Abstract
Modulation of voltage-dependent sodium and potassium currents by charged amphiphiles was investigated in cardiac ventricular myocytes using the patch-clamp technique. Negatively charged sodium dodecylsulfate (SDS) increased amplitude of INa, whereas positively charged dodecyltrimethylammonium (DDTMA) decreased INa. Furthermore, SDS shifted the steady-state activation and inactivation of INa in the negative direction, whereas DDTMA shifted the curves in the opposite direction. These shifts provided an explanation for the changes in current amplitude. Activation and inactivation kinetics of INa were accelerated by SDS but slowed by DDTMA. These changes in both steady- state gating and kinetics of INa are consistent with a decrease of the intramembrane field by SDS and an increase of the field by DDTMA due to an alteration of surface potential after their insertion into the outer monolayer of the sarcolemma. The effect of SDS on the steady-state inactivation of INa was concentration dependent and partially reversed by screening surface charges with increased extracellular [Ca2+]. These amphiphiles also altered the activation of the delayed rectifier K+ current (IK,del), producing a shift in the negative direction by SDS but in the positive direction by DDTMA. These results suggest that the insertion of charged amphiphiles into the cell membrane alters the behavior of voltage-dependent INa and IK,del by changing the surface charge density, and consequently the surface potential and implies, although indirectly, that the lipid surface charges are important to the voltage-dependent gating of these channels.
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- Armstrong C. M., Bezanilla F. Inactivation of the sodium channel. II. Gating current experiments. J Gen Physiol. 1977 Nov;70(5):567–590. doi: 10.1085/jgp.70.5.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M., Cota G. Modification of sodium channel gating by lanthanum. Some effects that cannot be explained by surface charge theory. J Gen Physiol. 1990 Dec;96(6):1129–1140. doi: 10.1085/jgp.96.6.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M., Matteson D. R. The role of calcium ions in the closing of K channels. J Gen Physiol. 1986 May;87(5):817–832. doi: 10.1085/jgp.87.5.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M. Sodium channels and gating currents. Physiol Rev. 1981 Jul;61(3):644–683. doi: 10.1152/physrev.1981.61.3.644. [DOI] [PubMed] [Google Scholar]
- Balser J. R., Bennett P. B., Roden D. M. Time-dependent outward current in guinea pig ventricular myocytes. Gating kinetics of the delayed rectifier. J Gen Physiol. 1990 Oct;96(4):835–863. doi: 10.1085/jgp.96.4.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barchi R. L. Probing the molecular structure of the voltage-dependent sodium channel. Annu Rev Neurosci. 1988;11:455–495. doi: 10.1146/annurev.ne.11.030188.002323. [DOI] [PubMed] [Google Scholar]
- Burt J. M., Langer G. A. Ca2+ displacement by Polymyxin B from sarcolemma isolated by 'gas dissection' from cultured neonatal rat myocardial cells. Biochim Biophys Acta. 1983 Mar 23;729(1):44–52. doi: 10.1016/0005-2736(83)90454-6. [DOI] [PubMed] [Google Scholar]
- Cahalan M. D., Pappone P. A. Chemical modification of sodium channel surface charges in frog skeletal muscle by trinitrobenzene sulphonic acid. J Physiol. 1981 Dec;321:127–139. doi: 10.1113/jphysiol.1981.sp013975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Campbell D. T., Hahin R. Altered sodium and gating current kinetics in frog skeletal muscle caused by low external pH. J Gen Physiol. 1984 Nov;84(5):771–788. doi: 10.1085/jgp.84.5.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Catterall W. A. Structure and function of voltage-sensitive ion channels. Science. 1988 Oct 7;242(4875):50–61. doi: 10.1126/science.2459775. [DOI] [PubMed] [Google Scholar]
- Cevc G. Membrane electrostatics. Biochim Biophys Acta. 1990 Oct 8;1031(3):311–382. doi: 10.1016/0304-4157(90)90015-5. [DOI] [PubMed] [Google Scholar]
- Cota G., Armstrong C. M. Sodium channel gating in clonal pituitary cells. The inactivation step is not voltage dependent. J Gen Physiol. 1989 Aug;94(2):213–232. doi: 10.1085/jgp.94.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cukierman S., Zinkand W. C., French R. J., Krueger B. K. Effects of membrane surface charge and calcium on the gating of rat brain sodium channels in planar bilayers. J Gen Physiol. 1988 Oct;92(4):431–447. doi: 10.1085/jgp.92.4.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Giles W., Nakajima T., Ono K., Shibata E. F. Modulation of the delayed rectifier K+ current by isoprenaline in bull-frog atrial myocytes. J Physiol. 1989 Aug;415:233–249. doi: 10.1113/jphysiol.1989.sp017720. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilly W. F., Armstrong C. M. Slowing of sodium channel opening kinetics in squid axon by extracellular zinc. J Gen Physiol. 1982 Jun;79(6):935–964. doi: 10.1085/jgp.79.6.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green W. N., Andersen O. S. Surface charges and ion channel function. Annu Rev Physiol. 1991;53:341–359. doi: 10.1146/annurev.ph.53.030191.002013. [DOI] [PubMed] [Google Scholar]
