Atrial fibrillation-linked GJA5/connexin40 mutants impaired gap junctions via different mechanisms

FEBS Letters

Volumn 588, Issue 8, 2014, Pages 1238-1243

  Bai, Donglin ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Atrial fibrillation; Autosomal dominant inheritance; Connexin40; Connexin43; Gap junction channel

Indexed keywords

ATRIAL FIBRILLATION; AUTOSOMAL DOMINANT INHERITANCE; CONNEXIN40; CONNEXIN43; GAP JUNCTION CHANNEL;

ATRIAL FIBRILLATION; CONNEXINS; GAP JUNCTIONS; HUMANS; MUTATION; PROTEIN TRANSPORT;

EID: 84898915536     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.02.064     Document Type: Conference Paper

References (108)

1. A.S. Go, E.M. Hylek, K.A. Phillips, Y. Chang, L.E. Henault, J.V. Selby, and D.E. Singer Prevalence of diagnosed atrial fibrillation in adults: national implications for rhythm management and stroke prevention: the anticoagulation and risk factors in atrial fibrillation (ATRIA) study JAMA 285 2001 2370 2375 (Pubitemid 32424106)
2. H. Stefansdottir, T. Aspelund, V. Gudnason, and D.O. Arnar Trends in the incidence and prevalence of atrial fibrillation in Iceland and future projections Europace 13 2011 1110 1117
3. V. Fuster et al. 2011 ACCF/AHA/HRS focused updates incorporated into the ACC/AHA/ESC 2006 guidelines for the management of patients with atrial fibrillation: a report of the American College of Cardiology Foundation/American Heart Association Task Force on practice guidelines Circulation 123 2011 e269 e367
4. E.J. Benjamin, P.A. Wolf, R.B. D'Agostino, H. Silbershatz, W.B. Kannel, and D. Levy Impact of atrial fibrillation on the risk of death: the Framingham Heart Study Circulation 98 1998 946 952 (Pubitemid 28446646)
5. R. Wakili, N. Voigt, S. Kaab, D. Dobrev, and S. Nattel Recent advances in the molecular pathophysiology of atrial fibrillation J. Clin. Invest. 121 2011 2955 2968
6. P.A. Wolf, R.D. Abbott, and W.B. Kannel Atrial fibrillation as an independent risk factor for stroke: the Framingham Study Stroke 22 1991 983 988
7. J.E. Saffitz Connexins, conduction, and atrial fibrillation N. Engl. J. Med. 354 2006 2712 2714
8. S. Nattel, A. Maguy, S. Le Bouter, and Y.H. Yeh Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation Physiol. Rev. 87 2007 425 456 (Pubitemid 47084677)
9. H.S. Duffy, and A.L. Wit Is there a role for remodeled connexins in AF? No simple answers J. Mol. Cell. Cardiol. 44 2008 4 13
10. 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
11. A. Pfeufer et al. Genome-wide association study of PR interval Nat. Genet. 42 2010 153 159
12. D. Fatkin, R. Otway, and J.I. Vandenberg Genes and atrial fibrillation: a new look at an old problem Circulation 116 2007 782 792 (Pubitemid 47255996)
13. J. Xiao, D. Liang, and Y.H. Chen The genetics of atrial fibrillation: from the bench to the bedside Annu. Rev. Genomics Hum. Genet. 12 2011 73 96
14. G. Sohl, and K. Willecke Gap junctions and the connexin protein family Cardiovasc. Res. 62 2004 228 232 (Pubitemid 38496536)
15. Q. Shao, Q. Liu, R. Lorentz, X.Q. Gong, D. Bai, G.S. Shaw, and D.W. Laird Structure and functional studies of N-terminal Cx43 mutants linked to oculodentodigital dysplasia Mol. Biol. Cell 23 2012 3312 3321
16. L. Xin, and D. Bai Functional roles of the amino terminal domain in determining biophysical properties of Cx50 gap junction channels Front. Physiol. 4 2013 1 7
17. S. Maeda, S. Nakagawa, M. Suga, E. Yamashita, A. Oshima, Y. Fujiyoshi, and T. Tsukihara Structure of the connexin 26 gap junction channel at 3.5 A resolution Nature 458 2009 597 602
