[en] BACKGROUND: Interactions between cells and the basement membrane glycoprotein laminin are altered during colon cancer progression. Colon carcinoma and normal mucosa cells express a variety of laminin-binding proteins, including the 67-kd laminin receptor (67 LR) and a 31-kd human laminin-binding protein (HLBP31) homologous to the 31-kd human IgE-binding protein/galactoside-binding lectin. PURPOSE: To investigate whether various laminin-binding proteins are differentially expressed in human colon carcinoma, we studied messenger RNA (mRNA) levels of the 67 LR and HLBP31 in matched tumor and adjacent normal mucosa samples from a series of 21 patients. METHODS: Total cellular RNA from tumor and normal mucosa was isolated and analyzed by Northern and slot blot hybridization. In addition, HLBP31 protein levels were assessed by the immunoblot technique. Quantitative laminin affinity chromatography was also used to measure the synthesis of HLBP31 protein in five human cancer cell lines. RESULTS: The steady-state mRNA level of HLBP31 was downregulated (i.e., decreased) in 18 of 21 human colon carcinomas compared with the level in their corresponding normal colonic mucosa. On average, the level of HLBP31 mRNA was decreased 50% +/- 30% (+/- SD) in the colon cancers. The mean ratio of colon cancer HLBP31 mRNA to adjacent normal mucosa HLBP31 mRNA was twofold lower in primary tumors of patients with metastases (0.3 +/- 0.2 SD) than in primary tumors of patients free of metastatic lesions (0.6 +/- 0.2 SD). The differences between the two groups of patients were statistically significant (P less than .05, Wilcoxon-Mann-Whitney test). We have previously shown that the ratio of colon cancer 67 LR mRNA to corresponding normal mucosa 67 LR mRNA was increased in the same patient population. When the two ratios (ratio of cancer to normal HLBP31 mRNA and ratio of cancer to normal 67 LR mRNA) were compared, HLBP31 mRNA/67 LR mRNA was significantly lower (P less than .05) in primary tumors with metastases (mean +/- SD, 0.3 +/- 0.2) than in primary cancers without metastases (mean +/- SD, 0.7 +/- 0.5). The steady-state level of HLBP31 mRNA was directly correlated with the amount of HLBP31 protein in both colon tissue samples and human cancer cell lines. CONCLUSION: HLBP31 mRNA expression in colon cancer tissues is modulated inversely to that of 67 LR mRNA expression. The down-regulation of HLBP31 appears to be associated with the metastatic capabilities of colon cancer cells. IMPLICATIONS: Prospective studies on a large cohort should determine if the systematic detection of HLBP31 and 67 LR protein and/or mRNA can be a valuable adjunct in the prognostic evaluation of primary colon cancers.
Castronovo, Vincenzo ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie générale et cellulaire - GIGA-R : Labo de recherche sur les métastases
Campo, E.
van den Brule, F. A.
Claysmith, A. P.
Cioce, V.
Liu, F. T.
Fernandez, P. L.
Sobel, M. E.
Language :
English
Title :
Inverse modulation of steady-state messenger RNA levels of two non-integrin laminin-binding proteins in human colon carcinoma.
