Galectin-1 accumulation in the ovary carcinoma peritumoral stroma is induced by ovary carcinoma cells and affects both cancer cell proliferation and adhesion to laminin-1 and fibronectin

van den Brule, Frédéric; Califice, Stéphane; Garnier, Frédérique; Fernandez, Pedro L; Berchuck, Andrew; Castronovo, Vincenzo

doi:10.1097/01.LAB.0000059949.01480.40

Article (Scientific journals)

Galectin-1 accumulation in the ovary carcinoma peritumoral stroma is induced by ovary carcinoma cells and affects both cancer cell proliferation and adhesion to laminin-1 and fibronectin

van den Brule, Frédéric; Califice, Stéphane; Garnier, Frédérique et al.

2003 • In Laboratory Investigation, 83 (3), p. 377-386

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/24077

DOI
10.1097/01.LAB.0000059949.01480.40

PubMed
12649338

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

VAN DEN BRULE LAB INVEST 2003.pdf

Publisher postprint (848.85 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Abstract :

[en] Galectin-1 (gal-1) is a 14-kDa laminin-binding galectin involved in several biologic events including regulation of cancer cell proliferation and adhesion to the matrix. In this study, we examined gal-1 expression in 30 human epithelial ovary carcinoma samples by Western and Northern blotting and by immunohistochemistry. Gal-1 mRNA levels were increased in more than 95% of the examined ovary carcinoma samples, compared with a wedge resection of a normal ovary. Immunohistochemical analysis of the samples demonstrated gal-1 expression in cancer epithelial cells from 17 of 30 samples, with a cytoplasmic pattern. Gal-1 immunostaining was significantly increased in the stroma associated with carcinoma cells compared with the normal, noninvaded stroma (p = 0.003). This pattern of expression was confirmed by examination of 12 other frozen epithelial ovary carcinomas, using in situ hybridization. Immunohistochemical staining of the specimens demonstrated colocalization of gal-1, laminin-1, and fibronectin. In vitro experiments were conducted to elucidate the potential biologic role of gal-1 in ovarian cancer progression. Gal-1 protein expression and release was detected in AZ364, SK-OV-3, and AZ224, but not in OVCAR-3, AZ419, and AZ382, human ovary carcinoma cell lines. Incubation of 84BR fibroblasts with conditioned media harvested from the ovary carcinoma cell lines induced an increased expression of gal-1 in the cultured fibroblasts in all cases except AZ419 and SK-OV-3. High concentrations of gal-1 (100 mug/ml) induced significantly decreased cell proliferation in all cell lines, as defined by bromodeoxyuridine incorporation. Additionally, recombinant gal-1 induced a dose-dependent increase in in vitro adhesion of AZ224, SK-OV-3, and AZ382 cells to laminin-1; adhesion to fibronectin was increased by gal-1 in OVCAR-3, AZ224, and SK-OV-3. No effect was observed in the other cases. Our data contribute to define a role for gal-1 during the interactions between human ovary carcinoma cells and host fibroblasts.

Disciplines :

Biochemistry, biophysics & molecular biology
Oncology

Author, co-author :

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

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

Garnier, Frédérique

Fernandez, Pedro L

Berchuck, Andrew

Castronovo, Vincenzo ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie générale et cellulaire

Language :

English

Title :

Galectin-1 accumulation in the ovary carcinoma peritumoral stroma is induced by ovary carcinoma cells and affects both cancer cell proliferation and adhesion to laminin-1 and fibronectin

Publication date :

March 2003

Journal title :

Laboratory Investigation

ISSN :

0023-6837

eISSN :

1530-0307

Publisher :

Lippincott Williams & Wilkins, Philadelphia, United States - Pennsylvania

Volume :

Issue :

Pages :

377-386

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique
Télévie

Available on ORBi :

since 28 September 2009

Statistics

Number of views

54 (1 by ULiège)

Number of downloads

1 (0 by ULiège)

