The involvement of gap junctions in the delayed phase of the protection induced by cardiac pacing in dogs

Clinical Science

Volumn 123, Issue 1, 2012, Pages 39-51

  Gönczi, Márton ^a   Kovács, Mária ^a   Seprényi, György ^a   Végh, Ágnes ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Arrhythmia; Cardiac pacing; Connexin43; Delayed protection; Gap junction; Ischaemia reperfusion

Indexed keywords

CONNEXIN 43; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIARRHYTHMIC ACTIVITY; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; EXPERIMENTAL DOG; FEMALE; GAP JUNCTION; HEART INFARCTION; HEART PACING; HEART PROTECTION; HEART VENTRICLE ARRHYTHMIA; HEART VENTRICLE EXTRASYSTOLE; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; ST SEGMENT; ANIMAL; CELL JUNCTION; DOG; FLUORESCENT ANTIBODY TECHNIQUE; HEART INFARCTION PREVENTION; HEART MUSCLE; HEART VENTRICLE FIBRILLATION; HEART VENTRICLE TACHYCARDIA; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CARDIAC PACING, ARTIFICIAL; CONNEXIN 43; CORONARY OCCLUSION; DOGS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GAP JUNCTIONS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MYOCARDIUM; REPERFUSION INJURY; TACHYCARDIA, VENTRICULAR; VENTRICULAR FIBRILLATION;

EID: 84860244727     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20110501     Document Type: Article

References (45)