Publication date :
1992
Journal title :
Journal of the National Cancer Institute
ISSN :
0027-8874
eISSN :
1460-2105
Publisher :
Oxford University Press, Cary, United States - North Carolina
Sugarbaker EV, Weingard DN, Roseman JM: Observations on cancer metastases. In Cancer Invasion and Metastases (Liotta LA, Hart IR, eds). The Hague: Martinus Nijhoff, 1982, pp 427–465
Poste G, Fidler IJ: The pathogenesis of cancer metastasis. Nature 283:139–146, 1980
Liotta LA: Tumor invasion and metastasis—role of extracellular matrix: Rhoads Memorial Award lecture. Cancer Res 46:1–7, 1986
Rosenberg SA: Surgical Treatment of Metastatic Cancer. New York: Lippincott, 1987
Silverberg E, Boring CC, Squires TS: Cancer statistics 1989. CA Cancer J Clin 40:9–26, 1990
Cohen AM, Shank B, Friedman MA: Colorectal cancer. In Cancer: Principles and Practice of Oncology (DeVita VT Jr, Heilman S, Rosenberg SA, eds). Philadelphia: Lippincott, 1989, pp 896–964
Jones PA, DeClerck YA: Destruction of extracellular matrices containing glycoproteins, elastin, and collagen by metastatic human tumor cells. Cancer Res 40:3222–3227, 1980
Timpl R, Rhode H, Robey PG, et al: Laminin—a glycoprotein from basement membranes. J Biol Chem 254:9933–9941, 1979
Barsky SH, Rao CN, Williams JE, et al: Laminin molecular domains which alter metastasis in a murine model. J Clin Invest 74:843–848, 1984
Varani J, Lovett EJ III, McCoy JP Jr, et al: Differential expression of a laminin-like substance by high- and low-metastatic cells. Am J Pathol 111:27–34, 1983
Terranova VP, Liotta LA, Russo RG, et al: Role of laminin in the attachment and metastasis of murine tumor cells. Cancer Res 42:2265–2269, 1982
Rao NC, Barsky SH, Terranova VP, et al: Isolation of a tumor cell laminin receptor. Biochem Biophys Res Commun 111:804–808, 1983
Malinoff H, Wicha MS: Isolation of a cell surface protein for laminin from murine fibrosarcoma cells. J Cell Biol 96:1475–1480, 1983
Albelda SM, Buck CA: Integrins and other cell adhesion molecules. FASEB J 4:2868–2880, 1990
Horwitz A, Duggan K, Greggs R, et al: The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol 101:2134–2144, 1985
Gehlsen KR, Dillner L, Engvall E, et al: The human laminin receptor is a member of the inteerin family of cell adhesion receptors. Science 241:1228–1229, 1988
Kleinman HK, Ogle RC, Cannon FB, et al: Laminin receptors for neurite formation. Proc Natl Acad Sci USA 83:1282–1286, 1988
Ruynan RB, Versalovic J, Shur BD: Functionally distinct laminin receptors mediate cell adhesion and spreading: The requirement for surface galactosyltransferase in cell spreading. J Cell Biol 107:1863–1871. 1988
Wewer UM, Liotta LA, Jaye M, et al: Altered levels of laminin receptor mRNA in various human carcinoma cells have different abilities to bind laminin. Proc Natl Acad Sci USA 83:7137–7141, 1986
Rao CN, Castronovo V, Schmitt MC, et al: Evidence for a precursor of the high-affinity metastasis-associated murine laminin receptor. Biochemistry 28:7476–7486. 1989
Yow HK, Wong JM, Chen HS, et al: Increased mRNA expression of a laminin-binding protein in human colon carcinoma: Complete sequence of a full-length cDNA encoding the protein. Proc Natl Acad Sci USA 85:6394–6398, 1988
Hand PH, Thor A, Schlom J. et al: Expression of laminin receptor in normal and carcinomatous human tissues as defined by a monoclonal antibody. Cancer Res 45:2713–2719, 1985
Castronovo V, Colin C, Claysmith AP, et al: Immunodetection of the metastasis-associated laminin receptor in human breast cancer cells obtained by fine-needle aspiration biopsy. Am J Pathol 137:1373–1381, 1990
Cioce V, Castronovo V, Shmookler BM, et al: Increased expression of the laminin receptor in human color cancer. J Natl Cancer Inst 83:29–36, 1991
Mafune K, Ravikumar TS, Wong JM, et al: Expression of a Mr-32,000 laminin-binding protein messenger RNA in human colon carcinoma correlates with disease progression. Cancer Res 50:3888–3891, 1990
D’Errico A, Garbisa S, Liotta LA, et al: Augmentation of type IV collagenase, laminin receptor, and Ki67 proliferation antigen associated with human colon, gastric, and breast carcinoma progression. Mod Pathol 4:239–246, 1991
