The stage-specific function of gap junctions during tumourigenesis

• Autorzy: Czyz J
• Języki publikacji: EN

Abstrakty

EN

Tumour development is a process resulting from the disturbance of various cellular functions including cell proliferation, adhesion and motility. While the role of these cell parameters in tumour promotion and progression has been widely recognized, the mechanisms that influence gap junctional coupling during tumorigenesis remain elusive. Neoplastic cells usually display decreased levels of connexin expression and/or gap junctional coupling. Thus, impaired intercellular communication via gap junctions may facilitate the release of a potentially neoplastic cell from the controlling regime of the surrounding tissue, leading to tumour promotion. However, recent data indicates that metastatic tumour cell lines are often characterized by relatively high levels of connexin expression and gap junctional coupling. This review outlines current knowledge on the role of connexins in tumorigenesis and the possible mechanisms of the interference of gap junctional coupling with the processes of tumour invasion and metastasis.

Słowa kluczowe

EN

gap junction; connexin; tumour; tumourigenesis; metastasis; tumour development; cell proliferation; adhesion; motility; cell parameter

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2008
• Tom: 13
• Numer: 1
• Opis fizyczny: p.92-102,fig.,ref.

Twórcy

autor

Czyz J

• Jagiellonian University, Gronostajowa 7, 30-378 Krakow, Poland

Bibliografia

• 1. Sohl, G. and Willecke, K. Gap junctions and the connexin protein family. Cardiovasc. Res. 62 (2004) 228-232.
• 2. Niessen, H., Harz, H., Bedner, P., Kramer, K. and Willecke, K. Selective permeability of different connexin channels to the second messenger inositol 1,4,5-trisphosphate. J. Cell Sci. 113 (2000) 1365-1372.
• 3. Plum, A., Hallas, G., Magin, T., Dombrowski, F., Hagendorff, A., Schumacher, B., Wolpert, C., Kim, J., Lamers, W.H., Evert, M., Meda, P., Traub, O. and Willecke, K. Unique and shared functions of different connexins in mice. Curr. Biol. 10 (2000) 1083-1091.
• 4. Bedner, P., Niessen, H., Odermatt, B., Kretz, M., Willecke, K. and Harz, H. Selective permeability of different connexin channels to the second messenger cyclic AMP. J. Biol. Chem. 281 (2006) 6673-6681.
• 5. Sohl, G., Maxeiner, S. and Willecke, K. Expression and functions of neuronal gap junctions. Nat. Rev. Neurosci. 6 (2005) 191-200.
• 6. Alexander, D.B. and Goldberg, G.S. Transfer of biologically important molecules between cells through gap junction channels. Curr. Med. Chem. 10 (2003) 2045-2058.
• 7. White, T.W. and Paul, D.L. Genetic diseases and gene knockouts reveal diverse connexin functions. Annu. Rev. Physiol. 61 (1999) 283-310.
• 8. Laird, D.W. Life cycle of connexins in health and disease. Biochem. J. 394 (2006) 527-543.
• 9. Wei, C.J., Xu, X. and Lo, C.W. Connexins and Cell Signaling in Development and Disease. Annu. Rev. Cell Dev. Biol. 20 (2004) 811-838.
• 10. Nelles, E., Butzler, C., Jung, D., Temme, A., Gabriel, H.D., Dahl, U., Traub, O., Stumpel, F., Jungermann, K., Zielasek, J., Toyka, K.V., Dermietzel, R. and Willecke, K. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. USA 93 (1996) 9565-9570.
• 11. Oyamada, M., Oyamada, Y. and Takamatsu, T. Regulation of connexin expression. Biochim. Biophys. Acta 1719 (2005) 6-23.
• 12. Peracchia, C. Chemical gating of gap junction channels; roles of calcium, pH and calmodulin. Biochim. Biophys. Acta 1662 (2004) 61-80.
• 13. Luebeck, E.G., Buchmann, A., Schneider, D., Moolgavkar, S.H. and Schwarz, M. Modulation of liver tumorigenesis in Connexin32-deficient mouse. Mutat. Res. 570 (2005) 33-47.
• 14. Naus, C.C., Bechberger, J.F., Caveney, S. and Wilson, J.X. Expression of gap junction genes in astrocytes and C6 glioma cells. Neurosci. Lett. 126 (1991) 33-36.
• 15. Jamieson, S., Going, J.J., D'Arcy, R. and George, W.D. Expression of gap junction proteins connexin 26 and connexin 43 in normal human breast and in breast tumours. J. Pathol. 184 (1998) 37-43.
• 16. Yamasaki, H., Krutovskikh, V., Mesnil, M., Tanaka, T., Zaidan-Dagli, M.L. and Omori, Y. Role of connexin (gap junction) genes in cell growth control and carcinogenesis. C. R. Acad. Sci. III 322 (1999) 151-159.
