Electrophysiological mechanisms of antiarrhythmic protection during hypothermia in winter hibernating versus nonhibernating mammals

Heart Rhythm

Volumn 5, Issue 11, 2008, Pages 1587-1596

  Fedorov, Vadim V ^a,b   Glukhov, Alexey V ^a,b   Sudharshan, Sangita ^a   Egorov, Yuri ^b   Rosenshtraukh, Leonid V ^b   Efimov, Igor R ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b INSTITUTE OF EXPERIMENTAL CARDIOLOGY   (Russian Federation)

Author keywords

Conduction anisotropy; Hibernation; Hypothermia; Optical mapping; Ventricular fibrillation

Indexed keywords

CONNEXIN 43; NERVE CELL ADHESION MOLECULE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANISOTROPY; ARTICLE; CONTROLLED STUDY; EPICARDIUM; GAP JUNCTION; HEART ELECTROPHYSIOLOGY; HEART MUSCLE POTENTIAL; HEART PACING; HEART REPOLARIZATION; HEART VENTRICLE FIBRILLATION; MAMMAL; MYOCARDIAL HIBERNATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; RABBIT; RUSSIAN FEDERATION; SQUIRREL; SUMMER; TEMPERATURE MEASUREMENT; WINTER;

ANIMALS; ARRHYTHMIAS, CARDIAC; ELECTROPHYSIOLOGIC TECHNIQUES, CARDIAC; HEART CONDUCTION SYSTEM; HIBERNATION; HYPOTHERMIA; MAMMALS; MYOCARDIAL REPERFUSION INJURY; RABBITS; SCIURIDAE;

EID: 57149147298     PISSN: 15475271     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.hrthm.2008.08.030     Document Type: Article

References (49)

