Redox Modulation of Basal and Beta-adrenergically Stimulated Cardiac L-type Ca(2+) Channel Activity by Phenylarsine Oxide

Overview

Journal Br J Pharmacol

Publisher Wiley

Specialty Pharmacology

Date 2004 Jun 3

PMID 15172960

Citations 10

Authors

Carl Sims

Robert D Harvey

Affiliations

Soon will be listed here.

Abstract

1. Phenylarsine oxide (PAO) is commonly used to inhibit tyrosine phosphatase activity. However, PAO can affect a variety of different processes because of its ability to promote sulfhydryl oxidation. In the present study, we investigated the effects that PAO has on basal and beta-adrenergically stimulated L-type Ca(2+) channel activity in isolated cardiac myocytes. 2. Extracellular application of PAO transiently stimulated the basal L-type Ca(2+) channel activity, whereas it irreversibly inhibited protein kinase A (PKA)-dependent regulation of channel activity by isoproterenol, forskolin and 8-CPT-cAMP (8-p-chlorophenylthioadenosine 3',5'-cyclic monophosphate). PAO also inhibited channel activity irreversibly stimulated in the presence of adenosine 5'-(3-thiotriphosphate) tetralithium salt. 3. Neither the stimulatory nor the inhibitory effects of PAO were affected by the tyrosine kinase inhibitor lavendustin A, suggesting that tyrosine phosphorylation is not involved. 4. Extracellular application of the sulfhydryl-reducing agent dithiothreitol (DTT) antagonized both the stimulatory and inhibitory effects of PAO. Yet, following intracellular dialysis with DTT, only the inhibitory effect of PAO was antagonized. 5. The inhibitory effect of PAO was mimicked by intracellular, but not extracellular application of the membrane impermeant thiol oxidant 5,5'-dithio-bis(2-nitrobenzoic acid). 6. These results suggest that the stimulatory effect of PAO results from oxidation of sulfhydryl residues at an extracellular site and the inhibitory effect is due to redox regulation of an intracellular site that affects the response of the channel to PKA-dependent phosphorylation. It is concluded that the redox state of the cell may play a critical role in modulating beta-adrenergic responsiveness of the L-type Ca(2+) channel in cardiac myocytes.

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References

Knutson V, Ronnett G, Lane M . Rapid, reversible internalization of cell surface insulin receptors. Correlation with insulin-induced down-regulation. J Biol Chem. 1983; 258(20):12139-42. View

Hamill O, Marty A, Neher E, Sakmann B, Sigworth F . Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981; 391(2):85-100. DOI: 10.1007/BF00656997. View

Belles B, Malecot C, Hescheler J, TRAUTWEIN W . "Run-down" of the Ca current during long whole-cell recordings in guinea pig heart cells: role of phosphorylation and intracellular calcium. Pflugers Arch. 1988; 411(4):353-60. DOI: 10.1007/BF00587713. View

Hartzell H . Regulation of cardiac ion channels by catecholamines, acetylcholine and second messenger systems. Prog Biophys Mol Biol. 1988; 52(3):165-247. DOI: 10.1016/0079-6107(88)90014-4. View

Onoda T, Iinuma H, Sasaki Y, Hamada M, Isshiki K, Naganawa H . Isolation of a novel tyrosine kinase inhibitor, lavendustin A, from Streptomyces griseolavendus. J Nat Prod. 1989; 52(6):1252-7. DOI: 10.1021/np50066a009. View

Garcia-Morales P, Minami Y, Luong E, Klausner R, Samelson L . Tyrosine phosphorylation in T cells is regulated by phosphatase activity: studies with phenylarsine oxide. Proc Natl Acad Sci U S A. 1990; 87(23):9255-9. PMC: 55143. DOI: 10.1073/pnas.87.23.9255. View

Nakajima T, Irisawa H, Giles W . N-ethylmaleimide uncouples muscarinic receptors from acetylcholine-sensitive potassium channels in bullfrog atrium. J Gen Physiol. 1990; 96(4):887-903. PMC: 2229007. DOI: 10.1085/jgp.96.4.887. View

Yang J, Clark A, Kozka I, Cushman S, Holman G . Development of an intracellular pool of glucose transporters in 3T3-L1 cells. J Biol Chem. 1992; 267(15):10393-9. View

Hecht D, Zick Y . Selective inhibition of protein tyrosine phosphatase activities by H2O2 and vanadate in vitro. Biochem Biophys Res Commun. 1992; 188(2):773-9. DOI: 10.1016/0006-291x(92)91123-8. View

10.

Schaefer T, Wiedemann C, Gitler C, Burger M . Effects of arsenicals on the secretory process in chromaffin cells. Ann N Y Acad Sci. 1994; 710:356-67. DOI: 10.1111/j.1749-6632.1994.tb26642.x. View

11.

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

12.

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

13.

Sullivan J, Traynelis S, Chen H, Escobar W, Heinemann S, Lipton S . Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron. 1994; 13(4):929-36. DOI: 10.1016/0896-6273(94)90258-5. View

14.

Le Cabec V . Complete and reversible inhibition of NADPH oxidase in human neutrophils by phenylarsine oxide at a step distal to membrane translocation of the enzyme subunits. J Biol Chem. 1995; 270(5):2067-73. DOI: 10.1074/jbc.270.5.2067. View

15.

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

16.

Omerovic A, Chen S, Leonard J, Kelso S . Subunit-specific redox modulation of NMDA receptors expressed in Xenopus oocytes. J Recept Signal Transduct Res. 1995; 15(6):811-27. DOI: 10.3109/10799899509049859. View

17.

Pafford C, Simples Jr J, Strong J . Effects of the protein tyrosine phosphatase inhibitor phenylarsine oxide on excision-activated calcium channels in Lymnaea neurons. Cell Calcium. 1995; 18(5):400-10. DOI: 10.1016/0143-4160(95)90055-1. View

18.

Lacampagne A, Duittoz A, Bolanos P, Peineau N, Argibay J . Effect of sulfhydryl oxidation on ionic and gating currents associated with L-type calcium channels in isolated guinea-pig ventricular myocytes. Cardiovasc Res. 1995; 30(5):799-806. View

19.

Shaver A, Ng J, Hall D, Posner B . The chemistry of peroxovanadium compounds relevant to insulin mimesis. Mol Cell Biochem. 1995; 153(1-2):5-15. DOI: 10.1007/BF01075913. View

20.

Campbell D, Stamler J, Strauss H . Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J Gen Physiol. 1996; 108(4):277-93. PMC: 2229328. DOI: 10.1085/jgp.108.4.277. View