Gap junction and hemichannel-independent actions of connexins on cell and tissue functions - An update

FEBS Letters

Volumn 588, Issue 8, 2014, Pages 1186-1192

  Zhou, Jade Z ^a   Jiang, Jean X ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Connexin; Gap junction; Hemichannel; Independent function

Indexed keywords

CONNEXIN; GAP JUNCTION; HEMICHANNEL; INDEPENDENT FUNCTION;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL MOVEMENT; CONNEXINS; GAP JUNCTIONS; HUMANS; SIGNAL TRANSDUCTION;

EID: 84898856565     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.01.001     Document Type: Conference Paper

References (59)

1. W.H. Evans, E. de Vuyst, and L. Leybaert The gap junction cellular internet: connexin hemichannels enter the signaling limelight Biochem. J. 397 2006 1 14 (Pubitemid 44032830)
2. D.B. Alexander, and G.S. Goldberg Transfer of biologically important molecules between cells through gap junction channels Curr. Med. Chem. 10 2003 2045 2058 (Pubitemid 37139061)
3. D.A. Goodenough, J.A. Goliger, and D.L. Paul Connexins, connexons, and intercellular communication Annu. Rev. Biochem. 65 1996 475 502 (Pubitemid 26250617)
4. D.W. Laird Life cycle of connexins in health and disease Biochem. J. 394 2006 527 543
5. M. Mesnil, S. Crespin, J.L. Avanzo, and M.L. Zaidan-Dagli Defective gap junctional intercellular communication in the carcinogenic process Biochim. Biophys. Acta 1719 2005 125 145 (Pubitemid 41785641)
6. J.X. Jiang, and S. Gu Gap junction- and hemichannel-independent actions of connexins Biochim. Biophys. Acta 1711 2005 208 214 (Pubitemid 40799295)
7. H.A. Dbouk, R.M. Mroue, M.E. El Sabban, and R.S. Talhouk Connexins: a myriad of functions extending beyond assembly of gap junction channels Cell Commun. Signal. 7 2009 4
8. C. Moorby, and M. Patel Dual functions for connexins: Cx43 regulates growth independently of gap junction formation Exp. Cell Res. 271 2001 238 248 (Pubitemid 33141205)
9. M. Vinken, E. Decrock, L. Leybaert, G. Bultynck, B. Himpens, T. Vanhaecke, and V. Rogiers Non-channel functions of connexins in cell growth and cell death Biochim. Biophys. Acta 1818 2012 2002 2008
10. M. Vinken, E. Decrock, E. de Vuyst, R. Ponsaerts, C. D'hondt, G. Bultynck, L. Ceelen, T. Vanhaecke, L. Leybaert, and V. Rogiers Connexins: sensors and regulators of cell cycling Biochim. Biophys. Acta 1815 2011 13 25
11. W.R. Loewenstein, and Y. Kanno Intercellular communication and the control of tissue growth: lack of communication between cancer cells Nature 209 1966 1248 1249
12. C.C. Naus Gap junctions and tumour progression Can. J. Physiol. Pharmacol. 80 2002 136 141 (Pubitemid 34258662)
13. L. Cronier, S. Crespin, P.-O. Strale, N. Defamie, and M. Mesnil Gap junctions and cancer: new functions for an old story Antioxid. Redox Signalling 11 2009 323 328
14. J. Kalra, Q. Shao, H. Qin, T. Thomas, M.A. Alaoui-Jamali, and D.W. Laird Cx26 inhibits breast MDA-MB-435 cell tumorigenic properties by a gap junctional intercellular communication-independent mechanism Carcinogenesis 27 2006 2528 2537 (Pubitemid 44884112)
15. H.T. Xu, Q.C. Li, Y.X. Zhang, Y. Zhao, Y. Liu, Z.Q. Yang, and E.H. Wang Connexin 43 recruits E-cadherin expression and inhibits the malignant behaviour of lung cancer cells Folia Histochem. Cytobiol. 46 2008 315 321
