Carbonic anhydrase IX reduces E-cadherin-mediated adhesion of MDCK cells via interaction with β-catenin

Experimental Cell Research

Volumn 290, Issue 2, 2003, Pages 332-345

  Švastová, Eliška ^a   Žilka, Norbert ^b   Zat'ovičová, Miriam ^a   Gibadulinová, Adriana ^a   Čiampor, Fedor ^a   Pastorek, Jaromír ^a   Pastoreková, Silvia ^a  

^a INSTITUTE OF VIROLOGY   (Slovakia)

^b INSTITUTE OF NEUROIMMUNOLOGY   (Slovakia)

Author keywords

Carbonic anhydrase IX; Cell adhesion; E cadherin; Hypoxia; Catenin

Indexed keywords

BETA CATENIN; CALCIUM; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE IX; CELL ADHESION MOLECULE; TYLOXAPOL; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ARTICLE; CANCER INVASION; CELL ADHESION; CELL CONTACT; CELL DISRUPTION; CELL MEMBRANE; CELL STRAIN; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; HYPOXIA; MEMBRANE; NONHUMAN; PHENOMENOLOGY; PRECIPITATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SOLUBILITY; TISSUE OXYGENATION;

EID: 0142121458     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00351-3     Document Type: Article

References (54)

1. Hewett-Emmett D. Evolution and distribution of the carbonic anhydrase gene families. Chegwidden W.R., Carter N., Edwards Y. The Carbonic Anhydrases New Horizons . 2000;29-76 Birkhauser Verlag, Base, Switzerland.
2. Parkkila S. An overview of the distribution and function of carbonic anhydrase in mammals. Chegwidden W.R., Carter N., Edwards Y. The Carbonic Anhydrases New Horizons . 2000;76-93 Birkhauser Verlag, Basel, Switzerland.
3. Pastorek J., Pastorekova S., Callebaut I., Mornon J.P., Zelnik V., Opavsky R., Zatovicova M., Liao S., Portetelle D., Stanbridge E.J., Zavada J., Burny A., Kettmann R. Cloning and characterization of MN, a human tumor-associated proten with a domain domologous to carbonic anhydrase and a putative helix-loop-helix DNA binding segment. Oncogene. 9:1994;2788-2888.
4. Opavsky R., Pastorekova S., Zelnik V., Gibadulinova A., Stanbridge E.J., Zavada J., Kettmann R., Pastorek J. Human MN/CA9 gene, a novel member of the carbonic anhydrase family structure and exon to protein domain relationships . Genomics. 33:1996;480-487.
5. Wingo T., Tu C.K., Laipis P.J., Silverman D.N. The catalytic properties of human carbonic anhydrase IX. Biochem. Biophys. Res. Commun. 288:2001;666-669.
6. Zavada J., Zavadova Z., Pastorek J., Biesova Z., Jezek J., Velek J. Human tumor-associated cell adhesion protein MN/CA IX identification of M75 epitope and of the region mediating cell adhesion . Br. J. Cancer. 82:2000;1508-1513.
7. Zavada J., Zavadova Z., Pastorekova S., Ciampor F., Pastorek J., Zelnik V. Expression of MaTu-MN protein in human tumor cultures and in clinical specimens. Int. J. Cancer. 54:1993;268-274.
8. Liao S.Y., Brewer C., Zavada J., Pastorek J., Pastorekova S., Manetta A., Berman M.L., DiSaia P.J., Stanbridge E.J. Identification of the MN antigen as a diagnostic biomarker of cervical intraepithelial neoplasia and cervical carcinoma. Am. J. Pathol. 145:1994;598-609.
9. Liao S.Y., Aurelio O.N., Jan K., Zavada J., Stanbridge E.J. Identification of the MN/CA9 protein as a reliable diagnostic biomarker of clear cell carcinoma of the kidney. Cancer Res. 57:1997;2827-2831.
10. Turner J.R., Odze R.D., Crum C.P., Resnick M.B. MN antigen expression in normal, preneoplastic and neoplastic esophagus a clinicopathological study of a new cancer-associated biomarker . Hum. Pathol. 28:1997;740-744.
11. Saarnio J., Parkkila S., Parkkila A.K., Haukipuro K., Pastorekova S., Pastorek J., Kairaluoma M.I., Karttunen T.J. Immunohistochemical study of colorectal tumors for expression of a novel transmembrane carbonic anhydrase, MN/CA IX, with potential value as a marker of cell proliferation. Am. J. Pathol. 153:1998;279-285.
12. Vermylen P., Roufosse C., Burny A., Verhest A., Bossehaerts T., Pastorekova S., Ninane V., Sculier J.P. Carbonic anhydrase IX antigen differentiates between preneoplastic and malignant lesions in non-small cell lung carcinomas. Eur. Respir. J. 14:1999;806-811.
