Electrophysiology of the Danio rerio Heart

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Tropical teleost fish Danio rerio is increasingly used as a model object for electrophysiological studies of human cardiac physiology and pathology. D. rerio is characterized by the similarity with humans in such functional parameters of the electrical activity of the heart as heart rate, action potential morphology, as well as in a set of ion currents depolarizing and repolarizing the cell membrane. D. rerio is easy to breed, easy to handle experimentally, and easy to genetically modify. This overview presents current data on the structural and functional organization of ion channels in D. rerio heart myocytes.

Full Text

Restricted Access

About the authors

A. V. Karpushev

Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences

Author for correspondence.
Email: akarpushev@yandex.ru
Russian Federation, St. Petersburg, 194223

V. B. Mikhailova

Almazov National Medical Research Centre

Email: akarpushev@yandex.ru
Russian Federation, St. Petersburg, 197341

A. A. Kostareva

Almazov National Medical Research Centre

Email: akarpushev@yandex.ru
Russian Federation, St. Petersburg, 197341

B. S. Zhorov

Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences; Almazov National Medical Research Centre

Email: akarpushev@yandex.ru
Russian Federation, St. Petersburg, 194223; St. Petersburg, 197341

References

  1. Leong I.U.S., Skinner J.R., Shelling A.N., Love D.R. 2010. Identification and expression analysis of kcnh2 genes in the zebrafish. Biochem. Biophys. Res. Commun. 396 (4), 817–824.
  2. Genge C.E., Lin E., Lee L., Sheng X., Rayani K., Gunawan M., Stevens C.M., Li A.Y., Talab S.S., Claydon T.W., Hove-Madsen L., Tibbits G.F. 2016. The zebrafish heart as a model of mammalian cardiac function. Rev. Physiol. Biochem. Pharmacol. 171, 99–136.
  3. Derangeon M., Montnach J., Baró I., Charpentier F. 2012. Mouse models of SCN5A-related cardiac arrhythmias. Front. Physiol. 3, 210.
  4. Nerbonne J.M., Nichols C.G., Schwarz T.L., Escande D. 2002. Genetic manipulation of cardiac K⁺ channel function in mice: What have we learned, and where do we go from here? Circ. Res. 89 (11), 944–956.
  5. Kaese S., Verheule S. 2012. Cardiac electrophysiology in mice: A matter of size. Front. Physiol. 3, 345.
  6. Mittelstadt S.W., Hemenway C.L., Craig M.P., Hove J.R. 2008. Evaluation of zebrafish embryos as a model for assessing inhibition of hERG. J. Pharmacol. Toxicol. Methods. 57 (2), 100–105.
  7. Bakkers J. 2011. Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc. Res. 91 (2), 279–288.
  8. Dahme T., Katus H.A., Rottbauer W. 2009. Fishing for the genetic basis of cardiovascular disease. Dis. Model. Mech. 2 (1–2), 18–22.
  9. Stainier D.Y., Fouquet B., Chen J.N., Warren K.S., Weinstein B.M., Meiler S.E., Mohideen M.A., Neuhauss S.C., Solnica-Krezel L., Schier A.F., Zwartkruis F., Stemple D.L., Malicki J., Driever W., Fishman M.C. 1996. Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development. 123, 285–292.
  10. Verkerk A.O., Remme C.A. 2012. Zebrafish: A novel research tool for cardiac (patho)electrophysiology and ion channel disorders. Front. Physiol. 3, 255.
  11. Harri M.N., Talo A. 1975. Effect of season and temperature acclimation on the heart rate-temperature relationship in the isolated frog’s heart (Rana temporaria). Comp. Biochem. Physiol. A Comp. Physiol. 52 (2), 409–412.
  12. Chapovetsky V., Katz U. 2003. Effects of season and temperature acclimation on electrocardiogram and heart rate of toads. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 134 (1), 77–83.
  13. Abramochkin D., Kuzmin V. 2018. Electrophysiological differences in cholinergic signaling between the hearts of summer and winter frogs (Rana temporaria). J. Comp. Physiol. B. 188 (4), 649–656.
  14. Abramochkin D.V., Filatova T.S., Pustovit K.B., Voronina Y.A., Kuzmin V.S., Vornanen M. 2022. 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. 268, 111204.
