Connexin43 cardiac gap junction remodeling: Lessons from genetically engineered murine models

Journal of Membrane Biology

Volumn 245, Issue 5-6, 2012, Pages 275-281

  Remo, Benjamin F ^a   Giovannone, Steven ^a   Fishman, Glenn I ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Arrhythmia; Connexins; Gap junctions; Mouse model; Phosphorylation

Indexed keywords

CONNEXIN 43; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE;

ARRHYTHMOGENESIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; GAP JUNCTION; GENE MUTATION; GENETIC ENGINEERING; HEART ARRHYTHMIA; HEART MUSCLE CELL; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARRHYTHMIAS, CARDIAC; CONNEXIN 43; GAP JUNCTIONS; HUMANS; MICE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

MURINAE;

EID: 84864340269     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-012-9448-0     Document Type: Article

References (46)

1. Akar FG, Nass RD, Hahn S, Cingolani E, Shah M, Hesketh GG, DiSilvestre D, Tunin RS, Kass DA, Tomaselli GF (2007) Dynamic changes in conduction velocity and gap junction properties during development of pacing-induced heart failure. Heart Circul Physiol 293:H1223-H1230 (Pubitemid 47254225)
2. Atkinson MM, Menko AS, Johnson RG, Sheppard JR, Sheridan JD (1981) Rapid and reversible reduction of junctional permeability in cells infected with a temperature-sensitive mutant of avian sarcoma virus. J Cell Biol 91:573-578 (Pubitemid 12215647)
3. Beardslee MA, Lerner DL, Tadros PN, Laing JG, Beyer EC, Yamada KA, Kleber AG, Schuessler RB, Saffitz JE (2000) Dephosphorylation and intracellular redistribution of ventricular connexin43 during electrical uncoupling induced by ischemia. Circ Res 87:656-662
4. Chang CC, Trosko JE, Kung HJ, Bombick D, Matsumura F (1985) Potential role of the src gene product in inhibition of gapjunctional communication in NIH/3T3 cells. Proc Natl Acad Sci USA 82:5360-5364 (Pubitemid 15012106)
5. Crow DS, Beyer EC, Paul DL, Kobe SS, Lau AF (1990) Phosphorylation of connexin43 gap junction protein in uninfected and Rous sarcoma virus-transformed mammalian fibroblasts. Mol Cell Biol 10:1754-1763
6. Filson AJ, Azarnia R, Beyer EC, Loewenstein WR, Brugge JS (1990) Tyrosine phosphorylation of a gap junction protein correlates with inhibition of cell-to-cell communication. Cell Growth Differ 1:661-668
7. Giepmans BN, Feiken E, Gebbink MF, Moolenaar WH (2003) Association of connexin43 with a receptor protein tyrosine phosphatase. Cell Commun Adhes 10:201-205 (Pubitemid 38081372)
8. Gilleron J, Fiorini C, Carette D, Avondet C, Falk MM, Segretain D, Pointis G (2008) Molecular reorganization of Cx43, Zo-1 and Src complexes during the endocytosis of gap junction plaques in response to a non-genomic carcinogen. J Cell Sci 121:4069-4078
9. Gilleron J, Carette D, Fiorini C, Dompierre J, Macia E, Denizot JP, Segretain D, Pointis G (2011) The large GTPase dynamin2: a new player in connexin 43 gap junction endocytosis, recycling and degradation. Int J Biochem Cell Biol 43:1208-1217
10. Giovannone S, Remo BF, Fishman GI (2011) Channeling diversity: gap junction expression in the heart. Heart Rhythm. doi:10.1016/ j.hrthm.2011.11.040
11. Gollob MH, Jones DL, Krahn AD, Danis L, Gong XQ, Shao Q, Liu X, Veinot JP, Tang AS, Stewart AF, Tesson F, Klein GJ, Yee R, Skanes AC, Guiraudon GM, Ebihara L, Bai D (2006) Somatic mutations in the connexin 40 gene (GJA5) in atrial fibrillation. N Engl J Med 354:2677-2688
