Connexins and cancer

Biology of the Cell

Volumn 94, Issue 7-8, 2002, Pages 493-500

  Mesnil, Marc ^a  

^a UNIVERSITÉ DE POITIERS   (France)

Author keywords

Cancer; Cell growth; Connexin; Gap junction; Gap junctional intercellular communication; Tomour suppression

Indexed keywords

GAP JUNCTION PROTEIN; TUMOR PROMOTER; TUMOR SUPPRESSOR PROTEIN;

BIOLOGICAL MODEL; CANCER CONTROL; CANCER GROWTH; CANCER INHIBITION; CANCER RESEARCH; CARCINOGENESIS; CELL ACTIVATION; CELL COMMUNICATION; CELL TRANSFORMATION; CELL TYPE; CELLULAR DISTRIBUTION; GAP JUNCTION; HISTORY OF MEDICINE; HUMAN; HYPOTHESIS; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR CLONING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SPECIES DIFFERENCE; TUMOR CELL; TUMOR PROMOTION;

ANIMALS; CELL COMMUNICATION; CELL TRANSFORMATION, NEOPLASTIC; CONNEXINS; HUMANS; NEOPLASMS; TUMOR SUPPRESSOR PROTEINS;

EID: 0036873006     PISSN: 02484900     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0248-4900(02)00025-4     Document Type: Review

References (67)

1. Ainsworth, P.J., Bolton, C.F., Murphy, B.C., Stuart, J.A., Hahn, A.F., 1998. Genotype/phenotype correlation in affected individuals of a family with a deletion of the entire coding sequence of the connexin32 gene. Hum. Genet. 103, 242-244.
2. Anzini, P., Neuberg, H., Schachner, M., Nelles, Willecke, K., Zielasek, J., Toyka, K.V., Suter, U., Martini, R., 1997. Structural abnormalities and deficient maintenance of peripheral nerve myelin in mice lacking the gap junction protein connexin32. J. Neurosci. 17, 4545-4551.
3. Asamoto, M., Takahashi, S., Imaida, K., Shirai, T., Fukushima, S., 1994. Increased gap junctional intercellular communication capacity and connexin43 and 26 expression in rat bladder carcinogenesis. Carcinogenesis 15, 2163-2166.
4. Asamoto, M., Toriyama-Baba, H., Krutovskikh, V., Cohen, S.M., Tsuda, H., 1998. Enhanced tumorigenicity of rat bladder squamous cell carcinoma cells by abrogation of gap junctional intercellular communication. Jpn. J. Cancer 89, 481-486.
5. Bager, Y., Kenne, K., Krutovskikh, V., Mesnil, M., Traub, O., Wärngard, L., 1994. Alteration in expression of gap junction proteins in rat liver after treatment with the tumour promoter 3,4,5,3′,4′-pentachlorobiphenyl. Carcinogenesis 15, 2439-2443.
6. Berenblum, I., 1941a. The cocarcinogenic action of croton resin. Cancer Res. 1, 44-48.
7. Berenblum, I., 1941b. The mechanism of carcinogenesis: a study of the significance of cocarcinogenic action and related phenomena. Cancer Res. 1, 807-814.
8. Bereblum, I., Shubik, P., 1947. A new, quantitative, approach to the study of the stages of chemical carcinogenesis in the mouse's skin. Br. J. Cancer 1, 383-391.
9. Beyer, E.C., Paul, D.L., Goodenough, D.A., 1987. Connexin43: a protein from rat heart homologous to a gap junction protein from liver. J. Cell Biol. 105, 2621-2629.
10. Bond, S.L., Bechberger, J.F., Khoo, N.K., Naus, C.C., 1994. Transfection of C6 glioma cells with connexin32: the effects of expression of a nonendogenous gap junction protein. Cell Growth Differ. 5, 179-186.
11. Budunova, I.V., Williams, G.M., 1994. Cell culture assays for chemicals with tumor-promoting or tumor-inbibiting activity based on the modulation of intercellular communication. Cell Biol. Toxicol. 10, 71-138.
12. Chanson, M., Fanjul, M., Bosco, D., Nelles, E., Suter, S., Willecke, K., Meda, P., 1998. Enhanced secretion of amylase from exocrine pancreas of connexin32-deficient mice. J. Cell Biol. 141, 1267-1275.
13. Chen, S.C., Pelletier, D.B., Ao, P., Boynton, A.L., 1995. Connexin43 reverses the phenotype of transformed cells and alters their expression of cyclin/cyclin-dependent kinases. Cell Growth Differ. 6, 681-690.
14. de Feijter, A.W., Matesic, D.F., Ruch, R.J., Guan, X., Chang, C.C., Trosko, J.E., 1996. Localization and function of the connexin43 gap-junction protein in normal and various oncogene-expressing rat liver epithelial cells. Mol. Carcinog. 16, 203-212.
15. De Sousa, P.A., Juneja, S.C., Caveney, S., Houghton, F.D., Davies, T.C., Reaume, A.G., Rossant, J., Kidder, G.M., 1997. Normal development of preimplantation mouse embryos deficient in gap junctional coupling. J. Cell Sci. 110, 1751-1758.
16. Duflot-Dancer, A., Mesnil, M., Yamasaki, H., 1997. Dominant-negative abrogation of connexin-mediated cell growth control by mutant connexin genes. Oncogene 15, 2151-2158.
17. Eghbali, B., Kessler, J.A., Reid, L.M., Roy, C., Spray, D.C., 1991. Involvement of gap junctions in tumorigenesis: transfection of tumor cells with connexin32 cDNA retards growth in vivo. Proc. Natl. Acad. Sci. USA 88, 10701-10705.
18. Enomoto, T., Yamasaki, H., 1984. Lack of intercellular communication between chemically transformed and surrounding non transformed BALB/c 3T3 cells. Cancer Res. 44, 5200-5203.
19. Fitzgerald, D.J., Mesnil, M., Oyamada, M., Tsuda, H., Ito, N., Yamasaki, H., 1989. Changes in gap junction protein (connexin32) gene expression during rat liver carcinogenesis. J. Cell Biochem. 41, 97-102.
20. Giepmans, B.N.G., Moolenaar, W.H., 1998. The gap junction protein connexin43 interacts with the second PDZ domain of the zona occludens-1 protein. Curr. Biol. 8, 931-934.
21. Goldberg, G.S., Lampe, P.D., Sheedy, D., Stewart, C.C., Nicholson, B.J., Naus, C.C., 1998. Direct isolation and analysis of endogenous transjunctional ADP from Cx43-transfected C6 glioma cells. Exp. Cell Res. 239, 82-91.
22. Hirschi, K.K., Xu, C., Tsukamoto, T., Sager, R., 1996. Gap junction genes Cx26 and Cx43 individually suppress the cancer phenotype of human mammary carcinoma cells and restore differentiation potential. Cell Growth Differ. 7, 861-870.
23. Huang, R.P., Fan, Y., Hossain, M.Z., Peng, A., Zeng, Z.L., Boynton, A.L., 1998. Reversion of the neoplastic phenotype of human glioblastoma cells by connexin43 (Cx43). Cancer Res. 58, 5089-5096.
24. Huang, R., Lin, Y., Wang, C.C., Gano, J., Lin, B., Shi, Q., Boynton, A., Burke, J., Huang, R.P., 2002. Connexin43 suppresses glioblastoma cell growth by down-regulation of monocyte chemotactic protein 1, as discovered using protein array technology. Cancer Res. 62, 2806-2812.
25. Jamakosmanovic, A., Loewenstein, W.R., 1968. Cellular uncoupling in cancerous thyroid epithelium. Nature 218, 775.
26. Kam, Y., Kim, D.Y., Koo, S.K., Joe, C.O., 1998. Transfer of second messengers through gap junction connexin43 channels reconstituted in liposomes. Biochim. Biophys. Acta 1372, 384-388.
27. Kanno, Y., Matsui, Y., 1968. Cellular uncoupling in cancerous stomach epithelium. Nature 218, 775-776.
28. King, T.J., Fukushima, L.H., Hieber, A.D., Shimabukuro, K.A., Sakr, W.A., Bertram, J.S., 2000a. Reduced levels of connexin43 in cervical dysplasia: inducible expression in a cervical carcinoma cell line decreases neoplastic potential with implications for tumor progression. Carcinogenesis 21, 1097-1109.
29. King, T.J., Fukushima, L.H., Donlon, T.A., Hieber, A.D., Shimabukuro, K.A., Bertram, J.S., 2000b. Correlation between growth control, neoplastic potential and endogenous connexin43 expression in HeLa cell lines: implications for tumor progression. Carcinogenesis 21, 311-315.
30. Koffier, L., Roshong, S., Kyu Park, I., Cesen-Cummings, K., Thompson, D.C., Dwyer-Nield, L.D., Rice, P., Mamay, C., Malkinson, A.M., Ruch, R.J., 2000. Growth inhibition in G(1) and altered expression of cyclin D1 and p27 (kip-1) after forced connexin expression in lung and liver carcinoma cells. J. Cell Biochem, 79, 347-354.
31. Krutovskikh, V., Oyamada, M., Yamasaki, H., 1991. Sequential changes of gap-junctional intercellular communication during multistage rat liver carcinogenesis: direct measurement of communication in vivo. Carcinogenesis 12, 1701-1706.
32. Krutovskikh, V., Mazzoleni, G., Mironov, N., Omori, Y., Aguelon, A.M. Mesnil, M., Berger, F., Partensky, C., Yamasaki, H., 1994. Altered homologous and heterologous gap-junctional intercellular communication in primary human liver tumors associated with aberrant protein localisation but not gene mutation of connexin32. Int. J. Cancer 56, 87-94.
33. Krutovskikh, V., Mesnil, M., Mazzoleni, G., Yamasaki, H., 1995. Inhibition of rat liver gap junction intercellular communication by tumorpromoting agents in vivo: association with aberrant localization of connexin proteins. Lab. Invest, 72, 571-577.
34. Krutovskikh, V.A., Yamasaki, H., Tsuda, H., Asamoto, M., 1998. Inhibition of intrinsic gap-junction intercellular communication and enhancement of tumorigenicity of the rat bladder carcinoma cell line BC31 by a dominant-negative connexin43 mutant. Mol. Carcinog. 23, 254-261.
35. Kumar, N.M., Gilula, N.B., 1986. Cloning and characterization of human and rat liver cDNAs coding for a gap junction protein. J. Cell Biol. 103, 767-776.
36. Loewenstein, W.R., Kanno, Y., 1966. Intercellular communication and the control of tissue growth: lack of communication between cancer cells. Nature 209, 1248-1249.
37. Loewenstein, W.R., Kanno, Y., 1967. Intercellular communication and tissue growth. I. Cancer growth. J. Cell Biol. 33, 225-234.
38. Loewenstein, W.R., 1979. Junctional intercellular communication and the control of growth. Biochim. Biophys. Acta. 560, 1-65.
39. Mehta, P.P., Bertram, J.S., Loewenstein, W.R., 1986. Growth inhibition of transformed cells correlates with their junctional communication with normal cells. Cell 44, 187-196.
40. Mehta, P.P., Perez-Stable, C., Nadji, M., Mian, M., Asotra, K., Roos, B.A., 1999. Suppression of human prostate cancer cell growth by forced expression of connexin genes. Dev. Genet. 24, 91-110.
41. Mesnil, M., Yamasaki, H., 1988. Selective gap-junctional communication capacity of transformed and nontransformed rat liver epithelial cell lines. Carcinogenesis 9, 1499-1502.
42. Mesnil, M., Yamasaki, H., 1993. Cell-cell communication and growth control of normal and cancer cells: evidence and hypothesis. Mol. Carcinog. 7, 14-17.
43. Mesnil, M., Piccoli, C., Yamasaki, H., 1993. An improved long-term culture of rat hepatocytes to detect liver tumour-promoting agents: results with phenobarbital. Eur. J. Pharmacol. 248, 59-66.
44. Mesnil, M., Krutovskikh, V., Piccoli, C., Elfgang, C., Traub, O., Willecke, K., Yamasaki, H., 1995. Negative growth control of HeLa cells by connexin genes: connexin species specificity. Cancer Res. 55, 629-639.
45. Mesnil, M., Yamasaki, H., 2000. Bystander effect in Herpes simplex virus - thymidine kinase/ganciclovir cancer gene therapy: role of gap-junctional intercelluiar communication. Cancer Res. 60, 3989-3999.
46. Murray, A.W., Fitzgerald, D.J., 1979. Tumor promoters inhibit metabolic cooperation in coculture of epidermal and 3T3 cells. Biochem. Biophys. Res. Commun. 91, 395-401.
47. Naus, C.C.G., Elisevich, K., Zhou, D., Beliveau, D.J., Del Maestro, R.F., 1992. In vivo growth of C6 glioma cells transfected with connexin43 cDNA. Cancer Res. 52, 4208-4213.
48. Naus, C.C.G., Bond, S.L., Bechberger, J.F., Rushlow, W., 2000. Identification of genes differentially expressed in C6 glioma cells transfected with connexin43. Brain Res. Brain Res. Rev. 32, 259-266.
49. Nelis, E., Haites, N., Van Broeckhoven, C., 1999. Mutations in the peripheral myelin genes and associated genes in inherited peripheral neuropathies. Hum. Mutat. 13, 11-28.
50. Nelles, E., Bützler, C., Jung, D., Temme, A., Gabriel, H.D., Dahl, U., Traub, O., Stümpel, F., Jungermann, K., Zielasek, J., Toyka, K.V, Dermietzel, R., Willecke, K., 1996. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. USA 93, 9565-9570.
51. Paul, D.L., 1986. Molecular cloning of cDNA for rat liver gap junction protein. J. Cell Biol. 103, 123-134.
52. Penn, R.D., 1966. Ionic communication between liver cells. J. Cell Biol. 29, 171-174.
53. Princen, F., Robe, P., Gros, D., Jarry-Guichard, T., Gielen, J., Merville, M.P., Bours, V., 2001. Rat gap junction connexin-30 inhibits proliferation of glioma cell lines. Carcinogenesis 22, 505-513.
54. Reaume, A.G., De Sousa, PA., Kulkarni, S., Langille, B.L., Zhu, D., Davies, T.C., Junega, S.C., Kidder, G.M., Rossant, J., 1995. Cardiac malformation in neonatal mice lacking connexin43. Science 267, 1831-1834.
55. Risek, B., Pozzi, A., Gilula, N.B., 1998. Modulation of gap junction expression during transient hyperplasia of rat epidermis. J. Cell Sci. 111, 1395-1404.
56. Rose, B., Mehta, P.P., Loewenstein, W.R., 1993. Gap junction protein gene suppresses tumorigenicity. Carcinogenesis 14, 1073-1075.
57. Saez, J.C., Connor, J.A., Spray, D.C., Bennett, M.W.L., 1989. Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-triphosphate, and to calcium ions. Proc. Natl. Acad. Sci. USA 86, 2708-2712.
58. Stoker, M., 1964. Regulation of growth and orientation in hamster cells transformed by polyoma virus. Virology 24, 165-174.
59. Stümpel, F., Ott, T., Willecke, K., Jungermann, K., 1998, Connexin32 gap junctions enhance stimulation of glucose output by glucagon and noradrenaline in mouse liver. Hepatology 28, 1616-1620.
60. Su, Y.A., Bittner, M.L., Chen, Y., Tao, L., Jiang, Y., Zhang, Y., Stephan, D.A., Trent, J.M., 2000. Identification of tumor-suppressor genes using human melanoma cell lines UACC903, UACC903(+6), and SRS3 by comparison of expression profiles. Mol. Carcinog. 28, 119-127.
61. Temme, A., Buchmann, A., Gabriel, H.D., Nelles, E., Schwartz, M., Willecke, K., 1997. High incidence of spontaneous and chemically induced liver tumors in mice deficient for connexin32. Curr. Biol. 7, 713-716.
62. Trosko, J.E., Chang, C.C., 2001. Mechanism of up-regulated gap junctional intercellular communication during chemoprevention and chemotherapy of cancer. Mutat. Res. 480-481, 219-229.
63. Yamasaki, H., Katoh, F., 1988. Further evidence for the involvement of gap-junctional intercellular communication in induction and maintenance of transformed foci in BALB/c 3T3 cells. Cancer Res. 48, 3490-3495.
64. Yamasaki, H., Naus, C.C.G., 1996. Role of connexin genes in growth control. Carcinogenesis 17, 1199-1213.
65. Yotti, L.P., Chang, C.C., Trosko, J.E., 1979. Elimination of metabolic cooperation in Chinese hamster cells by a tumor promoter. Science 206, 1089-1091.
66. Zhang, Z.Q., Zhang, W., Wang, N.Q., Bani-Yaghoub, M., Lin, Z.X., Naus, C.C.G., 1998. Suppression of tumorigenicity of human lung carcinoma cells after transfection with connexin43. Carcinogenesis 19, 1889-1894.
67. Zhu, D., Caveney, S., Kidder, G.M., Naus, C.C.G., 1991. Transfection of C6 glioma cells with connexin43 cDNA: analysis of expression, intercellular coupling, and cell proliferation. Proc. Natl. Acad. Sci. USA 88, 1883-1887.