Redox modulation of L-type calcium channels in ferret ventricular myocytes: Dual mechanism regulation by nitric oxide and S-nitrosothiols

Journal of General Physiology

Volumn 108, Issue 4, 1996, Pages 277-293

  Campbell, Donald L ^a   Stamler, Jonathan S ^a   Strauss, Harold C ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

calcium homeostasis; cardiac electrophysiology; ionic channels; N oxides; S nitrosylation

Indexed keywords

CALCIUM CHANNEL; NITRIC OXIDE;

ANIMAL CELL; ARTICLE; CALCIUM HOMEOSTASIS; CHANNEL GATING; FERRET; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CELL; HEART VENTRICLE; NONHUMAN; OXIDATION REDUCTION REACTION;

EID: 0029743817     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.108.4.277     Document Type: Article

References (99)

1. Aizenman, E., S.A. Lipton, and R.H. Loring. 1989. Selective modulation of NMDA responses by reduction and oxidation. Neuron. 2: 1257-1263.
2. +, and NO donation by S-nitrosothiols: implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch. Biochem. Biophys. 318:279-285.
3. 2+ is buffered. Circ. Res. 68:897-902.
4. Balligand, J.L., L. Kobzik, X. Han, D.M. Kaye, L. Belhassen, D.S. O'Hara, R.A. Kelly, T.W. Smith, and T. Michel. 1995. Nitric-oxide parasympathetic signalling is due to activation of constitutive endothelial (type III) nitric oxide synthase in cardiac myocytes. J. Biol. Chem. 270:14582-14586.
5. Balligand, J.L., D. Ungureanu-Longrois, W.W. Simmons, D. Pimental, T.A. Milinski, M. Kapturczak, Z. Taha, C.J. Lowenstein, A.J. Davidoff, R.A. Kelly, et al. 1994. Cytokine-inducible nitric oxide synthase (iNOS) expression in cardiac myocytes. J. Biol. Chem. 269:27:580-588.
6. Bers, D.M. 1991. Excitation-Contraction Coupling and Cardiac Contractile Force. Kluwer Academic Publishers, Dordrecht, The Netherlands. 258 pp.
7. Bolotina, V.M., S. Najibi, J.J. Palacino, P.J. Pagano, and R.A. Cohen. 1994. Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature (Lond). 368: 850-853.
8. Brady, A.J.B., P.A. Poole-Wilson, S.E. Harding, and J.B. Warren. 1992. Nitric oxide production within cardiac myocytes reduces their contractility in endotoxemia. Am. J Physiol. 263:H1963-H1966.
9. Brady, A.J.B., J.B. Warren, P.A. Poole-Wilson, T.J. Williams, and S.E. Harding. 1993. Nitric oxide attenuates cardiac myocyte contraction. Am. J. Physiol. 265:H176-H182.
10. Brown, A.M. 1993. Membrane-delimited cell signalling complexes: direct ion channel regulation by G proteins. J. Membr. Biol. 131: 93-104.
11. Campbell, D.L., R.L. Rasmusson, Y. Qu, and H.C. Strauss. 1993. The calcium-independent transient outward potassium current in isolated ferret right ventricular myocytes. I. Basic characterization and kinetic analysis. J. Gen. Physiol. 101:571-601.
12. Campbell, D.L., and H.C. Strauss. 1995. Regulation of calcium channels in the heart. In Advances in Second Messenger and Phosphoprotein Research 30. Calcium Regulation of Cellular Function. A. R. Means, editor. Raven Press, Ltd., New York. 25-88.
13. + channels. Circ. Res. 76:325-344.
14. Clapham, D.E. 1994. Direct G protein activation of ion channels? Annu. Rev. Neurosci. 17:441-446.
15. Consentino, F., J.C. Sill, and Z.S. Katusic. 1994. Role of superoxide anions in the mediation of endothelium-dependent contractions. Hypertension (Dallas). 23:229-235.
