Galectin-1 Expression in Prostate Tumor-Associated Capillary Endothelial Cells Is Increased by Prostate Carcinoma Cells and Modulates Heterotypic Cell-Cell Adhesion
Clausse, Nathalie; van den Brule, Frédéric; Waltregny, Davidet al.
[en] Besides providing tumors with nutrients, newly formed capillaries constitute a potential escape route for tumor cells favoring metastatic dissemination, and constitute an access for the anti-tumoral host immune cells. Galectin-1, a soluble human lectin, is involved in numerous biological functions including cell-cell and cell-substrate interactions. In addition, galectin-1 is able to induce apoptosis of activated T-lymphocytes. In this study, we have examined galectin-1 expression in capillaries associated to the carcinoma cells or present in the remote non-tumoral stroma of 100 human prostate carcinoma samples by immunoperoxidase staining. Galectin-1 was expressed by endothelial cells from capillaries infiltrating the tumor tissue in 64% (64/100) of the cases. On the contrary, endothelial cells in the adjacent non-tumoral stroma expressed galectin-1 in very few cases (7/100). Increased frequency of galectin-1-positive capillaries in the tumor-associated compared to the tumor-free areas was observed in 63% of the cases. This striking contrast led us to set up an in vitro model to test whether tumor cells could induce galectin-1 expression by endothelial cells. Incubation of human umbilical vein endothelial cells with conditioned media from PC-3 or DU 145 prostate carcinoma cells led to a significant increase of galectin-1 protein expression (+32.97% and 37.91% P < 0.01 and P < 0.05, respectively). PC-3 conditioned medium also induced increased adhesion values of PC-3 cells to the endothelial cells (53.4 +/- 4.7 vs. 38.5 +/- 3.5 after 30 min; 66.6 +/- 7.8 vs. 46.2 +/- 6.4 after 60 min). An anti-galectin-1 antiserum abolished this modulation, and recombinant galectin-1 also induced increased adhesion values in a dose-dependent fashion. This effect was specific as no such modulations were observed using normal lymphocytes instead of PC-3 cells. Preferential galectin-1 expression in the endothelial cells close to the cancer cells could provide these latter with increased abilities to interact with the endothelial cells as well as a defense against the host immune system.
Disciplines :
Oncology
Author, co-author :
Clausse, Nathalie
van den Brule, Frédéric
Waltregny, David ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Labo de recherche sur les métastases
Garnier, Frédérique
Castronovo, Vincenzo ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie générale et cellulaire
Language :
English
Title :
Galectin-1 Expression in Prostate Tumor-Associated Capillary Endothelial Cells Is Increased by Prostate Carcinoma Cells and Modulates Heterotypic Cell-Cell Adhesion
Hanahan D, Folkman J. Patterns ans emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996; 86: 353-64.
Rak J, Filmus J, Kerbel RS. Reciprocal paracrine interactions between tumour cells and endothelial cells: The 'angiogenesis progression' hypothesis. Eur J Cancer 1996; 32A: 2438-50.
Laine RA. The information-storing potential of the sugar code. In Gabius H-J, Gabius S (eds): Glycosciences: Status and Perspectives. Weinheim, Germany: Chapman & Hall 1997; 1-14.
Barondes SH, Castronovo V, Cooper DNW et al. Galectins: A family of animal β-galactoside-binding lectins. Cell 1994; 76: 597-8.
Barondes SH, Cooper DNW, Gitt MA, Leffler H. Galectins: Structure and function of a large family of animal lectins. J Biol Chem 1994; 269: 20807-10.
Allen HJ, Sucato D, Woynarowska B et al. Role of galaptin in ovarian carcinoma adhesion to extracellular matrix in vitro. J Cell Biochem 1990; 43: 43-57.
Skrincosky DM, Allen HJ, Bernacki RJ. Galaptin-mediated adhesion of human ovarian carcinoma A121 cells and detection of cellular galaptin-binding glycoproteins. Cancer Res 1993; 53: 2667-75.
van den Brûle FA, Buicu C, Baldet M et al. Galectin-1 modulates human melanoma cell adhesion to laminin. Biochem Biophys Res Commun 1995; 209: 760-7.