1. Wit, L. and Janse, M. J. (1993), The Ventricular Arrhythmias of Ischemia and Infarction: Electrophysiological Mechanisms, Futura Publishing Company, Mount Kisco, New York.
2. Peters, N. S. (1996) New insights into myocardial arrhythmogenesis: distribution of gap-junctional coupling in normal, ischaemic and hypertrophied human hearts. Clin. Sci. 6, 447-452.
3. Wojtczak, J. (1979) Contractures and increase in internal longitudinal resistance of cow ventricular muscle induced by hypoxia. Circ. Res. 44, 88-95.
4. Spach, M. S. and Heidlage, J. F. (1995) The stochastic nature of cardiac propagation at a microscopic level. Electrical description of myocardial architecture and its application to conduction. Circ. Res. 76, 366-380.
5. Spach, M. S., Dolbert, P. C. and Heidlage, J. F. (1988) Influence of the passive anisotropic properties on directional differences in propagation following modification of the sodium conductance in human atrial muscle. A model of reentry based anisotropic discontinuous propagation. Circ. Res. 62, 811-832.
6. Cascio, W. E. (2001) Myocardial ischemia: What factors determine arrhythmogenesis? J. Cardiovasc. Electrophysiol. 12, 726-729.
7. deGroot, J. R. and Coronel, R. (2004) Acute ischemia-induced gap junctional uncoupling and arrhythmogenesis. Cardiovasc. Res. 62, 323-334.
8. Kléber, A. G. and Rudy, Y. (2004) Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol. Rev. 84, 431-488.
9. Smith,W. T., Fleet, W. F., Johnson, T. A., Engle, C. L. and Cascio, W. E. (1995) The Ib phase of ventricular arrhythmias in ischaemic in situ porcine heart is related to changes in cell-to-cell electrical coupling. Circulation 92, 3051-3060.
10. Murry, C. E., Jennings, R. B. and Reimer, K. A. (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74, 1124-1136.
11. Végh, Á., Komori, S., Szekeres, L. and Parratt, J. R. (1992) Antiarrhythmic effects of preconditioning in anaesthetised dogs and rats. Cardiovasc. Res. 26, 487-495.
12. Végh, Á., Szekeres, L. and Parratt, J. R. (1991) Transient ischaemia induced by rapid cardiac pacing results in myocardial preconditioning. Cardiovasc. Res. 25, 1051-1053.
13. Végh, Á., Papp, J. Gy. and Parratt, J. R. (1994) Prevention by dexamethasone of the marked antiarrhythmic effects of preconditioning induced 20 h after rapid cardiac pacing. Br. J. Pharmacol. 113, 1081-1082.
14. Kaszala, K., Végh, Á., Papp, J. Gy. and Parratt, J. R. (1996) Time course of the protection against ischaemia and reperfusion-induced ventricular arrhythmias resulting from brief periods of cardiac pacing. J. Mol. Cell. Cardiol. 28, 2085-2095.
15. Kis, A., Végh, Á., Papp, J. Gy. and Parratt, J. R. (1999) Repeated cardiac pacing extends the time during which canine hearts are protected against ischaemia-induced arrhythmias: role of nitric oxide. J. Mol. Cell. Cardiol. 31, 1229-1241.
16. Babai, L., Szigeti, Z., Parratt, J. R. and Végh, Á. (2002) Delayed cardioprotective effects of exercise in dogs are aminoguanidine sensitive: possible involvement of nitric oxide. Clin. Sci. 102, 435-445.
17. Cinca, J., Warren, M., Carreno, A., Tresánchez, M., Armadans, L., Gómez, P. and Soler-Soler, J. (1997) Changes in myocardial electrical impedance induced by coronary artery occlusion in pigs with and without preconditioning: correlation with local ST-segment potential and ventricular arrhythmias. Circulation 96, 3079-3086.
18. Papp, R., Gönczi, M., Kovács, M., Seprényi, G. and Végh, Á. (2007) Gap junctional uncoupling plays a trigger role in the antiarrhythmic effect of ischaemic preconditioning. Cardiovasc. Res. 74, 396-405.
19. Kontogeorgis, A., Kaba, R. A., Kang, E., Feig, J. E., Gupta, P. P., Ponzio, M., Liu, F., Rindler, M. J., Wit, A. L., Fisher, E. A. et al. (2008) Short-term pacing in the mouse alters cardiac expression of connexin43. BMC Physiol. 8, 1-12.
20. Matsushita, S., Tran, V. N., Pelleg, A., Wechsler, A. S. and Kresh, J. Y. (2009) Pacing-induced cardiac gap junction remodelling: modulation of connexin 43 phosphorlylation state. Am. J. Ther. 16, 224-230.
21. Akar, F. G., Nass, R. D., Hahn, S., Cingolani, E., Shah, M., Hesketh, G. G., DiSilvestre, D., Tunin, R. S., Kass, D. A. and Tomaselli, G. F. (2007) Dynamic changes in conduction velocity and gap junction properties during development of pacing-induced heart failure. Am. J. Physiol. Heart Circ. Physiol. 293, H1223-H1230.
22. Patel, P. M., Plotnikov, A., Kanagaratnam, P., Shvilkin, A., Sheehan, C.T, Xiong, W., Danilo, P., Rosen, Jr, M. R. and Peters, N. S. (2001) Altering ventricular activation remodels gap junction distribution in canine heart. J. Cardiovasc. Electrophysiol. 12, 570-577.
23. Poelzing, S. and Rosembaum, D. S. (2004) Altered connexin43 expression produces arrhythmia substrate in heart failure. Am. J. Physiol. Heart Circ. Physiol. 287, H1762-H1770.
24. Gönczi, M., Papp, R., Kovács, M., Seprényi, G. and Végh, Á. (2009) Modulation of gap junctions by nitric oxide contributes to the anti-arrhythmic effect of sodium nitroprusside. Br. J. Pharmacol. 156, 786-793.
