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Ultraviolet Photoalteration of Late Na+ Current in Guinea-pig Ventricular Myocytes

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Abstract

UV irradiation has multiple effects on mammalian cells, including modification of ion channel function. The present study was undertaken to investigate the response of membrane currents in guinea-pig ventricular myocytes to the type A (355, 380 nm) irradiation commonly used in Ca2+ imaging studies. Myocytes configured for whole-cell voltage clamp were generally held at −80 mV, dialyzed with K+-, Na+-free pipette solution, and bathed with K+-free Tyrode’s solution at 22°C. During experiments that lasted for ≈ 35 min, UVA irradiation caused a progressive increase in slowly-inactivating inward current elicited by 200-ms depolarizations from −80 to −40 mV, but had little effect on background current or on L-type Ca2+ current. Trials with depolarized holding potential, Ca2+ channel blockers, and tetrodotoxin (TTX) established that the current induced by irradiation was late (slowly-inactivating) Na+ current (I Na). The amplitude of the late inward current sensitive to 100 μM TTX was increased by 3.5-fold after 20–30 min of irradiation. UVA modulation of late I Na may (i) interfere with imaging studies, and (ii) provide a paradigm for investigation of intracellular factors likely to influence slow inactivation of cardiac I Na.

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References

  • Ahern G.P., Hsu S.F., Klyachko V.A., Jackson M.B. 2000. Induction of persistent sodium current by exogenous and endogenous nitric oxide. J. Biol. Chem. 275:28810–28815

    Article  PubMed  CAS  Google Scholar 

  • Aikawa R., Komuro I., Yamazaki T., Zou Y., Kudoh S., Tanaka M., Shiojima I., Hiroi Y., Yazaki Y. 1997. Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J. Clin. Invest. 100:1813–1821

    Article  PubMed  CAS  Google Scholar 

  • Andrews K.L., McGuire J.J., Triggle C.R. 2003. A photosensitive vascular smooth muscle store of nitric oxide in mouse aorta: no dependence on expression of endothelial nitric oxide synthase. Br. J. Pharmacol. 138:932–940

    Article  PubMed  CAS  Google Scholar 

  • Antoni H., Bocker D., Eickhorn R. 1988. Sodium current kinetics in intact rat papillary muscle: measurements with the loose-patch-clamp technique. J. Physiol. 406:199–213

    PubMed  CAS  Google Scholar 

  • Audiat J., Auger D., Fessard A. 1931. Etude des courants d’action du nerf sournis au rayonnement ultra-violet. Compt. Rend. Soc. Biol. 107:1218–1221

    Google Scholar 

  • Barrington P.L., Martin R.L., Zhang K. 1997. Slowly inactivating sodium currents are reduced by exposure to oxidative stress. J. Mol. Cell. Cardiol. 29:3251–3265

    Article  PubMed  CAS  Google Scholar 

  • Bender K., Blattner C., Knebel A., Iordanov M., Herrlich P., Rahmsdorf H.J. 1997. UV-induced signal transduction. J. Photochem. Photobiol. B 37:1–17

    Article  PubMed  CAS  Google Scholar 

  • Beresewicz A., Horackova M. 1991. Alterations in electrical and contractile behavior of isolated cardiomyocytes by hydrogen peroxide: possible ionic mechanisms. J. Mol. Cell. Cardiol. 23:899–918

    Article  PubMed  CAS  Google Scholar 

  • Booth J.A., von Muralt A., Stämpfli R. 1950. The photochemical action of ultraviolet light on isolated single nerve fibers. Helv. Physiol. Acta. 8:110–127

    CAS  Google Scholar 

  • Chang Y., Xie Y., Weiss D.S. 2001. Positive allosteric modulation by ultraviolet irradiation on GABAA, but not GABAC, receptors expressed in Xenopus oocytes. J. Physiol. 536:471–478

    Article  PubMed  CAS  Google Scholar 

  • Cole W.C., Chartier D., Martin M., Leblanc N. 1997. Ca2+ permeation through Na+ channels in guinea pig ventricular myocytes. Am. J. Physiol. 273:H128–H137

    PubMed  CAS  Google Scholar 

  • Combes A., McTiernan C., Brooks S.S., Feldman A.M. 2001. UV light synergistically enhances the cardiotoxic effects of interleukin 1beta through peroxynitrite formation. J. Card. Fail. 7:165–175

    Article  PubMed  CAS  Google Scholar 

  • Conti F., Cantu A.M., Duclohier H. 1988. Orientation of the tryptophans responsible for the photoinactivation of nerve sodium channels. Eur. Biophys. J. 16:73–81

    Article  PubMed  CAS  Google Scholar 

  • Cormier J.W., Rivolta I., Tateyama M., Yang A.S., Kass R.S. 2002. Secondary structure of the human cardiac Na+ channel C terminus: evidence for a role of helical structures in modulation of channel inactivation. J. Biol. Chem. 277:9233–9241

