Role of connexin 43 in cardiovascular diseases

European Journal of Pharmacology

Volumn 768, Issue , 2015, Pages 71-76

  Michela, Pecoraro ^a   Velia, Verrilli ^a   Aldo, Pinto ^a   Ada, Popolo ^a  

^a UNIVERSITY OF SALERNO   (Italy)

Author keywords

Cardiovascular disease; Connexin 43; Gap junction; Mitochondria

Indexed keywords

AAP 10; CARDIOVASCULAR AGENT; CONNEXIN 40; CONNEXIN 43; DANEGAPTIDE; MESSENGER RNA; MICRORNA 1; ROTIGAPTIDE; UNCLASSIFIED DRUG;

ATRIAL FIBRILLATION; CARDIOVASCULAR DISEASE; DISEASE ASSOCIATION; DOWN REGULATION; DRUG MECHANISM; GAP JUNCTION; GENE EXPRESSION REGULATION; HEART ARRHYTHMIA; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE CONDUCTANCE; HEART MUSCLE ISCHEMIA; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; INTRACELLULAR SIGNALING; ISCHEMIC CARDIOMYOPATHY; MITOCHONDRIAL MEMBRANE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SODIUM CURRENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CARDIOVASCULAR DISEASES; METABOLISM;

ANIMALS; CARDIOVASCULAR DISEASES; CONNEXIN 43; HUMANS;

EID: 84947556404     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2015.10.030     Document Type: Review

References (67)