  15. Giles W.R., Shibata E.F. 1985. Voltage clamp of bull-frog cardiac pace-maker cells: A quantitative analysis of potassium currents. J. Physiol. 368, 265–292.
  16. Simmons M.A., Creazzo T., Hartzell H.C. 1986. A time-dependent and voltage-sensitive K⁺ current in single cells from frog atrium. J. Gen. Physiol. 88 (6), 739–755.
  17. Hume J.R., Giles W., Robinson K., Shibata E.F., Nathan R.D., Kanai K., Rasmusson R. 1986. A time- and voltage-dependent K⁺ current in single cardiac cells from bullfrog atrium. J. Gen. Physiol. 88 (6), 777–798.
  18. Nemtsas P., Wettwer E., Christ T., Weidinger G., Ravens U. 2010. Adult zebrafish heart as a model for human heart? An electrophysiological study. J. Mol. Cell Cardiol. 48 (1), 161–171.
  19. Karpushev A.V., Mikhailova V.B., Klimenko E.S., Kulikov A.N., Ivkin D.Y., Kaschina E., Okovityi S.V. 2022. SGLT2 inhibitor empagliflozin modulates ion channels in adult zebrafish heart. Int. J. Mol. Sci. 23 (17), 9559.
  20. Jou C.J., Spitzer K.W., Tristani-Firouzi M. 2010. Blebbistatin effectively uncouples the excitation-contraction process in zebrafish embryonic heart. Cell Physiol. Biochem. 25 (4–5), 419–424.
  21. Panáková D., Werdich A.A., Macrae C.A. 2010. Wnt11 patterns a myocardial electrical gradient through regulation of the L-type Ca²⁺ channel. Nature. 466 (7308), 874–878.
  22. Wythe J.D., Jurynec M.J., Urness L.D., Jones C.A., Sabeh M.K., Werdich A.A., Sato M., Yost H.J., Grunwald D.J., Macrae C.A., Li D.Y. 2011. Hadp1, a newly identified pleckstrin homology domain protein, is required for cardiac contractility in zebrafish. Dis. Model. Mech. 4 (5), 607–621.
  23. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (3), 253–310.
  24. Serluca F.C. 2008. Development of the proepicardial organ in the zebrafish. Dev. Biol. 315 (1), 18–27.
  25. Peralta M., González-Rosa J.M., Marques I.J., Mercader N. 2014. The epicardium in the embryonic and adult zebrafish. J. Dev. Biol. 2 (2), 101–116.
  26. Weinberger M., Simões F.C., Patient R., Sauka-Spengler T., Riley P.R. 2020. Functional heterogeneity within the developing zebrafish epicardium. Dev. Cell. 52 (5), 574–590.
  27. Liu J., Bressan M., Hassel D., Huisken J., Staudt D., Kikuchi K., Poss K.D., Mikawa T., Stainier D.Y. 2010. A dual role for ErbB2 signaling in cardiac trabeculation. Development. 137 (22), 3867–3875.
  28. Staudt D.W., Liu J., Thorn K.S., Stuurman N., Liebling M., Stainier D.Y. 2014. High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation. Development. 141 (3), 585–593.
  29. Beis D., Bartman T., Jin S.W., Scott I.C., D’Amico L.A., Ober E.A., Verkade H., Frantsve J., Field H.A., Wehman A., Baier H., Tallafuss A., Bally-Cuif L., Chen J.N., Stainier D.Y., Jungblut B. 2005. Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development. 132 (18), 4193–4204.
  30. Scherz P.J., Huisken J., Sahai-Hernandez P., Stainier D.Y. 2008. High-speed imaging of developing heart valves reveals interplay of morphogenesis and function. Development. 135 (6), 1179–1187.
  31. Harrison M.R., Bussmann J., Huang Y., Zhao L., Osorio A., Burns C.G., Burns C.E., Sucov H.M., Siekmann A.F., Lien C.L. 2015. Chemokine-guided angiogenesis directs coronary vasculature formation in zebrafish. Dev. Cell. 33 (4), 442–454.
  32. Hu N., Yost H.J., Clark E.B. 2001. Cardiac morphology and blood pressure in the adult zebrafish. Anat. Rec. 264 (1), 1–12.
  33. Mahmoud A.I., O’Meara C.C., Gemberling M., Zhao L., Bryant D.M., Zheng R., Gannon J.B., Cai L., Choi W.Y., Egnaczyk G.F., Burns C.E., Burns C.G., MacRae C.A., Poss K.D., Lee R.T. 2015. Nerves regulate cardiomyocyte proliferation and heart regeneration. Dev. Cell. 34 (4), 387–399.
  34. Pott A., Rottbauer W., Just S. 2014. Functional genomics in zebrafish as a tool to identify novel antiarrhythmic targets. Curr. Med. Chem. 21 (11), 1320–1329.
