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Vestnik Moskovskogo universiteta. Seriya 16. Biologiya

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Adaptive seasonal changes in cardiac electrical activity of ectothermic vertebrates

https://doi.org/10.55959/MSU0137-0952-16-80-2-1

Abstract

One of the problems which ectothermic animals have to face during the fall of the ambient temperature is the negative change in parameters of the cardiac electrical activity leading to the decrease in the cardiac output. This is crucially important for those ectotherms which remain highly active during the cold season. The present review discusses the known physiological mechanisms which allow the ectothermic vertebrates, primarily various fish species, to reduce at least partially the cold-induced changes of cardiac electrical activity and to maintain the functional capacity of the heart at sufficient level for the active life during the winter. These mechanisms include the increase of density and/or changes in steady-state activation and inactivation parameters of ionic currents in cardiac myocytes. The acute temperature-dependent changes in ionic currents and electrical activity are also discussed, including the temperature effects on the excitability of cardiac myocytes.

About the Authors

D. V. Abramochkin
Department of Human and Animal Physiology, Faculty of Biology, Lomonosov Moscow State University
Russian Federation

1–12 Leninskie gory, Moscow, 119234



I. Dzhumaniiazova
Department of Human and Animal Physiology, Faculty of Biology, Lomonosov Moscow State University
Russian Federation

1–12 Leninskie gory, Moscow, 119234



O. B. Pustovit
Department of Human and Animal Physiology, Faculty of Biology, Lomonosov Moscow State University
Russian Federation

1–12 Leninskie gory, Moscow, 119234



T. S. Filatova
Department of Human and Animal Physiology, Faculty of Biology, Lomonosov Moscow State University
Russian Federation

1–12 Leninskie gory, Moscow, 119234



References

1. Ivanov K.P. Physiological blocking of the mechanisms of cold death: theoretical and experimental considerations. J. Therm. Biol. 2000;25(6):467–479.

2. Gillis T.E., Marshall C.R., Xue X.-H., Borgford T.J., Tibbits G.F. Ca2+ binding to cardiac troponin C: effects of temperature and pH on mammalian and salmonid isoforms. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000;279(5):R1707–R1715.

3. Keen A.N., Klaiman J.M., Shiels H.A., Gillis T.E. Temperature-induced cardiac remodeling in fish. J. Exp. Biol. 2017;220(2):147–160.

4. Gamperl A.K., Farrell A.P. Cardiac plasticity in fi- shes: environmental influences and intraspecific differences. J. Exp. Biol. 2004;207(15):2539–2550.

5. Aho E., Vornanen M. Contractile properties of atrial and ventricular myocardium of the heart of rainbow trout Oncorhynchus mykiss: effects of thermal acclimation. J. Exp. Biol. 1999;202(19):2663–2677.

6. Filatova T.S., Abramochkin D.V., Shiels H.A. Thermal acclimation and seasonal acclimatization: a comparative study of cardiac response to prolonged temperature change in shorthorn sculpin. J. Exp. Biol. 2019;222(16):jeb.202242.

7. Brouillette J., Clark R.B., Giles W.R., Fiset C. Functional properties of K+ currents in adult mouse ventricular myocytes. J. Physiol. 2004;559(3):777–798.

8. Huo R., Sheng Y., Guo W.-T., Dong D.-L. The potential role of Kv4.3 K+ channel in heart hypertrophy. Channels. 2014;8(3):203–209.

9. Abramochkin D.V., Filatova T.S., Pustovit K.B., Voronina Y.A., Kuzmin V.S., Vornanen M. Ionic currents underlying different patterns of electrical activity in working cardiac myocytes of mammals and non-mammalian vertebrates. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2022;268:111204.

10. Gamperl A.K. Integrated Responses of the Circulatory System to Temperature. Encyclopedia of Fish Physiology: From Genome to Environment. Ed. A.P. Farrell. L.: Elsevier; 2011:1197–1205.

11. Haverinen J., Abramochkin D.V., Kamkin A., Vornanen M. Maximum heart rate in brown trout (Salmo trutta fario) is not limited by firing rate of pacemaker cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2017;312(2):R165–R171.

12. Badr A., El-Sayed M.F., Vornanen M. Effects of seasonal acclimatization on temperature-dependence of cardiac excitability in the roach, Rutilus rutilus. J. Exp. Biol. 2016;219(10):1495–1504.