More statistics

Scopus citations^®

150

Scopus citations^®
without self-citations

150

OpenCitations

122

OpenAlex citations

174

Bibliography

Adams L, Scott GK, and Weinberg CS (1996). Biphasic modulation of cell growth by recombinant human galectin-1. Biochim Biophys Acta 1312:137-144.
Ahmed H, Sharma A, DiCioccio RA, and Allen HJ (1992). Lymphoblastoid cell adhesion mediated by a dimeric and polymeric endogenous β-galactoside-binding lectin (galaptin). J Mol Recognit 5:1-8.
Barondes SH, Cooper DNW, Gitt MA, and Leffler H (1994). Galectins: Structure and function of a large family of animal lectins. J Biol Chem 269:20807-20810.
Berberat PO, Friess H, Wang L, Zhu Z, Bley T, Frigeri L, Zimmermann A, and Buchler MW (2001). Comparative analysis of galectins in primary tumors and tumor metastasis in human pancreatic cancer. J Histochem Cytochem 49:539-549.
Bourne Y, Bolgiano B, Liao DI, Strecker G, Cantau P, Herzberg O, Feizi T, and Cambillau C (1994). Crosslinking of mammalian lectin (galectin-1) by complex biantennary saccharides. Nat Struct Biol 1:863-870.
Chiariotti L, Berlingieri MT, Battaglia C, Benvenuto G, Martelli ML, Salvatore P, Chiappetta G, Bruni CB, and Fusco A (1995). Expression of galectin-1 in normal human thyroid gland and in differentiated and poorly differentiated thyroid tumors. Int J Cancer (Pred Oncol) 64:171-175.
Chiariotti L, Berlingieri MT, De Rosa P, Battaglia C, Berger N, Bruni CB, and Fusco A (1992). Increased expression of the negative growth factor, galactoside-binding protein, gene in transformed thyroid cells and in human thyroid carcinomas. Oncogene 7:2507-2511.
Christensen L (1992). The distribution of fibronectin, laminin and tetranectin in human breast cancer with special attention to the extracellular matrix. APMIS Suppl 26:1-39.
Cindolo L, Benvenuto G, Salvatore P, Pero R, Salvatore G, Mirone V, Prezioso D, Altieri V, Bruni CB, and Chiariotti L (1999). Galectin-1 and galectin-3 expression in human bladder transitional-cell carcinomas. Int J Cancer 84:39-43.
Cooper DNW (1997). Galectin-1: Secretion and modulation of cell interactions with laminin. Trends Glycosci Glycotechnol 9:57-67.
Cooper DN and Barondes SH (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 DN, Massa SM, and Barondes SH (1991). Endogenous muscle lectin inhibits myoblast adhesion to laminin. J Cell Biol 115:1437-1448.
Ellerhorst J, Nguyen T, Cooper DN, Lotan D, and Lotan R (1999). Differential expression of endogenous galectin-1 and galectin-3 in human prostate cancer cell lines and effects of overexpressing galectin-1 on cell phenotype. Int J Oncol 14:217-224.
Ercolani L, Florence B, Denaro M, and Alexander M (1988). Isolation and complete sequence of a functional human glyceraldehyde-3-phosphate dehydrogenase gene. J Biol Chem 263:15335-15341.
Gillenwater A, Xu X-C, El-Naggar AK, Clayman GL, and Lotan R (1996). Expression of galectins in head and neck squamous cell carcinoma. Head Neck 18:422-432.
Glisin V, Crkvenjakov R, and Byus C (1974). Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry 13:2633-2637.
Graham C and Karnovsky MJ (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.
Hafer-Macko C, Pang M, Seilhamer JJ, and Baum LG (1996). Galectin-1 is expressed by thymic epithelial cells in myasthenia gravis. Glycoconj J 13:591-597.
Hsu SM, Raine L, and Fanger H (1981). Use of avidin-biotinperoxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577-580.
Hunt G (1989). The role of laminin in cancer invasion and metastasis. Exp Cell Biol 57:165-176.
International Federation of Gynecology and Obstetrics (1987). Changes in definitions of clinical staging for carcinoma of the cervix and ovary. Am J Obstet Gynecol 156:236.
Liao DI, Kapadia G, Ahmed H, Vasta GR, and Herzberg O (1994). Structure of S-lectin, a developmentally regulated vertebrate beta-galactoside-binding protein. Proc Natl Acad Sci USA 91:1428-1432.
Mahanthappa NK, Cooper DNW, Barondes SH, and Schwarting GA (1994). Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 120:1373-1384.