  35. Wang L.W., Huttner I.G., Santiago C.F., Kesteven S.H., Yu Z.Y., Feneley M.P., Fatkin D. 2017. Standardized echocardiographic assessment of cardiac function in normal adult zebrafish and heart disease models. Dis. Model Mech. 10 (1), 63–76.
  36. Barrionuevo W.R., Burggren W.W. 1999. O2 consumption and heart rate in developing zebrafish (Danio rerio): Influence of temperature and ambient O2. Am. J. Physiol. 276 (2), R505–R513.
  37. Tsai C.T., Wu C.K., Chiang F.T., Tseng C.D., Lee J.K., Yu C.C., Wang Y.C., Lai L.P., Lin J.L., Hwang J.J. 2011. In-vitro recording of adult zebrafish heart electrocardiogram – a platform for pharmacological testing. Clin. Chim. Acta. 412 (21–22), 1963–1967.
  38. Schweizer M., Dieterich A., Triebskorn R., Köhler H.R. 2017. Drifting away of a FET endpoint: The heart rate in Danio rerio embryos is extremely sensitive to variation in ambient temperature. Bull. Environ. Contam. Toxicol. 99 (6), 684–689.
  39. Milan D.J., Jones I.L., Ellinor P.T., MacRae C.A. 2006. In vivo recording of adult zebrafish electrocardiogram and assessment of drug-induced QT prolongation. Am. J. Physiol. Heart Circ. Physiol. 291 (1), H269–H273.
  40. Leong I.U., Skinner J.R., Shelling A.N., Love D.R. 2010. Zebrafish as a model for long QT syndrome: The evidence and the means of manipulating zebrafish gene expression. Acta Physiol. (Oxf). 199 (3), 257–276.
  41. Liu C.C., Li L., Lam Y.W., Siu C.W., Cheng S.H. 2016. Improvement of surface ECG recording in adult zebrafish reveals that the value of this model exceeds our expectation. Sci. Rep. 6, 25073.
  42. Zhao Y., James N.A., Beshay A.R., Chang E.E., Lin A., Bashar F., Wassily A., Nguyen B., Nguyen T.P. 2021. Adult zebrafish ventricular electrical gradients as tissue mechanisms of ECG patterns under baseline vs. oxidative stress. Cardiovasc. Res. 117 (8), 1891–1907.
  43. Zhao Y., Chen C., Yun M., Issa T., Lin A., Nguyen T.P. 2021. Constructing adult zebrafish einthoven’s triangle to define electrical heart axes. Front. Physiol. 12, 708938.
  44. Arel E., Rolland L., Thireau J., Torrente A.G., Bechard E., Bride J., Jopling C., Demion M., Le Guennec J.Y. 2022. The effect of hypothermia and osmotic shock on the electrocardiogram of adult zebrafish. Biology (Basel). 11 (4), 603.
  45. D’Ascenzi F., Anselmi F., Adami P.E., Pelliccia A. 2020. Interpretation of T-wave inversion in physiological and pathological conditions: Current state and future perspectives. Clin. Cardiol. 43 (8), 827–833.
  46. Sun P., Zhang Y., Yu F., Parks E., Lyman A., Wu Q., Ai L., Hu C.H., Zhou Q., Shung K., Lien C.L., Hsiai T.K. 2009. Micro-electrocardiograms to study post-ventricular amputation of zebrafish heart. Ann. Biomed. Eng. 37 (5), 890–901.
  47. Lin M.H., Chou H.C., Chen Y.F., Liu W., Lee C.C., Liu L.Y., Chuang Y.J. 2018. Development of a rapid and economic in vivo electrocardiogram platform for cardiovascular drug assay and electrophysiology research in adult zebrafish. Sci. Rep. 8 (1), 15986.
  48. Zhao Y., Yun M., Nguyen S.A., Tran M., Nguyen T.P. 2019. In vivo surface electrocardiography for adult zebrafish. J. Vis. Exp. 150, 10.3791/60011.
  49. Abu Nahia K., Migdał M., Quinn T.A., Poon K.L., Łapiński M., Sulej A., Liu J., Mondal S.S., Pawlak M., Bugajski Ł., Piwocka K., Brand T., Kohl P., Korzh V., Winata C. 2021. Genomic and physiological analyses of the zebrafish atrioventricular canal reveal molecular building blocks of the secondary pacemaker region. Cell Mol. Life Sci. 78 (19–20), 6669–6687.
  50. Stoyek M.R., MacDonald E.A., Mantifel M., Baillie J.S., Selig B.M., Croll R.P., Smith F.M., Quinn T.A. 2022. Drivers of sinoatrial node automaticity in zebrafish: comparison with mechanisms of mammalian pacemaker function. Front. Physiol. 13, 818122.