16. M. Ionta, R.A. Ferreira, S.C. Pfister, and G.M. Machado-Santelli Exogenous Cx43 expression decrease cell proliferation rate in rat hepatocarcinoma cells independently of functional gap junction Cancer Cell Int. 9 2009 22
17. Q. Li, Y. Omori, Y. Nishikawa, T. Yoshioka, Y. Yamamoto, and K. Enomoto Cytoplasmic accumulation of connexin32 protein enhances motility and metastatic ability of human hepatoma cells in vitro and in vivo Int. J. Cancer 121 2007 536 546 (Pubitemid 46986486)
18. C. Lamiche, J. Clarhaut, P.O. Strale, S. Crespin, N. Pedretti, F.X. Bernard, C.C. Naus, V.C. Chen, L.J. Foster, N. Defamie, M. Mesnil, F. Debiais, and L. Cronier The gap junction protein Cx43 is involved in the bone-targeted metastatic behaviour of human prostate cancer cells Clin. Exp. Metastasis 29 2012 111 122
19. S.N. Zucker, T.A. Bancroft, D.E. Place, S.B. Des, A. Bagati, and R. Berezney A dominant negative Cx43 mutant differentially affects tumorigenic and invasive properties in human metastatic melanoma cells J. Cell Physiol. 228 2013 853 859
20. D. Zhang, C. Chen, Y. Li, X. Fu, Y. Xie, Y. Li, and Y. Huang Cx31.1 acts as a tumour suppressor in non-small cell lung cancer (NSCLC) cell lines through inhibition of cell proliferation and metastasis J. Cell Mol. Med. 16 2012 1047 1059
21. E. McLachlan, Q. Shao, H.L. Wang, S. Langlois, and D.W. Laird Connexins act as tumor suppressors in three-dimensional mammary cell organoids by regulating differentiation and angiogenesis Cancer Res. 66 2006 9886 9894 (Pubitemid 44672040)
22. M. Fukushima, Y. Hattori, T. Yoshizawa, and Y. Maitani Combination of non-viral connexin 43 gene therapy and docetaxel inhibits the growth of human prostate cancer in mice Int. J. Oncol. 30 2007 225 231
23. V. Mauro, D. Carette, R. Pontier-Bres, J. Dompierre, D. Czerucka, D. Segretain, J. Gilleron, and G. Pointis The anti-mitotic drug griseofulvin induces apoptosis of human germ cell tumor cells through a connexin 43-dependent molecular mechanism Apoptosis 18 2013 480 491
24. Y. Sun, X. Zhao, Y. Yao, X. Qi, Y. Yuan, and Y. Hu Connexin 43 interacts with Bax to regulate apoptosis of pancreatic cancer through a gap junction-independent pathway Int. J. Oncol. 41 2012 941 948
25. H. Sato, K. Fukumoto, S. Hada, H. Hagiwara, E. Fujimoto, E. Negishi, K. Ueno, and T. Yano Enhancing effect of connexin 32 gene on vinorelbine-induced cytotoxicity in A549 lung adenocarcinoma cells Cancer Chemother. Pharmacol. 60 2007 449 457 (Pubitemid 46944588)
26. G. Olbina, and W. Eckhart Mutations in the second extracellular region of connexin 43 prevent localization to the plasma membrane, but do not affect its ability to suppress cell growth Mol. Cancer Res. 1 2003 690 700 (Pubitemid 36870522)
27. F. Princen, P. Robe, D. Gros, T. Jarry-Guichard, J. Gielen, M.P. Merville, and V. Bours Rat gap junction connexin-30 inhibits proliferation of glioma cell lines Carcinogenesis 22 2001 507 513 (Pubitemid 32203832)
28. H. Qin, Q. Shao, T. Thomas, J. Kalra, M.A. Alaoui-Jamali, and D.W. Laird Connexin26 regulates the expression of angiogenesis-related genes in human breast tumor cells by both GJIC-dependent and -independent mechanisms Cell Commun. Adhes. 10 2003 387 393 (Pubitemid 38081402)