13. Ivanov S., Liao S.Y., Ivanova A., Danilkovich-Miagkova A., Tarasova N., Weirich G., Merrill M.J., Proescholdt M.A., Oldfield E.H., Lee J., Zavada J., Waheed A., Sly W., Lerman M.I., Stanbridge E.J. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am. J. Pathol. 158:2001;905-919.
14. Wykoff C., Beasley N., Watson P., Turner L., Pastorek J., Wilson G., Turley H., Maxwell P., Pugh C., Ratcliffe P., Harris A. Hypoxia-inducible regulation of tumor-associated carbonic anhydrases. Cancer Res. 60:2000;7075-7083.
15. Wykoff C.C., Beasley N., Watson P.H., Campo L., Chia S.K., English R., Pastorek J., Sly W.S., Ratcliffe P., Harris A.L. Expression of the hypoxia-inducible and tumor-associated carbonic anhydrases in ductal carcinoma in situ of the breast. Am. J. Pathol. 158:2001;1011-1019.
16. Chia S.K., Wykoff C.C., Watson P.H., Han C., Leek R.D., Pastorek J., Gatter K.C., Ratcliffe P., Harris A.L. Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma. J. Clin. Oncol. 19:2001;3660-3668.
17. Koukourakis M.I., Giatromanolaki A., Sivridis E., Simopoulos K., Pastorek J., Wykoff C.C., Gatter K.C., Harris A.L. Hypoxia-regulated carbonic anhydrase-9 (CA9) relates to poor vascularization and resistance of squamous cell head and neck cancer to chemoradiotherapy. Clin. Cancer Res. 7:2001;3399-3403.
18. Loncaster J.A., Harris A.L., Davidson S.E., Logue J.P., Hunter R.D., Wykoff C.C., Pastorek J., Ratcliffe P., Stratford I.J., West C.M.L. Carbonic anhydrase IX expression, a potential new intrinsic marker of hypoxia correlations with tumour oxygen measurements and prognosis in locally advanced carcinoma of the cervix . Cancer Res. 61:2001;6394-6399.
19. Giatromanolaki A., Koukourakis M.I., Sivridis E., Pastorek J., Wykoff C.C., Gatter K.C., Harris A.L. Expression of hypoxia-inducible carbonic anhydrase-9 relates to angiogenic pathways and independently to poor outcome in non-small cell lung cancer. Cancer Res. 61:2001;7992-7998.
20. Pastoreková S., Parkkila S., Parkkila A.K., Opavský R., Zelnik V., Saarnio J., Pastorek J. Carbonic anhydrase IX, MN/CA IX analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts . Gastroenterology. 112:1997;398-408.
21. Saarnio J., Parkkila S., Parkkila A.K., Waheed A., Casey M.C., Zhou X.Y., Pastorekova S., Pastorek J., Karttunen T., Haukipuro K., Kairaluoma M.I., Sly W.S. Immunohistochemistry of carbonic anhydrase isozyme IX (MN/CA IX) in human gut reveals polarized expression in the epithelial cells with the highest proliferative capacity. J. Histochem. Cytochem. 46:1998;497-504.
22. Gumbiner B.M. Cell adhesion the molecular basis of tissue architecture and morphogenesis . Cell. 84:1996;345-357.
23. Guilford P. E-cadherin downregulation in cancer fuel or fire? Mol. Med. Today. 5:1999;172-177.
24. Beavon I.R.G. The E-cadherin-catenin complex in tumour metastasis structure, function and regulation . Eur. J. Cancer. 36:2000;1607-1620.
25. Takeda H., Nagafuchi A., Yonemura S., Tsukita S., Behrens J., Birchmeier W., Tsukita S. V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and β-catenin is not required for the shift. J. Cell Biol. 131:1995;1839-1847.
26. Pastorekova S., Zavadova Z., Kostal M., Babusikova O., Zavada J. A novel quasi-viral agent, MaTu, is a two component system. Virology. 187:1992;620-626.
27. Kilmartin J.V., Wright B., Milstein C. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J. Cell Biol. 93:1982;576-582.
28. Adams C.L., Chen Y.T., Smith S.J., Nelson W.J. Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J. Cell Biol. 142:1998;1105-1119.
29. +-ATPase and E-cadherin . J. Cell Sci. 107:1994;3315-3324.
30. Le T.L., Yap A.S., Stow J.L. Recycling of E-cadherin a potential mechanism for regulating cadherin dynamics . J. Cell Biol. 146:1999;219-232.
31. Shore E.M., Nelson W.J. Biosynthesis of the cell adhesion molecule uvomorulin (E-cadherin) in Madin-Darby canine kidney epithelial cells. J. Biol. chem. 266:1991;19672-19680.
32. Beavon I.R.G. Regulation of E-cadherin does hypoxia initiate the metastatic cascade? J. Clin. Pathol. Mol. Pathol. 52:1999;179-188.