  51. Sedmera D., Reckova M., deAlmeida A., Sedmerova M., Biermann M., Volejnik J., Sarre A., Raddatz E., McCarthy R.A., Gourdie R.G., Thompson R.P. 2003. Functional and morphological evidence for a ventricular conduction system in zebrafish and Xenopus hearts. Am. J. Physiol. Heart Circ. Physiol. 284 (4), H1152–H1160.
  52. Brette F., Luxan G., Cros C., Dixey H., Wilson C., Shiels H.A. 2008. Characterization of isolated ventricular myocytes from adult zebrafish (Danio rerio). Biochem. Biophys. Res. Commun. 374 (1), 143–146.
  53. Vornanen M., Shiels H.A., Farrell A.P. 2002. Plasticity of excitation-contraction coupling in fish cardiac myocytes. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 132 (4), 827–846.
  54. Asimaki A., Kapoor S., Plovie E., Karin Arndt A., Adams E., Liu Z., James C.A., Judge D.P., Calkins H., Churko J., Wu J.C., MacRae C.A., Kléber A.G., Saffitz J.E. 2014. Identification of a new modulator of the intercalated disc in a zebrafish model of arrhythmogenic cardiomyopathy. Sci. Transl. Med. 6 (240), 240ra74.
  55. Yu F., Zhao Y., Gu J., Quigley K.L., Chi N.C., Tai Y.C., Hsiai T.K. 2012. Flexible microelectrode arrays to interface epicardial electrical signals with intracardial calcium transients in zebrafish hearts. Biomed. Microdevices. 14 (2), 357–366.
  56. Lovering R.C., Roncaglia P., Howe D.G., Laulederkind S.J.F., Khodiyar V.K., Berardini T.Z., Tweedie S., Foulger R.E., Osumi-Sutherland D., Campbell N.H., Huntley R.P., Talmud P.J., Blake J.A., Breckenridge R., Riley P.R., Lambiase P.D., Elliott P.M., Clapp L., Tinker A., Hill D.P. 2018. Improving interpretation of cardiac phenotypes and enhancing discovery with expanded knowledge in the gene ontology. Circ. Genom. Precis. Med. 11 (2), e001813.
  57. Alday A., Alonso H., Gallego M., Urrutia J., Letamendia A., Callol C., Casis O. 2014. Ionic channels underlying the ventricular action potential in zebrafish embryo. Pharmacol. Res. 84, 26–31.
  58. Coutts C.A., Patten S.A., Balt L.N., Ali D.W. 2006. Development of ionic currents of zebrafish slow and fast skeletal muscle fibers. J. Neurobiol. 66 (3), 220–235.
  59. Miranda M., Egaña J.T., Allende M.L., Eblen-Zajjur A. 2019. Myocardial monophasic action potential recorded by suction electrode for ionic current studies in zebrafish. Zebrafish. 16 (5), 427–433.
  60. Gosselin-Badaroudine P., Moreau A., Chahine M. 2014. Nav 1.5 mutations linked to dilated cardiomyopathy phenotypes: Is the gating pore current the missing link? Channels (Austin). 8 (1), 90–94.
  61. Rook M.B., Evers M.M., Vos M.A., Bierhuizen M.F. 2012. Biology of cardiac sodium channel Nav1.5 expression. Cardiovasc. Res. 93 (1), 12–23.
  62. Warren K.S., Baker K., Fishman M.C. 2001. The slow mo mutation reduces pacemaker current and heart rate in adult zebrafish. Am. J. Physiol. Heart Circ. Physiol. 281 (4), H1711–H1719.
  63. Furukawa T., Koumi S., Sakakibara Y., Singer D.H., Jia H., Arentzen C.E., Backer C.L., Wasserstrom J.A. 1995. An analysis of lidocaine block of sodium current in isolated human atrial and ventricular myocytes. J. Mol. Cell Cardiol. 27 (2), 831–846.
  64. Novak A.E., Taylor A.D., Pineda R.H., Lasda E.L., Wright M.A., Ribera A.B. 2006. Embryonic and larval expression of zebrafish voltage-gated sodium channel alpha-subunit genes. Dev. Dyn. 235 (7), 1962–1973.
  65. Chopra S.S., Stroud D.M., Watanabe H., Bennett J.S., Burns C.G., Wells K.S., Yang T., Zhong T.P., Roden D.M. 2010. Voltage-gated sodium channels are required for heart development in zebrafish. Circ. Res. 106 (8), 1342–1350.
  66. Haverinen J., Hassinen M., Vornanen M. 2007. Fish cardiac sodium channels are tetrodotoxin sensitive. Acta Physiol. (Oxf). 191 (3), 197–204.
  67. Vornanen M., Hassinen M., Haverinen J. 2011. Tetrodotoxin sensitivity of the vertebrate cardiac Na+ current. Mar. Drugs. 9 (11), 2409–2422.
  68. Baker K., Warren K.S., Yellen G., Fishman M.C. 1997. Defective “pacemaker” current (Ih) in a zebrafish mutant with a slow heart rate. Proc. Natl. Acad. Sci. USA. 94 (9), 4554–4559.
