Inward rectifier currents IK1 and IKACh in working myocardium of Japanese quail (Coturnix japonica)
Abstract
Birds acquired endothermy and four-chambered heart independently from mammals in the course of evolution. Though avian embryos are widely used in experiments, little is known about adult avian heart. Recent studies have shown that despite of big evolutionary distance, the set of repolarizing potassium currents in avian myocardium resembles that in mammalian heart as well as in humans. That allows to propose birds as a potential model in experimental cardiology. The present study for the first time describes inward rectifier potassium currents in working myocardium of quail. Using patch clamp method, we recorded main background inward rectifier current IK1 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 quail right atrium carbachol induced hyperpolarization and shortening of action potentials, while in preparations of right ventricle no such effects were observed. Activation of IKACh upon application of carbachol was dose-dependent with EC50=4,922∙10-7М. 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.
Keywords
About the Authors
T. S. FilatovaRussian Federation
Department of Human and Animal Physiology
Laboratory of Cardiac Electrophysiology
Department of Physiology
Leninskiye gory, 1–12, Moscow, 119234
3rd Cherepkovskaya str., 15A, Moscow
Ostrovityanova str., 1, Moscow
D. V. Abramochkin
Russian Federation
Department of Human and Animal Physiology
Laboratory of Cardiac Electrophysiology
Department of Physiology
Leninskiye gory, 1–12, Moscow, 119234
3rd Cherepkovskaya str., 15A, Moscow
Ostrovityanova str., 1, Moscow
References
1. Shiels H.A., Galli G.L.J. The sarcoplasmic reticulum and the evolution of the vertebrate heart // Physiology. 2014. Vol. 29. N 6. P. 456–469.
2. Jensen B., Wang T., Christoffels V.M., Moorman A.F.M. Evolution and development of the building plan of the vertebrate heart // Biochim. Biophys. Acta. Mol. Cell Res. 2013. Vol. 1833. N 4. P. 783–794.
3. Filatova T.S., Abramochkin D. V., Pavlova N.S., Pustovit K.B., Konovalova O.P., Kuzmin V.S., 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.
4. Filatova T.S., Abramochkin D. V., Shiels H.A. Warmer, faster, stronger: Ca 2+ cycling in avian myocardium // J. Exp. Biol. 2020. Vol. 223. N 19: jeb228205.
5. Vornanen M., Hassinen M., Haverinen J. Tetrodotoxin sensitivity of the vertebrate cardiac Na+ current // Mar. Drugs. 2011. Vol. 9. N 11. P. 2409–2422.
6. 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 Biochem. Syst. Environ. Physiol. 2020. Vol. 190. N 1. P. 63–73.
7. Cavero I., 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. P. K53–K63.
8. Jost N., Virág L., Bitay M., Takács J., Lengyel C., Biliczki P., Nagy Z., Bogáts G., Lathrop D.A., Papp J.G., Varró A. Restricting excessive cardiac action potential and QT prolongation: A vital role for I Ks in human ventricular muscle // Circulation. 2005. Vol. 112. N 10. P. 1392–1399.
9. Ehrlich J.R. Inward rectifier potassium currents as a target for atrial fibrillation therapy // J. Cardiovasc. Pharmacol. 2008. Vol. 52. N 2. P. 129–135.
10. Klein M.G., Shou M., Stohlman J., Solhjoo S., Haigney M., Tidwell R.R., Goldstein R.E., Flagg T.P., 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. N 8. P. 1217–1223.
11. Isenberg G., Klockner U. Calcium tolerant ventricular myocytes prepared by preincubation in a “KB medium” // Pflügers Arch. Eur. J. Physiol. 1982. Vol. 395. N 1. P. 6–18.
12. Valance D., Després G., Richard S., Constantin P., Mignon-Grasteau S., Leman S., Boissy A., Faure J.M., Leterrier C. Changes in heart rate variability during a tonic immobility test in quail // Physiol. Behav. 2008. Vol. 93. N 3. P. 512–520.
13. 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. Vol. 82. N 5. P. 468–482.
14. Varro A., Nanasi P.P., Lathrop D.A. Potassium currents in isolated human atrial and ventricular cardiocytes // Acta Physiol. Scand. 1993. Vol. 149. N 2. P. 133–142.
15. Panama B.K., McLerie M., Lopatin A.N. Heterogeneity of I K1 in the mouse heart // Am. J. Physiol. Hear. Circ. Physiol. 2007. Vol. 293. N 6. P. H3558–H3567.
16. Ward C.A., Ma Z., Lee S.S., 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. N 2. P. G537–G544.
17. Hassinen M., Haverinen J., Hardy M.E., Shiels H.A., Vornanen M. Inward rectifier potassium current (IK1 ) and Kir2 composition of the zebrafish (Danio rerio) heart // Pflugers Arch. Eur. J. Physiol. 2015. Vol. 467. N 12. P. 2437–2446.
18. Skarsfeldt M.A., Bomholtz S.H., Lundegaard P.R., Lopez-Izquierdo A., Tristani-Firouzi M., Bentzen B.H. Atriumspecific ion channels in the zebrafish-A role of I KACh in atrial repolarization // Acta Physiol. 2018. Vol. 223. N 3: e13049.
19. Dobrzynski H., Marples D.D.R., Musa H., Yamanushi T.T., Henderson Z., Takagishi Y., Honjo H., Kodama I., 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. N 10. P. 1221–1234.
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., Jespersen T. G-protein-coupled inward rectifier potassium current contributes to ventricular repolarization // Cardiovasc. Res. 2014. Vol. 101. N 1. P. 175–184.
21. Beckmann C., Rinne A., Littwitz C., Mintert E., Bosche L.I., Kienitz M.-C., Pott L., Bender K. G ProteinActivated (GIRK) Current in Rat Ventricular Myocytes is Masked by Constitutive Inward Rectifier Current (IK1 ) // Cell. Physiol. Biochem. 2008. Vol. 21. N 4. P. 259–268.
22. Dobrev D., Graf E., Wettwer E., Himmel H.M., Hála O., Doerfel C., Christ T., Schüler S., Ravens U. Molecular basis of downregulation of G-protein-coupled inward rectifying K + current (IK,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. N 21. P. 2551–2557.
23. Abramochkin D. V., 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. N 2. P. 329–338.
24. Lomax A.E., Rose R.A., Giles W.R. Electrophysiological evidence for a gradient of G proteingated K + current in adult mouse atria // Br. J. Pharmacol. 2003. Vol. 140. N 3. P. 576–584.
Review
For citations:
Filatova T.S., Abramochkin D.V. Inward rectifier currents IK1 and IKACh in working myocardium of Japanese quail (Coturnix japonica). Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2021;76(2):83-89. (In Russ.)