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A characterization of the electrophysiological properties of the cardiomyocytes from ventricle, atrium and sinus venosus of the snake heart

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Abstract

A detailed description of the electrophysiological features of cardiomyocytes in the various contractile chambers of the vertebrate heart is essential to understand the evolution of cardiac electrical activity, yet very little is known about reptiles. The present study characterizes major ionic currents (INa, ICaL, IKr, IK1 and IKACh) and action potential (AP) configuration in cardiomyocytes from the ventricle, the right atrium and the sinus venosus (SV) of Burmese pythons (Python molurus) using sharp microelectrode and patch clamp recordings. Special attention was given to SV, since it consists of myocardial cells and appears to contribute to right atrial filling in snakes. We demonstrate that most of the SV in pythons has a stable resting potential of − 82.3 ± 2.6 mV (n = 9) and lacks pacemaker activity. AP duration at 50% repolarization was similar in cells from SV and atria (350.2 ± 8.7 and 330.4 ± 17.2 ms, respectively; n = 7), but shorter than ventricular APs (557.6 ± 19.2 ms, n = 5) at 30 °C. The densities of ionic currents, however, differed substantially between atrial and SV cells, where the latter had much lower densities of INa, ICaL and IKr than atrial and ventricular myocytes. IK1 in ventricle was ninefold greater than in atrial cells and 23-fold greater than in myocytes from SV. However, IKACh was absent in ventricular cells, while it was equally large in atrial and SV myocytes. Consistent with this observation, APs of atrium and SV, but not ventricle, were greatly shortened upon addition of acetylcholine (10−6 M). Thus, snake SV, right atrium and ventricle have distinct patterns of ionic currents, but the resulting electrical activity is similar in atrium and SV.

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References

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Abramochkin DV, Hassinen M, Vornanen M (2018) Transcripts of Kv7.1 and MinK channels and slow delayed rectifier K+ current (IKs) are expressed in zebrafish (Danio rerio) heart. Pflugers Arch 470:1753–1764

    Article  CAS  Google Scholar 

  • Brouillette J, Clark RB, Giles WR, Fiset C (2004) Functional properties of K+ currents in adult mouse ventricular myocytes. J Physiol 559:777–798

    Article  CAS  Google Scholar 

  • Davies F (1942) The conducting system of the vertebrate heart. Br Heart J. 4:66–76

    Article  CAS  Google Scholar 

  • Galli GLJ, Taylor EW, Shiels HA (2006) Calcium flux in turtle ventricular myocytes. Am J Physiol 291:R1781–R1789

    CAS  Google Scholar 

  • Galli GL, Warren DE, Shiels HA (2009) Ca2+ cycling in cardiomyocytes from a high-performance reptile, the varanid lizard (Varanus exanthematicus). Am J Physiol 297:R1636–R1644

    CAS  Google Scholar 

  • Hassinen M, Paajanen V, Haverinen J, Eronen H, Vornanen M (2007) Cloning and expression of cardiac Kir2.1 and Kir 2.2 channels in thermally acclimated rainbow trout. Am J Physiol 292:R2328–R2339

    CAS  Google Scholar 

  • Hassinen M, Laulaja S, Paajanen V, Haverinen J, Vornanen M (2011) Thermal adaptation of the crucian carp (Carassius carassius) cardiac delayed rectifier current, IKs, by homomeric assembly of Kv7.1 subunits without MinK. Am J Physiol 301:R255–R2665

    Article  CAS  Google Scholar 

  • Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 90:291–366

    Article  CAS  Google Scholar 

  • Jeevaratnam K, Chadda KR, Huang CL-H, Camm AJ (2018) Cardiac potassium channels: physiological insights for targeted therapy. J Cardiovasc Pharmacol Ther 23:119–129

    Article  CAS  Google Scholar 

  • Jensen B, Wang T, Christoffels VM, Moorman AF (2013) Evolution and development of the building plan of the vertebrate heart. Biochim Biophys Acta 1833:783–794

    Article  CAS  Google Scholar 

  • Jensen B, Boukens BJ, Wang T, Moorman AF, Christoffels VM (2014a) Evolution of the sinus venosus from fish to humans. J Cardiovasc Dev Dis 1:14–28

    Article  Google Scholar 

  • Jensen B, Moorman AF, Wang T (2014b) Structure and function of the hearts of lizards and snakes. Biol Rev Camb Philos Soc 89:302–336

    Article  Google Scholar 

  • Jensen B, Vesterskov S, Boukens BJ, Nielsen JM, Moorman AFM, Christoffels VM, Wang T (2017) Morpho-functional characterization of the systemic venous pole of the reptile heart. Sci Rep 7:6644

    Article  Google Scholar 

  • Kleber AG, Rudy Y (2004) Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev 84:431–488