  69. Rottbauer W., Baker K., Wo Z.G., Mohideen M.A., Cantiello H.F., Fishman M.C. 2001. Growth and function of the embryonic heart depend upon the cardiac-specific L-type calcium channel alpha1 subunit. Dev. Cell. 1 (2), 265–275.
  70. McDonald T.F., Pelzer S., Trautwein W., Pelzer D.J. 1994. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol. Rev. 74 (2), 365–507.
  71. Bers D.M. 2008. Calcium cycling and signaling in cardiac myocytes. Annu. Rev. Physiol. 70, 23–49.
  72. Vassort G., Talavera K., Alvarez J.L. 2006. Role of T-type Ca²⁺ channels in the heart. Cell Calcium. 40 (2), 205–220.
  73. Shah K., Seeley S., Schulz C., Fisher J., Gururaja Rao S. 2022. Calcium channels in the heart: Disease states and drugs. Cells. 11 (6), 943.
  74. Haverinen J., Hassinen M., Dash S.N., Vornanen M. 2018. Expression of calcium channel transcripts in the zebrafish heart: Dominance of T-type channels. J. Exp. Biol. 221 (Pt 10), jeb179226.
  75. Ebert A.M., McAnelly C.A., Srinivasan A., Linker J.L., Horne W.A., Garrity D.M. 2008. Ca²⁺ channel-independent requirement for MAGUK family CACNB4 genes in initiation of zebrafish epiboly. Proc. Natl. Acad. Sci. USA. 105 (1), 198–203.
  76. Chernyavskaya Y., Ebert A.M., Milligan E., Garrity D.M. 2012. Voltage-gated calcium channel CACNB2 (β2.1) protein is required in the heart for control of cell proliferation and heart tube integrity. Dev. Dyn. 241 (4), 648–662.
  77. Howe K., Clark M.D., Torroja C.F., Torrance J., Berthelot C., Muffato M., Collins J.E., Humphray S., McLaren K., Matthews L., McLaren S., Sealy I., Caccamo M., Churcher C., Scott C., Barrett J.C., Koch R., Rauch G.J., White S., Chow W., Kilian B., Quintais L.T., Guerra-Assunção J.A., Zhou Y., Gu Y., Yen J., Vogel J.H., Eyre T., Redmond S., Banerjee R., Chi J., Fu B., Langley E., Maguire S.F., Laird G.K., Lloyd D., Kenyon E., Donaldson S., Sehra H., Almeida-King J., Loveland J., Trevanion S., Jones M., Quail M., Willey D., Hunt A., Burton J., Sims S., McLay K., Plumb B., Davis J., Clee C., Oliver K., Clark R., Riddle C., Elliot D., Threadgold G., Harden G., Ware D., Begum S., Mortimore B., Kerry G., Heath P., Phillimore B., Tracey A., Corby N., Dunn M., Johnson C., Wood J., Clark S., Pelan S., Griffiths G., Smith M., Glithero R., Howden P., Barker N., Lloyd C., Stevens C., Harley J., Holt K., Panagiotidis G., Lovell J., Beasley H., Henderson C., Gordon D., Auger K., Wright D., Collins J., Raisen C., Dyer L., Leung K., Robertson L., Ambridge K., Leongamornlert D., McGuire S., Gilderthorp R., Griffiths C., Manthravadi D., Nichol S., Barker G., Whitehead S., Kay M., Brown J., Murnane C., Gray E., Humphries M., Sycamore N., Barker D., Saunders D., Wallis J., Babbage A., Hammond S., Mashreghi-Mohammadi M., Barr L., Martin S., Wray P., Ellington A., Matthews N., Ellwood M., Woodmansey R., Clark G., Cooper J., Tromans A., Grafham D., Skuce C., Pandian R., Andrews R., Harrison E., Kimberley A., Garnett J., Fosker N., Hall R., Garner P., Kelly D., Bird C., Palmer S., Gehring I., Berger A., Dooley C.M., Ersan-Ürün Z., Eser C., Geiger H., Geisler M., Karotki L., Kirn A., Konantz J., Konantz M., Oberländer M., Rudolph-Geiger S., Teucke M., Lanz C., Raddatz G., Osoegawa K., Zhu B., Rapp A., Widaa S., Langford C., Yang F., Schuster S.C., Carter N.P., Harrow J., Ning Z., Herrero J., Searle S.M., Enright A., Geisler R., Plasterk R.H., Lee C., Westerfield M., de Jong P.J., Zon L.I., Postlethwait J.H., Nüsslein-Volhard C., Hubbard T.J., Roest Crollius H., Rogers J., Stemple D.L. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 496 (7446), 498–503.
  78. Bovo E., Dvornikov A.V., Mazurek S.R., de Tombe P.P., Zima A.V. 2013. Mechanisms of Ca²+ handling in zebrafish ventricular myocytes. Pflügers Arch. 465 (12), 1775–1784.
  79. Jost N., Virág L., Bitay M., Takács J., Lengyel C., Biliczki P., Nagy Z., Bogáts G., Lathrop D.A., Papp J.G., Varró A. 2005. Restricting excessive cardiac action potential and QT prolongation: A vital role for IKs in human ventricular muscle. Circulation. 112 (10), 1392–1399.