13. Badr A., Korajoki H., Abu-Amra E.-S., El-Sayed M.F., Vornanen M. Effects of seasonal acclimatization on thermal tolerance of inward currents in roach (Rutilus rutilus) cardiac myocytes. J. Comp. Physiol. B. 2018;188(2):255–269.

14. Badr A., Abu-Amra E.-S., El-Sayed M.F., Vornanen M. Electrical excitability of roach (Rutilus rutilus) ventricular myocytes: effects of extracellular K+ , temperature, and pacing frequency. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2018;315(2):R303–R311.

15. Abramochkin D.V., Haverinen J., Mitenkov Y.A., Vornanen M. Temperature- and external K+-dependence of electrical excitation in ventricular myocytes of cod-like fishes. J. Exp. Biol. 2019;222(5):jeb.193607.

16. Vornanen M. The temperature dependence of electrical excitability in fish hearts. J. Exp. Biol. 2016;219(13):1941–1952.

17. Lukyanov A.N., Sukhova G.S., Udel’nov M.G. Localization structural and functional organization of cardiac pacemaker in the cod Gadus morhua. Zh. Evol. Biokhim. Fiziol. 1983;19:231–236.

18. Mangoni M. Properties of the hyperpolarizationactivated current (If) in isolated mouse sino-atrial cells. Cardiovasc. Res. 2001;52(1):51–64.

19. Wilders R., Verheijck E.E., Kumar R., Goolsby W.N., Van Ginneken A.C., Joyner R.W., Jongsma H.J. Model clamp and its application to synchronization of rabbit sinoatrial node cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1996;271(5):H2168–H2182.

20. Hassinen M., Haverinen J., Vornanen M. Small functional If current in sinoatrial pacemaker cells of the brown trout (Salmo trutta fario) heart despite strong expression of HCN channel transcripts. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2017;313(6):R711–R722.

21. Donald L., Lakatta E.G. What makes the sinoatrial node tick? A question not for the faint of heart. Phil. Trans R Soc. B. 2023;378(1879):20220180.

22. Badr A., Hassinen M., El-Sayed M.F., Vornanen M. Effects of seasonal acclimatization on action potentials and sarcolemmal K+ currents in roach (Rutilus rutilus) cardiac myocytes. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2017;205:15–27.

23. Paajanen V., Vornanen M. Regulation of action potential duration under acute heat stress by IK,ATP and IK1 in fish cardiac myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004;286(2):R405–R415.

24. Abramochkin D.V., Shamshura A., Dzhumaniiazova I., Pustovit O.B., Mishchenko A.A. High temperature and hyperkalemia increase vulnerability of navaga cod (Eleginus nawaga) cardiomyocytes to the ecotoxicant 3-methyl-phenanthrene. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2025;299:111761.

25. Haverinen J., Dzhumaniiazova I., Abramoch kin D.V., Hassinen M., Vornanen M. Effects of Na+ channel isoforms and cellular environment on temperature tolerance of cardiac Na+ current in zebrafish (Danio rerio) and rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 2021;224(8):jeb241067.

26. Haverinen J., Vornanen M. Temperature acclimation modifies Na+ current in fish cardiac myocytes. J. Exp. Biol. 2004;207(16):2823–2833.

27. Filatova T.S., Kuzmin V.S., Guskova V.O., Abramochkin D.V. Sodium current preserves electrical excitability in the heart of hibernating ground squirrel (Citellus undulatus). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2023;282:111452.

28. Shiels H.A., Vornanen M., Farrell A.P. Effects of temperature on intracellular [Ca2+] in trout atrial myocytes. J. Exp. Biol. 2002;205(23):3641–3650.

29. Churcott C.S., Moyes C.D., Bressler B.H., Baldwin K.M., Tibbits G.F. Temperature and pH effects on Ca2+ sensitivity of cardiac myofibrils: a comparison of trout with mammals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1994;267(1):R62–R70.

30. Haverinen J., Vornanen M. Temperature acclimation modifies sinoatrial pacemaker mechanism of the rainbow trout heart. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007;292(2):R1023–R1032.

31. Vornanen M., Ryökkynen A., Nurmi A. Temperature-dependent expression of sarcolemmal K+ currents in rainbow trout atrial and ventricular myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002;282(4):R1191–R1199.