1. Johansson B.W. The hibernator heart-nature's model of resistance to ventricular fibrillation. Cardiovasc Res 31 (1996) 826-832
2. Carey H.V., Andrews M.T., and Martin S.L. Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83 (2003) 1153-1181
3. Andrews M.T. Advances in molecular biology of hibernation in mammals. Bioessays 29 (2007) 431-440
4. Barnes B.M. Freeze avoidance in a mammal: body temperatures below 0 degree C in an Arctic hibernator. Science 244 (1989) 1593-1595
5. Fedorov V.V., Li L., Glukhov A., et al. Hibernator Citellus undulatus maintains safe cardiac conduction and is protected against tachyarrhythmias during extreme hypothermia: possible role of Cx43 and Cx45 up-regulation. Heart Rhythm 2 (2005) 966-975
6. Rozenshtraukh L.V., Fedorov V.V., Aliev R.R., et al. [Pattern of excitation in isolated heart of hibernator ground squirrel Citellus undulatus.]. Kardiologiia 45 (2005) 4-10
7. Li J., Patel V.V., Kostetskii I., et al. Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ Res 97 (2005) 474-481
8. Cheng Y., Li L., Nikolski V., et al. Shock-induced arrhythmogenesis is enhanced by 2,3-butanedione monoxime compared with cytochalasin D. Am J Physiol Heart Circ Physiol 286 (2004) H310-H318
9. Fedorov V.V., Hepmpill M., Kostecki G., et al. Low electroporation threshold, conduction block, focal activity and reentrant arrhythmia in the rabbit atria: possible mechanisms of stunning and defibrillation failure. Heart Rhythm 5 (2008) 593-604
10. Fedorov V.V., Hucker W.J., Dobrzynski H., et al. Postganglionic nerve stimulation induces temporal inhibition of excitability in the rabbit sinoatrial node. Am J Physiol 291 (2006) H612-H623
11. Hucker W.J., McCain M.L., Laughner J.I., et al. Connexin 43 expression delineates two discrete pathways in the human atrioventricular junction. Anat Rec 291 (2008) 204-215
12. Smeets J.L., Allessie M.A., Lammers W.J., et al. The wavelength of the cardiac impulse and reentrant arrhythmias in isolated rabbit atrium. The role of heart rate, autonomic transmitters, temperature, and potassium. Circ Res 58 (1986) 96-108
13. Severs N.J., Coppen S.R., Dupont E., et al. Gap junction alterations in human cardiac disease. Cardiovasc Res 62 (2004) 368-377
14. Akar F.G., Spragg D.D., Tunin R.S., et al. Mechanisms underlying conduction slowing and arrhythmogenesis in nonischemic dilated cardiomyopathy. Circ Res 95 (2004) 717-725
15. Wu J., Wu J., and Zipes D.P. Mechanisms of initiation of ventricular tachyarrhythmias. In: Zipes D.P., and Jalife J. (Eds). Cardiac Electrophysiology: From Cell to Bedside (2004), Saunders, Philadelphia 380-389
16. Panfilov A.V. Is heart size a factor in ventricular fibrillation?. Or how close are rabbit and human hearts? Heart Rhythm 3 (2006) 862-864
17. Cao J.M., Qu Z., Kim Y.H., et al. Spatiotemporal heterogeneity in the induction of ventricular fibrillation by rapid pacing: importance of cardiac restitution properties. Circ Res 84 (1999) 1318-1331
18. Weiss J.N., Qu Z., Chen P.S., et al. The dynamics of cardiac fibrillation. Circulation 112 (2005) 1232-1240
19. White J.D. Cardiac arrest in hypothermia. JAMA 244 (1980) 2262
20. Dave A.R., and Morrison P.R. Characteristics of the hibernating heart. Am Heart J 124 (1955) 367-384
21. Duker G., Sjoquist P.O., and Johansson B.W. Monophasic action potentials during induced hypothermia in hedgehog and guinea pig hearts. Am J Physiol 253 (1987) H1083-H1088
22. Salama G., Kanai A.J., Huang D., et al. Hypoxia and hypothermia enhance spatial heterogeneities of repolarization in guinea pig hearts: analysis of spatial autocorrelation of optically recorded action potential durations. J Cardiovasc Electrophysiol 9 (1998) 164-183
23. Saitongdee P., Milner P., Becker D.L., et al. Increased connexin43 gap junction protein in hamster cardiomyocytes during cold acclimatization and hibernation. Cardiovasc Res 47 (2000) 108-115
24. Anufriev AI, Akhremenko AK. Dependence of frequency of Citellus undulatus arousal on ambient temperature. In: Kolaeva S, Popova M, Solomonov N, Wang L, editors. Mechanisms of Natural Hypometabolic States. PSC RAS Puschino, Moscow 1992;8:34-38.
25. Glukhov A.V., Egorov Y., Fedorov V.V., et al. [The effect of hypothermia on the wavelength and vulnerability to ventricular arrhythmias in mammals]. Ross Fiziol Zh Im I M Sechenova 93 (2007) 289-299