29. H. Qin, Q. Shao, H. Gurtis, J. Galipeau, D.J. Belliveau, T. Wang, M.A. Alaoui-Jamali, and D.W. Laird 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
30. Y.W. Zhang, I. Morita, M. Ikeda, K.W. Ma, and S. Murota Connexin43 suppresses proliferation of osteosarcoma U2OS cells through post-transcriptional regulation of p27 Oncogene 20 2001 4138 4149 (Pubitemid 32762188)
31. W. Zhang, C. Nwagwu, D.M. Le, V.W. Yong, H. Song, and W.T. Couldwell Increased invasive capacity of connexin43-overexpressing malignant glioma cells J. Neurosurg. 99 2003 1039 1046 (Pubitemid 44717400)
32. E. Fujimoto, H. Sato, S. Shirai, Y. Nagashima, N. Virgona, K. Hagiwara, H. Yamasaki, E. Negishi, K. Ueno, and T. Yano Inhibition of Src activity enhances the tumor-suppressive effect of the connexin 32 gene in Caki-1 renal cancer cells Oncol. Rep. 15 2006 1359 1365
33. Y. Yonezawa, Y. Nagashima, H. Sato, N. Virgona, K. Fukumoto, S. Shirai, H. Hagiwara, T. Seki, T. Ariga, H. Senba, K. Suzuki, R. Asano, K. Hagiwara, and T. Yano Contribution of the Src family of kinases to the appearance of malignant phenotypes in renal cancer cells Mol. Carcinog. 43 2005 188 197 (Pubitemid 41134426)
34. S. Langlois, K.N. Cowan, Q. Shao, B.J. Cowan, and D.W. Laird The tumor-suppressive function of Connexin43 in keratinocytes is mediated in part via interaction with caveolin-1 Cancer Res. 70 2010 4222 4232
35. S. Herrero-González, E. Gangoso, C. Giaume, C.C. Naus, J.M. Medina, and A. Tabemero Connexin43 inhibits the oncogenic activity of c-Src in C6 glioma cells Oncogene 29 2010 5712 5723
36. B.N. Giepmans, T. Hengeveld, F.R. Postma, and W.H. Moolenaar Interaction of c-Src with gap junction protein connexin-43. Role in the regulation of cell-cell communication J. Biol. Chem. 276 2001 8544 8549
37. S. Crespin, J. Bechberger, M. Mesnil, C.C. Naus, and W.C. Sin The carboxy-terminal tail of connexin43 gap junction protein is sufficient to mediate cytoskeleton changes in human glioma cells J. Cell Biochem. 110 2010 589 597
38. A. Gellhaus, C. Wotzlaw, T. Otto, J. Fandrey, and E. Winterhager More insights into the CCN3/Connexin43 interaction complex and its role for signaling J. Cell Biochem. 110 2010 129 140
39. S.R. Johnstone, A.K. Best, C.S. Wright, B.E. Isakson, R.J. Errington, and P.E. Martin Enhanced connexin 43 expression delays intra-mitotic duration and cell cycle traverse independently of gap junction channel function J. Cell Biochem. 110 2010 772 782
40. M. Freidin, S. Asche, T.A. Bargiello, M.V. Bennett, and C.K. Abrams Connexin 32 increases the proliferative response of Schwann cells to neuregulin-1 (Nrg1) Proc. Natl. Acad. Sci. U S A 106 2009 3567 3572
41. B. Homkajorn, N.R. Sims, and H. Muyderman Connexin 43 regulates astrocytic migration and proliferation in response to injury Neurosci. Lett. 486 2010 197 201
42. X. Xu, R. Francis, C.J. Wei, K.L. Linask, and C.W. Lo Connexin 43-mediated modulation of polarized cell movement and the directional migration of cardiac neural crest cells Development 133 2006 3629 3639 (Pubitemid 44614285)
43. L.A.B. Elias, D.D. Wang, and A.R. Kriegstein Gap junction adhesion is necessary for radial migration in the neocortex Nature 448 2007 901 907 (Pubitemid 47312775)