Stallmach A, Schuppan D, Dax J, et al: Identification of laminin binding proteins in cell membranes of a human colon adenocarcinoma cell line. Gut 31:70–76, 1990
Koretz K, Schlag P, Boumsell L, et al: Expression of VLA-alpha 2, VLA-alpha 6, and VLA-β1 chains in normal mucosa and adenomas of the colon, and in colon carcinomas and their liver metastases. Am J Pathol 138:741–750, 1991
Castronovo V, Luytens F, Cioce V, et al: 31 and 12 kD galactoside binding lectins are cell surface laminin binding proteins in human cancer cells: Possible relationship with the 67 kD laminin receptor. J Cell Biol 111:12a, 1990
Woo HJ, Shaw LA, Messier JM, et al: The major non-integrin laminin binding protein of macrophages is identical to carbohydrate binding protein 35 (Mac-2). J Biol Chem 265:7097–7099, 1990
Zhou Q, Cummings RD: The S-type lectin from heart tissue binds selectively to the carbohydrate chains of laminin. Arch Biochem Biophys 281:27–35, 1990
Castronovo V, Kridelka F, Hsu D, et al: The 31 kDa human IgE binding protein/galactoside binding lectin/Mac-2 antigen is a high affinity laminin binding protein. J Cell Biol 115:289a, 1991
Castronovo V, Luyten F, van den Brûle F, et al: Identification of a 14 kd laminin binding protein (HLBP14) in human melanoma cells that is identical to the 14 kd galactoside binding lectin. Arch Biochem Biophys. In press
Gitt MA, Barondes SH: Evidence that the human soluble β-galactoside-binding lectin is encoded by a family of genes. Proc Natl Acad Sci USA 83:7603–7607, 1986
Abbott WM, Feizi T: Evidence that the 14 kDa soluble β-galactoside-binding lectin in man is encoded by a single gene. Biochem J 259:291–294, 1989
Raz A, Carmi P, Raz T, et al: Molecular cloning and chromosomal mapping of a human galactoside-binding protein. Cancer Res 51:2173–2178, 1991
Robertson MW, Albrandt K, Keller D, et al: Human IgE-binding protein: A soluble lectin exhibiting a highly conserved interspecies sequence and differential recognition of IgE glycoforms. Biochemistry 29:8093–8100, 1990
Cherayil BJ, Chaitovitz S, Wong C, et al: Molecular cloning of a human macrophage lectin specific for galactose. Proc Natl Acad Sci USA 87:7324–7328, 1990
Raz A, Carmi P, Pazerini G: The expression of two different endogenous galactoside-binding lectins sharing sequence homology. Cancer Res 48:645–649, 1990
Raz A, Meromsky L, Zvibel I, et al: Identification of the metastasis-associated, galactoside-binding lectin as a chimeric gene product with homology to an IgE-binding protein. Int J Cancer 39:353–360, 1989
Raz A, Zhu D, Hogan V, et al: Evidence for the role of the 34-kDa galactoside-binding lectin in transformation and metastasis. Int J Cancer 46:871–877, 1990
Castronovo V, Taraboletti G, Liotta LA, et al: Modulation of laminin receptor expression by estrogen and progestins in human breast cancer cell lines. J Natl Cancer Inst 81:781–788, 1989
Frigeri LG, Robertson MW, Liu FT: Expression of biologically active recombinant rat IgE-binding protein in Escherichia coli. J Biol Chem 265:20763–20769, 1990
Lathe R: Synthetic oligonucleotide probes deduced from amino acid sequence data. Theoretical and practical considerations. J Mol Biol 183:1–12, 1985
Piechaczyk M, Blanchard JM, Marty L, et al: Post-transcriptional regulation of glyceraldehyde-3-phosphate-dehydrogenase gene expression in rat tissues. Nucleic Acids Res 12:6951–6963, 1984
Frigeri LG, Liu FT: Surface expression of functional IgE binding protein, an endogenous lectin on mast cells and macrophages. J Immunol 148:861–867, 1992
Irimura T, Matsushita Y, Sutton RC, et al: Increased content of an endogenous lactose-binding lectin in human colorectal carcinoma progressed to metastatic stages. Cancer Res 51:387–393, 1991
Beck K, Hunter I, Engel J: Structure and function of laminin: Anatomy of a multidomain glycoprotein. FASEB J 4:148–160, 1990
Basson CT, Knowles WJ, Bell L, et al: Spatiotemporal segregation of endothelial cell integrin and nonintegrin extracellular matrix-binding proteins during adhesion events. J Cell Biol 110:789–801, 1990