12. Gutstein DE, Morley GE, Tamaddon H, Vaidya D, Schneider MD, Chen J, Chien KR, Stuhlmann H, Fishman GI (2001) Conduction slowing and sudden arrhythmic death in mice with cardiacrestricted inactivation of connexin43. Circ Res 88:333-339 (Pubitemid 32173758)
13. Harris AL (2001) Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34:325-472 (Pubitemid 34123306)
14. Huang S, Dudez T, Scerri I, Thomas MA, Giepmans BN, Suter S, Chanson M (2003) Defective activation of c-Src in cystic fibrosis airway epithelial cells results in loss of tumor necrosis factor-alphainduced gap junction regulation. J Biol Chem 278:8326-8332 (Pubitemid 36800580)
15. Kalcheva N, Qu J, Sandeep N, Garcia L, Zhang J, Wang Z, Lampe PD, Suadicani SO, Spray DC, Fishman GI (2007) Gap junction remodeling and cardiac arrhythmogenesis in a murine model of oculodentodigital dysplasia. Proc Natl Acad Sci USA 104: 20512-20516
16. Kanno S, Saffitz JE (2001) The role of myocardial gap junctions in electrical conduction and arrhythmogenesis. Cardiovasc Pathol 10:169-177 (Pubitemid 32916370)
17. Kieken F, Mutsaers N, Dolmatova E, Virgil K, Wit AL, Kellezi A, Hirst-Jensen BJ, Duffy HS, Sorgen PL (2009) Structural and molecular mechanisms of gap junction remodeling in epicardial border zone myocytes following myocardial infarction. Circ Res 104:1103-1112
18. Kobayashi N, Yoshida K, Nakano S, Ohno T, Honda T, Tsubokou Y, Matsuoka H (2006) Cardioprotective mechanisms of eplerenone on cardiac performance and remodeling in failing rat hearts. Hypertension 47:671-679 (Pubitemid 43740237)
19. Lampe PD, Lau AF (2000) Regulation of gap junctions by phosphorylation of connexins. Arch Biochem Biophys 384:205-215 (Pubitemid 32012794)
20. Lampe PD, Lau AF (2004) The effects of connexin phosphorylation on gap junctional communication. Int J Biochem Cell Biol 36:1171-1186 (Pubitemid 38515659)
21. Lidington D, Tyml K, Ouellette Y (2002) Lipopolysaccharideinduced reductions in cellular coupling correlate with tyrosine phosphorylation of connexin 43. J Cell Physiol 193:373-379 (Pubitemid 35265956)
22. Marcotte R, Smith HW, Sanguin-Gendreau V, McDonough RV, Muller WJ (2012) Mammary epithelial-specific disruption of c-Src impairs cell cycle progression and tumorigenesis. Proc Natl Acad Sci USA 109:2808-2813
23. Matsushita S, Kurihara H, Watanabe M, Okada T, Sakai T, Amano A (2006) Alterations of phosphorylation state of connexin 43 during hypoxia and reoxygenation are associated with cardiac function. J Histochem Cytochem 54:343-353 (Pubitemid 43291279)
24. Paznekas WA, Boyadjiev SA, Shapiro RE, Daniels O, Wollnik B, Keegan CE, Innis JW, Dinulos MB, Christian C, Hannibal MC, Jabs EW (2003) Connexin 43 (GJA1) mutations cause the pleiotropic phenotype of oculodentodigital dysplasia. Am J Hum Genet 72:408-418 (Pubitemid 36194249)
25. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, Palensky J, Wittes J (1999) The effect of spironolactone on morbidity and mortality in patients with severe heart failure. randomized aldactone evaluation study investigators. N Engl J Med 341:709-717 (Pubitemid 29407370)
26. Poelzing S, Akar FG, Baron E, Rosenbaum DS (2004) Heterogeneous connexin43 expression produces electrophysiological heterogeneities across ventricular wall. Am J Physiol Heart Circ Physiol 286:H2001-H2009 (Pubitemid 38525492)
27. Postma FR, Hengeveld T, Alblas J, Giepmans BN, Zondag GC, Jalink K, Moolenaar WH (1998) Acute loss of cell-cell communication caused by G protein-coupled receptors: a critical role for c-Src. J Cell Biol 140:1199-1209 (Pubitemid 28128879)