16. Dinerman, J.L., C.J. Lowenstein, and S.H. Snyder. 1993. Molecular mechanisms of nitric oxide regulation: potential relevance to cardiovascular disease. Circ. Res. 73:217-222.
17. Disrioil, R., P.J. Pearson, Y.L. Chua, P.R. Evora, J.F. Seccombe, and H.V. Schaff. 1995. Novel technique to bioassay endocardium-derived nitric oxide from the beating heart. Ann. Thorac. Surg. 59:1182-1186.
18. Duhe, R.J., M.D. Nielsen, A.H. Dittman, E.C. Villacres, E.J. Choi, and J.R. Storm. 1994. 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. 269:7290-7296.
19. Feelisch, M. 1991. The biochemical pathways of nitric oxide formation from nitrovasodilators: appropriate choice of exogenous NO donors and aspects of preparation and handling of aqueous NO solutions. J. Cardiovasc. Pharmacol. 17 (Suppl. 3):S25-S33.
20. Feelisch, M., and J.S. Stamler. 1996. Donors of nitrogen oxides: In Methods in Nitric Oxide Research. M. Feelisch and J.S. Stamler, editors. John Wiley and Sons, Ltd. 69-114.
21. Finkel, M.S., C.V. Oddis, T.D. Jacob, S.C. Watkins, B.G. Hattler, and R.L. Simmons. 1992. Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science (Wash. DC). 257: 387-389.
22. 2+ current in frog ventricular myocytes. J. Physiol. (Lond). 417:231-239.
23. Franco-Obregón, A., and J. López-Barneo. 1996. Differential oxygen sensitivity of calcium channels in rabbit smooth muscle cells of conduit and resistance pulmonary arteries. J. Physiol. (Lond.). 491.2:511-518.
24. Gopalakrishna, R., Z.H. Chen, and U. Gundimeda. 1993. Nitric oxide and nitric oxide-generating agents induce a reversible inactivation of protein kinase C activity and phorbol ester binding. J. Biol. Chem. 268:27180-27185.
25. Gozlan, H., and Y. Ben-Ari. 1995. NMDA receptor redox sites: are they targets for selective neuronal protection? Trends. Pharmacol. Sci. 16:368-374.
26. Hamill, O.P., A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archiv. 391:85-100.
27. Han, X., Y. Shimoni, and W.R. Giles. 1994. An obligatory role for nitric oxide in autonomic control of mammalian heart rate. J. Physiol. 476.2:309-314.
28. Han, X., Y. Shimoni, and W.R. Giles. 1995. A cellular mechanism for nitric oxide-mediated cholinergic control of mammalian heart rate. J. Gen. Physiol. 106:45-65.
29. Hare, J.M., J.F. Keaney, J.L. Balligand, J. Loscalzo, T.W. Smith, and W.S. Colluci. 1995. Role of nitric oxide in parasympathetic modulation of β-adrenergic myocardial contractility in normal dogs. J. Clin. Invest. 95:360-366.
30. Hartzell, H.C. 1988. Regulation of cardiac ion channels by catecholamines, acetylcholine and second messenger systems. Prog. Biophys. Mol. Biol. 52:165-247.
31. Hartzell, H.C., Y. Hirayama, and J. Petit-Jacques. 1995. Effects of protein phosphatase and kinase inhibitors on the cardiac L-type Ca current suggest two sites are phosphorylated by protein kinase A and another protein kinase. J. Gen. Physiol. 106:393-414.
32. Haywood, G., P.S. Tsao, H.E. von der Leyen, M.J. Mann, P.J. Keeling, P.T. Trindale, N.P. Lewis, C.D. Byrne P.R. Rickenbacher, N.H. Bishopric, et al. 1996. Expression of inducible nitric oxide synthase in human heart failure. Circulation. 93:1087-1094.
33. 2+ channels revealed by discrete-time Markov analysis of slow gating. Biophys. J. 65:1599-1612.
34. 2+ channel diversity. Annu. Rev. Neurosci. 17:399-418.