  80. Wettwer E., Scholtysik G., Schaad A., Himmel H., Ravens U. 1991. Effects of the new class III antiarrhythmic drug E-4031 on myocardial contractility and electrophysiological parameters. J. Cardiovasc. Pharmacol. 17 (3), 480–487.
  81. Yang T., Tande P.M., Refsum H. 1991. Negative chronotropic effect of a novel class III antiarrhythmic drug, UK-68,798, devoid of beta-blocking action on isolated guinea-pig atria. Br. J. Pharmacol. 103 (2), 1417–1420.
  82. Schmitt N., Grunnet M., Olesen S.P. 2014. Cardiac potassium channel subtypes: New roles in repolarization and arrhythmia. Physiol. Rev. 94 (2), 609–653.
  83. Warmke J.W., Ganetzky B. 1994. A family of potassium channel genes related to eag in Drosophila and mammals. Proc. Natl. Acad. Sci. USA. 91 (8), 3438–3442.
  84. Vornanen M., Hassinen M. 2016. Zebrafish heart as a model for human cardiac electrophysiology. Channels (Austin). 10 (2), 101–110.
  85. Scholz E.P., Niemer N., Hassel D., Zitron E., Bürgers H.F., Bloehs R., Seyler C., Scherer D., Thomas D., Kathöfer S., Katus H.A., Rottbauer W.A., Karle C.A. 2009. Biophysical properties of zebrafish ether-à-go-go related gene potassium channels. Biochem. Biophys. Res. Commun. 381 (2), 159–164.
  86. Arnaout R., Ferrer T., Huisken J., Spitzer K., Stainier D.Y., Tristani-Firouzi M., Chi N.C. 2007. Zebrafish model for human long QT syndrome. Proc. Natl. Acad. Sci. USA. 104 (27), 11316–11321.
  87. Hassel D., Scholz E.P., Trano N., Friedrich O., Just S., Meder B., Weiss D.L., Zitron E., Marquart S., Vogel B., Karle C.A., Seemann G., Fishman M.C., Katus H.A., Rottbauer W. 2008. Deficient zebrafish ether-à-go-go-related gene channel gating causes short-QT syndrome in zebrafish reggae mutants. Circulation. 117 (7), 866–875.
  88. Langheinrich U., Vacun G., Wagner T. 2003. Zebrafish embryos express an orthologue of HERG and are sensitive toward a range of QT-prolonging drugs inducing severe arrhythmia. Toxicol. Appl. Pharmacol. 193 (3), 370–382.
  89. Milan D.J., Peterson T.A., Ruskin J.N., Peterson R.T., MacRae C.A. 2003. Drugs that induce repolarization abnormalities cause bradycardia in zebrafish. Circulation. 107 (10), 1355–1358.
  90. Abramochkin D.V., 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. Pflügers Arch. 470 (12), 1753–1764.
  91. Wu C., Sharma K., Laster K., Hersi M., Torres C., Lukas T.J., Moore E.J. 2014. Kcnq1-5 (Kv7.1-5) potassium channel expression in the adult zebrafish. BMC Physiol. 14, 1.
  92. Ravens U., Odening K.E. 2017. Atrial fibrillation: Therapeutic potential of atrial K⁺ channel blockers. Pharmacol. Ther. 176, 13–21.
  93. Skarsfeldt M.A., Bomholtz S.H., Lundegaard P.R., Lopez-Izquierdo A., Tristani-Firouzi M., Bentzen B.H. 2018. Atrium-specific ion channels in the zebrafish-A role of IKACh in atrial repolarization. Acta Physiol. (Oxf). 223 (3), e13049.
  94. Koumi S., Backer C.L., Arentzen C.E. 1995. Characterization of inwardly rectifying K⁺ channel in human cardiac myocytes. Alterations in channel behavior in myocytes isolated from patients with idiopathic dilated cardiomyopathy. Circulation. 92 (2), 164–174.
  95. Amos G.J., Wettwer E., Metzger F., Li Q., Himmel H.M., Ravens U. 1996. Differences between outward currents of human atrial and subepicardial ventricular myocytes. J. Physiol. 491, 31–50.
  96. Panama B.K., McLerie M., Lopatin A.N. 2007. Heterogeneity of IK1 in the mouse heart. Am. J. Physiol. Heart Circ. Physiol. 293 (6), H3558–H3567.
  97. Ravens U. 2018. Ionic basis of cardiac electrophysiology in zebrafish compared to human hearts. Prog. Biophys. Mol. Biol. 138, 38–44.
  98. Hassinen M., Haverinen J., Hardy M.E., Shiels H.A., Vornanen M. 2015. Inward rectifier potassium current (I K1) and Kir2 composition of the zebrafish (Danio rerio) heart. Pflügers Arch. 467 (12), 2437–2446.
