Redox Modulation of L-type Calcium Channels in Ferret Ventricular Myocytes. Dual Mechanism Regulation by Nitric Oxide and S-nitrosothiols

Overview

Journal J Gen Physiol

Specialty Physiology

Date 1996 Oct 1

PMID 8894977

Citations 123

Authors

D L Campbell

J S Stamler

H C Strauss

Affiliations

Soon will be listed here.

Abstract

The effects of NO-related activity and cellular thiol redox state on basal L-type calcium current, ICa,L, in ferret right ventricular myocytes were studied using the patch clamp technique. SIN-1, which generates both NO. and O2-, either inhibited or stimulated ICa,L. In the presence of superoxide dismutase only inhibition was seen. 8-Br-cGMP also inhibited ICa,L, suggesting that the NO inhibition is cGMP-dependent. On the other hand, S-nitrosothiols (RSNOs), which donate NO+, stimulated ICa,L. RSNO effects were not dependent upon cell permeability, modulation of SR Ca2+ release, activation of kinases, inhibition of phosphatases, or alterations in cGMP levels. Similar activation of ICa,L by thiol oxidants, and reversal by thiol reductants, identifies an allosteric thiol-containing "redox switch" on the L-type calcium channel subunit complex by which NO/O2- and NO+ transfer can exert effects opposite to those produced by NO. In sum, our results suggest that: (a) both indirect (cGMP-dependent) and direct (S-nitrosylation/oxidation) regulation of ventricular ICa,L, and (b) sarcolemma thiol redox state may be an important determinant of ICa,L activity.

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References

Qu Y, Campbell D, Strauss H . Modulation of L-type Ca2+ current by extracellular ATP in ferret isolated right ventricular myocytes. J Physiol. 1993; 471:295-317. PMC: 1143963. DOI: 10.1113/jphysiol.1993.sp019902. View

Duhe R, Nielsen M, Dittman A, Villacres E, Choi E, Storm D . Oxidation of critical cysteine residues of type I adenylyl cyclase by o-iodosobenzoate or nitric oxide reversibly inhibits stimulation by calcium and calmodulin. J Biol Chem. 1994; 269(10):7290-6. View

Bolotina V, Najibi S, Palacino J, Pagano P, Cohen R . Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature. 1994; 368(6474):850-3. DOI: 10.1038/368850a0. View

McDONALD T, Pelzer S, TRAUTWEIN W, Pelzer D . Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol Rev. 1994; 74(2):365-507. DOI: 10.1152/physrev.1994.74.2.365. View

Kohr G, Eckardt S, Luddens H, Monyer H, Seeburg P . NMDA receptor channels: subunit-specific potentiation by reducing agents. Neuron. 1994; 12(5):1031-40. DOI: 10.1016/0896-6273(94)90311-5. View

Hofmann F, Biel M, Flockerzi V . Molecular basis for Ca2+ channel diversity. Annu Rev Neurosci. 1994; 17:399-418. DOI: 10.1146/annurev.ne.17.030194.002151. View

Clapham D . Direct G protein activation of ion channels?. Annu Rev Neurosci. 1994; 17:441-64. DOI: 10.1146/annurev.ne.17.030194.002301. View

Isom L, De Jongh K, Catterall W . Auxiliary subunits of voltage-gated ion channels. Neuron. 1994; 12(6):1183-94. DOI: 10.1016/0896-6273(94)90436-7. View

Chiamvimonvat N, ORourke B, Kamp T, Kallen R, Hofmann F, Flockerzi V . Functional consequences of sulfhydryl modification in the pore-forming subunits of cardiovascular Ca2+ and Na+ channels. Circ Res. 1995; 76(3):325-34. DOI: 10.1161/01.res.76.3.325. View

10.

Johnson T . Modulation of channel function by polyamines. Trends Pharmacol Sci. 1996; 17(1):22-7. DOI: 10.1016/0165-6147(96)81566-5. View

11.

Franco-Obregon A, Lopez-Barneo J . Differential oxygen sensitivity of calcium channels in rabbit smooth muscle cells of conduit and resistance pulmonary arteries. J Physiol. 1996; 491 ( Pt 2):511-8. PMC: 1158745. DOI: 10.1113/jphysiol.1996.sp021235. View

12.

Kuryatov A, Laube B, Betz H, Kuhse J . Mutational analysis of the glycine-binding site of the NMDA receptor: structural similarity with bacterial amino acid-binding proteins. Neuron. 1994; 12(6):1291-300. DOI: 10.1016/0896-6273(94)90445-6. View

13.

Imredy J, Yue D . Mechanism of Ca(2+)-sensitive inactivation of L-type Ca2+ channels. Neuron. 1994; 12(6):1301-18. DOI: 10.1016/0896-6273(94)90446-4. View

14.

Omerovic A, Leonard J, Kelso S . Effects of nitroprusside and redox reagents on NMDA receptors expressed in Xenopus oocytes. Brain Res Mol Brain Res. 1994; 22(1-4):89-96. DOI: 10.1016/0169-328x(94)90035-3. View

15.

Pan Z, Bahring R, Grantyn R, Lipton S . Differential modulation by sulfhydryl redox agents and glutathione of GABA- and glycine-evoked currents in rat retinal ganglion cells. J Neurosci. 1995; 15(2):1384-91. PMC: 6577822. View

16.

Campbell D, Strauss H . Regulation of calcium channels in the heart. Adv Second Messenger Phosphoprotein Res. 1995; 30:25-88. DOI: 10.1016/s1040-7952(05)80004-7. View

17.

Arnelle D, Stamler J . NO+, NO, and NO- donation by S-nitrosothiols: implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch Biochem Biophys. 1995; 318(2):279-85. DOI: 10.1006/abbi.1995.1231. View

18.

Discigil B, Pearson P, Chua Y, Evora P, Seccombe J, Schaff H . Novel technique to bioassay endocardium-derived nitric oxide from the beating heart. Ann Thorac Surg. 1995; 59(5):1182-6. DOI: 10.1016/0003-4975(95)00127-7. View

19.

Perez-Garcia M, Kamp T, Marban E . Functional properties of cardiac L-type calcium channels transiently expressed in HEK293 cells. Roles of alpha 1 and beta subunits. J Gen Physiol. 1995; 105(2):289-305. PMC: 2216941. DOI: 10.1085/jgp.105.2.289. View

20.

Balligand J, Kobzik L, Han X, Kaye D, Belhassen L, OHara D . Nitric oxide-dependent parasympathetic signaling is due to activation of constitutive endothelial (type III) nitric oxide synthase in cardiac myocytes. J Biol Chem. 1995; 270(24):14582-6. DOI: 10.1074/jbc.270.24.14582. View