35. Horn, R., and A. Marty. 1988. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J. Gen. Physiol. 94:145-159.
36. Ignarro, L.J. 1990. Nitric oxide: a novel signal transduction mechanism for transcellular communication. Hypertension (Dallas). 16: 477-483.
37. 2+ channels. Neuron. 12:1301-1318.
38. Isom, L.L., K.S. De Jongh, and W.A. Catterall. 1994. Auxiliary subunits of voltage-gated ion channels. Neuron. 12:1183-1194.
39. 2-subunit and the associated δ peptides. J. Biol. Chem. 266:3287-3293.
40. Johnson, T.D. 1996. Modulation of channel function by polyamines. Trends Pharmacol. Sci. 17:22-27.
41. Kanai, A.J., S. Mesaros, M.S. Finkel, C.V. Oddis, H.C. Strauss, and T. Malinski. 1995. Nitric oxide release measured directly with a porphyrinic microsensor reveals adrenergic control of constitutive nitric oxide synthase in cardiac myocytes. Circulation. 92:1-563.
42. Klimaschewski, L., W. Kummer, B. Mayer, J.Y. Couraud, U. Preissler, B. Philipin, and C. Heym. 1992. Nitric oxide synthase in cardiac nerve fibers and neurons of rat and guinea pig heart. Circ. Res. 71:1533-1537.
43. Köhr, G., S. Eckardt, H. Lüddens, H. Monyer, and P.H. Seeburg. 1994. NMDA receptor channels: subunit specific potentiation by reducing agents. Neuron. 12:1031-1040.
44. Kuryatov, A., B. Laube, H. Betz, and J. Kuhse. 1994. Mutational analysis of the glycine binding site of the NMDA receptor: Structural similiarity with bacterial amino acid-binding proteins. Neuron. 12:1291-1300.
45. Lander, H.M., P.K. Sehajpal, and A. Novogrodsyk. 1993. Nitric oxide signalling: a possible role for G proteins. Immunology. 151: 7182-7187.
46. Lei, S.Z., Z.-H. Pan, S.K. Aggarwal, H.-S.V. Chen, and S.A. Lipton. 1992. Effectt of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron. 8:1087-1099.
47. Levi, R., G. Alloatti, and R. Fischmeister. 1989. Cyclic GMP regulates the Ca-channel current in guinea pig ventricular myocytes. Pflügers Archiv. 413:685-687.
48. Ga by carbachol and sodium nitroprusside. Pflügers Archiv. 426:419-426.
49. Lincoln, T.M. 1994. Cyclic GMP: Biochemistry, Physiology, and Pathophysiology. R.G. Landes, Austin, TX. 173 pp.
50. Lipton, S.A., Y.-B. Choi, Z.H. Pan, S.Z. Lei, H.-S.V. Chen, N.J. Sucher, J. Loscalzo, D.J. Singel, and J.S. Stamler. 1993. A redox-based mechanism for the neuroprotective and neurostructive effects of nitric oxide and related nitroso-compounds. Nature (Lond.). 364:626-632.
51. Lipton, S.A., Y.-B. Choi, N.J. Sucher, Z.-H. Pan, and J.S. Stamler. 1996. Redox state, NMDA receptors and NO-related species. Trends Pharmacol. Sci. 17:186-187.
52. Marletta, M.A., M.A. Tayeh, and J.M. Hevel. 1990. Unraveling the biological significance of nitric oxide. Biofactors. 2:219-225.
53. Marty, A., and E. Neher. 1995. Tight-seal whole-cell recording. In Single Channel Recording, Second Ed. B. Sakmann and E. Neher, editors. Plenum Press, New York. 31-52.
54. McDonald, T.F., P. Pelzer, W. Trautwein, and D.J. Pelzer. 1994. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol. Rev. 74:365-507.
55. Meissner, G. 1995. Sarcoplasmic reticulum ion channels. In Cardiac Electrophysiology: From Cell to Bedside. D.P. Zipes and J. Jalife, editors. W.B. Saunders Company, Philadelphia. 49-56.
56. 2+ current is regulated by cyclic GMP-dependent protein kinase in mammalian cardiac myocytes. Proc. Natl. Acad. Sci. USA. 88:1197-1201.