Pace KE, Hahn HP, Pang M, Nguyen JT, and Baum LG (2000). CD7 delivers a pro-apoptotic signal during galectin-1-induced T cell death. J Immunol 165:2331-2334.
Pace KE, Lee C, Stewart PL, and Baum LG (1999). Restricted receptor segregation into membrane microdomains occurs on human T cells during apoptosis induced by galectin-1. J Immunol 163:3801-3811.
Perillo NL, Pace KE, Seilhamer JJ, and Baum LG (1995). Apoptosis of T cells mediated by galectin-1. Nature 378:736-739.
Piechaczyk M, Blanchard JM, Marty L, Dani C, Panabieres F, El Sabouty S, Fort P, and Jeanteur P (1984). Post-transcriptional regulation of glyceraldehyde-3-phosphatedehydrogenase gene expression in rat tissues. Nucleic Acids Res 12:6951-6963.
Rabinovich GA, Ariel A, Hershkoviz R, Hirabayashi J, Kasai K, and Lider O (1999). Specific inhibition of T-cell adhesion to extracellular matrix and proinflammatory cytokine secretion by human recombinant galectin-1. Immunology 97:100-106.
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, and Camby I (2001). Galectin-1 is highly expressed in human gliomas with relevance for modulation of invasion of tumor astrocytes into the brain parenchyma. Glia 33:241-255.
Sanjuan X, Fernandez PL, Castelis A, Castronovo V, van den Brule F, Liu FT, Cardesa A, and Campo E (1997). Differential expression of galectin 3 and galectin 1 in colorectal cancer progression. Gastroenterology 113:1906-1915.
Shimonishi T, Miyazaki K, Kono N, Sabit H, Tuneyama K, Harada K, Hirabayashi J, Kasai K, and Nakanuma Y (2001). Expression of endogenous galectin-1 and galectin-3 in intrahepatic cholangiocarcinoma. Hum Pathol 32:302-310.
Stojanovic D, Hughes RC, Feizi T, and Childs RA (1983). Interactions of a mammalian beta-galactoside-binding lectin with hamster fibroblasts. J Cell Biochem 21:119-127.
Vaarala MH, Porvari K, Kyllonen A, and Vihko P (2000). Differentially expressed genes in two LNCaP prostate cancer cell lines reflecting changes during prostate cancer progression. Lab Invest 80:1259-1268.
van den Brûle F, Clausse N, Waltregny D, and Castronovo V (1999). Increased frequency of galectin-1 expression in prostatic tumor-associated capillary endothelial cells: Possible induction by prostate carcinoma cells. Angiogenesis 3:317-325.
van den Brûle FA, Berchuck A, Bast RC, Liu F-T, Gillet C, Sobel ME, and Castronovo V (1994). Differential expression of the 67-kD laminin receptor and 31-kD human laminin-binding protein in human ovarian carcinomas. Eur J Cancer 30A:1096-1099.
van den Brûle FA, Buicu C, Baldet M, Sobel ME, Cooper DNW, Marschal P, and Castronovo V (1995). Galectin-1 modulates human melanoma cell adhesion to laminin. Biochem Biophys Res Commun 209:760-767.
van den Brûle FA, Buicu C, Berchuck A, Bast RC, Deprez M, Liu F-T, Cooper DNW, Pieters C, Sobel ME, and Castronovo V (1996). Expression of the 67-kD laminin receptor, galectin-1, and galectin-3 in advanced human uterine adenocarcinoma. Hum Pathol 27:1185-1191.
van den Brûle FA and Castronovo V (2000). Laminin-binding lectins during cancer invasion and metastasis. In: Caron M and Sève A-P, editors. Lectins and pathology. Amsterdam: Harwood Academic Publishers, 79-121.
van den Brûle FA, Waltregny D, and Castronovo V (2001). Increased expression of galectin-1 in carcinoma-associated stroma predicts poor outcome in prostate carcinoma patients. J Pathol 193:80-87.
Vespa GN, Lewis LA, Kozak KR, Moran M, Nguyen JT, Baum LG, and Miceli MC (1999). Galectin-1 specifically modulates TCR signals to enhance TCR apoptosis but inhibit IL-2 production and proliferation. J Immunol 162:799-806.
Vyakarnam A, Dagher SF, Wang JL, and Patterson RJ (1997). Evidence for a role for galectin-1 in pre-mRNA splicing. Mol Cell Biol 17:4730-4737.
Xu XC, El-Naggar A, and Lotan R (1995). Differential expression of galectin-1 and galectin-3 in thyroid tumors. Am J Pathol 147:815-822.
Zhou Q and Cummings RD (1990). The S-type lectin from calf heart tissue binds selectively to the carbohydrate chains of laminin. Arch Biochem Biophys 281:27-35.