25. Walker, M. J. A., Curtis, M. J., Hearse, D. J., Campbell, R. W. F., Janse, M. J., Yellon, D. M., Cobbe, S. M., Coker, S. J., Harness, J. B., Harron, D. W. et al. (1988) The Lambeth Conventions: guidelines for the study of arrhythmias in ischaemia, infarction, and reperfusion. Cardiovasc. Res. 22, 447-455.
26. Puskás, L., Bereczki, E., Sántha, M., Vígh, L., Csanádi, G., Spender, F., Ferdinándy, P., Onody, A. and Kitajka, K. (2004) Cholesterol and cholesterol plus DHA diet-induced gene expression and fatty acid changes in mouse eye and brain. Biochimie 86, 817-824.
27. Kovács, M., Papp, R., Varga-Orvos, Z., Ménesi, D., Puskás, L. G. and Végh, Á. (2010) Changes in gene expression following cardiac pacing-induced delayed cardioprotection in the canine heart. Acta Biol. Hung. 61, 434-448.
28. Parratt, J. R., Végh, Á., Kaszala, K. and Papp, J. Gy. (1996) Suppression of life-threatening ventricular arrhythmias by brief periods of ischaemia and by cardiac pacing with particular reference to delayed myocardial protection. In Ischaemia, Preconditioning and Adaptation (Marber, M. S. and Yellon, D. M., eds), pp. 85-111, Bios Scientific Publishers, Oxford.
29. Schulz, R. and Heusch, G. (2006) Connexin43 and ischaemic preconditioning. Adv. Cardiol. 42, 213-227.
30. Zhao, J., Su, Y., Zhang, Y., Pan, Z., Yang, I., Chen, X., Liu, Y., Lu, Y., Du, Z. and Yang, B. (2010) Activation of cardiac muscarinic M3 receptors induces delayed cardioprotection by preserving phosphorylated connexin-43 and up-regulating cyclooxygenase-2 expression. Br. J. Pharmacol. 159, 1217-1225.
31. Daleau, P., Boudriau, S., Michaud, M., Jolicoeur, C. and Kingma, Jr, J. G. (2001) Preconditioning in the absence or presence of sustained ischaemia modulates myocardial C×43 protein levels and gap junction distribution. Can. J. Physiol. Pharmacol. 79, 371-381.
32. Lin, J., Li, Y., Lin, S., Liang, Q. and Tan, X. (2007) The effect of delayed preconditioning on connexin43 in ischaemic myocardium. Biochem. Cell. Biol. 85, 175-181.
33. Matsushita, S., Kurihara, H., Watanabe, M., Okada, T., Sakai, T. and Amano, A. (2005) Alterations of phosphorylation state of connexin 43 during hypoxia and reoxygenation are associated with cardiac function. J. Histochem. Cytochem. 54, 343-353.
34. Beardslee, M. A., Lerner, D. L., Tadros, P. N., Laing, J. G., Beyer, E. C., Yamada, K. A., Kléber, A. G., Schuessler, R. B. and Saffitz, J. E. (2000) Dephosphorylation and intracellular redistribution of ventricular connexin43 during electrical uncoupling induced by ischemia. Circ. Res. 87, 656-662.
35. Tansey, E. E., Kwaku, K. F., Hammer, P. E., Cowan, D. B., Federman, M., Levitsky, S. and McCully, J. D. (2006) Reduction and redistribution of gap and adherens junction proteins after ischemia and reperfusion. Ann. Thorac. Surg. 82, 1472-1479.
36. Hesketh, G. G., Van Eyk, J. E. and Tomaselli, G. F. (2009) Mechanisms of gap junction traffic in health and disease. J. Cardiovasc. Pharmacol. 54, 263-272.
37. Kim, S.K., Pak, H. N., Park, J. H., Fang, Y. F.,Kim,G. I., Park, Y. D., Hwang, Y. H. and Kim, B. S. (2010) Cardiac cell therapy with mesenchimal stem cell induces cardiac nerve sprouting, angiogenesis, and reduced connexin43-positive gap junctions, but concomitant electrical pacing increases connexin43-positive gap junctions in canine heart. Cardiol. Young 20, 308-317.
38. Végh, Á., Szekeres, L. and Parratt, J. R. (1992) Preconditioning of the ischaemic myocardium; involvement of the L-arginine nitric oxide pathway. Br. J. Pharmacol. 107, 648-652.
39. Jackson, P. E. M., Feng, Q. P. and Jones, D. L. (2008) Nitric oxide depresses connexin 43 myocardial infarction in mice. Acta Physiol. (Oxf.) 194, 23-33.
40. Roh, C. R., Heo, J. H., Yang, S. H. and Bae, D. S. (2002) Regulation of connexin 43 by nitric oxide in primary uterine myocytes from term pregnant women. Am. J. Obstet. Gynecol. 187, 434-440.
41. Yao, J., Hiramatsu, N., Zhu, Y., Morioka, T., Takeda, M., Oite, T. and Kitamura, M. (2005) Nitric oxide-mediated regulation of connexin43 expression and gap junctional intercellular communication in mesangial cells. J. Am. Soc. Nephrol. 16, 58-67.
42. Hoffmann, A., Gloe, T., Pohl, U. and Zahler, S. (2003) Nitric oxide enhances de novo formation of endothelial gap junctions. Cardiovac. Res. 60, 421-430.
43. Radosinska, J., Bacova, B., Bertanova, I, Navarova, J., Zhukovska, A., Shysh, A, Okruhlicova, L. and Tribulova, N. (2011) Myocardial NOS activity and connexin43 expression in untreated and omega-3 fatty acids-treated spontaneously hypertensive and hereditary hypertriglyceridemic rats. Mol. Cell. Biochem. 347, 163-173.
44. Parratt, J. R. and Végh, Á. (1997) Delayed protection against ventricular arrhythmias by cardiac pacing. Heart 78, 423-425.
45. Willich, S. N., Lewis, M., Löwel, H., Arntz, H. R., Schubert, F. and Schröder, R. (1993) Physical exertion as a trigger of acute myocardial infarction. N. Engl. J. Med. 329, 1684-1690.