Kaltner H, Stierstorfer B. Animal lectins as cell adhesion molecules. Acta Anat 1998; 161: 162-79.
Chiariotti L, Berlingieri MT, De Rosa P et al. Increased expression of the negative growth factor, galactoside-binding protein, gene in transformed thyroid cells and in human thyroid carcinomas. Oncogene 1992; 7: 2507-11.
Chiariotti L, Berlingieri MT, Battaglia C et al. Expression of galectin-1 in normal human thyroid gland and in differentiated and poorly differentiated thyroid tumors. Int J Cancer 1995; 64: 171-5.
Xu XC, el-Naggar AK, Lotan R. Differential expression of galectin-1 and galectin-3 in thyroid tumors. Potential diagnostic implications. Am J Pathol 1995; 147: 815-22.
van den Brûle FA, Buicu C, Berchuck A et al. Expression of the 67 kD laminin receptor, galectin-1 and galectin-3 in advanced uterine carcinoma. Hum Pathol 1996; 27: 1185-91.
Cindolo L, Benvenuto G, Salvatore P et al. Galectin-1 and galectin-3 expression in human bladder transitional-cell carcinomas. Int J Cancer 1999; 84: 39-43.
Sanjuan X, Fernandez PL, Castells A et al. Differential expression of galectin 3 and galectin 1 in colorectal cancer progression. Gastroenterology 1997; 113: 1906-15.
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) 1986; 52: 107-15.
Baum LG, Seilhamer JJ, Pang M et al. Synthesis of an endogenous lectin, galectin-1, by human endothelial cells, is up-regulated by endothelial cell activation. Glycoconj J 1995; 12: 63-8.
Perillo NL, Pace KE, Seilhamer JJ, Baum LG. Apoptosis of T cells mediated by galectin-1. Nature 1995; 378: 736-9.
Lehr JE, Pienta KJ. Preferential adhesion of prostate cancer cells to a human bone marrow endothelial cell line. J Natl Cancer Inst 1998; 90: 118-23.
Schroder FH, Hermanek P, Denis L et al. The TNM classification of prostate cancer. Prostate 1992; 4: 129-38.
Gleason DF, Mellinger GT. Prediction of prognosis for prostatic adenocarcinoma by combined histological grading and clinical staging. J Urol 1974; 111: 58-64.
Waltregny D, Bellahcène A, Van Riet I et al. Prognostic value of bone sialoprotein expression in localized human prostate cancer. JNCI 1998; 13: 1000-7.
Cooper DNW, Barondes SH. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol 1990; 110: 1681-91.
Jaffe EA, Nachmann RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins: Identification by morphologic and immunologic criteria. J Clin Invest 1973; 52: 2745-56.
Baijum A. Isolation of morphonuclear cells and granulocytes from human blood. Scand J Clin Lab Invest 1968; 21S: 77-89.
Cooper DN, Massa SM, Barondes SH. Endogenous muscle lectin inhibits myoblast adhesion to laminin. J Cell Biol 1991; 115: 1437-48.
Ozeki Y, Matsui T, Titani K. Cell adhesive activity of two animal lectins through different recognition mechanisms. FEBS Lett 1991; 289: 145-7.
Zhou Q, Cummings RD. L-14 lectin recognition of laminin and its promotion of in vitro cell adhesion. Arch Biochem Biophys 1993; 300: 6-17.
Mahanthappa NK, Cooper DN, Barondes SH, Schwarting GA. Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 1994; 120: 1373-84.
Ozeki Y, Matsui T, Yamamoto Y et al. Tissue fibronectin is an endogenous ligand for galectin-1. Glycobiology 1995; 5: 255-61.
Kopitz J, von Reitzenstein C, Burchert M et al. Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J Biol Chem 1998; 273: 11205-11.
Moiseeva EP, Spring EL, Baron JH, de Bono DP. Galectin-1 modulates attachment, spreading and migration of cultured vascular smooth muscle cells via interactions with cellular receptors and components of extracellular matrix. J Vasc Res 1999; 36: 47-58.
Lotan R, Belloni PN, Tressler RJ et al. Expression of galectins on microvessel endothelial cells and their involvement in tumour cell adhesion. Glycoconj J 1994; 11: 462-8.