• 17. Saunders, M.M., Seraj, M.J., Li, Z., Zhou, Z., Winter, C.R., Welch, D.R. and Donahue, H.J. Breast cancer metastatic potential correlates with a breakdown in homospecific and heterospecific gap junctional intercellular communication. Cancer Res. 61 (2001) 1765-1767.
• 18. Zhu, D., Caveney, S., Kidder, G.M. and Naus, C.C. Transfection of C6 glioma cells with connexin 43 cDNA: analysis of expression, intercellular coupling, and cell proliferation. Proc. Natl. Acad. Sci. USA 88 (1991) 1883-1887.
• 19. Hirschi, K.K., Xu, C.E., Tsukamoto, T. and Sager, R. Gap junction genes Cx26 and Cx43 individually suppress the cancer phenotype of human mammary carcinoma cells and restore differentiation potential. Cell Growth Differ. 7 (1996) 861-870.
• 20. Yamasaki, H., Omori, Y., Zaidan-Dagli, M.L., Mironov, N., Mesnil, M. and Krutovskikh, V. Genetic and epigenetic changes of intercellular communication genes during multistage carcinogenesis. Cancer Detect. Prev. 23 (1999) 273-279.
• 21. Goldberg, G.S., Bechberger, J.F., Tajima, Y., Merritt, M., Omori, Y., Gawinowicz, M.A., Narayanan, R., Tan, Y., Sanai, Y., Yamasaki, H., Naus, C.C., Tsuda, H. and Nicholson, B.J. Connexin43 suppresses MFG-E8 while inducing contact growth inhibition of glioma cells. Cancer Res. 60 (2000) 6018-6026.
• 22. Chen, S.C., Pelletier, D.B., Ao, P. and Boynton, A.L. Connexin43 reverses the phenotype of transformed cells and alters their expression of cyclin/cyclin-dependent kinases. Cell Growth Differ. 6 (1995) 681-690.
• 23. Fujimoto, E., Satoh, H., Negishi, E., Ueno, K., Nagashima, Y., Hagiwara, K., Yamasaki, H. and Yano, T. Negative growth control of renal cell carcinoma cell by connexin 32: possible involvement of Her-2. Mol. Carcinog. 40 (2004) 135-142.
• 24. Loewenstein, W.R. and Rose, B. The cell-cell channel in the control of growth. Semin. Cell Biol. 3 (1992) 59-79.
• 25. Rose, B., Mehta, P.P. and Loewenstein, W.R. Gap-junction protein gene suppresses tumorigenicity. Carcinogenesis 14 (1993) 1073-1075.
• 26. Moorby, C. and Patel, M. Dual functions for connexins: Cx43 regulates growth independently of gap junction formation. Exp. Cell Res. 271 (2001) 238-248.
• 27. Lesueur, F., Mesnil, M., Delouvee, A., Girault, J. M., Yamasaki, H., Thiery, J.P. and Jouanneau, J. NBT-II carcinoma behaviour is not dependent on cellcell communication through gap junctions. Biochem. Biophys. Res. Commun. 294 (2002) 108-115.
• 28. Qin, H., Shao, Q., Curtis, H., Galipeau, J., Belliveau, D.J., Wang, T., Alaoui-Jamali, M.A. and Laird, D.W. Retroviral delivery of connexin genes to human breast tumor cells inhibits in vivo tumor growth by a mechanism that is independent of significant gap junctional intercellular communication. J. Biol. Chem. 277 (2002) 29132-29138.
• 29. Alexander, D.B., Ichikawa, H., Bechberger, J.F., Valiunas, V., Ohki, M., Naus, C. C., Kunimoto, T., Tsuda, H., Miller, W.T. and Goldberg, G.S. Normal cells control the growth of neighboring transformed cells independent of gap junctional communication and SRC activity. Cancer Res. 64 (2004) 1347-1358.
• 30. Zhang, Y.W., Kaneda, M. and Morita, I. The gap junction-independent tumor-suppressing effect of connexin 43. J. Biol. Chem. 278 (2003) 44852- 44856.
• 31. Zhang, Y. W., Nakayama, K., Nakayama, K. and Morita, I. A novel route for connexin 43 to inhibit cell proliferation: negative regulation of S-phase kinase-associated protein (Skp 2). Cancer Res. 63 (2003) 1623-1630.
• 32. Dang, X., Jeyaraman, M. and Kardami, E. Regulation of connexin-43- mediated growth inhibition by a phosphorylatable amino-acid is independent of gap junction-forming ability. Mol. Cell Biochem. 289 (2006) 201-207.
• 33. Chambers, A.F. The metastatic process: basic research and clinical implications. Oncol. Res. 11 (1999) 161-168.
• 34. Guo, W. and Giancotti, F.G. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5 (2004) 816-826.
• 35. Kanczuga-Koda, L., Sulkowski, S., Lenczewski, A., Koda, M., Wincewicz, A., Baltaziak, M. and Sulkowska, M. Increased expression of connexins 26 and 43 in lymph node metastases of breast cancer. J. Clin. Pathol. 59 (2006) 429-433.
• 36. Kamibayashi, Y., Oyamada, Y., Mori, M. and Oyamada, M. Aberrant expression of gap junction proteins (connexins) is associated with tumor progression during multistage mouse skin carcinogenesis in vivo. Carcinogenesis 16 (1995) 1287-1297.
