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Inward Rectifier Currents IK1 and IKACh in Working Myocardium of Japanese Quail (Coturnix japonica)

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Abstract

Birds acquired endothermy and a four-chambered heart independently from mammals in the course of evolution. Though avian embryos are widely used in experiments, little is known about the adult avian heart. Recent studies have shown that, despite a large evolutionary distance, the set of repolarizing potassium currents in avian myocardium resembles that in mammalian heart as well as that in humans. This allows for proposing birds as a potential model in experimental cardiology. The present study for the first time describes inward rectifier currents in working myocardium of quail. Using patch clamp method, we recorded main background inward rectifier current IK1 was recorded in isolated atrial and ventricular cardiomyocytes of quail. Both inward and outward components of IK1 in ventricular cells were larger than those in atrial cells, while there were no differences in voltage dependence of inward rectification. Acetylcholine and carbachol induced activation of acetylcholine-dependent inward rectifier current IKACh in atrial but not in ventricular myocytes. IKACh in atrial myocytes was sensitive to tertiapin. Constitutively active IKACh has not been detected. In multicellular preparations of the quail right atrium, carbachol induced hyperpolarization and shortening of action potentials, while no such effects were observed in preparations of the right ventricle. Activation of IKACh upon application of carbachol was dose-dependent with EC50 = 4.922 × 10–7 М. The described distribution of inward rectifier currents in avian myocardium is similar to that in mammalian species, which are widely used as model objects in experimental cardiology.

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REFERENCES

  1. Shiels, H.A. and Galli, G.L.J., The sarcoplasmic reticulum and the evolution of the vertebrate heart, Physiology, 2014, vol. 29, no. 6, pp. 456–469.

    Article  CAS  Google Scholar 

  2. Jensen, B., Wang, T., Christoffels, V.M., and Moorman, A.F.M., Evolution and development of the building plan of the vertebrate heart, Biochim. Biophys. Acta. Mol. Cell Res., 2013, vol. 1833, no. 4, pp. 783–794.

    CAS  Google Scholar 

  3. Filatova, T.S., Abramochkin, D.V., Pavlova, N.S., Pustovit, K.B., Konovalova, O.P., Kuzmin, V.S., and Dobrzynski, H., Repolarizing potassium currents in working myocardium of Japanese quail: Novel translational model for cardiac electrophysiology, Comp. Biochem. Physiol. Part A Mol. Integr. Physiol., 2021, vol. 255, 110919.

    Article  CAS  Google Scholar 

  4. Filatova, T.S., Abramochkin, D.V., and Shiels, H.A., Warmer, faster, stronger: Ca2+ cycling in avian myocardium, J. Exp. Biol., 2020, vol. 223, no. 19, jev228205.

    Article  Google Scholar 

  5. Vornanen, M., Hassinen, M., and Haverinen, J., Tetrodotoxin sensitivity of the vertebrate cardiac Na+ current, Mar. Drugs, 2011, vol. 9, no. 11, pp. 2409–2422.

    Article  CAS  Google Scholar 

  6. Abramochkin, D.V., Matchkov, V., and 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 Biochem. Syst. Environ. Physiol., 2020, vol. 190, no. 1, pp. 63–73.

    Article  CAS  Google Scholar 

  7. Cavero, I. and Crumb, W., Native and cloned ion channels from human heart: Laboratory models for evaluating the cardiac safety of new drugs, Eur. Hear. J. Suppl., 2001, vol. 3, suppl. K, pp. K53–K63.

  8. Jost, N., Virag, L., Bitay, M., Takács, J., Lengyel, C., Biliczki, P., Nagy, Z., Bogats, G., Lathrop, D.A., Papp, J.G., and Varró, A., Restricting excessive cardiac action potential and QT prolongation: A vital role for I Ks in human ventricular muscle, Circulation, 2005, vol. 112, no. 10, pp. 1392–1399.

    Article  Google Scholar 

  9. Ehrlich, J.R., Inward rectifier potassium currents as a target for atrial fibrillation therapy, J. Cardiovasc. Pharmacol., 2008, vol. 52, no. 2, pp. 129–135.

    Article  CAS  Google Scholar 

  10. Klein, M.G., Shou, M., Stohlman, J., Solhjoo, S., Haigney, M., Tidwell, R.R., Goldstein, R.E., Flagg, T.P., and Haigney, M.C., Role of suppression of the inward rectifier current in terminal action potential repolarization in the failing heart, Heart Rhythm, 2017, vol. 14, no. 8, pp. 1217–1223.

    Article  Google Scholar 

  11. Isenberg, G. and Klockner, U., Calcium tolerant ventricular myocytes prepared by preincubation in a “KB medium,” Pflügers Arch. Eur. J. Physiol., 1982, vol. 395, no. 1, pp. 6–18.

    Article  CAS  Google Scholar 

  12. Valance, D., Despres, G., Richard, S., Constantin, P., Mignon-Grasteau, S., Leman, S., Boissy, A., Faure, J.M., and Leterrier, C., Changes in heart rate variability during a tonic immobility test in quail, Physiol. Behav., 2008, vol. 93, no. 3, pp. 512–520.

    Article  CAS  Google Scholar 

  13. Haverinen, J. and Vornanen, M., Responses of action potential and K+ currents to temperature acclimation in fish hearts: Phylogeny or thermal preferences?, Physiol. Biochem. Zool., 2009, vol. 82, no. 5, pp. 468–482.