18. P.E. Purnick, D.C. Benjamin, V.K. Verselis, T.A. Bargiello, and T.L. Dowd Structure of the amino terminus of a gap junction protein Arch. Biochem. Biophys. 381 2000 181 190 (Pubitemid 32260304)
19. J.C. Saez, V.M. Berthoud, M.C. Branes, A.D. Martinez, and E.C. Beyer Plasma membrane channels formed by connexins: their regulation and functions Physiol. Rev. 83 2003 1359 1400 (Pubitemid 37222275)
20. D.B. Gros, and H.J. Jongsma Connexins in mammalian heart function BioEssays 18 1996 719 730 (Pubitemid 26351964)
21. F.F. Bukauskas, M.M. Kreuzberg, M. Rackauskas, A. Bukauskiene, M.V. Bennett, V.K. Verselis, and K. Willecke Properties of mouse connexin 30.2 and human connexin 31.9 hemichannels: implications for atrioventricular conduction in the heart Proc. Natl. Acad. Sci. USA 103 2006 9726 9731 (Pubitemid 43955892)
22. R.G. Gourdie, N.J. Severs, C.R. Green, S. Rothery, P. Germroth, and R.P. Thompson The spatial distribution and relative abundance of gap-junctional connexin40 and connexin43 correlate to functional properties of components of the cardiac atrioventricular conduction system J. Cell Sci. 105 1993 985 991 (Pubitemid 23258661)
23. H.L. Kanter, J.G. Laing, E.C. Beyer, K.G. Green, and J.E. Saffitz Multiple connexins colocalize in canine ventricular myocyte gap junctions Circ. Res. 73 1993 344 350 (Pubitemid 23212114)
24. D.S. He, J.X. Jiang, S.M. Taffet, and J.M. Burt Formation of heteromeric gap junction channels by connexins 40 and 43 in vascular smooth muscle cells Proc. Natl. Acad. Sci. USA 96 1999 6495 6500 (Pubitemid 29256694)
25. V. Valiunas, J. Gemel, P.R. Brink, and E.C. Beyer Gap junction channels formed by coexpressed connexin40 and connexin43 Am. J. Physiol. Heart Circ. Physiol. 281 2001 H1675 H1689
26. H. Gu, J.F. Ek-Vitorin, S.M. Taffet, and M. Delmar Coexpression of connexins 40 and 43 enhances the ph sensitivity of gap junctions: a model for synergistic interactions among connexins Circ. Res. 86 2000 E98 E103
27. G.T. Cottrell, Y. Wu, and J.M. Burt Cx40 and Cx43 expression ratio influences heteromeric/heterotypic gap junction channel properties Am. J. Physiol. Cell Physiol. 282 2002 C1469 C1482
28. V. Valiunas, R. Weingart, and P.R. Brink Formation of heterotypic gap junction channels by connexins 40 and 43 Circ. Res. 86 2000 E42 E49
29. G.T. Cottrell, and J.M. Burt Heterotypic gap junction channel formation between heteromeric and homomeric Cx40 and Cx43 connexons Am. J. Physiol. Cell Physiol. 281 2001 C1559 C1567
30. M. Rackauskas, M.M. Kreuzberg, M. Pranevicius, K. Willecke, V.K. Verselis, and F.F. Bukauskas Gating properties of heterotypic gap junction channels formed of connexins 40, 43, and 45 Biophys. J. 92 2007 1952 1965 (Pubitemid 46495259)
31. C. Elfgang, R. Eckert, H. Lichtenberg-Frate, A. Butterweck, O. Traub, R.A. Klein, D.F. Hulser, and K. Willecke Specific permeability and selective formation of gap junction channels in connexin-transfected hela cells J. Cell Biol. 129 1995 805 817
32. C. Vozzi, E. Dupont, S.R. Coppen, H.I. Yeh, and N.J. Severs Chamber-related differences in connexin expression in the human heart J. Mol. Cell. Cardiol. 31 1999 991 1003 (Pubitemid 29241535)
33. D. Gros, L. Dupays, S. Alcolea, S. Meysen, L. Miquerol, and M. Theveniau-Ruissy Genetically modified mice: tools to decode the functions of connexins in the heart-new models for cardiovascular research Cardiovasc. Res. 62 2004 299 308 (Pubitemid 38496543)