  99. Gaborit N., Le Bouter S., Szuts V., Varro A., Escande D., Nattel S., Demolombe S. 2007. Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J. Physiol. 582 (Pt 2), 675–693.
  100. Hughes B.A., Kumar G., Yuan Y., Swaminathan A., Yan D., Sharma A., Plumley L., Yang-Feng T.L., Swaroop A. 2000. Cloning and functional expression of human retinal kir2.4, a pH-sensitive inwardly rectifying K⁺ channel. Am. J. Physiol. Cell Physiol. 279 (3), C771–C784.
  101. Singareddy S.S., Roessler H.I., McClenaghan C., Ikle J.M., Tryon R.C., van Haaften G., Nichols C.G. 2022. ATP-sensitive potassium channels in zebrafish cardiac and vascular smooth muscle. J. Physiol. 600 (2), 299–312.
  102. Anumonwo J.M., Lopatin A.N. 2010. Cardiac strong inward rectifier potassium channels. J. Mol. Cell Cardiol. 48 (1), 45–54.
  103. Stoyek M.R., Quinn T.A., Croll R.P., Smith F.M. 2016. Zebrafish heart as a model to study the integrative autonomic control of pacemaker function. Am. J. Physiol. Heart Circ. Physiol. 311 (3), H676–H688.
  104. Tessadori F., van Weerd J.H., Burkhard S.B., Verkerk A.O., de Pater E., Boukens B.J., Vink A., Christoffels V.M., Bakkers J. 2012. Identification and functional characterization of cardiac pacemaker cells in zebrafish. PLoS One. 7 (10), e47644.
  105. Verkerk A.O., Wilders R., van Borren M.M., Peters R.J., Broekhuis E., Lam K., Coronel R., de Bakker J.M., Tan H.L. 2007. Pacemaker current (If) in the human sinoatrial node. Eur. Heart J. 28 (20), 2472–2478.
  106. Han W., Zhang L., Schram G., Nattel S. 2002. Properties of potassium currents in Purkinje cells of failing human hearts. Am. J. Physiol. Heart Circ. Physiol. 283 (6), H2495–H2503.
  107. Hoppe U.C., Beuckelmann D.J. 1998. Characterization of the hyperpolarization-activated inward current in isolated human atrial myocytes. Cardiovasc. Res. 38 (3), 788–801.
  108. Cerbai E., Sartiani L., DePaoli P., Pino R., Maccherini M., Bizzarri F., DiCiolla F., Davoli G., Sani G., Mugelli A. 2001. The properties of the pacemaker current I(F) in human ventricular myocytes are modulated by cardiac disease. J. Mol. Cell Cardiol. 33 (3), 441–448.
  109. Fenske S., Mader R., Scharr A., Paparizos C., Cao-Ehlker X., Michalakis S., Shaltiel L., Weidinger M., Stieber J., Feil S., Feil R., Hofmann F., Wahl-Schott C., Biel M. 2011. HCN3 contributes to the ventricular action potential waveform in the murine heart. Circ. Res. 109 (9), 1015–1023.
  110. Herrmann S., Schnorr S., Ludwig A. 2015. HCN channels–modulators of cardiac and neuronal excitability. Int. J. Mol. Sci. 16 (1), 1429–1447.
  111. Fenske S., Krause S.C., Hassan S.I., Becirovic E., Auer F., Bernard R., Kupatt C., Lange P., Ziegler T., Wotjak C.T., Zhang H., Hammelmann V., Paparizos C., Biel M., Wahl-Schott C.A. 2013. Sick sinus syndrome in HCN1-deficient mice. Circulation. 128 (24), 2585–2594.
  112. Herrmann S., Layh B., Ludwig A. 2011. Novel insights into the distribution of cardiac HCN channels: an expression study in the mouse heart. J. Mol. Cell Cardiol. 51 (6), 997–1006.
  113. Liu J., Kasuya G., Zempo B., Nakajo K. 2022. Two HCN4 channels play functional roles in the zebrafish heart. Front. Physiol. 13, 901571.
  114. van Opbergen C.J.M., van der Voorn S.M., Vos M.A., de Boer T.P., van Veen T.A.B. 2018. Cardiac Ca²⁺ signalling in zebrafish: Translation of findings to man. Prog. Biophys. Mol. Biol. 138, 45–58.
  115. Ottolia M., Torres N., Bridge J.H., Philipson K.D., Goldhaber J.I. 2013. Na/Ca exchange and contraction of the heart. J. Mol. Cell Cardiol. 61, 28–33.
  116. Shigekawa M., Iwamoto T. 2001. Cardiac Na+-Ca²⁺ exchange: Molecular and pharmacological aspects. Circ. Res. 88 (9), 864–876.
  117. Khananshvili D. 2013. The SLC8 gene family of sodium-calcium exchangers (NCX) – structure, function, and regulation in health and disease. Mol. Aspects Med. 34 (2–3), 220–235.