    Article  PubMed  CAS  Google Scholar 

  • Devary Y., Gottlieb R.A., Smeal T., Karin M. 1992. The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell 71:1081–1091

    Article  PubMed  CAS  Google Scholar 

  • Fox J.M. 1974. Selective blocking of the nodal sodium channels by ultraviolet radiation. I. Phenomenology of the radiation effect. Pfluegers Arch. 351:287–301

    Article  CAS  Google Scholar 

  • Fox J.M., Stämpfli R. 1971. Modification of ionic membrane currents of Ranvier nodes by UV-radiation under voltage clamp conditions. Experientia 27:1289–1290

    Article  PubMed  CAS  Google Scholar 

  • Hilborn M.D., Vaillancourt R.R., Rane S.G. 1998. Growth factor receptor tyrosine kinases acutely regulate neuronal sodium channels through the src signaling pathway. J. Neurosci. 18:590–600

    PubMed  CAS  Google Scholar 

  • Honerjäger P. 1982. Cardioactive substances that prolong the open state of sodium channels. Rev. Physiol. Biochem. Pharmacol. 92:1–74

    PubMed  Google Scholar 

  • Huang C., Li J., Ding M., Leonard S.S., Wang L., Castranova V., Vallyathan V., Shi X. 2001. UV Induces phosphorylation of protein kinase B (Akt) at Ser-473 and Thr-308 in mouse epidermal Cl 41 cells through hydrogen peroxide. J. Biol. Chem. 276:40234–40240

    PubMed  CAS  Google Scholar 

  • Huang L.Y., Yatani A., Brown A.M. 1987. The properties of batrachotoxin-modified cardiac Na channels, including state-dependent block by tetrodotoxin. J. Gen. Physiol. 90:341–360

    Article  PubMed  CAS  Google Scholar 

  • Jones D., Hayon E., Busath D. 1986. Tryptophan photolysis is responsible for gramicidin-channel inactivation by ultraviolet light. Biochim. Biophys. Acta 861:62–66

    PubMed  CAS  Google Scholar 

  • Katiyar S.K. 2001. A single physiologic dose of ultraviolet light exposure to human skin in vivo induces phosphorylation of epidermal growth factor receptor. Int. J. Oncol. 19:459–464

    PubMed  CAS  Google Scholar 

  • Klotz L.O., Briviba K., Sies H. 1997. Singlet oxygen mediates the activation of JNK by UVA radiation in human skin fibroblasts. FEBS Lett. 408:289–291

    Article  PubMed  CAS  Google Scholar 

  • Leszkiewicz D.N., Kandler K., Aizenman E. 2000. Enhancement of NMDA receptor-mediated currents by light in rat neurones in vitro. J. Physiol. 524:365–374

    Article  PubMed  CAS  Google Scholar 

  • Maier S.K., Westenbroek R.E., Schenkman K.A., Feigl E.O., Scheuer T., Catterall W.A. 2002. An unexpected role for brain-type sodium channels in coupling of cell surface depolarization to contraction in the heart. Proc. Natl. Acad. Sci. USA 99:4073–4078

    Article  PubMed  CAS  Google Scholar 

  • Maltsev V.A., Sabbah H.N., Higgins R.S., Silverman N., Lesch M., Undrovinas A.I. 1998. Novel, ultraslow inactivating sodium current in human ventricular cardiomyocytes. Circulation 98:2545–2552

    PubMed  CAS  Google Scholar 

  • 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. 74:365–507

    PubMed  CAS  Google Scholar 

  • Mendez F., Penner R. 1998. Near-visible ultraviolet light induces a novel ubiquitous calcium-permeable cation current in mammalian cell lines. J. Physiol. 507:365–377

    Article  PubMed  CAS  Google Scholar 

  • Middendorf T.R., Aldrich R.W. 2000. Effects of ultraviolet modification on the gating energetics of cyclic nucleotide-gated channels. J. Gen. Physiol. 116:253–282

    Article  PubMed  CAS  Google Scholar 

  • Middendorf T.R., Aldrich R.W., Baylor D.A. 2000. Modification of cyclic nucleotide-gated ion channels by ultraviolet light. J. Gen. Physiol. 116:227–252

    Article  PubMed  CAS  Google Scholar 

  • Morliere P., Moysan A., Santus R., Huppe G., Maziere J.C., Dubertret L. 1991. UVA-induced lipid peroxidation in cultured human fibroblasts. Biochim. Biophys. Acta 1084:261–268

    PubMed  CAS  Google Scholar 

  • Nathan R.D., Pooler J.P., DeHaan R.L. 1976. Ultraviolet-induced alterations of beat rate and electrical properties of embryonic chick heart cell aggregates. J. Gen. Physiol. 67:27–44

    Article  PubMed  CAS  Google Scholar 

  • Nilius B., Boldt W., Benndorf K. 1986. Properties of aconitine-modified sodium channels in single cells of mouse ventricular myocardium. Gen. Physiol. Biophys. 5:473–484