57. 2+ current: involvement of cGMP-inhibited and cGMP-stimulated phosphodiesterases through guanylyl cylcase activation. J. Biol. Chem. 268:26286-26295.
58. Michel, T., and T.W. Smith. 1993. Nitric oxide synthases and cardiovascular signalling. Am. J. Cardiol. 72:33C-38C.
59. 2+ -currents while suppressing contraction in rat ventricular muscle cells. Br. J. Pharmacol. 81:13-15.
60. Mohan, P., D.L. Brutsaert, W.J. Paulus, and S.U. Sys. 1996. Myocardial contractile response to nitric oxide and cGMP. Circulation. 93:1223-1229.
61. Moncada, S., R.M.J. Palmer, and E.A. Higgs. 1991. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol. Rev. 433:109-142.
62. Mori, Y. 1994. Molecular biology of voltage-dependent calcium channels. In Handbook of Membrane Channels. Molecular and Cellular Physiology. C. Peracchia, editor. Academic Press, San Diego, CA. 163-176.
63. Mubagwa, K., T. Shirayama, M. Moreau, and A.J. Pappano. 1993. Effects of PDE inhibitors and carbachol on the L-type Ca current in guinea pig ventricular myocytes. Am. J. Physiol. 265:H1353-H1363.
64. Neumann, J., K. Boknik, S. Herzig, W. Schmitz, H. Scholz, R.C. Gupta, and A.M. Watanabe. 1993. Evidence for physiological functions of protein phosphatases in the heart: evaluation with okadaic acid. Am. J. Physiol. 265:H257-H266.
65. Omerovic, A., S.-J. Chen, J.P. Leonard, and S.R. Kelso. 1995. Subunit-specific redox modulation of NMDA receptors expressed in Xenopus oocytes. J. Recept. Signal Transduct. Res. 15:811-827.
66. Omerovic, A., J.P. Leonard, and S.R.T. Kelso. 1994. Effects of nitroprusside and redox reagents on NMDA receptors expressed in Xenopus oocytes. Molec. Brain Res. 22:89-96.
67. Ono, K., and H.A. Fozzard. 1992. Phosphorylation restores activity of L-type channels after rundown in inside-out patches from rabbit cardiac cells. J. Physiol. (Lond.). 454:673-688.
68. 2+ channel affecting different kinetic functions. J. Physiol. (Lond.). 470:73-84.
69. Pan, Z. -H., R. Bähring, R. Grantyn, and S.A. Lipton. 1995. Differential modulation by sulfhydryl redox agents and glutathione of GABA- and glycine-evoked currents in rat retinal ganglion cells. J. Neurosci. 15:1384-1391.
70. 1 and β subunits. J. Gen. Physiol. 105:289-305.
71. 2+ current by extracellular ATP in ferret isolated right ventricular myocytes. J. Physiol. (Lond.). 471:295-317.
72. 2+ current by adenosine in ferret isolated right ventricular myocytes. J. Physiol. (Lond.). 471:269-293.
73. Reid, M.B., K.E. Haack, K.M. Franchek, P.A. Valberg, L. Kobzik, and M.S. West. 1992. Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J. Appl. Physiol. 73: 1797-1804.
74. KLM channels by cysteine oxidation. Nature (Lond.). 352:711-714.
75. 2. Implications for the action of endothelium derived relaxing factor (EDRF). Free Radical Res. Commun. 10:221-226.
76. Schmidt, H.H.H.W., S.M. Lohman, and U. Walter. 1993. The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochem. Biophys. Acta. 1178:153-175.
77. Schmidt, M.H.H.W., and U. Walter. 1994. NO. at work. Cell. 78: 919-925.
78. Schulz, R., J.A. Smith, M.J. Lewis, and S. Moncada. 1991. Nitric oxide synthase in cultured endocardial cells of the pig. Br. J. Pharmacol. 104:21-24.
79. Shah, A.M., and M.J. Lewis. 1993. Modulation of myorardial contraction by endocardial and coronary vascular endothelium. Trends Cardiovasc. Med. 3:98-103.
80. Shah, A.M., M.J. Shattock, and M.J. Lewis. 1992. Action potential duration and endocardial modulation of myocardial contraction. Cardiovasc. Res. 26:376-378.
81. Shenolikar, S., and A.C. Nairn. 1991. Protein phosphatases: recent progress. In Advances in Second Messenger and Phosphoprotein Research 23. P. Greengard and G.A. Robinson, editors. Raven Press, New York. 1-121.
82. Siney, L., and M.J. Lewis. 1993. Nitric oxide release from porcine mitral valves. Cardiovasc. Res. 27:1657-1661.
83. Snyder, S.H. 1992. Nitric oxide: first in a new class of neurotransmitters? Science (Wash. DC). 257:494-496.
84. Stamler, J.S. 1994. Redox signalling: nitrosylation and related target interactions of nitric oxide. Cell. 78:931-936.
85. Stamler, J.S. 1995. S-nitrosothiols and the bioregulatory actions of nitrogen oxides through reactions with thiol groups. Curr. Top. Microbiol. Immunol. 196:19-36.
86. Stamler, J.S. 1996. A radical vascular connection. Nature (Lond.). 380:108-111.
87. Stamler, J.S., D.I. Simon, J.A. Osborne, M. E. Mullins, O. Jaraki, T. Michel, D.J. Singel, and J. Loscalzo. 1992a. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc. Natl. Acad. Sci. USA. 89:444-448.
88. Stamler, J.S., D.J. Singel, and J. Loscalzo. 1992b. Biochemistry of nitric oxide and its redox-activated forms. Science (Wash. DC). 258: 1898-1902.
89. Stea, A., T.W. Soong, and T.P. Snutch. 1995. Voltage-gated calcium channels. In Handbook of Receptors and Channels. Ligand- and Voltage Gated Ion Channels. R.A. North, editor. CRC Press, Boca Raton, FL. 113-151.
90. Sullivan, J.M., S.F. Traynelis, H.-S. V. Chen, W. Escobar, S.F. Heinemann, and S.H. Lipton. 1994. Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron. 13:929-936.
91. 2+ current in rat ventricular myocytes. Circ. Res. 77:803-812.
92. Tanaka, K., and T. Chiba. 1995. Nitric oxide synthase containing nerves in the atrioventricular node of the guinea pig heart. J. Auton. Nerv. Sys. 51:245-253.
93. Tang, L.-H., and E. Aizenman. 1993. The modulation of N-methyl-D-aspartate receptors by redox and alkylating agents in rat cortical neurones in vitro. J. Physiol. (Lond.). 465:303-323.
94. Tsien, R.W., B.P. Bean, P. Hess, J.B. Lansman, B. Nilius, and M. Nowycky. 1986. Mechanisms of calcium channel modulation by β-adrenergic agents and dihydropyridine calcium channel agonists. J. Mol. Cell. Cardiol. 18:691-710.
95. Wahler, G.M., and S.J. Dollinger. 1995. Nitric oxide donor SIN-1 inhibits mammalian caridac calcium current through cGMP-dependent protein kinase. Am. J. Physiol. 268:C45-C54.
96. Wang, J., and J.P. Morgan. 1992. Endocardial endothelium modulates myofilament responsiveness in aequorin-loaded ferret myocardium. Circ. Res. 70:754-760.
97. 1 subunit by skeletal muscle β and γ subunits. J. Biol. Chem. 266:21943-21947.
98. Welling, A., Y.W. Kwan, E. Bosse, V. Flockerzi, F. Hofmann, and R.S. Kass. 1993. Subunit-dependent modulation of recombinant L-type calcium channels. Circ. Res. 73:974-980.
99. 2+] transients during excitation-contraction coupling of mammalian heart. In The Heart and Cardiovascular System. Scientific Foundations. Second Edition. H.A. Fozzard, R.B. Jennings, E. Haber, A.M. Katz, and H.E. Morgan, editors. Raven Press, New York. 1223-1248.