32. Haverinen J., Vornanen M. Responses of action potential and K+ currents to temperature acclimation in fish hearts: Phylogeny or thermal preferences? Physiol. Biochem. Zool. 2009;82(5):468–482.

33. Hassinen M., Haverinen J., Vornanen M. Electrophysiological properties and expression of the delayed rectifier potassium (ERG) channels in the heart of thermally acclimated rainbow trout. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008;295(1):R297–R308.

34. Dzhumaniiazova I., Filatova T.S., Shamshura A., Abramochkin D.V., Shiels H.A. Seasonal remodelling of the fish heart alters sensitivity to petrochemical pollutant, 3-methylphenanthrene. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2024;288:110082.

35. Abramochkin D.V., Vornanen M. Seasonal acclimatization of the cardiac potassium currents (IK1 and IKr) in an arctic marine teleost, the navaga cod (Eleginus navaga). J. Comp. Physiol. B. 2015;185(8):883–890.

36. Hassinen M., Abramochkin D.V., Vornanen M. Seasonal acclimatization of the cardiac action potential in the Arctic navaga cod (Eleginus navaga, Gadidae). J. Comp. Physiol. B. 2014;184(3):319–327.

37. Stecyk J.A.W., Couturier C.S., Abramochkin D.V., Hall D., Arrant-Howell A., Kubly K.L., Lockmann Sh., Logue K., Trueblood L., Swalling C., Pinard J., Vogt A. Cardiophysiological responses of the air-breathing Alaska blackfish to cold acclimation and chronic hypoxic submergence at 5C. J. Exp. Biol. 2020;223(22):jeb225730.

38. Hassinen M., Laulaja S., Paajanen V., Haverinen J., Vornanen M. Thermal adaptation of the crucian carp (Carassius carassius) cardiac delayed rectifier current, IKs , by homomeric assembly of Kv 7.1 subunits without MinK. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011;301(1):R255–R265.

39. Haverinen J., Hassinen M., Dash S.N., Vornanen M. Expression of calcium channel transcripts in the ze brafish heart: dominance of T-type channels. J. Exp. Biol. 2018;221(10):jeb179226.

40. Haworth T.E., Haverinen J., Shiels H.A., Vornanen M. Electrical excitability of the heart in a Chondrostei fish, the Siberian sturgeon (Acipenser baerii). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2014;307(9):R1157–R1166.

41. Vornanen M. L-Type Ca2+ current in fish cardiac myocytes: Effects of thermal acclimation and β-adrenergic stimulation. J. Exp. Biol. 1998;201(4):533–547.

42. Vornanen M., Paajanen V. Seasonality of dihydropyridine receptor binding in the heart of an anoxia-tolerant vertebrate, the crucian carp (Carassius carassius L.). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004;287(5):R1263–R1269.

43. Abramochkin D., Kuzmin V. Electrophysiological differences in cholinergic signaling between the hearts of summer and winter frogs (Rana temporaria). J. Comp. Physiol. B. 2018;188(4):649–656.

44. Stecyk J.A.W., Paajanen V., Farrell A.P., Vornanen M. Effect of temperature and prolonged anoxia exposure on electrophysiological properties of the turtle (Trachemys scripta) heart. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007;293(1):R421–R437.

45. Galli G.L.J., Warren D.E., Shiels H.A. Ca2+ cycling in cardiomyocytes from a high-performance reptile, the varanid lizard (Varanus exanthematicus). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009;297(6):R1636–R1644.

46. Abramochkin D.V., Matchkov V., Wang T. A characterization of the electrophysiological properties of the cardiomyocytes from ventricle, atrium and sinus venosus of the snake heart. J. Comp. Physiol. B. 2020;190(1):63–73.

47. Abramochkin D.V., Kuzmin V.S., Matchkov V., Kamensky A.A., Wang T. The snake heart pacemaker is localized near the sinoatrial valve. J. Exp. Biol. 2021;224(16):jeb242778.


Review

For citations:


Abramochkin D.V., Dzhumaniiazova I., Pustovit O.B., Filatova T.S. Adaptive seasonal changes in cardiac electrical activity of ectothermic vertebrates. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2025;80(2):53-64. (In Russ.) https://doi.org/10.55959/MSU0137-0952-16-80-2-1

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