34. J. von Maltzahn, M.M. Kreuzberg, G. Matern, C. Euwens, T. Hoher, P. Worsdorfer, and K. Willecke C-terminal tagging with egfp yields new insights into expression of connexin45 but prevents rescue of embryonic lethal connexin45-deficient mice Eur. J. Cell Biol. 88 2009 481 494
35. M.M. Kreuzberg et al. Human connexin31.9, unlike its orthologous protein connexin30.2 in the mouse, is not detectable in the human cardiac conduction system J. Mol. Cell. Cardiol. 46 2009 553 559
36. L.J. Klaassen et al. Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels PLoS Biol. 9 2011 e1001107
37. D.L. Paul, L. Ebihara, L.J. Takemoto, K.I. Swenson, and D.A. Goodenough Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes J. Cell Biol. 115 1991 1077 1089 (Pubitemid 21909955)
38. V. Valiunas, and R. Weingart Electrical properties of gap junction hemichannels identified in transfected hela cells Pflugers Arch. 440 2000 366 379 (Pubitemid 30445710)
39. W.H. Evans, E. De Vuyst, and L. Leybaert The gap junction cellular internet: connexin hemichannels enter the signalling limelight Biochem. J. 397 2006 1 14 (Pubitemid 44032830)
40. R. Dobrowolski et al. The conditional connexin43 G138R mouse mutant represents a new model of hereditary oculodentodigital dysplasia in humans Hum. Mol. Genet. 17 2008 539 554 (Pubitemid 351201767)
41. J.E. Contreras et al. Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture Proc. Natl. Acad. Sci. USA 99 2002 495 500 (Pubitemid 34060389)
42. S. Ramachandran, L.H. Xie, S.A. John, S. Subramaniam, and R. Lal A novel role for connexin hemichannel in oxidative stress and smoking-induced cell injury PLoS ONE 2 2007 e712
43. J.E. Contreras, J.C. Saez, F.F. Bukauskas, and M.V. Bennett Gating and regulation of connexin 43 (Cx43) hemichannels Proc. Natl. Acad. Sci. USA 100 2003 11388 11393 (Pubitemid 37205945)
44. V. Valiunas Biophysical properties of connexin-45 gap junction hemichannels studied in vertebrate cells J. Gen. Physiol. 119 2002 147 164 (Pubitemid 34522232)
45. M.J. Allen, J. Gemel, E.C. Beyer, and R. Lal Atomic force microscopy of connexin40 gap junction hemichannels reveals calcium-dependent three-dimensional molecular topography and open-closed conformations of both the extracellular and cytoplasmic faces J. Biol. Chem. 286 2011 22139 22146
46. M.E. Spira, D.C. Spray, and M.V. Bennett Synaptic organization of expansion motoneurons of Navanax inermis Brain Res. 195 1980 241 269 (Pubitemid 10090546)
47. D.C. Spray, and M.V. Bennett Physiology and pharmacology of gap junctions Annu. Rev. Physiol. 47 1985 281 303 (Pubitemid 15142383)
48. K. Shintani-Ishida, K. Uemura, and K. Yoshida Hemichannels in cardiomyocytes open transiently during ischemia and contribute to reperfusion injury following brief ischemia Am. J. Physiol. Heart Circ. Physiol. 293 2007 H1714 H1720
49. F. Li, K. Sugishita, Z. Su, I. Ueda, and W.H. Barry Activation of connexin-43 hemichannels can elevate [Ca(2+)]i and [Na(+)]i in rabbit ventricular myocytes during metabolic inhibition J. Mol. Cell. Cardiol. 33 2001 2145 2155 (Pubitemid 34073057)
50. S.A. John, R. Kondo, S.Y. Wang, J.I. Goldhaber, and J.N. Weiss Connexin-43 hemichannels opened by metabolic inhibition J. Biol. Chem. 274 1999 236 240 (Pubitemid 29035054)
51. 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 2010 583 592
52. D. Johansen, V. Cruciani, R. Sundset, K. Ytrehus, and S.O. 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
53. J.M. Rhett, R. Veeraraghavan, S. Poelzing, and R.G. Gourdie The perinexus: sign-post on the path to a new model of cardiac conduction? Trends Cardiovasc. Med. 23 2013 222 228
54. J.M. Rhett, J. Jourdan, and R.G. Gourdie Connexin 43 connexon to gap junction transition is regulated by zonula occludens-1 Mol. Biol. Cell 22 2011 1516 1528
55. R. Vroman, L.J. Klaassen, and M. Kamermans Ephaptic communication in the vertebrate retina Front. Hum. Neurosci. 7 2013 612
56. L.J. Klaassen, I. Fahrenfort, and M. Kamermans Connexin hemichannel mediated ephaptic inhibition in the retina Brain Res. 1487 2012 25 38
57. G.S. Liang, M. de Miguel, J.M. Gomez-Hernandez, J.D. Glass, S.S. Scherer, M. Mintz, L.C. Barrio, and K.H. Fischbeck Severe neuropathy with leaky connexin32 hemichannels Ann. Neurol. 57 2005 749 754 (Pubitemid 40628866)
58. G.M. Essenfelder, R. Bruzzone, J. Lamartine, A. Charollais, C. Blanchet-Bardon, M.T. Barbe, P. Meda, and G. Waksman Connexin30 mutations responsible for hidrotic ectodermal dysplasia cause abnormal hemichannel activity Hum. Mol. Genet. 13 2004 1703 1714 (Pubitemid 39173440)
59. G.I. Fishman Gap junction remodeling and ventricular arrhythmias Heart Rhythm 2 2005 887 889 (Pubitemid 41030737)
60. P.D. Lampe, and A.F. Lau The effects of connexin phosphorylation on gap junctional communication Int. J. Biochem. Cell Biol. 36 2004 1171 1186 (Pubitemid 38515659)
61. D.P. Zipes Mechanisms of clinical arrhythmias J. Cardiovasc. Electrophysiol. 14 2003 902 912 (Pubitemid 36994115)
62. S. Rohr Role of gap junctions in the propagation of the cardiac action potential Cardiovasc. Res. 62 2004 309 322 (Pubitemid 38496544)
63. X. Lin, J. Gemel, E.C. Beyer, and R.D. Veenstra Dynamic model for ventricular junctional conductance during the cardiac action potential Am. J. Physiol. Heart Circ. Physiol. 288 2005 H1113 H1123
64. D.A. Beblo, H.Z. Wang, E.C. Beyer, E.M. Westphale, and R.D. Veenstra Unique conductance, gating, and selective permeability properties of gap junction channels formed by connexin40 Circ. Res. 77 1995 813 822
65. F.F. Bukauskas, and V.K. Verselis Gap junction channel gating Biochim. Biophys. Acta 1662 2004 42 60 (Pubitemid 38366512)
66. J.M. Burt, and D.C. Spray Single-channel events and gating behavior of the cardiac gap junction channel Proc. Natl. Acad. Sci. USA 85 1988 3431 3434
67. A.G. Kleber, and Y. Rudy Basic mechanisms of cardiac impulse propagation and associated arrhythmias Physiol. Rev. 84 2004 431 488 (Pubitemid 38365490)
68. A.G. Reaume et al. Cardiac malformation in neonatal mice lacking connexin43 Science 267 1995 1831 1834
69. D.E. Gutstein et al. Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43 Circ. Res. 88 2001 333 339 (Pubitemid 32173758)
70. J.A. Yao, D.E. Gutstein, F. Liu, G.I. Fishman, and A.L. Wit Cell coupling between ventricular myocyte pairs from connexin43-deficient murine hearts Circ. Res. 93 2003 736 743 (Pubitemid 37288668)
71. W.A. Paznekas et al. Connexin 43 (GJA1) mutations cause the pleiotropic phenotype of oculodentodigital dysplasia Am. J. Hum. Genet. 72 2003 408 418 (Pubitemid 36194249)
72. W.A. Paznekas et al. GJA1 mutations, variants, and connexin 43 dysfunction as it relates to the oculodentodigital dysplasia phenotype Hum. Mutat. 30 2009 724 733
73. M. Himi, T. Fujimaki, T. Yokoyama, K. Fujiki, T. Takizawa, and A. Murakami A case of oculodentodigital dysplasia syndrome with novel GJA1 gene mutation Jpn. J. Ophthalmol. 53 2009 541 545
74. M.J. Alao et al. Oculo-dento-digital dysplasia: lack of genotype-phenotype correlation for GJA1 mutations and usefulness of neuro-imaging Eur. J. Med. Genet. 53 2010 19 22
75. X.Q. Gong, Q. Shao, S. Langlois, D. Bai, and D.W. Laird Differential potency of dominant negative connexin43 mutants in oculodentodigital dysplasia J. Biol. Chem. 282 2007 19190 19202 (Pubitemid 47100175)
76. X.Q. Gong, Q. Shao, C.S. Lounsbury, D. Bai, and D.W. Laird Functional characterization of a GJA1 frameshift mutation causing oculodentodigital dysplasia and palmoplantar keratoderma J. Biol. Chem. 281 2006 31801 31811 (Pubitemid 46041445)
77. W. Roscoe et al. Oculodentodigital dysplasia-causing connexin43 mutants are non-functional and exhibit dominant effects on wild-type connexin43 J. Biol. Chem. 280 2005 11458 11466 (Pubitemid 40418455)
78. A.M. Flenniken et al. A Gja1 missense mutation in a mouse model of oculodentodigital dysplasia Development 132 2005 4375 4386 (Pubitemid 41576698)
79. J.M. Tuomi, K. Tyml, and D.L. Jones Atrial tachycardia/fibrillation in the connexin 43 G60S mutant (Oculodentodigital Dysplasia) mouse Am. J. Physiol. Heart Circ. Physiol. 300 2011 H1402 H1411
80. R. Dobrowolski, A. Sommershof, and K. Willecke Some oculodentodigital dysplasia-associated Cx43 mutations cause increased hemichannel activity in addition to deficient gap junction channels J. Membr. Biol. 219 2007 9 17 (Pubitemid 350197761)
81. I.L. Thibodeau et al. Paradigm of genetic mosaicism and lone atrial fibrillation: physiological characterization of a connexin 43-deletion mutant identified from atrial tissue Circulation 122 2010 236 244
82. D.W. Van Norstrand et al. Connexin43 mutation causes heterogeneous gap junction loss and sudden infant death Circulation 125 2012 474 481
83. I. Lubkemeier et al. Deletion of the last five C-terminal amino acid residues of connexin43 leads to lethal ventricular arrhythmias in mice without affecting coupling via gap junction channels Basic Res. Cardiol. 108 2013 348
84. M.P. O'Quinn, J.A. Palatinus, B.S. Harris, K.W. Hewett, and R.G. Gourdie A peptide mimetic of the connexin43 carboxyl terminus reduces gap junction remodeling and induced arrhythmia following ventricular injury Circ. Res. 108 2011 704 715
85. S. Kirchhoff, E. Nelles, A. Hagendorff, O. Kruger, O. Traub, and K. Willecke Reduced cardiac conduction velocity and predisposition to arrhythmias in connexin40-deficient mice Curr. Biol. 8 1998 299 302 (Pubitemid 28111463)
86. A.M. Simon, D.A. Goodenough, and D.L. Paul Mice lacking connexin40 have cardiac conduction abnormalities characteristic of atrioventricular block and bundle branch block Curr. Biol. 8 1998 295 298 (Pubitemid 28111462)
87. A. Hagendorff, B. Schumacher, S. Kirchhoff, B. Luderitz, and K. Willecke Conduction disturbances and increased atrial vulnerability in Connexin40-deficient mice analyzed by transesophageal stimulation Circulation 99 1999 1508 1515 (Pubitemid 29140919)
88. S. Bagwe, O. Berenfeld, D. Vaidya, G.E. Morley, and J. Jalife Altered right atrial excitation and propagation in connexin40 knockout mice Circulation 112 2005 2245 2253 (Pubitemid 41464566)
89. P. Beauchamp, K.A. Yamada, A.J. Baertschi, K. Green, E.M. Kanter, J.E. Saffitz, and A.G. Kleber Relative contributions of connexins 40 and 43 to atrial impulse propagation in synthetic strands of neonatal and fetal murine cardiomyocytes Circ. Res. 99 2006 1216 1224 (Pubitemid 44808658)
90. D.E. Leaf et al. Connexin40 imparts conduction heterogeneity to atrial tissue Circ. Res. 103 2008 1001 1008