  118. Langenbacher A.D., Dong Y., Shu X., Choi J., Nicoll D.A., Goldhaber J.I., Philipson K.D., Chen J.N. 2005. Mutation in sodium-calcium exchanger 1 (NCX1) causes cardiac fibrillation in zebrafish. Proc. Natl. Acad. Sci. USA. 102 (49), 17699–17704.
  119. Chu L., Yin H., Gao L., Gao L., Xia Y., Zhang C., Chen Y., Liu T., Huang J., Boheler K.R., Zhou Y., Yang H.T. 2021. Cardiac Na+-Ca²⁺ exchanger 1 (ncx1h) is critical for the ventricular cardiomyocyte formation via regulating the expression levels of gata4 and hand2 in zebrafish. Sci. China Life Sci. 64 (2), 255–268.
  120. Zhang P.C., Llach A., Sheng X.Y., Hove-Madsen L., Tibbits G.F. 2011. Calcium handling in zebrafish ventricular myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 (1), R56–R66.
  121. Birkedal R., Shiels H.A. 2007. High [Na+]i in cardiomyocytes from rainbow trout. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2), R861–R866.
  122. Hove-Madsen L., Llach A., Tibbits G.F., Tort L. 2003. Triggering of sarcoplasmic reticulum Ca²⁺ release and contraction by reverse mode Na+/Ca²⁺ exchange in trout atrial myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284 (5), R1330–R1339.
  123. Hove-Madsen L., Llach A., Tort L. 2000. Na+/Ca²⁺-exchange activity regulates contraction and SR Ca²⁺ content in rainbow trout atrial myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (5), R1856–R1864.
  124. Wiedmann F., Frey N., Schmidt C. 2021. Two-pore-domain potassium (K2P-) channels: Cardiac expression patterns and disease-specific remodelling processes. Cells. 10 (11), 2914.
  125. Liang B., Soka M., Christensen A.H., Olesen M.S., Larsen A.P., Knop F.K., Wang F., Nielsen J.B., Andersen M.N., Humphreys D., Mann S.A., Huttner I.G., Vandenberg J.I., Svendsen J.H., Haunsø S., Preiss T., Seebohm G., Olesen S.P., Schmitt N., Fatkin D. 2014. Genetic variation in the two-pore domain potassium channel, TASK-1, may contribute to an atrial substrate for arrhythmogenesis. J. Mol. Cell Cardiol. 67, 69–76.
  126. Christensen A.H., Chatelain F.C., Huttner I.G., Olesen M.S., Soka M., Feliciangeli S., Horvat C., Santiago C.F., Vandenberg J.I., Schmitt N., Olesen S.P., Lesage F., Fatkin D. 2016. The two-pore domain potassium channel, TWIK-1, has a role in the regulation of heart rate and atrial size. J. Mol. Cell Cardiol. 97, 24–35.
  127. Weisbrod D. 2020. Small and intermediate calcium activated potassium channels in the heart: Role and strategies in the treatment of cardiovascular diseases. Front. Physiol. 11, 590534.
  128. Maqoud F., Cetrone M., Mele A., Tricarico D. 2017. Molecular structure and function of big calcium-activated potassium channels in skeletal muscle: Pharmacological perspectives. Physiol. Genomics. 49 (6), 306–317.
  129. Singh H., Stefani E., Toro L. 2012. Intracellular BKCa (iBKCa) channels. J. Physiol. 590 (23), 5937–5947.
  130. Kulawiak B., Szewczyk A. 2022. Current challenges of mitochondrial potassium channel research. Front. Physiol. 13, 907015.
  131. Pineda S., Nikolova-Krstevski V., Leimena C., Atkinson A.J., Altekoester A.K., Cox C.D., Jacoby A., Huttner I.G., Ju Y.K., Soka M., Ohanian M., Trivedi G., Kalvakuri S., Birker K., Johnson R., Molenaar P., Kuchar D., Allen D.G., van Helden D.F., Harvey R.P., Hill A.P., Bodmer R., Vogler G., Dobrzynski H., Ocorr K., Fatkin D. 2021. conserved role of the large conductance calcium-activated potassium channel, KCa1.1, in sinus node function and arrhythmia risk. Circ. Genom. Precis. Med. 14 (2), e003144.
  132. Rohmann K.N., Deitcher D.L., Bass A.H. 2009. Calcium-activated potassium (BK) channels are encoded by duplicate slo1 genes in teleost fishes. Mol. Biol. Evol. 26 (7), 1509–1521.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig.1

Download (201KB)
Indexing metadata
3. Fig.2

Download (152KB)
Indexing metadata
4. Fig.3

Download (181KB)
Indexing metadata
5. Fig.4

Download (157KB)
Indexing metadata

Copyright (c) 2024 The Russian Academy of Sciences

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies