A functional channel is necessary for growth suppression by Cx37

Journal of Cell Science

Volumn 124, Issue 14, 2011, Pages 2448-2456

  Good, Miranda E ^a   Nelson, Tasha K ^a   Simon, Alexander M ^a   Burt, Janis M ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Cell cycle; Connexin 37; Gap junction

Indexed keywords

ALANINE; CONNEXIN 37; CONNEXIN 43; THREONINE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; NUCLEAR PORE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ANIMALS; CELL CYCLE; CELL GROWTH PROCESSES; CELL LINE; CELL LINE, TUMOR; CONNEXINS; DOGS; GAP JUNCTIONS; INSULINOMA; MUTAGENESIS, SITE-DIRECTED; RATS;

RATTUS;

EID: 79960401710     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.081695     Document Type: Article

References (47)

1. Alcolea, S., Jarry-Guichard, T., de Bakker, J., Gonzalez, D., Lamers, W., Coppen, S., Barrio, L., Jongsma, H., Gros, D. and Van Rijen, H. (2004). Replacement of connexin40 by connexin45 in the mouse: impact on cardiac electrical conduction. Circ. Res. 94, 100-109.
2. Ambrosi, C., Boassa, D., Pranskevich, J., Smock, A., Oshima, A., Xu, J., Nicholson, B. J. and Sosinsky, G. E. (2010). Analysis of four connexin26 mutant gap junctions and hemichannels reveals variations in hexamer stability. Biophys. J. 98, 1809-1819.
3. Bao, X., Lee, S. C., Reuss, L. and Altenberg, G. A. (2007). Change in permeant size selectivity by phosphorylation of connexin 43 gap-junctional hemichannels by PKC. Proc. Natl. Acad. Sci. USA 104, 4919-4924.
4. Beahm, D. L., Oshima, A., Gaietta, G. M., Hand, G. M., Smock, A. E., Zucker, S. N., Toloue, M. M., Chandrasekhar, A., Nicholson, B. J. and Sosinsky, G. E. (2006). Mutation of a conserved threonine in the third transmembrane helix of alpha- and betaconnexins creates a dominant-negative closed gap junction channel. J. Biol. Chem. 281, 7994-8009.
5. Brink, P. R., Cronin, K., Banach, K., Peterson, E., Westphale, E. M., Seul, K. H., Ramanan, S. V. and Beyer, E. C. (1997). Evidence for heteromeric gap junction channels formed from rat connexin43 and human connexin37. Am. J. Physiol. 273, C1386-C1396.
6. Burt, J. M., Nelson, T. K., Simon, A. M. and Fang, J. S. (2008). Connexin 37 profoundly slows cell cycle progression in rat insulinoma cells. Am. J. Physiol. Cell Physiol. 295, C1103-C1112.
7. Clark, S. A., Burnham, B. L. and Chick, W. L. (1990). Modulation of glucose-induced insulin secretion from a rat clonal beta-cell line. Endocrinology 127, 2779-2788.
8. Dang, X., Jeyaraman, M. and Kardami, E. (2006). Regulation of connexin-43-mediated growth inhibition by a phosphorylatable amino-acid is independent of gap junctionforming ability. Mol. Cell. Biochem. 289, 201-207.
9. Doble, B. W., Dang, X., Ping, P., Fandrich, R. R., Nickel, B. E., Jin, Y., Cattini, P. A. and Kardami, E. (2004). Phosphorylation of serine 262 in the gap junction protein connexin-43 regulates DNA synthesis in cell-cell contact forming cardiomyocytes. J. Cell Sci. 117, 507-514.
10. Ek-Vitorin, J. F. and Burt, J. M. (2005). Quantification of gap junction selectivity. Am. J. Physiol. Cell Physiol. 289, C1535-C1546.
11. Fu, C. T., Bechberger, J. F., Ozog, M. A., Perbal, B. and Naus, C. C. (2004). CCN3 (NOV) interacts with connexin43 in C6 glioma cells: possible mechanism of connexinmediated growth suppression. J. Biol. Chem. 279, 36943-36950.
12. Gazdar, A. F., Chick, W. L., Oie, H. K., Sims, H. L., King, D. L., Weir, G. C. and Lauris, V. (1980). Continuous, clonal, insulin- and somatostatin-secreting cell lines established from a transplatable rat islet cell tumor. Cell Biol. 77, 3519-3523.