- Green W. N., Weiss L. B., Andersen O. S. Batrachotoxin-modified sodium channels in planar lipid bilayers. Ion permeation and block. J Gen Physiol. 1987 Jun;89(6):841–872. doi: 10.1085/jgp.89.6.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hahin R., Campbell D. T. Simple shifts in the voltage dependence of sodium channel gating caused by divalent cations. J Gen Physiol. 1983 Dec;82(6):785–805. doi: 10.1085/jgp.82.6.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Helenius A., McCaslin D. R., Fries E., Tanford C. Properties of detergents. Methods Enzymol. 1979;56:734–749. doi: 10.1016/0076-6879(79)56066-2. [DOI] [PubMed] [Google Scholar]
- Hille B., Woodhull A. M., Shapiro B. I. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):301–318. doi: 10.1098/rstb.1975.0011. [DOI] [PubMed] [Google Scholar]
- Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi: 10.1146/annurev.bi.54.070185.003215. [DOI] [PubMed] [Google Scholar]
- Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
- Langer G. A., Rich T. L. Augmentation of sarcolemmal Ca by anionic amphiphile: contractile response of three ventricular tissues. Am J Physiol. 1986 Feb;250(2 Pt 2):H247–H254. doi: 10.1152/ajpheart.1986.250.2.H247. [DOI] [PubMed] [Google Scholar]
- Levinson S. R., Thornhill W. B., Duch D. S., Recio-Pinto E., Urban B. W. The role of nonprotein domains in the function and synthesis of voltage-gated sodium channels. Ion Channels. 1990;2:33–64. doi: 10.1007/978-1-4615-7305-0_2. [DOI] [PubMed] [Google Scholar]
- Matsuura H., Ehara T., Imoto Y. An analysis of the delayed outward current in single ventricular cells of the guinea-pig. Pflugers Arch. 1987 Dec;410(6):596–603. doi: 10.1007/BF00581319. [DOI] [PubMed] [Google Scholar]
- McLaughlin S. G., Szabo G., Eisenman G. Divalent ions and the surface potential of charged phospholipid membranes. J Gen Physiol. 1971 Dec;58(6):667–687. doi: 10.1085/jgp.58.6.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mitra R., Morad M. A uniform enzymatic method for dissociation of myocytes from hearts and stomachs of vertebrates. Am J Physiol. 1985 Nov;249(5 Pt 2):H1056–H1060. doi: 10.1152/ajpheart.1985.249.5.H1056. [DOI] [PubMed] [Google Scholar]
- Perozo E., Bezanilla F., Dipolo R. Modulation of K channels in dialyzed squid axons. ATP-mediated phosphorylation. J Gen Physiol. 1989 Jun;93(6):1195–1218. doi: 10.1085/jgp.93.6.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Philipson K. D., Langer G. A., Rich T. L. Charged amphiphiles regulate heart contractility and sarcolemma-Ca2+ interactions. Am J Physiol. 1985 Jan;248(1 Pt 2):H147–H150. doi: 10.1152/ajpheart.1985.248.1.H147. [DOI] [PubMed] [Google Scholar]
- Post J. A., Ji S., Leonards K. S., Langer G. A. Effects of charged amphiphiles on cardiac cell contractility are mediated via effects on Ca2+ current. Am J Physiol. 1991 Mar;260(3 Pt 2):H759–H769. doi: 10.1152/ajpheart.1991.260.3.H759. [DOI] [PubMed] [Google Scholar]
- Sammar M., Spira G., Meiri H. Depolarization exposes the voltage sensor of the sodium channels to the extracellular region. J Membr Biol. 1992 Jan;125(1):1–11. doi: 10.1007/BF00235793. [DOI] [PubMed] [Google Scholar]
- Sanguinetti M. C., Jurkiewicz N. K. Lanthanum blocks a specific component of IK and screens membrane surface change in cardiac cells. Am J Physiol. 1990 Dec;259(6 Pt 2):H1881–H1889. doi: 10.1152/ajpheart.1990.259.6.H1881. [DOI] [PubMed] [Google Scholar]
- Stühmer W., Conti F., Suzuki H., Wang X. D., Noda M., Yahagi N., Kubo H., Numa S. Structural parts involved in activation and inactivation of the sodium channel. Nature. 1989 Jun 22;339(6226):597–603. doi: 10.1038/339597a0. [DOI] [PubMed] [Google Scholar]
- Yamamoto D., Yeh J. Z., Narahashi T. Interactions of permeant cations with sodium channels of squid axon membranes. Biophys J. 1985 Sep;48(3):361–368. doi: 10.1016/S0006-3495(85)83792-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto D., Yeh J. Z., Narahashi T. Voltage-dependent calcium block of normal and tetramethrin-modified single sodium channels. Biophys J. 1984 Jan;45(1):337–344. doi: 10.1016/S0006-3495(84)84159-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yee H. F., Jr, Weiss J. N., Langer G. A. Neuraminidase selectively enhances transient Ca2+ current in cardiac myocytes. Am J Physiol. 1989 Jun;256(6 Pt 1):C1267–C1272. doi: 10.1152/ajpcell.1989.256.6.C1267. [DOI] [PubMed] [Google Scholar]
- Zhang J. F., Siegelbaum S. A. Effects of external protons on single cardiac sodium channels from guinea pig ventricular myocytes. J Gen Physiol. 1991 Dec;98(6):1065–1083. doi: 10.1085/jgp.98.6.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]