28. Qu J, Volpicelli FM, Garcia LI, Sandeep N, Zhang J, Marquez- Rosado L, Lampe PD, Fishman GI (2009) Gap junction remodeling and spironolactone-dependent reverse remodeling in the hypertrophied heart. Circ Res 104:365-371
29. Remo BF, Qu J, Volpicelli FM, Giovannone S, Shin D, Lader J, Liu FY, Zhang J, Lent DS, Morley GE, Fishman GI (2011) Phosphatase-resistant gap junctions inhibit pathological remodeling and prevent arrhythmias. Circ Res 108:1459-1466
30. Saffitz JE (2009) Arrhythmogenic cardiomyopathy and abnormalities of cell-to-cell coupling. Heart Rhythm 6:S62-S65
31. Severs NJ (2002) Gap junction remodeling in heart failure. J Card Fail 8:S293-S299 (Pubitemid 36083074)
32. Severs NJ, Coppen SR, Dupont E, Yeh HI, Ko YS, Matsushita T (2004) Gap junction alterations in human cardiac disease. Cardiovasc Res 62:368-377 (Pubitemid 38496549)
33. Severs NJ, Dupont E, Thomas N, Kaba R, Rothery S, Jain R, Sharpey K, Fry CH (2006) Alterations in cardiac connexin expression in cardiomyopathies. Adv Cardiol 42:228-242 (Pubitemid 43805867)
34. Severs NJ, Bruce AF, Dupont E, Rothery S (2008) Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res 80:9-19
35. Shi G, Fu Y, Jiang W, Yin A, Feng M, Wu Y, Kawai Y, Miyamori I, Fan C (2011) Activation of Src-ATF1 pathway is involved in upregulation of Nox1, a catalytic subunit of NADPH oxidase, by aldosterone. Endocr J 58:491-499
36. Solan JL, Lampe PD (2009) Connexin43 phosphorylation: structural changes and biological effects. Biochem J 419:261-272
37. Soriano P, Montgomery C, Geske R, Bradley A (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64:693-702 (Pubitemid 121001157)
38. Sovari AA, Iravanian S, Dolmatova E, Jiao Z, Liu H, Zandieh S, Kumar V, Wang K, Bernstein KE, Bonini MG, Duffy HS, Dudley SC (2011) Inhibition of c-Src tyrosine kinase prevents angiotensin II-mediated connexin-43 remodeling and sudden cardiac death. J Am Coll Cardiol 58:2332-2339
39. Spray DC, Burt JM (1990) Structure-activity relations of the cardiac gap junction channel. Am J Physiol 258:C195-C205 (Pubitemid 20094614)
40. Spray DC, Moreno AP, Eghbali B, Chanson M, Fishman GI (1992) Gating of gap junction channels as revealed in cells stably transfected with wild type and mutant connexin cDNAs. Biophys J 62:48-50
41. Swenson KI, Piwnica-Worms H, McNamee H, Paul DL (1990) Tyrosine phosphorylation of the gap junction protein connexin43 is required for the pp 60v-src-induced inhibition of communication. Cell Regul 1:989-1002
42. Thibodeau IL, Xu J, Li Q, Liu G, Lam K, Veinot JP, Birnie DH, Jones DL, Krahn AD, Lemery R, Nicholson BJ, Gollob MH (2010) Paradigm of genetic mosaicism and lone atrial fibrillation: physiological characterization of a connexin 43-deletion mutant identified from atrial tissue. Circulation 122:236-244
43. Toyofuku T, Yabuki M, Otsu K, Kuzuya T, Tada M, Hori M (1999) Functional role of c-Src in gap junctions of the cardiomyopathic heart. Circ Res 85:672-681 (Pubitemid 29480807)
44. Toyofuku T, Akamatsu Y, Zhang H, Kuzuya T, Tada M, Hori M (2001) c-Src regulates the interaction between connexin-43 and ZO-1 in cardiac myocytes. J Biol Chem 276:1780-1788 (Pubitemid 32109650)
45. van Rijen HV, Eckardt D, Degen J, Theis M, Ott T, Willecke K, Jongsma HJ, Opthof T, de Bakker JM (2004) Slow conduction and enhanced anisotropy increase the propensity for ventricular tachyarrhythmias in adult mice with induced deletion of connexin43. Circulation 109:1048-1055 (Pubitemid 38282860)
46. Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Guldenagel M, Deutsch U, Sohl G (2002) Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem 383:725-737 (Pubitemid 34649891)