33. Hoschuetzky H., Aberle H., Kemler R. β-Catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127:1994;1375-1380.
34. Ochiai A., Akimoto S., Kanai Y., Shibata T., Oyama T., Hirohashi S. C-erbB-2 gene product associates with catenins in human cancer cells. Biochem. Biophys. Res. Commun. 205:1994;73-78.
35. Yamamoto M., Bharti A., Li Y., Kufe D. Interaction of the DF3/MUC1 breast carcinoma-associated antigen and β-catenin in cell adhesion. J. Biol. Chem. 272:1997;12492-12494.
36. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1991;1451-1455.
37. Birchmeier W., Behrens J. Cadherin expression in carcinomas role in the formation of cell junctions and the prevention of invasiveness . Biochim. Biophys. Acta. 1198:1994;11-26.
38. Pearl A.K., Wilgenbus P., Dahl U., Semb H., Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature. 392:1998;190-193.
39. Gumbiner B.M. Regulation of cadherin adhesive activity. J. Cell Biol. 148:2000;399-403.
40. Bartosova M., Parkkila S., Pohlodek K., Karttunen K.J., Galbavy S., Mucha V., Harris A.L., Pastorek J., Pastorekova S. Expression of carbonic anhydrase IX in breast is associated with malignant tissues and is related to overexpression of c-erbB2. J. Pathol. 197:2002;314-321.
41. Ortova Gut M., Parkkila S., Vernerová Z., Rohde E., Závada J., Höcker M., Pastorek J., Karttunen T., Zavadová Z., Knobeloch K.P., Wiedenmann B., Svoboda J., Horak I., Pastoreková S. Gastric hyperplasia in mice with targeted disruption of the carbonic anhydrase gene. Car9. Gastroenterology. 123:2002;1889-1903.
42. Kuroda S., Fukata M., Nakagawa M., Fujii K., Nakamura T., Ohkubo T., Izawa I., Nagase T., Nomura N., Tani H., Shoji I., Matsuura Y., Yonehara S., Kaibuchi K. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science. 281:1998;832-835.
43. Li S., Wang Q., Chakladar A., Bronson R.T., Bernards A. Gastric hyperplasia in mice lacking the putative Cdc42 effector IQGAP1. Mol. Cell. Biol. 20:2000;697-701.
44. Kamei T., Matozaki T., Sakisaka T., Kodama A., Yokoyama S., Peng Y.F., Nakano K., Takaishi K., Takai Y. Coendocytosis of cadherin and c-Met coupled to disruption of cell-cell adhesion in MDCK cells regulation by Rho, Rac and Rab small G proteins . Oncogene. 18:1999;6776-6784.
45. Semenza G.L. Hypoxia, clonal selection, and the role of HIF in tumor progression. Crit. Rev. Biochem. Mol. Biol. 35:2000;71-103.
46. Dang C.V., Semenza G.L. Oncogenic alterations of metabolism. Treats. Biochem. Sci. 24:1999;68-72.
47. Maxwell P.H., Pugh C.W., Ratcliffe P.J. Activation of the HIF pathway in cancer. Curr. Opin. Genet. Dev. 11:2000;293-299.
48. Bush K.T., Keller S.H., Nigam K. Genesis and reversal of the ischemic phenotype in epithelial cells. J. Clin. Invest. 106:2000;621-626.
49. Ivanov S.V., Kuzmin I., Wei M.H., Pack S., Geil L., Johnson B.E., Stanbridge E.J., Lerman M.I. Down-regulation of transmembrane carbonic anhydrases in renal cell carcinoma cell lines by wild-type von Hippel-Lindau transgenes. Proc. Natl. Acad. Sci. USA. 95:1998;12596-12601.
50. Parkkila S., Rajaniemi H., Parkkila A.K., Kivela J., Waheed A., Pastorekova S., Pastorek J., Sly W.S. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc. Natl. Acad. Sci. USA. 97:2000;2220-2224.
51. Sterling D., Reithmeier R.A.F., Casey J.R. A transport metabolon functional interaction of carbonic anhydrase II and chloride/bicarbonate exchangers . J. Biol. Chem. 276:2001;47886-47894.
52. Sterling D., Brown N.J., Supuran C.T., Casey J.R. The functional and physical relationship between the DRA bicarbonate transporter and carbonic anhydrase II. Am. J. Physiol. Cell Physiol. 283:2002;C1522-C1529.
53. Schwab A. Function and spatial distribution of ion channels and transporters in cell migration. Am. J. Physiol. Renal Physiol. 280:2001;F739-F747.
54. Peles E., Nativ M., Campbell P.L., Sakurai T., Martinez R., Lev S., Clary D., Schilling J., Barnea G., Plowman G.D., Grumet M., Schlessinger J. The carbonic anhydrase domain of receptor tyrosine phosphatase β is a functional ligand for the axonal cell recognition molecule contactin. Cell. 82:1995;251-260.