    PubMed  CAS  Google Scholar 

  • Oxford G.S., Pooler J.P. 1975. Ultraviolet photoalteration of ion channels in voltage-clamped lobster giant axons. J. Membrane. Biol. 20:13–30

    Article  CAS  Google Scholar 

  • Pascarel C., Brette F., Le Guennec J.Y. 2001. Enhancement of the T-type calcium current by hyposmotic shock in isolated guinea-pig ventricular myocytes. J. Mol. Cell. Cardiol. 33:1363–1369

    Article  PubMed  CAS  Google Scholar 

  • Qu Y., Rogers J., Tanada T., Scheuer T., Catterall W.A. 1994. Modulation of cardiac Na+ channels expressed in a mammalian cell line and in ventricular myocytes by protein kinase C. Proc. Natl. Acad. Sci. USA 91:3289–3293

    Article  PubMed  CAS  Google Scholar 

  • Ratcliffe C.F., Qu Y., McCormick K.A., Tibbs V.C., Dixon J.E., Scheuer T., Catterall W.A. 2000. A sodium channel signaling complex: modulation by associated receptor protein tyrosine phosphatase beta. Nat. Neurosci. 3:437–444

    Article  PubMed  CAS  Google Scholar 

  • Sakmann B.F., Spindler A.J., Bryant S.M., Linz K.W., Noble D. 2000. Distribution of a persistent sodium current across the ventricular wall in guinea pigs. Circ. Res. 87:910–914

    PubMed  CAS  Google Scholar 

  • Schneider M., Proebstle T., Hombach V., Hannekum A., Rudel R. 1994. Characterization of the sodium currents in isolated human cardiocytes. Pfluegers Arch. 428:84–90

    Article  CAS  Google Scholar 

  • Su Z., Sugishita K., Ritter M., Li F., Spitzer K.W., Barry W.H. 2001. The sodium pump modulates the influence of I Na on [Ca2+]i transients in mouse ventricular myocytes. Biophys. J. 80:1230–1237

    Article  PubMed  CAS  Google Scholar 

  • Tan H.L., Bezzina C.R., Smits J.P., Verkerk A.O., Wilde A.A. 2003. Genetic control of sodium channel function. Cardiovasc. Res. 57:961–973

    Article  PubMed  CAS  Google Scholar 

  • Wang G.K., Wang S.Y. 2002. Modifications of human cardiac sodium channel gating by UVA light. J. Membrane. Biol. 189:153–165

    Article  CAS  Google Scholar 

  • Wang Y., Wagner M.B., Kumar R., Cheng J., Joyner R.W. 2003. Inhibition of fast sodium current in rabbit ventricular myocytes by protein tyrosine kinase inhibitors. Pfluegers Arch. 446:485–491

    Article  CAS  Google Scholar 

  • Ward C.A., Giles W.R. 1997. Ionic mechanism of the effects of hydrogen peroxide in rat ventricular myocytes. J. Physiol. 500:631–642

    PubMed  CAS  Google Scholar 

  • Ward C.A., Moffat M.P. 1995. Role of protein kinase C in mediating effects of hydrogen peroxide in guinea-pig ventricular myocytes. J. Mol. Cell. Cardiol. 27:1089–1097

    Article  PubMed  CAS  Google Scholar 

  • Warmuth I., Harth Y., Matsui M.S., Wang N., DeLeo V.A. 1994. Ultraviolet radiation induces phosphorylation of the epidermal growth factor receptor. Cancer Res. 54:374–376

    PubMed  CAS  Google Scholar 

  • Watson C.L., Gold M.R. 1997. Modulation of Na+ current inactivation by stimulation of protein kinase C in cardiac cells. Circ. Res. 81:380–386

    PubMed  CAS  Google Scholar 

  • Wetlaufer D.B. 1962. Ultraviolet spectra of proteins and amino acids. Adv. Protein Chem. 17:303–390

    Article  CAS  Google Scholar 

  • Wright S.N. 2002. Comparison of aconitine-modified human heart (hH1) and rat skeletal (mu1) muscle Na+ channels: an important role for external Na+ ions. J. Physiol. 538:759–771

    Article  PubMed  CAS  Google Scholar 

  • Zong X.G., Dugas M., Honerjäger P. 1992. Relation between veratridine reaction dynamics and macroscopic Na current in single cardiac cells. J. Gen. Physiol. 99:683–697

    Article  PubMed  CAS  Google Scholar 

  • Zygmunt A.C., Eddlestone G.T., Thomas G.P., Nesterenko V.V., Antzelevitch C. 2001. Larger late sodium conductance in M cells contributes to electrical heterogeneity in canine ventricle. Am. J. Physiol. 281:H689–H697

    CAS  Google Scholar 

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Correspondence to T.F. McDonald.

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La, C., You, Y., Zhabyeyev, P. et al. Ultraviolet Photoalteration of Late Na+ Current in Guinea-pig Ventricular Myocytes. J Membrane Biol 210, 43–50 (2006). https://doi.org/10.1007/s00232-005-0844-6

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  • DOI: https://doi.org/10.1007/s00232-005-0844-6

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