1. E. Agullo-Pascual, M. Cerrone, and M. Delmar Arrhythmogenic cardiomyopathy and Brugada syndrome: diseases of the connexome FEBS Lett. 588 8 2014 1322 1330 10.1016/j.febslet.2014.02.008 2014 Apr 17
2. A. Allen The cardiotoxicity of chemotherapeutic drugs Semin. Oncol. 19 1992 529 542
3. M.A. Beardslee, D.L. Lerner, P.N. Tadros, J.G. Laing, E.C. Beyer, K.A. Yamada, A.G. Kléber, R.B. Schuessler, and J.E. Saffitz Dephosphorylation and intracellular redistribution of ventricular connexin43 during electrical uncoupling induced by ischemia Circ. Res. 87 2000 656 662
4. E.J.T. Birgit, J.J. Habo, and F.A.B. Marti Regulation of myocardial connexins during hypertrophic remodelling Eur. Heart J. 2004 1979 1989 10.1016/j.ehj.2004.08.007
5. K. Boengler, R. Schulz, and G. Heusch Connexin 43 signalling and cardioprotection Heart 92 12 2006 1724 1727 10.1136/hrt.066878 PMCID: PMC1861299
6. K. Boengler, G. Dodoni, A. Rodriguez-Sinovas, A. Cabestrero, M. Ruiz-Meana, P. Gres, I. Konietzka, C. Lopez-Iglesias, D. Garcia-Dorado, F. Di Lisa, G. Heusch, and R. Schulz Connexin 43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning Cardiovasc. Res. 67 2 2005 234 244
7. A. Curcio, D. Torella, C. Iaconetti, E. Pasceri, J. Sabatino, S. Sorrentino, S. Giampà, M. Micieli, A. Polimeni, B.J. Henning, A. Leone, D. Catalucci, G.M. Ellison, G. Condorelli, and C. Indolfi MicroRNA-1 downregulation increases connexin 43 displacement and induces ventricular tachyarrhythmias in rodent hypertrophic hearts Plos One 8 7 2013 e70158 10.1371/journal.pone.0070158
8. P. Daleau, S. Boudriau, M. Michaud, C. Jolicoeur, and J.G. Kingma Jr. Preconditioning in the absence or presence of sustained ischemia modulates myocardial Cx43 protein levels and gap junction distribution Can. J. Physiol. Pharmacol. 79 5 2001 371 378
9. E. De Vuyst, K. Boengler, G. Antoons, K.R. Sipido, R. Schulz, and L. Leybaert Pharmacological modulation of connexin-formed channels in cardiac pathophysiology Br. J. Pharmacol. 163 3 2011 469 483 10.1111/j.1476-5381.2011.01244.x
10. S. Del Rya, S. Moscato, F. Bianchi, M.A. Morales, Q.A. Dolfi, S. Burchielli, M. Cabiati, and L. Mattii Altered expression of connexin 43 and related molecular partners in a pig model of left ventricular dysfunction with and without dipyrydamole therapy Pharmacol. Res. 2015 28 31
11. T. Desplantez, M.L. McCain, P. Beauchamp, G. Rigoli, B. Rothen-Rutishauser, K.K. Parker, and A.G. Kleber Connexin 43 ablation in foetal atrial myocytes decreases electrical coupling, partner connexins, and sodium current Cardiovasc. Res. 94 2012 58 65
12. H.S. Duffy The molecular mechanisms of gap junction remodeling Heart Rhythm. 8 2012 1331 1334 10.1016/j.hrthm.2011.11.048
13. E. Dupont, T. Matsushita, R.A. Kaba, C. Vozzi, S.R. Coppen, N. Khan, R. Kaprielian, M.H. Yacoub, and N.J. Severs Altered connexin expression in human congestive heart failure J. Mol. Cell. Cardiol. 33 2001 359 371
14. L. Emdad, M. Uzzaman, Y. Takagishi, H. Honjo, T. Uchida, N.J. Severs, I. Kodama, and Y. Murata Gap junction remodeling in hypertrophied left ventricles of aortic-banded rats: prevention by angiotensin II type 1 receptor blockade J. Mol. Cell. Cardiol. 33 2001 219 231
15. M.S. Fontes, T.A. van Veen, J.M. de Bakker, and H.V. van Rijen Functional consequences of abnormal Cx43 expression in the heart Biochim. Et. Biophys. Acta 1818 2012 2020 2029
16. L. Formigli, L. Ibba-Manneschi, A.M. Perna, A. Pacini, L. Polidori, C. Nediani, P.A. Modesti, D. Nosi, A. Tani, A. Celli, G.G. Neri-Serneri, F. Quercioli, and S. Zecchi-Orlandini Altered Cx43 expression during myocardial adaptation to acute and chronic volume overloading Histol. Histopathol. 18 2003 359 369
17. 2+ and connexin 43 BMC Complement. Altern. Med. 15 2015 5 10.1186/s12906-015-0521-y
18. F. Goubaeva, M. Mikami, S. Giardina, B. Ding, J. Abe, and J. Yang Cardiac mitochondrial connexin 43 regulates apoptosis Biochem. Biophys. Res. Commun. 352 1 2007 97 103
19. G. Hawat, M. Benderdour, G. Rousseau, and G. Baroudi Connexin 43 mimetic peptide Gap26 confers protection to intact heart against myocardial ischemia injury Pflugers Arch. 460 3 2010 583 592 10.1007/s00424-010-0849-6
20. M. Itoh, Y. Takeishi, S. Nakada, T. Miyamoto, Y. Tsunoda, H. Takahashi, I. Kubota, and H. Tomoike Long-term treatment with angiotensin II type 1 receptor antagonist, CV-11974, restores bcatenin mRNA expression in volume-overloaded rabbit hearts Heart Vessel. 17 2002 36 41
21. Y.K. Iwasaki, K. Nishida, T. Kato, and S. Nattel Atrial fibrillation pathophysiology: implications for management Circulation 124 2011 2264 2274
22. D. Jacob, M.L. Main, S. Gupta, K. Gosch, M. McCoy, and A. Magalski Prevalence and significance of isolated T wave inversion in 1755 consecutive American collegiate athletes J. Electrocardiol. 48 3 2015 407 414 10.1016/j.jelectrocard.2015.03.005 2015 May-Jun
23. S.K. Jain, R.B. Schuessler, and J.E. Saffitz Mechanisms of delayed electrical uncoupling induced by ischemic preconditioning Circ. Res. 92 2003 1138 1144
24. J.A. Jansen Cardiac connexins and impulse propagation J. Mol. Cell. Cardiol. 48 1 2010 76 82
25. J.A. Jansen, M. Noorman, H. Musa, M. Stein, S. de Jong, R. van der Nagel, T.J. Hund, P.J. Mohler, M.A. Vos, T.A. van Veen, J.M. de Bakker, M. Delmar, and H.V. van Rijen Reduced heterogeneous expression of cx43 results in decreased nav1.5 expression and reduced sodium current that accounts for arrhythmia vulnerability in conditional cx43 knockout mice Heart Rhythm. 9 2012 600 607
26. M.M. Jeyaraman, W. Srisakuldee, B.E. Nickel, and E. Kardami Connexin43 phosphorylation and cytoprotection in the heart Biochim. Biophys. Acta 1818 8 2012 2009 2013 10.1016/j.bbamem.2011.06.023
27. D. Johansen, V. Cruciani, R. Sundset, K. Ytrehus, and S. Mikalsen Ischemia induces closure of gap junctional channels and opening of hemichannels in heart-derived cells and tissue Cell. Physiol. Biochem. 28 2011 103 114
28. J. Jozwiak, and S. Dhein Local effects and mechanisms of antiarrhythmic peptide AAP10 in acute regional myocardial ischemia: electrophysiological and molecular findings Naunyn Schmiedebergs Arch. Pharmacol. 378 5 2008 459 470 10.1007/s00210-008-0317-4
29. A. Kalvelyte, A. Imbrasaite, A. Bukauskiene, V.K. Verselis, and F.F. Bukauskas Connexins and apoptotic transformation Biochem. Pharmacol. 66 8 2003 1661 1672
30. V. Knezl, B. Bacova, L. Kolenova, M. Mitasikova, P. Weismann, J. Drimal, and N. Tribulova Distinct lethal arrhythmias susceptibility is associated with sex-related difference in myocardial connexin-43 expression Neuroendocr. Lett. 29 5 2008 798 801
31. S. Kostin, S. Dammer, S. Hein, W.P. Klovekorn, E.P. Bauer, and J. Schaper Connexin 43 expression and distribution in compensated and decompensated cardiac hypertrophy in patients with aortic stenosis Cardiovasc. Res. 62 2004 426 436
32. P.D. Lampe, and A.D. Martinez The effects of connexin phosphorylation on gap junctional communication Int. J. Biochem. Cell. Biol. 36 7 2004 1171 1186
33. P.D. Lampe, E.M. TenBroek, J.M. Burt, W.E. Kurata, R.G. Johnson, and A.F. Lau Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication J. Cell. Biol. 149 7 2000 (2000 Jun 26)
34. G. Laurent, H. Leong-Poi, I. Mangat, G.W. Moe, X. Hu, P.P. So, E. Tarulli, A. Ramadeen, E.I. Rossman, J.K. Hennan, and P. Dorian Effects of chronic gap junction conduction-enhancing antiarrhythmic peptide GAP-134 administration on experimental atrial fibrillation in dogs Circ. Arrhythm. Electrophysiol. 2 2 2009 171 178 10.1161/CIRCEP.108.790212
35. G. Li, P. Whittaker, and M. Yao The gap junction uncoupler heptanol abrogates infarct size reduction with preconditioning in mouse hearts Cardiovasc. Pathol. 11 2002 158 165
36. D.J. Lips, L.J. DeWindt, D.J. van Kraaij, and P.A. Doevendans Molecular determinants of myocardial hypertrophy and failure: alternative pathways for beneficial and maladaptive hypertrophy Eur. Heart J. 24 2003 883 896
37. B.J. Maron Hypertrophic cardiomyopathy: a systematic review JAMA 287 2002 1308 1320
38. B.J. Maron, W.J. McKenna, G.K. Danielson, L.J. Kappenberger, H.J. Kuhn, C.E. Seidman, P.M. Shah, W.H. Spencer 3rd, P. Spirito, F.J. Ten Cate, and E.D. Wigle American College of Cardiology/ European Society of Cardiology clinical expert consensus document on hypertrophic cardiomyopathy. A report of the American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents and the European Society of Cardiology Committee for Practice Guidelines J. Am. Coll. Cardiol. 42 2003 1687 1713
39. C.E. Murry, R.B. Jennings, and K.A. Reimer Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium Circulation 74 5 1986 1124
40. C. Nambara, Y. Kawasaki, and H. Yamasaki Role of the cytoplasmic loop domain of Cx43 in its intracellular localization and function: possible interaction with cadherin J. Membr. Cell. Biol. 217 1-3 2007 63 69
41. D.L. Paul Molecular cloning of cdna for rat liver gap junction protein J. Cell. Biol. 103 1986 123 134
42. M. Pecoraro, R. Sorrentino, S. Franceschelli, M. Del Pizzo, A. Pinto, and A. Popolo Doxorubicin-Mediated Cardiotoxicity: Role of Mitochondrial Connexin 43 Cardiovasc. Toxicol. 15 4 2015 366 376 10.1007/s12012-014-9305-8
43. S. Pieperhoff, and W.W. Franke The area composita of adhering junctions connecting heart muscle cells of vertebrates-IV: coalescence and amalgamation of desmosomal and adhaerens junction components-late processes in mammalian heart development Eur. J. Cell. Biol. 86 3 2007 77 391
44. A. Popolo, M. Pecoraro, and A. Pinto Effect of adenosine on isoproterenol-induced hypertrophy in vitro. A preliminary study PhOL 1 2014 121 126
45. A. Popolo, S. Morello, R. Sorrentino, and A. Pinto Antiadrenergic effect of adenosine involves connexin43 turn-over in H9c2 cells Eur. J. Pharmacol. 715 2013 56 61
46. A. Rodriguez-Sinovas, K. Boengler, A. Cabestrero, P. Gres, M. Morente, M. Ruiz-Meana, I. Konietzka, E. Miró, A. Totzeck, G. Heusch, R. Schulz, and D. Garcia-Dorado Translocation of connexin 43 to the inner mitochondrial membrane of cardiomyocytes through the heat shock protein 90-dependent TOM pathway and its importance for cardioprotection Circ. Res. 99 1 2006 93 101
47. M. Ruiz-Meana, A. Rodríguez-Sinovas, A. Cabestrero, K. Boengler, G. Heusch, and D. Garcia-Dorado Mitochondrial connexin43 as a new player in the pathophysiology of myocardial ischaemia-reperfusion injury Cardiovasc. Res. 77 2 2008 325 333
48. M. Ruiz-Meana, P. Pina, D. Garcia-Dorado, A. Rodríguez-Sinovas, I. Barba, E. Miró-Casas, M. Mirabet, and J. Soler-Soler Glycine protects cardiomyocytes against lethal reoxygenation injury by inhibiting mitochondrial permeability transition J. Physiol. 558 Pt 3 2004 873 882 2004 Aug 1
49. J.C. Sáeza, K.A. Schalpera, M.A. Retamalc, J.A. Orellanaa, K.F. Shojia, and M.V.L. Bennettd Cell membrane permeabilization via connexin hemichannels in living and dying cells Exp. Cell. Res. 316 2010 2377 2389
50. T. Sakurai, M. Tsuchida, P.D. Lampe, and M. Murakami Cardiomyocyte FGF signaling is required for Cx43 phosphorylation and cardiac gap junction maintenance Exp. Cell. Res. 319 14 2013 2152 2165