44. S.F. Giardina, M. Mikami, F. Goubaeva, and J. Yang Connexin 43 confers resistance to hydrogen peroxide-mediated apoptosis Biochem. Biophys. Res. Commun. 362 2007 747 752 (Pubitemid 47368157)
45. W.R. Loewenstein, and B. Rose The cell-cell channel in the control of growth Semin. Cell Biol. 3 1992 59 79
46. X. Dang, M. Jeyaraman, and E. Kardami 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 (Pubitemid 44322490)
47. A. Rodriguez-Sinovas, A. Cabestrero, D. Lopez, I. Torre, M. Morente, A. Abellan, E. Miro, M. Ruiz-Meana, and D. Garcia-Dorado The modulatory effects of connexin 43 on cell death/survival beyond cell coupling Prog. Biophys. Mol. Biol. 94 2007 219 232 (Pubitemid 46782978)
48. W. Srisakuldee, M.M. Jeyaraman, B.E. Nickel, S. Tanguy, Z.S. Jiang, and E. Kardami Phosphorylation of connexin-43 at serine 262 promotes a cardiac injury-resistant state Cardiovasc. Res. 83 2009 672 681
49. X. Li, F.R. Heinzel, K. Boengler, R. Schulz, and G. Heusch Role of connexin 43 in ischemic preconditioning does not involve intercellular communication through gap junctions J. Mol. Cell Cardiol. 36 2004 161 163 (Pubitemid 38084801)
50. K.K. Hirschi, J.M. Burt, K.D. Hirschi, and C. Dai Gap junction communication mediates transforming growth factor-beta activation and endothelial-induced mural cell differentiation Circ. Res. 93 2003 429 437 (Pubitemid 37100008)
51. P. Dai, T. Nakagami, H. Tanaka, T. Hitomi, and T. Takamatsu Cx43 mediates TGF-β signaling through competitive smads binding to microtubules Mol. Biol. Cell 18 2007 2264 2273 (Pubitemid 46911376)
52. S.R. Johnstone, B.M. Kroncke, A.C. Straub, A.K. Best, C.A. Dunn, L.A. Mitchell, Y. Peskova, R.K. Nakamoto, M. Koval, C.W. Lo, P.D. Lampe, L. Columbus, and B.E. Isakson MAPK phosphorylation of connexin 43 promotes binding of cyclin E and smooth muscle cell proliferation Circ. Res. 111 2012 201 211
53. S.R. Johnstone, J. Ross, M.J. Rizzo, A.C. Straub, P.D. Lampe, N. Leitinger, and B.E. Isakson Oxidized phospholipid species promote in vivo differential cx43 phosphorylation and vascular smooth muscle cell proliferation Am. J. Pathol. 175 2009 916 924
54. X. Gong, C. Cheng, and C. Xia Connexins in lens development and cataractogenesis J. Membr. Biol. 218 2007 9 12 (Pubitemid 350132118)
55. J.X. Jiang Gap junctions or hemichannel-dependent and independent roles of connexins in cataractogenesis and lens development Curr. Mol. Med. 10 2010 851 863
56. S. Gu, X.S. Yu, X. Yin, and J.X. Jiang Stimulation of lens cell differentiation by gap junction protein connexin 45.6 Invest. Ophthalmol. Vis. Sci. 44 2003 2103 2111 (Pubitemid 36520305)
57. E.A. Banks, X.S. Yu, Q. Shi, and J.X. Jiang Promotion of lens epithelial-fiber differentiation by the C-terminus of connexin 45.6 a role independent of gap junction communication J. Cell Sci. 120 2007 3602 3612 (Pubitemid 350120952)
58. Q. Shi, E.A. Banks, X.S. Yu, S. Gu, J. Lauer, G.B. Field, and J.X. Jiang Amino acid residue Val362 plays a critical role in maintaining the structure of C terminus of connexin 50 and in lens epithelial-fiber differentiation J. Biol. Chem. 285 2010 18415 18422
59. C.C. Naus, and D.W. Laird Implications and challenges of connexin connections to cancer Nat. Rev. Cancer 10 2010 435 441