, Differential reactivity for Galectin-3 in hurthle cell adenomas and carcinomas, Endocr Pathol 12, 275-9 (2001).
Nascimento MC, Bisi H, Alves VA, Longatto-Filho A, Kanamura CT, Medeiros-Neto G, Differential reactivity for galectin-3 in Hurthle cell adenomas and carcinomas, Endocr Pathol 12, 275-9 (2001).
Terris B, Blaveri E, Crnogorac-Jurcevic T, Jones M, Missiaglia E, Ruszniewski P, Sauvanet A, Lemoine NR, Characterization of gene expression profiles in intraductal papillary- mucinous tumors of the pancreas, Am J Pathol 160, 1745-54 (2002).
Coli A, Bigotti G, Zucchetti F, Negro F, Massi G, Galectin-3, a marker of well-differentiated thyroid carcinoma, is expressed in thyroid nodules with cytological atypia, Histopathology 40, 80-7 (2002).
Herrmann ME, LiVolsi VA, Pasha TL, Roberts SA, Wojcik EM, Baloch ZW, Immunohistochemical expression of galectin-3 in benign and malignant thyroid lesions, Arch Pathol Lab Med 126, 710-3 (2002).
Papotti M, Volante M, Saggiorato E, Deandreis D, Veltri A, Orlandi F, Role of galectin-3 immunodetection in the cytological diagnosis of thyroid cystic papillary carcinoma, Eur J Endocrinol 147, 515-21 (2002).
Aratake Y, Umeki K, Kiyoyama K, Hinoura Y, Sato S, Ohno A, Kuribayashi T, Hirai K, Nabeshima K, Kotani T, Diagnostic utility of galectin-3 and CD26/ DPPIV as preoperative diagnostic markers for thyroid nodules, Diagn Cytopathol 26, 366-72 (2002).
Beesley MF, McLaren KM, Cytokeratin 19 and galectin-3 immunohistochemistry in the differential diagnosis of solitary thyroid nodules, Histopathology 41, 236-43 (2002).
Chen Y, Zhu M, Zhou X, Lin W, Ni C, Li F, Zhang S, Gong Z, [Expression of TTF-1 in thyroid tumors originating from follicular epithelium and its correlation with expression of RET, Galectin-3 and Mucin-1 genes], Zhonghua Yi Xue Za Zhi 82, 257-61 (2002).
Bernet VJ, Anderson J, Vaishnav Y, Solomon B, Adair CF, Saji M, Burman KD, Burch HB, Ringel MD, Determination of galectin-3 messenger ribonucleic Acid overexpression in papillary thyroid cancer by quantitative reverse transcription- polymerase chain reaction, J Clin Endocrinol Metab 87, 4792-6 (2002).
Martins L, Matsuo SE, Ebina KN, Kulcsar MA, Friguglietti CU, Kimura ET, Galectin-3 messenger ribonucleic acid and protein are expressed in benign thyroid tumors, J Clin Endocrinol Metab 87, 4806-10 (2002).
Niedziela M, Maceluch J, Korman E, Galectin-3 is not an universal marker of malignancy in thyroid nodular disease in children and adolescents, J Clin Endocrinol Metab 87, 4411-5 (2002).
Casey MB, Lohse CM, Lloyd RV, Distinction between papillary thyroid hyperplasia and papillary thyroid carcinoma by immunohistochemical staining for cytokeratin 19, galectin-3, and HBME-1, Endocr Pathol 14, 55-60 (2003).
Raphael SJ, The meanings of markers: Ancillary techniques in diagnosis of thyroid neoplasia, Endocr Pathol 13, 301-11 (2002).
Bartolazzi A, Papotti M, Orlandi F, Methodological considerations regarding the use of galectin-3 expression analysis in preoperative evaluation of thyroid nodules, J Clin Endocrinol Metab 88, 950; author reply 950-1 (2003).
Moutsatsos IK, Davis JM, Wang JL, Endogenous lectins from cultured cells: Subcellular localization of carbohydrate-binding protein 35 in 3T3 fibroblasts, J Cell Biol 102, 477-83 (1986).
Moutsatsos IK, Wade M, Schindler M, Wang JL, Endogenous lectins from cultured cells: Nuclear localization of carbohydrate-binding protein 35 in proliferating 3T3 fibroblasts, Proc Natl Acad Sci USA 4, 6452-6 (1987).
Agrwal N, Sun Q, Wang SY, Wang JL, Carbohydrate-binding protein 35.I. Properties of the recombinant polypeptide and the individuality of the domains, J Biol Chem 268, 14932-9 (1993).
Agrwal N, Wang JL, Voss PG, Carbohydrate-binding protein 35. Levels of transcription and mRNA accumulation in quiescent and proliferating cells, J Biol Chem 264, 17236-42 (1989).
Cowles EA, Agrwal N, Anderson RL, Wang JL, Carbohydrate-binding protein 35. Isoelectric points of the polypeptide and a phosphorylated derivative, J Biol Chem 265, 17706-12 (1990).
Laing JG, Wang JL, Identification of Carbohydrate Binding protein 35 in heterologous nuclear ribonucleoprotein complex, Biochemistry 27, 5329-34 (1998).
Wang L, Inohara H, Pienta KJ, Raz A, Galectin-3 is a nuclear matrix protein which binds RNA, Biochem Biophys Res Commun 217, 292-303 (1995).
Dagher SF, Wang JL, Patterson RJ, Identification of galectin-3 as a factor in pre-mRNA splicing, Proc Natl Acad Sci USA 92, 1213-17 (1995).
Honjo Y, Inohara H, Akahani S, Yoshii T, Takenaka Y, Yoshida J, Hattori K, Tomiyama Y, Raz A, Kubo T, Expression of cytoplasmic galectin-3 as a prognostic marker in tongue carcinoma, Clin Cancer Res 6, 4635-40 (2000).