    Article  CAS  Google Scholar 

  • Kumari N, Gaur H, Bhargava A (2018) Cardiac voltage gated calcium channels and their regulation by β-adrenergic signaling. Life Sci 194:139–149

    Article  CAS  Google Scholar 

  • Li GR, Feng J, Yue L, Carrier M, Nattel S (1996) Evidence for two components of delayed rectifier K+ current in human ventricular myocytes. Circ Res 78:689–696

    Article  CAS  Google Scholar 

  • Paajanen V, Vornanen M (2004) Regulation of action potential duration under acute heat stress by I(K, ATP) and I(K1) in fish cardiac myocytes. Am J Physiol 286:R405–R415

    CAS  Google Scholar 

  • Panama BK, McLerie M, Lopatin AN (2007) Heterogeneity of IK1 in the mouse heart. Am J Physiol 293:H3558–3567

    CAS  Google Scholar 

  • Sauviat MP, Colas A, Pages N (2002) Does lindane (gamma-hexachlorocyclohexane) increase the rapid delayed rectifier outward K+ current (IKr) in frog atrial myocytes? BMC Pharmacol 2:15

    Article  Google Scholar 

  • Savio-Galimberti E, Argenziano M, Antzelevitch C (2018) Cardiac arrhythmias related to sodium channel dysfunction. Handb Exp Pharmacol 246:331–354

    Article  CAS  Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2002) The force-frequency relationship in fish hearts—a review. Comp Biochem Physiol 132A:811–826

    Article  CAS  Google Scholar 

  • Shih HT (1994) Anatomy of the action potential in the heart. Tex Heart Inst J 21:30–41

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stecyk JAW, Paajanen V, Farrell AP, Vornanen M (2007) Effect of temperature and prolonged anoxia exposure on electrophysiological properties of the turtle (Trachemys scripta) heart. Am J Physiol 293:R421–R437

    CAS  Google Scholar 

  • Tamargo J, Caballero R, Gomez R, Valenzuela C, Delpon E (2004) Pharmacology of cardiac potassium channels. Cardiovasc Res 62:9–33

    Article  CAS  Google Scholar 

  • Varro A, Nanasi PP, Lathrop DA (1993) Potassium currents in isolated human atrial and ventricular cardiomyocytes. Acta Physiol Scand 149:133–142

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Vornanen M, Ryokkynen A, Nurmi A (2002) Temperature-dependent expression of sarcolemmal K(+) currents in rainbow trout atrial and ventricular myocytes. Am J Physiol 282:R1191–R1199

    Article  CAS  Google Scholar 

  • Vornanen M, Hassinen M, Haverinen J (2011) Tetrodotoxin sensitivity of the vertebrate cardiac Na+ current. Mar Drugs 9:2409–2422

    Article  CAS  Google Scholar 

  • Warren DE, Galli GLJ, Patrick SM, Shiels HA (2010) The cellular force-frequency response in ventricular myocytes from the varanid lizard, Varanus exanthematicus. Am J Physiol 298:R567–R574

    CAS  Google Scholar 

  • Zaar M, Overgaard J, Gesser H, Wang T (2007) Contractile properties of the functionally divided python heart: two sides of the same matter. Comp Biochem Physiol 146A:163–173

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Elin Petersen for excellent technical assistance and Heidi Meldgaard for animal care. The study was supported by the Russian Foundation for Basic Research [17-04-01921 to D.V.A.] and the Danish Research Council (Natur og Univers, Danmarks Frie Forskningsfond).

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Authors and Affiliations

  1. Department of Human and Animal Physiology, Biological Faculty of the Moscow State University, Lomonosov Moscow State University, Leninskiye Gory, 1, 12, Moscow, Russia

    Denis V. Abramochkin

  2. Ural Federal University, Mira 19, Ekaterinburg, Russia

    Denis V. Abramochkin

  3. Laboratory of Cardiac Physiology, Institute of Physiology of Кomi Science Centre of the Ural Branch of the Russian Academy of Sciences, FRC Komi SC UB RAS, Pervomayskaya str., 50, 167982, Syktyvkar, Komi Republic, Russia

    Denis V. Abramochkin

  4. Department of Physiology, Pirogov Russian National Research Medical University, Ostrovityanova str., 1, Moscow, Russia

    Denis V. Abramochkin

  5. Department of Medicine, Health, University of Aarhus, Aarhus, Denmark

    Vladimir Matchkov

  6. Department of Zoophysiology, University of Aarhus, Aarhus, Denmark

    Tobias Wang

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  1. Denis V. Abramochkin
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  2. Vladimir Matchkov
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Correspondence to Denis V. Abramochkin.

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Communicated by H. V. Carey.

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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 190, 63–73 (2020). https://doi.org/10.1007/s00360-019-01253-5

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  • DOI: https://doi.org/10.1007/s00360-019-01253-5

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