• 37. Miekus, K., Czernik, M., Sroka, J., Czyz, J. and Madeja, Z. Contact stimulation of prostate cancer cell migration: the role of gap junctional coupling and migration stimulated by heterotypic cell-to-cell contacts in determination of the metastatic phenotype of Dunning rat prostate cancer cells. Biol. Cell 97 (2005) 893-903.
• 38. Tate, A.W., Lung, T., Radhakrishnan, A., Lim, S.D., Lin, X. and Edlund, M. Changes in gap junctional connexin isoforms during prostate cancer progression. Prostate 66 (2006) 19-31.
• 39. Zhang, W., Nwagwu, C., Le, D.M., Yong, V.W., Song, H. and Couldwell, W.T. Increased invasive capacity of connexin43-overexpressing malignant glioma cells. J. Neurosurg. 99 (2003) 1039-1046.
• 40. El Sabban, M.E. and Pauli, B.U. Cytoplasmic dye transfer between metastatic tumor cells and vascular endothelium. J. Cell Biol. 115 (1991) 1375-1382.
• 41. Ito, A., Katoh, F., Kataoka, T.R., Okada, M., Tsubota, N., Asada, H., Yoshikawa, K., Maeda, S., Kitamura, Y., Yamasaki, H. and Nojima, H. A role for heterologous gap junctions between melanoma and endothelial cells in metastasis. J. Clin. Invest. 105 (2000) 1189-1197.
• 42. Graeber, S.H. and Hulser, D.F. Connexin transfection induces invasive properties in HeLa cells. Exp. Cell Res. 243 (1998) 142-149.
• 43. Czyz, J., Irmer, U., Zappe, C., Mauz, M. and Hulser, D.F. Hierarchy of carcinoma cell responses to apigenin: gap junctional coupling versus proliferation. Oncol. Rep. 11 (2004) 739-744. 44.
• 44. Czyz, J., Madeja, Z., Irmer, U., Korohoda, W. and Hulser, D. F. Flavonoid apigenin inhibits motility and invasiveness of carcinoma cells in vitro. Int. J. Cancer 114 (2005) 12-18.
• 45. Traub, O., Eckert, R., Lichtenberg-Frate, H., Elfgang, C., Bastide, B., Scheidtmann, K.H., Hulser, D.F. and Willecke, K. Immunochemical and electrophysiological characterization of murine connexin40 and -43 in mouse tissues and transfected human cells. Eur. J. Cell Biol. 64 (1994) 101- 112.
• 46. Koffler, L., Roshong, S., Kyu, P.I, Cesen-Cummings, K., Thompson, D.C., Dwyer-Nield, L.D., Rice, P., Mamay, C., Malkinson, A.M. and Ruch, R.J. Growth inhibition in G(1) and altered expression of cyclin D1 and p27(kip1) after forced connexin expression in lung and liver carcinoma cells. J. Cell Biochem. 79 (2000) 347-354.
• 47. Madeja, Z., Szymkiewicz, I., Zaczek, A., Sroka, J., Miekus, K. and Korohoda, W. Contact-activated migration of melanoma B16 and sarcoma XC cells. Biochem. Cell Biol. 79 (2001) 425-440.
• 48. Sroka, J., Kaminski, R., Michalik, M., Madeja, Z., Przestalski, S. and Korohoda, W. The effect of triethyllead on the motile activity of walker 256 carcinosarcoma cells. Cell. Mol. Biol. Lett. 9 (2004) 15-30.
• 49. Czyz, J., Irmer, U., Schulz, G., Mindermann, A. and Hulser, D.F. Gapjunctional coupling measured by flow cytometry. Exp. Cell Res. 255 (2000) 40-46.
• 50. Madeja, Z., Miekus, K., Sroka, J., Djamgoz, M.B. and Korohoda, W. Homotypic cell-cell contacts stimulate the motile activity of rat prostate cancer cells. BJU Int. 88 (2001) 776-786.
• 51. Eugenin, E.A., Branes, M.C., Berman, J.W. and Saez, J.C. TNF-alpha plus IFN-gamma induce connexin43 expression and formation of gap junctions between human monocytes/macrophages that enhance physiological responses. J. Immunol. 170 (2003) 1320-1328.
• 52. Van Rijen, H.V., van Kempen, M.J., Postma, S. and Jongsma, H.J. Tumour necrosis factor alpha alters the expression of connexin43, connexin40, and connexin37 in human umbilical vein endothelial cells. Cytokine 10 (1998) 258-264.
• 53. Van Kempen, M.J. and Jongsma, H.J. Distribution of connexin37, connexin40 and connexin43 in the aorta and coronary artery of several mammals. Histochem. Cell Biol. 112 (1999) 479-486.
• 54. Kwak, B.R., Mulhaupt, F., Veillard, N., Gros, D.B. and Mach, F. Altered pattern of vascular connexin expression in atherosclerotic plaques. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 225-230.
• 55. Lewalle, J.M., Cataldo, D., Bajou, K., Lambert, C.A. and Foidart, J.M. Endothelial cell intracellular Ca2+ concentration is increased upon breast tumor cell contact and mediates tumor cell transendothelial migration. Clin. Exp. Metastasis 16 (1998) 21-29.