51. J.G. Schultz, S. Andersen, A. Andersen, J.E. Nielsen-Kudsk, and J.M. Nielsen Evaluation of cardiac electrophysiological properties in an experimental model of right ventricular hypertrophy and failure Cardiol. Young 14 2015 1 8 10.1017/ S10479511150 00402
52. J.G. Schultz, S. Andersen, A. Andersen, J.E. Nielsen-Kudsk, and J.M. Nielsen Altered patterns of cardiac intercellular junction distribution in hypertrophic cardiomyopathy Heart. 76 5 2015 412 417
53. R. Schulz, P. Gres, A. Skyschally, A. Duschin, S. Belosjorow, I. Konietzka, and G. Heusch Ischemic preconditioning preserves connexin 43 phosphorylation during sustained ischemia in pig hearts in vivo FASEB J. 17 2003 1355 1357
54. Schulz, R., Heusch, G., 2004. Connexin 43 and Ischemic Preconditioning. DOI: http://dx.doi.org/10.1016/j.cardiores.2003.12.017 335-344
55. U. Schwanke, I. Konietzka, A. Duschin, X. Li, R. Schulz, and G. Heusch No ischemic preconditioning in heterozygous connexin43-deficient mice Am. J. Physiol. Heart Circ. Physiol. 283 4 2002 H1740-2 (2002 Oct)
56. N.J. Severs, A.F. Bruce, E. Dupont, and S. Rothery Remodelling of gap junctions and connexin expression in diseased myocardium Cardiovasc. Res. 80 2008 9 19
57. N.J. Severs, S.R. Coppena, E. Dupont, H. Yehb, Y. Koc, and T. Matsushitad Gap junction alterations in human cardiac disease Cardiovasc. Res. 62 2004 368 377
58. D. Soetkamp, T.T. Nguyen, S. Menazza, C. Hirschhäuser, U.B. Hendgen-Cotta, T. Rassaf, K.D. Schlüter, K. Boengler, E. Murphy, and R. Schulz S-nitrosation of mitochondrial connexin 43 regulates mitochondrial function Basic Res. Cardiol. 109 2014 2014 433
59. J.L. Solan, and P.D. Lampe Connexin phosphorylation as a regulatory event linked to gap junction channel assembly. Biochimica et Biophysica Acta (BBA) Biomembranes 1711 2 2005 154 163
60. W. Srisakuldee, Z. Makazan, B.E. Nickel, F. Zhang, J.A. Thliveris, K.B. Pasumarthi, and E. Kardami The FGF-2-triggered protection of cardiac subsarcolemmal mitochondria from calcium overload is mitochondrial connexin 43-dependent Cardiovasc. Res. 103 2014 72 80
61. M. Stahlhut, J.S. Petersen, J.K. Hennan, and M.T. Ramirez The antiarrhythmic peptide rotigaptide (ZP123) increases connexin 43 protein expression in neonatal rat ventricular cardiomyocytes Cell. Commun. Adhes. 13 1-2 2006 21 27 (PMID: 16613777)
62. B.E. Teunissen, H.J. Jongsma, and M.F. Bierhuizen Regulation of myocardial connexins during hypertrophic remodelling Eur. Heart J. 25 22 2004 1979 1989
63. M. Uzzaman, H. Honjo, Y. Takagishi, L. Emdad, A.I. Magee, N.J. Severs, and I. Kodama Remodeling of gap junctional coupling in hypertrophied right ventricles of rats with monocrotalineinduced pulmonary hypertension Circ. Res. 86 2000 871 878
64. H.V. Van Rijen, D. Eckardt, J. Degen, M. Theis, T. Ott, K. Willecke, H.J. Jongsma, T. Opthof, and J.M. de Bakker Slow conduction and enhanced anisotropy increase the propensity for ventricular tachyarrhythmias in adult mice with induced deletion of connexin43 Circulation 109 8 2004 1048 1055 (PMID: 14967725)
65. A.A. Waza, K. Andrabi, and M.U. Hussain Protein kinase C (PKC) mediated interaction between conexin43 (Cx43) and K(+)(ATP) channel subunit (Kir6.1) in cardiomyocyte mitochondria: Implications in cytoprotection against hypoxia induced cell apoptosis Cell. Signal. 26 9 2014 1909 1917 10.1016/j.cellsig.2014.05.002 2014 Sep
66. K.A. Yamada, J.G. Rogers, R. Sundset, T.H. Steinberg, and J. Saffitz Up-regulation of connexin45 in heart failure J. Cardiovasc. Electrophysiol. 14 2003 1205 1212
67. Y. Yue, Q. Qin, M.V. Cohen, J.M. Downey, and S.D. Critz The relative order of mK(ATP) channels, free radicals and p38 MAPK in preconditioning's protective pathway in rat heart Cardiovasc. Res. 55 2002 681 689