    Article  CAS  Google Scholar 

  14. Varro, A., Nanasi, P.P., and Lathrop, D.A., Potassium currents in isolated human atrial and ventricular cardiocytes, Acta Physiol. Scand., 1993, vol. 149, no. 2, pp. 133–142.

    Article  CAS  Google Scholar 

  15. Panama, B.K., McLerie, M., and Lopatin, A.N., Heterogeneity of I K1 in the mouse heart, Am. J. Physiol. Hear. Circ. Physiol., 2007, vol. 293, no. 6, pp. H3558–H3567.

    Article  CAS  Google Scholar 

  16. Ward, C.A., Ma, Z., Lee, S.S., and Giles, W.R., Potassium currents in atrial and ventricular myocytes from a rat model of cirrhosis, Am. J. Physiol. Gastrointest. Liver Physiol., 1997, vol. 273, no. 2, pp. G537–G544.

    Article  CAS  Google Scholar 

  17. Hassinen, M., Haverinen, J., Hardy, M.E., Shiels, H.A., and Vornanen, M., Inward rectifier potassium current (I K1) and Kir2 composition of the zebrafish (Danio rerio) heart, Pflügers Arch. Eur. J. Physiol., 2015, vol. 467, no. 12, pp. 2437–2446.

    Article  CAS  Google Scholar 

  18. Skarsfeldt, M.A., Bomholtz, S.H., Lundegaard, P.R., Lopez-Izquierdo, A., Tristani-Firouzi, M., and Bentzen, B.H., Atrium-specific ion channels in the zebrafish-a role of I KACh in atrial repolarization, Acta Physiol., 2018, vol. 223, no. 3, e13049.

    Article  CAS  Google Scholar 

  19. Dobrzynski, H., Marples, D.D.R., Musa, H., Yamanu-shi, T.T., Henderson, Z., Takagishi, Y., Honjo, H., Kodama, I., and Boyett, M.R., Distribution of the muscarinic K+ channel proteins Kir3.1 and Kir3.4 in the ventricle, atrium, and sinoatrial node of heart, J. Histochem. Cytochem., 2001, vol. 49, no. 10, pp. 1221–1234.

    Article  CAS  Google Scholar 

  20. Liang, B., Nissen, J.D., Laursen, M., Wang, X., Skibsbye, L., Hearing, M.C., Andersen, M.N., Rasmussen, H.B., Wickman, K., Grunnet, M., Olesen, S.-P., and Jespersen, T., G-protein-coupled inward rectifier potassium current contributes to ventricular repolarization, Cardiovasc. Res., 2014, vol. 101, no. 1, pp. 175–184.

    Article  CAS  Google Scholar 

  21. Beckmann, C., Rinne, A., Littwitz, C., Mintert, E., Bosche, L.I., Kienitz, M.-C., Pott, L., and Bender, K., G protein-activated (GIRK) current in rat ventricular myocytes is masked by constitutive inward rectifier current (I K1), Cell. Physiol. Biochem., 2008, vol. 21, no. 4, pp. 259–268.

    Article  CAS  Google Scholar 

  22. Dobrev, D., Graf, E., Wettwer, E., Himmel, H.M., Hála, O., Doerfel, C., Christ, T., Schuler, S., and Ravens, U., Molecular basis of downregulation of G-protein-coupled inward rectifying K+ current (I K,ACh) in chronic human atrial fibrillation decrease in GIRK4 mRNA correlates with reduced I K,ACh and muscarinic receptor-mediated shortening of action potentials, Circulation, 2001, vol. 104, no. 21, pp. 2551–2557.

    Article  CAS  Google Scholar 

  23. Abramochkin, D.V. and Vornanen, M., Seasonal changes of cholinergic response in the atrium of Arctic navaga cod (Eleginus navaga), J. Comp. Physiol. B Biochem. Syst. Environ. Physiol., 2017, vol. 187, no. 2, pp. 329–338.

    Article  CAS  Google Scholar 

  24. Lomax, A.E., Rose, R.A., and Giles, W.R., Electrophysiological evidence for a gradient of G protein-gated K+ current in adult mouse atria, Br. J. Pharmacol., 2003, vol. 140, no. 3, pp. 576–584.

    Article  CAS  Google Scholar 

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Funding

This work was financially supported by the Russian Foundation for Basic Research (project no. 19-34-90142).

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Authors and Affiliations

  1. Department of Human and Animal Physiology, Moscow State University, 119234, Moscow, Russia

    T. S. Filatova & D. V. Abramochkin

  2. Laboratory of Cardiac Electrophysiology, National Medical Research Center for Cardiology, 121552, Moscow, Russia

    T. S. Filatova & D. V. Abramochkin

  3. Department of Physiology, Pirogov Russian National Research Medical University, 117997, Moscow, Russia

    T. S. Filatova & D. V. Abramochkin

Authors
  1. T. S. Filatova
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  2. D. V. Abramochkin
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Correspondence to T. S. Filatova.

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Conflict of interests. The authors declare that they have no conflict of interests.

Statement on the welfare of animals. All experiments were performed in accordance with Directive 86/609/EEC on the handling of laboratory animals.

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Translated by P. Kuchina

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Filatova, T.S., Abramochkin, D.V. Inward Rectifier Currents IK1 and IKACh in Working Myocardium of Japanese Quail (Coturnix japonica). Moscow Univ. Biol.Sci. Bull. 76, 65–70 (2021). https://doi.org/10.3103/S0096392521020012

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  • DOI: https://doi.org/10.3103/S0096392521020012

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