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The Role of Nitric Oxide in the Regulation of Ion Channels in the Cardiomyocytes: Link to Mechanically Gated Channels

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Book cover Mechanically Gated Channels and their Regulation

Part of the book series: Mechanosensitivity in Cells and Tissues ((MECT,volume 6))

Abstract

This review is devoted to the role of nitric oxide in the regulation of ion channels in the cardiomyocytes. Here we consider issues of regulation of mechanically gated channels by means of NO. Firstly we address the modulatory effect of nitric oxide on voltage gated Na+-, Ca2+-, K+-channels, which contribute them most to formation of action potential and its shape under normal as well as under pathological conditions in heart. We address separately effect of nitric oxide on leak channels (two-pore potassium channels), some of which are mechanosensitive. Finally we discuss the effect of nitric oxide on mechanically gated ion channels and mechanically gated currents. In our manuscript we show that without consideration of NO effects on voltage gated channels, investigation of nitric oxide effect on mechanically gated channels in heart under normal of pathological conditions would be incomplete.

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References

  • Abi-Gerges N, Fischmeister R, Méry P (2001) G protein mediated inhibitory effect of a nitric oxide donor on the Ltype Ca2+ current in rat ventricular myocytes. J Physiol 531(1):117–130

    Article  PubMed  CAS  Google Scholar 

  • Abramochkin DV, Makarenko EYu, Mitrokhin VM, Tian Bo, Kalugin LYu, Sutiagin PV, Kamkin A (2012) Effect of nitric oxide on mechanoelectrical feedback. Bull Exp Biol Med 1:39–42 (Russian, English)

    Google Scholar 

  • Ahern GP, Hsu S, Klyachko VA, Jackson MB (2000) Induction of persistent sodium current by exogenous and endogenous nitric oxide. J Biol Chem 275(37):28810–28815

    Article  PubMed  CAS  Google Scholar 

  • Ahmmed GU, Xu Y, Dong PH, Zhang Z, Eiserich J, Chiamvimonvat N (2001) Nitric oxide modulates cardiac Na+ channel via protein kinase A and protein kinase G Circ Res 89:1005–1013

    CAS  Google Scholar 

  • Bai C, Takahashi K, Masumiya H, Sawanobori T, Furukawa T (2004) Nitric oxide-dependent modulation of the delayed rectifier K+ current and the L-type Ca2+ current by ginsenoside Re, an ingredient of Panax ginseng, in guinea-pig cardiomyocytes. Br J Pharm 142:567–575

    Article  CAS  Google Scholar 

  • Bai C, Namekata I, Kurokawa J, Tanaka H, Shigenobu K, Furukawa T (2005) Role of nitric oxide in Ca2+ sensitivity of the slowly activating delayed rectifier K+ current in cardiac myocytes. Circ Res 96:64–72

    Article  PubMed  CAS  Google Scholar 

  • Bang L, Boesgaard S, Nielsen-Kudsk JE, Vejlstrup NG, Aldershvile J (1999) Nitroglycerin-mediated vasorelaxation is modulated by endothelial calcium-activated potassium channels. Cardiovasc Res 43:772–778

    Article  PubMed  CAS  Google Scholar 

  • Campbell DL, Stamler JS, Strauss HC (1996) Redox modulation of L-type calcium channels in ferret ventricular myocytes. J Gen Physiol 108:277–293

    Article  PubMed  CAS  Google Scholar 

  • Chiang C, Luk H, Wang T (2004) Swelling-activated chloride current is activated in guinea pig cardiomyocytes from endotoxic shock. Cardiovasc Res 62:96–104

    Article  PubMed  CAS  Google Scholar 

  • Cuong DV, Kim N, Youm JB, Joo H, Warda M, Lee J, Park WS, Kim T, Kang S, Kim H, Han J (2006) Nitric oxide-cGMP-protein kinase G signaling pathway induces anoxic preconditioning through activation of ATP-sensitive K+ channels in rat hearts. Am J Physiol Heart Circ Physiol 290:H1808–H1817

    Article  PubMed  Google Scholar 

  • Dittrich M, Jureviacius J, Georget M, Rochais F, Fleischmann BK, Hescheler J, Fischmeister R (2001) Local response of L-type Ca2+ current to nitric oxide in frog ventricular myocytes. J Physiol 534(1):109–121

    Article  PubMed  CAS  Google Scholar 

  • Donoso P, Sanchez G, Bull R, Hidalgo C (2011) Modulation of cardiac ryanodine receptor activity by ROS and RNS. Front Biosci 16:553–567

    Article  PubMed  CAS  Google Scholar 

  • Dyachenko V, Christ A, Gubanov R, Isenberg G (2008) Bending of z-lines by mechanical stimuli: an input signal for integrin dependent modulation of ion channels? Prog Biophys Mol Biol 97(2-3):196–216

    Google Scholar 

  • Dyachenko V, Rueckschloss U, Isenberg G (2009) Modulation of cardiac mechanosensitive ion channels involves superoxide, nitric oxide and peroxynitrite. Cell Calcium 45(1):55–64

    Article  PubMed  CAS  Google Scholar 

  • Gallo MP, Ghigo D, Bosia A, Alloatti G, Costamagna C, Penna C, Levi RC (1998) Modulation of guinea-pig cardiac L-type calcium current bynitric oxide synthase inhibitors. J Physiol 506(3):639–651

    Article  PubMed  CAS  Google Scholar 

  • Gallo MP, Malan D, Bedendi I, Biasin C, Alloatti G, Levi RC (2001) Regulation of cardiac calcium current by NO and cGMP-modulating agents. Pflügers Arch—Eur J Physiol 441:621–628

    Article  CAS  Google Scholar 

  • Gómez R, Núňez L, Vaquero M, Amorós I, Barana A, de Prada T, Macaya C, Maroto L, Rodrıguez E, Caballero R, López-Farré A, Tamargo J, Delpón E (2008) Nitric oxide inhibits Kv4.3 and human cardiac transient outward potassium current (Ito1). Cardiovasc Res 80:375–384

    Article  PubMed  Google Scholar 

  • Gómez R, Caballero R, Barana A, Amorós I, Calvo E, López J, Klein H, Vaquero M, Osuna L, Atienza F, Almendral J, Pinto A, Tamargo J, Delpón E (2009) Nitric oxide increases cardiac IK1 by nitrosylation of cysteine 76 of Kir2.1 channels. Circ Res 105:383–392

    Article  PubMed  Google Scholar 

  • Han X, Shimoni Y, Giles WR (1994) An obligatory role for nitric oxide in autonomic control of mammalian heart rate. J Physiol 476(2):309–314

    PubMed  CAS  Google Scholar 

  • Han X, Shimoni Y, Giles WR (1995) A cellular mechanism for nitric oxide-mediated cholinergic control of mammalian heart rate. J Gen Physiol 106:45–65

    Article  PubMed  CAS  Google Scholar 

  • Han X, Kobzik L, Balligand J-L, Kelly RA, Smith TW (1996) Nitric oxide synthase (NOS3)–mediated cholinergic modulation of Ca2+ current in adult rabbit atrioventricular nodal cells. Circ Res 78:998–1008

    Article  PubMed  CAS  Google Scholar 

  • Han J, Kim K, Joo H, Kim E, Earm YE (2002) ATP-sensitive K+ channel activation by nitric oxide and protein kinase G in rabbit ventricular myocytes. Am J Physiol Heart Circ Physiol 283:H1545–H1554

    PubMed  CAS  Google Scholar 

  • Hu H, Chiamvimonvat N, Yamagishi T, Marban E (1997) Direct inhibition of expressed cardiac L-type Ca2+ channels by S-nitrosothiol nitric oxide donors. Circ Res 81:742–752

    Article  PubMed  CAS  Google Scholar 

  • Kamkin A, Kiseleva I, Isenberg G (2000) Stretch-activated currents in ventricular myocytes: amplitude and arrhythmogenic effects increase with hypertrophy. Cardivasc Res 48(3):409–420

    Article  CAS  Google Scholar 

  • Kamkin A, Kiseleva I, Isenberg G (2003) Ion selectivity of stretch-activated cation currents in mouse ventricular myocytes. Pflugers Arch—Europ J Physiol 446(2):220–231

    CAS  Google Scholar 

  • Kazanski VE, Kamkin AG, Makarenko EY, Lysenko NN, Sutiagin PV, Bo T, Kiseleva IS (2010a) Role of nitric oxide in activity control of mechanically gated ionic channels in cardiomyocytes: NO-donor study. Bull Exp Biol Med 150(1):1–5

    Article  CAS  Google Scholar 

  • Kazanski VE, Kamkin AG, Makarenko EY, Lysenko NN, Sutiagin PV, Kiseleva IS (2010b) Role of nitric oxide in the regulation of mechanosesnsitive ionic channels in cardiomyocytes: contribution of NO-synthases. Bull Exp Biol Med 150(2):263–267

    Article  CAS  Google Scholar 

  • Kazanski V, Kamkin A, Makarenko E, Lysenko N, Lapina N, Kiseleva I (2011) The role of nitric oxide in the regulation of mechanically gated channels in the heart. In: Kamkin A, Kiseleva I (eds) Mechanosensitivity in Cells and Tissues 4. Mechanosensitivity and mechanotransduction. Springer, Berlin, pp 109–140

    Google Scholar 

  • Kelly RA, Balligand JL, Smith TW (1996) Nitric oxide and cardiac function. Circ Res 79(3):363–380

    Article  PubMed  CAS  Google Scholar 

  • Kirstein M, Rivet-Bastide M, Hatem S, Benardeau A, Mercadier J, Fischmeister R (1995) Nitric oxide regulates the calcium current in isolated human atrial myocytes. J Clin Invest 95:794–802

    Article  PubMed  CAS  Google Scholar 

  • Kumar R, Namiki T, Joyner RW (1997) Effects of cGMP on L-type calcium current of adult and newborn rabbit ventricular cells. Cardiovasc Res 33:573–582

    Article  PubMed  CAS  Google Scholar 

  • Levi RC, Alloatti G, Penna C, Gallo MP (1994) Guanylate-cyclase-mediated inhibition of cardiac ICa by carbachol and sodium nitroprusside. Pflugers Arch 426(5):419–426

    Article  PubMed  CAS  Google Scholar 

  • Lim G, Venetucci L, Eisner DA, Casadei B (2008) Does nitric oxide modulate cardiac ryanodine receptor function? Implications for excitation–contraction coupling. Cardiovasc Res 77:256–264

    Article  PubMed  CAS  Google Scholar 

  • Ljubkovic M, Shi Y, Cheng Q, Bosnjak Z, Jiang MT (2007) Cardiac mitochondrial ATP-sensitive potassium channel is activated by nitric oxide in vitro. FEBS Lett 581:4255–4259

    Article  PubMed  CAS  Google Scholar 

  • Lu Z, Gao J, Zuckerman J, Mathias RT, Gaudette G, Krukenkamp I, Cohen IS (2007) Two-pore K+ channels, NO and metabolic inhibition. Biochem Biophys Res Commun 363(1):194–196

    Article  PubMed  CAS  Google Scholar 

  • Méry P, Pavoine C, Belhassen L, Pecker F, Fischmeister R (1993) Nitric oxide regulates cardiac Ca2+ current. J Biol Chem 268(35):26286–26295

    PubMed  Google Scholar 

  • Musialek P, Lei M, Brown HF, Paterson DJ, Casadei B (1997) Nitric oxide can increase heart rate by stimulating the hyperpolarization-activated inward current, If. Circ Res 81:60–68

    Article  PubMed  CAS  Google Scholar 

  • Nakayama H, Bodi I, Correll RN, Chen X, Lorenz J, Houser SR, Robbins J, Schwartz A, Molkentin JD (2009) α1G-dependent T-type Ca2+ current antagonizes cardiac hypertrophy through a NOS3-dependent mechanism in mice. J Clin Invest 119:3787–3796

    Article  PubMed  CAS  Google Scholar 

  • Nishimura N, Reien Y, Matsumoto A, Ogura T, Miyata Y, Suzuki K, Nakazato Y, Daida H, Nakaya H (2010) Effects of nicorandil on the cAMP-dependent Cl current in guinea-pig ventricular cells. J Pharmacol Sci 112:415–423

    Article  PubMed  CAS  Google Scholar 

  • Núñez L, Vaquero M, Gómez R, Caballero R, Mateos-Cáceres P, Macaya C, Iriepa I, Gálvez E, López-Farré A, Tamargo J, Delpón E (2006) Nitric oxide blocks hKv1.5 channels by S-nitrosylation and by a cyclic GMP-dependent mechanism. Cardiovasc Res 72:80–89

    Article  PubMed  Google Scholar 

  • Nuss HB, Houser SR (1993) T-type Ca2+ current is expressed in hypertrophied adult feline left ventricular myocytes. Circ Res 73(4):777–782

    Article  PubMed  CAS  Google Scholar 

  • Petroff MG, Kim SH, Pepe S, Dessy C, Marbán E, Balligand JL, Sollott SJ (2001) Endogenous nitric oxide mechanisms mediate the stretch dependence of Ca2+ release in cardiomyocytes. Nat Cell Biol 3(10):867–873

    Article  PubMed  CAS  Google Scholar 

  • Pinsky DJ, Patton S, Mesaros S, Brovkovych V, Kubaszewski E, Grunfeld S, Malinski T (1997) Mechanical transduction of nitric oxide synthesis in the beating heart. Circ Res 81(3):372–379

    Article  PubMed  CAS  Google Scholar 

  • Sasaki N, Sato T, Ohler A, O'Rourke B, Marbán E (2000) Activation of mitochondrial ATP-dependent potassium channels by nitric oxide. Circulation 101:439–445

    Article  PubMed  CAS  Google Scholar 

  • Schröder F, Klein G, Fiedler B, Bastein M, Schnasse N, Hillmer A, Ames S, Gambaryan S, Drexler H, Walter U, Lohmann SM, Wollert KC (2003) Single L-type Ca2+ channel regulation by cGMP-dependent protein kinase type I in adult cardiomyocytes from PKG I transgenic mice. Cardiovasc Res 60:268–277

    Article  PubMed  Google Scholar 

  • Stoyanovsky D, Murphy T, Anno PR, Kim Y, Salama G (1997) Nitric oxide activates skeletal and cardiac ryanodine receptors. Cell Calcium 21(1):19–29

    Article  PubMed  CAS  Google Scholar 

  • Taglialatela M, Pannaccione A, Iossa S, Castaldo P, Annunziato L (1999) Modulation of the K+ channels encoded by the human ethera-gogo-related gene-1 (hERG1) by nitric oxide. Mol Pharm 56:1298–1308

    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  PubMed  CAS  Google Scholar 

  • Tamargo J, Caballero R, Gomez R, Delpon E (2010) Cardiac electrophysiological effects of nitric oxide. Cardiovasc Res 87:593–600

    Article  PubMed  CAS  Google Scholar 

  • Vandecasteele G, Eschenhagen T, Fischmeister R (1998) Role of the NO—cGMP pathway in the muscarinic regulation of the L-type Ca2+ current in human atrial myocytes. J Physiol 506(3):653–663

    Article  PubMed  CAS  Google Scholar 

  • Vulcu SD, Wegener JW, Nawrath H (2000) Differences in the nitric oxidersoluble guanylyl cyclase signaling pathway in the myocardium of neonatal and adult rats. Eur J Pharm 406:247–255

    Article  CAS  Google Scholar 

  • Wahler GM, Dollinger SJ (1995) Nitric oxide donor SIN-l inhibits mammalian cardiac calcium current through cGMP-dependent protein kinase. Am J Physiol 268(37):45–54

    Google Scholar 

  • Wang Y, Wagner MB, Joyner RW, Kumar R (2000) cGMP-dependent protein kinase mediates stimulation of L-type calcium current by cGMP in rabbit atrial cells. Cardiovasc Res 48:310–322

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Yin C, Xi L, Kukreja RC (2004) Opening of Ca2+-activated K+ channels triggers early and delayed preconditioning against I/R injury independent of NOS in mice. Am J Physiol Heart Circ Physiol 287:H2070–H2077

    Article  PubMed  CAS  Google Scholar 

  • Wang G, Strang C, Pfaffinger PJ, Covarrubias M (2007) Zn2+-dependent Redox Switch in the Intracellular T1-T1 Interface of a Kv Channel. J Biol Chem 282(18):13637–13647

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Viatchenko-Karpinski S, Sun J, Györke I, Benkusky NA, Kohr MJ, Valdivia HH, Murphy E, Györke S, Ziolo MT (2010) Regulation of myocyte contraction via neuronal nitric oxide synthase: role of ryanodine receptor S-nitrosylation. J Physiol 588(15):2905–2917

    Article  PubMed  CAS  Google Scholar 

  • Yoo S, Lee SH, Choi BH, Yeom JB, Ho WK, Earm YE (1998) Dual effect of nitric oxide on the hyperpolarization-activated inward current (If) in sino-atrial node cells of the rabbit. J Mol Cell Cardiol 30:2729–2738

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Russian Foundation for Basic Research (grant no. 09-04-01277-a). Department of Fundamental and Applied Physiology (Professor and Chairman—Andre Kamkin) was supported by Ministry of Education and Science of the Russian Federation. The Order of Ministry of Education and Science of the Russian Federation No. 743 from 01 July 2010, Supplement, Event 4.4, the Period of Financing 2010–2019.

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Correspondence to Andre Kamkin .

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Makarenko, E.Y., Lozinsky, I., Kamkin, A. (2012). The Role of Nitric Oxide in the Regulation of Ion Channels in the Cardiomyocytes: Link to Mechanically Gated Channels. In: Kamkin, A., Lozinsky, I. (eds) Mechanically Gated Channels and their Regulation. Mechanosensitivity in Cells and Tissues, vol 6. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5073-9_8

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