91. I. Lubkemeier et al. The Connexin40A96S mutation from a patient with atrial fibrillation causes decreased atrial conduction velocities and sustained episodes of induced atrial fibrillation in mice J. Mol. Cell. Cardiol. 65 2013 19 32
92. M. Firouzi, H. Ramanna, B. Kok, H.J. Jongsma, B.P. Koeleman, P.A. Doevendans, W.A. Groenewegen, and R.N. Hauer Association of human connexin40 gene polymorphisms with atrial vulnerability as a risk factor for idiopathic atrial fibrillation Circ. Res. 95 2004 e29 e33
93. W.A. Groenewegen et al. A cardiac sodium channel mutation cosegregates with a rare connexin40 genotype in familial atrial standstill Circ. Res. 92 2003 14 22 (Pubitemid 36105602)
94. J.M. Juang et al. The association of human connexin 40 genetic polymorphisms with atrial fibrillation Int. J. Cardiol. 116 2007 107 112
95. R.C. Wirka et al. A common connexin-40 gene promoter variant affects connexin-40 expression in human atria and is associated with atrial fibrillation Circ. Arrhythm. Electrophysiol. 4 2011 87 93
96. M.H. Gollob et al. Somatic mutations in the connexin 40 gene (GJA5) in atrial fibrillation N. Engl. J. Med. 354 2006 2677 2688
97. I.E. Christophersen, H.N. Holmegard, J. Jabbari, A. Sajadieh, S. Haunso, A. Tveit, J.H. Svendsen, and M.S. Olesen Rare variants in GJA5 are associated with early-onset lone atrial fibrillation Can. J. Cardiol. 29 2013 111 116
98. Y.Q. Yang, X. Liu, X.L. Zhang, X.H. Wang, H.W. Tan, H.F. Shi, W.F. Jiang, and W.Y. Fang Novel connexin40 missense mutations in patients with familial atrial fibrillation Europace 12 2010 1421 1427
99. Y.Q. Yang, X.L. Zhang, X.H. Wang, H.W. Tan, H.F. Shi, W.F. Jiang, W.Y. Fang, and X. Liu Connexin40 nonsense mutation in familial atrial fibrillation Int. J. Mol. Med. 26 2010 605 610
100. Y. Sun et al. Novel germline GJA5/connexin40 mutations associated with lone atrial fibrillation impair gap junctional intercellular communication Hum. Mutat. 34 2013 603 609
101. Y. Sun, X. Tong, H. Chen, T. Huang, Q. Shao, W. Huang, D.W. Laird, and D. Bai An endoplasmic reticulum-retained atrial fibrillation-linked connexin40 mutant impairs atrial gap junction channel function Dis. Model Mech. 2014 10.1242/dmm.013813
102. Y. Sun, M.D. Hills, W.G. Ye, X. Tong, and D. Bai Atrial fibrillation-linked germline GJA5/connexin40 mutants showed an increased hemichannel function PLoS ONE 2014 accepted for publication
103. J. Gemel, A.R. Simon, D. Patel, Q. Xu, A. Matiukas, R.D. Veenstra, and E.C. Beyer Accelerated Degradation and Functional Abnormalities of a Connexin40 Mutant Linked to Atrial Fibrillation 2013 IGJC Charleston, SC
104. N. Makita et al. A connexin40 mutation associated with a malignant variant of progressive familial heart block type I Circ. Arrhythm. Electrophysiol. 5 2012 163 172
105. T. Igarashi, J.E. Finet, A. Takeuchi, Y. Fujino, M. Strom, I.D. Greener, D.S. Rosenbaum, and J.K. Donahue Connexin gene transfer preserves conduction velocity and prevents atrial fibrillation Circulation 125 2012 216 225
106. O. Bikou et al. Connexin 43 gene therapy prevents persistent atrial fibrillation in a porcine model Cardiovasc. Res. 92 2011 218 225
107. R. Wilders, and H.J. Jongsma Limitations of the dual voltage clamp method in assaying conductance and kinetics of gap junction channels Biophys. J. 63 1992 942 953
108. A.P. Moreno, B. Eghbali, and D.C. Spray Connexin32 gap junction channels in stably transfected cells equilibrium and kinetic properties Biophys. J. 60 1991 1267 1277.