Relative contributions of connexins 40 and 43 to atrial impulse propagation in synthetic strands of neonatal and fetal murine cardiomyocytes

Circulation Research

Volumn 99, Issue 11, 2006, Pages 1216-1224

  Beauchamp, Philippe ^a   Yamada, Kathryn A ^c   Baertschi, Alex J ^b   Green, Karen ^d   Kanter, Evelyn M ^c   Saffitz, Jeffrey E ^c,d,e   Kléber, André G ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c Department of Medicine   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Atrial myocyte; Basic science; Cardiac gap junction connexins; Cardiovascular genomics; Cell culture; Conduction velocity; Connexin 40; Connexin 43; Mapping; Neonatal mouse cardiomyocytes; Optical mapping

Indexed keywords

CONNEXIN 40; CONNEXIN 43; FLUORESCENT DYE; TRITON X 100;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FETUS; GAP JUNCTION; HEART ATRIUM CONDUCTION; HEART MUSCLE CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SARCOLEMMA;

ANIMALS; ANIMALS, NEWBORN; ATRIAL FUNCTION; CONNEXIN 43; CONNEXINS; ELECTROPHYSIOLOGY; FETUS; HEART CONDUCTION SYSTEM; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCYTES, CARDIAC; STAINING AND LABELING; TIME FACTORS;

EID: 33751318437     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000250607.34498.b4     Document Type: Article

References (46)

1. Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Guldenagel M, Deutsch U, Sohl G. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem. 2002;383:725-737.
2. Saffitz JE, Davis LM, Darrow BJ, Kanter HL, Laing JG, Beyer EC. The molecular basis of anisotropy: role of gap junctions. J Cardiovasc Electrophysiol. 1995;6:498-510.
3. Davis LM, Rodefeld ME, Green K, Beyer EC, Saffitz JE. Gap junction protein phenotypes of the human heart and conduction system. J Cardiovasc Electrophysiol. 1995;6:813-822.
4. Johnson CM, Kanter EM, Green KG, Laing JG, Betsuyaku T, Beyer EC, Steinberg TH, Saffitz JE, Yamada KA. Redistribution of connexin45 in gap junctions of connexin43-deficient hearts. Cardiovasc Res. 2002;53:921-935.
5. Beauchamp P, Choby C, Desplantez T, de Peyer K, Green K, Yamada KA, Weingart R, Saffitz JE, Kleber AG. Electrical propagation in synthetic ventricular myocyte strands from germline connexin43 knockout mice. Circ Res. 2004;95:170-178.
6. Harris AL. Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys. 2001;34:325-472.
7. Valiunas V, Gemel J, Brink PR, Beyer EC. Gap junction channels formed by coexpressed connexin40 and connexin43. Am J Physiol Heart Circ Physiol. 2001;281:H1675-H1689.
8. Polontchouk LO, Valiunas V, Haefliger JA, Eppenberger HM, Weingart R. Expression and regulation of connexins in cultured ventricular myocytes isolated from adult rat hearts. Pflugers Arch. 2002;443:676-689.
9. Desplantez T, Halliday D, Dupont E, Weingart R. Cardiac connexins Cx43 and Cx45: formation of diverse gap junction channels with diverse electrical properties. Pflugers Arch. 2004;448:363-375.
10. Elenes S, Martinez AD, Delmar M, Beyer EC, Moreno AP. Heterotypic docking of Cx43 and Cx45 connexons blocks fast voltage gating of Cx43. Biophys J. 2001;81:1406-1418.
11. Valiunas V, Weingart R, Brink PR. Formation of heterotypic gap junction channels by connexins 40 and 43. Circ Res. 2000;86:e42-e49.
12. Peters NS, Green CR, Poole-Wilson PA, Severs NJ. Reduced content of connexin43 gap junctions in ventricular myocardium from hypertrophied and ischemic human hearts. Circulation. 1993;88:864-875.
13. Kostin S, Klein G, Szalay Z, Hein S, Bauer EP, Schaper J. Structural correlate of atrial fibrillation in human patients. Cardiovasc Res. 2002;54:361-379.
14. van der Velden HM, Ausma J, Rook MB, Hellemons AJ, van Veen TA, Allessie MA, Jongsma HJ. Gap junctional remodeling in relation to stabilization of atrial fibrillation in the goat. Cardiovasc Res. 2000;46:476-486.
15. Elvan A, Huang XD, Pressler ML, Zipes DP. Radiofrequency catheter ablation of the atria eliminates pacing-induced sustained atrial fibrillation and reduces connexin 43 in dogs. Circulation. 1997;96:1675-1685.
16. Dupont E, Ko Y, Rothery S, Coppen SR, Baghai M, Haw M, Severs NJ. The gap-junctional protein connexin40 is elevated in patients susceptible to postoperative atrial fibrillation. Circulation. 2001;103:842-849.
17. Nao T, Ohkusa T, Hisamatsu Y, Inoue N, Matsumoto T, Yamada J, Shimizu A, Yoshiga Y, Yamagata T, Kobayashi S, Yano M, Hamano K, Matsuzaki M. Comparison of expression of connexin in right atrial myocardium in patients with chronic atrial fibrillation versus those in sinus rhythm. Am J Cardiol. 2003;91:678-683.
18. Polontchouk L, Haefliger JA, Ebelt B, Schaefer T, Stuhlmann D, Mehlhorn U, Kuhn-Regnier F, De Vivie ER, Dhein S. Effects of chronic atrial fibrillation on gap junction distribution in human and rat atria. J Am Coll Cardiol. 2001;38:883-891.
19. Ausma J, van der Velden HM, Lenders MH, van Ankeren EP, Jongsma HJ, Ramaekers FC, Borgers M, Allessie MA. Reverse structural and gap-junctional remodeling after prolonged atrial fibrillation in the goat. Circulation. 2003;107:2051-2058.
20. van der Velden HM, van Kempen MJ, Wijffels MC, van Zijverden M, Groenewegen WA, Allessie MA, Jongsma HJ. Altered pattern of connexin40 distribution in persistent atrial fibrillation in the goat. J Cardiovasc Electrophysiol. 1998;9:596-607.
21. Kanagaratnam P, Rothery S, Patel P, Severs NJ, Peters NS. Relative expression of immunolocalized connexins 40 and 43 correlates with human atrial conduction properties. J Am Coll Cardiol. 2002;39:116-123.
22. Eloff BC, Lerner DL, Yamada KA, Schuessler RB, Saffitz JE, Rosenbaum DS. High resolution optical mapping reveals conduction slowing in connexin43 deficient mice. Cardiovasc Res. 2001;51:681-690.
23. Guerrero PA, Schuessler RB, Davis LM, Beyer EC, Johnson CM, Yamada KA, Saffitz JE. Slow ventricular conduction in mice heterozygous for a connexin43 null mutation. J Clin Invest. 1997;99:1991-1998.