13. Gellhaus, A., Dong, X., Propson, S., Maass, K., Klein-Hitpass, L., Kibschull, M., Traub, O., Willecke, K., Perbal, B., Lye, S. J. et al. (2004). Connexin43 interacts with NOV: a possible mechanism for negative regulation of cell growth in choriocarcinoma cells. J. Biol. Chem. 279, 36931-36942.
14. Goodenough, D. A. and Paul, D. L. (2003). Beyond the gap: functions of unpaired connexon channels. Nat. Rev. Mol. Cell Biol. 4, 285-294.
15. Harris, A. L. (2001). Emerging issues of connexin channels: biophysics fills the gap. Q. Rev. Biophys. 34, 325-472.
16. Johnstone, S. R., Best, A. K., Wright, C. S., Isakson, B. E., Errington, R. J. and Martin, P. E. (2010). Enhanced connexin 43 expression delays intra-mitotic duration and cell cycle traverse independently of gap junction channel function. J. Cell. Biochem. 110, 772-782.
17. Kardami, E., Dang, X., Iacobas, D. A., Nickel, B. E., Jeyaraman, M., Srisakuldee, W., Makazan, J., Tanguy, S. and Spray, D. C. (2007). The role of connexins in controlling cell growth and gene expression. Prog. Biophys. Mol. Biol. 94, 245-264.
18. King, T. J. and Bertram, J. S. (2005). Connexins as targets for cancer chemoprevention and chemotherapy. Biochim. Biophys. Acta 1719, 146-160.
19. Kruger, O., Plum, A., Kim, J. S., Winterhager, E., Maxeiner, S., Hallas, G., Kirchhoff, S., Traub, O., Lamers, W. H. and Willecke, K. (2000). Defective vascular development in connexin 45-deficient mice. Development 127, 4179-4193.
20. Kumari, S. S., Varadaraj, K., Valiunas, V. and Brink, P. R. (2001). Site-directed mutations in the transmembrane domain M3 of human connexin37 alter channel conductance and gating. Biochem. Biophys. Res. Commun. 280, 440-447.
21. Kurjiaka, D. T., Steele, T. D., Olsen, M. V. and Burt, J. M. (1998). Gap junction permeability is diminished in proliferating vascular smooth muscle cells. Am. J. Physiol. 275, C1674-C1682.
22. Kyle, J. W., Minogue, P. J., Thomas, B. C., Domowicz, D. A., Berthoud, V. M., Hanck, D. A. and Beyer, E. C. (2008). An intact connexin N-terminus is required for function but not gap junction formation. J. Cell Sci. 121, 2744-2750.
23. Laird, D. W. (2010). The gap junction proteome and its relationship to disease. Trends Cell Biol. 20, 92-101.
24. Larson, D. M., Seul, K. H., Berthoud, V. M., Lau, A. F., Sagar, G. D. and Beyer, E. C. (2000). Functional expression and biochemical characterization of an epitope-tagged connexin37. Mol. Cell Biol. Res. Commun. 3, 115-121.
25. Liu, S., Taffet, S., Stoner, L., Delmar, M., Vallano, M. L. and Jalife, J. (1993). A structural basis for the unequal sensitivity of the major cardiac and liver gap junctions to intracellular acidification: the carboxyl tail length. Biophys. J. 64, 1422-1433.
26. Maeda, S., Nakagawa, S., Suga, M. and Yamashita, E. (2009). Structure of the connexin 26 gap junction channel at 3.5 A resolution. Nature 458, 597-602.
27. Morel, S., Burnier, L., Roatti, A., Chassot, A., Roth, I., Sutter, E., Galan, K., Pfenniger, A., Chanson, M. and Kwak, B. R. (2010). Unexpected role for the human Cx37 C1019T polymorphism in tumour cell proliferation. Carcinogenesis 31, 1922-1931.
28. Musil, L. S. and Goodenough, D. A. (1991). Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J. Cell Biol. 115, 1357-1374.
29. Paulauskas, N., Pranevicius, M., Pranevicius, H. and Bukauskas, F. F. (2009). A stochastic four-state model of contingent gating of gap junction channels containing two "fast" gates sensitive to transjunctional voltage. Biophys. J. 96, 3936-3948.
30. Pfenniger, A., Derouette, J. P., Verma, V., Lin, X., Foglia, B., Coombs, W., Roth, I., Satta, N., Dunoyer-Geindre, S., Sorgen, P. et al. (2010). Gap junction protein Cx37 interacts with endothelial nitric oxide synthase in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 30, 827-834.
31. Plum, A., Hallas, G., Magin, T., Dombrowski, F., Hagendorff, A., Schumacher, B., Wolpert, C., Kim, J., Lamers, W. H., Evert, M. et al. (2000). Unique and shared functions of different connexins in mice. Curr. Biol. 10, 1083-1091.
32. Reaume, A. G., De Sousa, P. A., Kulkarni, S., Langille, B. L., Zhu, D., Davies, T. C., Juneja, S. C., Kidder, G. M. and Rossant, J. (1995). Cardiac malformation in neonatal mice lacking connexin43. Science 267, 1831-1834.
33. Reed, K. E., Westphale, E. M., Larson, D. M., Wang, H.-Z., Veenstra, R. D. and Beyer, E. C. (1993). Molecular cloning and functional expression of human connexin37, an endothelial cell gap junction protein. J. Clin. Invest. 91, 997-1004.
34. Scherer, S. S., Xu, Y. T., Nelles, E., Fischbeck, K., Willecke, K. and Bone, L. J. (1998). Connexin32-null mice develop demyelinating peripheral neuropathy. Glia 24, 8-20.
35. Simon, A. M., Goodenough, D. A., Li, E. and Paul, D. L. (1997). Female infertility in mice lacking connexin 37. Nature 385, 525-529.
36. Simon, A. M., Chen, H. and Jackson, C. L. (2006). Cx37 and Cx43 localize to zona pellucida in mouse ovarian follicles. Cell Commun. Adhes. 13, 61-77.
37. Sohl, G. and Willecke, K. (2004). Gap junctions and the connexin protein family. Cardiovasc. Res. 62, 228-232.
38. Solan, J. L. and Lampe, P. D. (2007). Key connexin 43 phosphorylation events regulate the gap junction life cycle. J. Membr. Biol. 217, 35-41.
39. Solan, J. L. and Lampe, P. D. (2009). Connexin43 phosphorylation: structural changes and biological effects. Biochem. J. 419, 261-272.
40. Sorgen, P. L., Duffy, H. S., Spray, D. C. and Delmar, M. (2004). pH-dependent dimerization of the carboxyl terminal domain of Cx43. Biophys. J. 87, 574-581.
41. Stergiopoulos, K., Alvarado, J. L., Mastroianni, M., Ek-Vitorin, J. F., Taffet, S. M. and Delmar, M. (1999). Hetero-domain interactions as a mechanism for the regulation of connexin channels. Circ. Res. 84, 1144-1155.
42. Traub, O., Hertlein, B., Kasper, M., Eckert, R., Krisciukaitis, A., Hulser, D. and Willecke, K. (1998). Characterization of the gap junction protein connexin37 in murine endothelium, respiratory epithelium, and after transfection in human HeLa cells. Eur. J. Cell Biol. 77, 313-322.
43. Weber, P. A., Chang, H. C., Spaeth, K. E., Nitsche, J. M. and Nicholson, B. J. (2004). The permeability of gap junction channels to probes of different size is dependent on connexin composition and permeant-pore affinities. Biophys. J. 87, 958-973.
44. White, T. W. (2002). Unique and redundant connexin contributions to lens development. Science 295, 319-320.
45. Wong, C. W., Christen, T., Roth, I., Chadjichristos, C. E., Derouette, J. P., Foglia, B. F., Chanson, M., Goodenough, D. A. and Kwak, B. R. (2006). Connexin37 protects against atherosclerosis by regulating monocyte adhesion. Nat. Med. 12, 950-954.
46. Zhang, Y. W., Kaneda, M. and Morita, I. (2003a). The gap junction-independent tumorsuppressing effect of connexin 43. J. Biol. Chem. 278, 44852-44856.
47. Zhang, Y. W., Nakayama, K., Nakayama, K. and Morita, I. (2003b). A novel route for connexin 43 to inhibit cell proliferation: negative regulation of S-phase kinase-associated protein (Skp 2). Cancer Res. 63, 1623-1630.