26. Spach M.S., Miller III W.T., Geselowitz D.B., et al. The discontinuous nature of propagation in normal canine cardiac muscle. Evidence for recurrent discontinuities of intracellular resistance that affect the membrane currents. Circ Res 48 (1981) 39-54
27. Spach M.S., Heidlage J.F., Dolber P.C., et al. Mechanism of origin of conduction disturbances in aging human atrial bundles: experimental and model study. Heart Rhythm 4 (2007) 175-185
28. Duker G.D., Olsson S.O., Hecht N.H., et al. Ventricular fibrillation in hibernators and nonhibernators. Cryobiology 20 (1983) 407-420
29. Kirchhof P.F., Fabritz C.L., and Franz M.R. Postrepolarization refractoriness versus conduction slowing caused by class I antiarrhythmic drugs: antiarrhythmic and proarrhythmic effects. Circulation 97 (1998) 2567-2574
30. Spach M.S., Heidlage J.F., Dolber P.C., et al. Electrophysiological effects of remodeling cardiac gap junctions and cell size: experimental and model studies of normal cardiac growth. Circ Res 86 (2000) 302-311
31. Shaw R.M., and Rudy Y. Ionic mechanisms of propagation in cardiac tissue. Roles of the sodium and L-type calcium currents during reduced excitability and decreased gap junction coupling. Circ Res 81 (1997) 727-741
32. Poelzing S., Akar F.G., Baron E., et al. Heterogeneous connexin43 expression produces electrophysiological heterogeneities across ventricular wall. Am J Physiol Heart Circ Physiol 286 (2004) H2001-H2009
33. Rohr S., Kucera J.P., Fast V.G., et al. Paradoxical improvement of impulse conduction in cardiac tissue by partial cellular uncoupling. Science 275 (1997) 841-844
34. Gutstein D.E., Morley G.E., Tamaddon H., et al. Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ Res 88 (2001) 333-339
35. Danik S.B., Liu F., Zhang J., et al. Modulation of cardiac gap junction expression and arrhythmic susceptibility. Circ Res 95 (2004) 1035-1041
36. Bukauskas F.F., and Weingart R. Temperature dependence of gap junction properties in neonatal rat heart cells. Pflugers Arch 423 (1993) 133-139
37. Kojodjojo P., Kanagaratnam P., Segal O.R., et al. The effects of carbenoxolone on human myocardial conduction: a tool to investigate the role of gap junctional uncoupling in human arrhythmogenesis. J Am Coll Cardiol 48 (2006) 1242-1249
38. Eloff B.C., Gilat E., Wan X., et al. Pharmacological modulation of cardiac gap junctions to enhance cardiac conduction: evidence supporting a novel target for antiarrhythmic therapy. Circulation 108 (2003) 3157-3163
39. Xing D., Kjolbye A.L., Nielsen M.S., et al. ZP123 increases gap junctional conductance and prevents reentrant ventricular tachycardia during myocardial ischemia in open chest dogs. J Cardiovasc Electrophysiol 14 (2003) 510-520
40. Gutstein D.E., Liu F.Y., Meyers M.B., et al. The organization of adherens junctions and desmosomes at the cardiac intercalated disc is independent of gap junctions. J Cell Sci 116 (2003) 875-885
41. Shaw R.M., Fay A.J., Puthenveedu M.A., et al. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell 128 (2007) 547-560
42. Ferreira-Cornwell M.C., Luo Y., Narula N., et al. Remodeling the intercalated disc leads to cardiomyopathy in mice misexpressing cadherins in the heart. J Cell Sci 115 (2002) 1623-1634
43. Wei C.J., Francis R., Xu X., et al. Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells. J Biol Chem 280 (2005) 19925-19936
44. Hertig C.M., Eppenberger-Eberhardt M., Koch S., et al. N-cadherin in adult rat cardiomyocytes in culture. I. Functional role of N-cadherin and impairment of cell-cell contact by a truncated N-cadherin mutant. J Cell Sci 109 (1996) 1-10
45. Stein M., Noorman M., van Veen T.A., et al. Dominant arrhythmia vulnerability of the right ventricle in senescent mice. Heart Rhythm 5 (2008) 438-448
46. Liu B., Zhao M.J., and Chao I. Effect of cold on transmembrane potentials in cardiac cells of the hedgehog. J Therm Biol 12 (1987) 77-80
47. Liu B., Arlock P., Wohlfart B., et al. Temperature effects on the Na and Ca currents in rat and hedgehog ventricular muscle. Cryobiology 28 (1991) 96-104
48. Yatani A., Kim S.J., Kudej R.K., et al. Insights into cardioprotection obtained from study of cellular Ca2+ handling in myocardium of true hibernating mammals. Am J Physiol Heart Circ Physiol 286 (2004) H2219-H2228
49. Wang S.Q., Lakatta E.G., Cheng H., et al. Adaptive mechanisms of intracellular calcium homeostasis in mammalian hibernators. J Exp Biol 205 (2002) 2957-2962