24. Morley GE, Vaidya D, Samie FH, Lo C, Delmar M, Jalife J. Characterization of conduction in the ventricles of normal and heterozygous Cx43 knockout mice using optical mapping. J Cardiovasc Electrophysiol. 1999;10:1361-1375.
25. Thomas SA, Schuessler RB, Berul CI, Beardslee MA, Beyer EC, Mendelsohn ME, Saffitz JE. Disparate effects of deficient expression of connexin43 on atrial and ventricular conduction: evidence for chamber-specific molecular determinants of conduction. Circulation. 1998;97:686-691.
26. Vaidya D, Tamaddon HS, Lo CW, Taffet SM, Delmar M, Morley GE, Jalife J. Null mutation of connexin43 causes slow propagation of ventricular activation in the late stages of mouse embryonic development. Circ Res. 2001;88:1196-1202.
27. Verheule S, van Batenburg CA, Coenjaerts FE, Kirchhoff S, Willecke K, Jongsma HJ. Cardiac conduction abnormalities in mice lacking the gap junction protein connexin40. J Cardiovasc Electrophysiol. 1999;10:1380-1389.
28. Thomas SP, Bircher-Lehmann L, Thomas SA, Zhuang J, Saffitz JE, Kleber AG. Synthetic strands of neonatal mouse cardiac myocytes: structural and electrophysiological properties. Circ Res. 2000;87:467-473.
29. Thomas SP, Kucera JP, Bircher-Lehmann L, Rudy Y, Saffitz JE, Kleber AG. Impulse propagation in synthetic strands of neonatal cardiac myocytes with genetically reduced levels of connexin43. Circ Res. 2003;92:1209-1216.
30. Rohr S, Scholly DM, Kleber AG. Patterned growth of neonatal rat heart cells in culture. Morphological and electrophysiological characterization. Circ Res. 1991;68:114-130.
31. Labrador V, Brun C, Konig S, Roatti A, Baertschi AJ. Peptidyl-glycine alpha-amidating monooxygenase targeting and shaping of atrial secretory vesicles: inhibition by mutated N-terminal ProANP and PBA. Circ Res. 2004;95:e98-e109.
32. Saffitz JE, Green KG, Kraft WJ, Schechtman KB, Yamada KA. Effects of diminished expression of connexin43 on gap junction number and size in ventricular myocardium. Am J Physiol Heart Circ Physiol. 2000;278:H1662-H1670.
33. VanSlyke J, Musil L. Biochemical analysis of connexon assembly. In: Bruzzone R, Giaume C, eds. Connexin Methods and Protocols. Totowa, NJ: Humana; 2001:117-134.
34. Fast VG, Darrow BJ, Saffitz JE, Kleber AG. Anisotropic activation spread in heart cell monolayers assessed by high-resolution optical mapping. Role of tissue discontinuities. Circ Res. 1996;79:115-127.
35. Kléber AG, Janse MJ, Fast VG. Normal and abnomal conduction in the heart. In: Page E, Fozzard H, Solaro R, eds. The Handbook of Physiology. Volume 1: The Heart. New York: Oxford University Press; 2002:455-530.
36. Hagendorff A, Schumacher B, Kirchhoff S, Luderitz B, Willecke K. Conduction disturbances and increased atrial vulnerability in Connexin40-deficient mice analyzed by transesophageal stimulation. Circulation. 1999;99:1508-1515.
37. Hyatt CJ, Mironov SF, Vetter FJ, Zemlin CW, Pertsov AM. Optical action potential upstroke morphology reveals near-surface transmural propagation direction. Circ Res. 2005;97:277-284.
38. Gu H, Smith FC, Taffet SM, Delmar M. High incidence of cardiac malformations in connexin40-deficient mice. Circ Res. 2003;93:201-206.
39. Vozzi C, Dupont E, Coppen SR, Yeh HI, Severs NJ. Chamber-related differences in connexin expression in the human heart. J Mol Cell Cardiol. 1999;31:991-1003.
40. Kirchhoff S, Kim JS, Hagendorff A, Thonnissen E, Kruger O, Lamers WH, Willecke K. Abnormal cardiac conduction and morphogenesis in connexin40 and connexin43 double-deficient mice. Circ Res. 2000;87:399-405.
41. Kirchhoff S, Nelles E, Hagendorff A, Kruger O, Traub O, Willecke K. Reduced cardiac conduction velocity and predisposition to arrhythmias in connexin40-deficient mice. Curr Biol. 1998;8:299-302.
42. Tamaddon HS, Vaidya D, Simon AM, Paul DL, Jalife J, Morley GE. High-resolution optical mapping of the right bundle branch in connexin40 knockout mice reveals slow conduction in the specialized conduction system. Circ Res. 2000;87:929-936.
43. Bagwe S, Berenfeld O, Vaidya D, Morley GE, Jalife J. Altered right atrial excitation and propagation in connexin40 knockout mice. Circulation. 2005;112:2245-2253.
44. James TN. The connecting pathways between the sinus node and A-V node and between the right and the left atrium in the human heart. Am Heart J. 1963;66:498-508.
45. Janse M, Anderson R. Specialized internodal atrial pathways - fact or fiction? Eur J Cardiol. 1974;2:117-136.
46. Hogan PM, Davis LD. Electrophysiological characteristics of canine atrial plateau fibers. Circ Res. 1971;28:62-73.