Nitric oxide activates or inhibits skeletal muscle ryanodine receptors depending on its concentration, membrane potential and ligand binding

Journal of Membrane Biology

Volumn 173, Issue 3, 2000, Pages 227-236

  Hart, J D E ^a   Dulhunty, A F ^a  

^a Australian National University   (Australia)

Author keywords

Calcium channels; Nitric oxide; Oxidation; Regulatory thiols; Ryanodine receptors; Skeletal Muscle

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM CHANNEL; DITHIOTHREITOL; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; NITROPRUSSIDE SODIUM; PEPTIDE; RYANODINE RECEPTOR;

ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CHANNEL GATING; CONCENTRATION RESPONSE; ELECTRIC POTENTIAL; LIPID BILAYER; MEMBRANE POTENTIAL; NONHUMAN; OXIDATION; RABBIT; SKELETAL MUSCLE; VOLTAGE CLAMP;

ADENOSINE TRIPHOSPHATE; ANIMALS; DITHIOTHREITOL; ION CHANNELS; MEMBRANE POTENTIALS; MUSCLE, SKELETAL; NITRIC OXIDE; NITRIC OXIDE DONORS; NITROPRUSSIDE; PATCH-CLAMP TECHNIQUES; PENICILLAMINE; RABBITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; S-NITROSO-N-ACETYLPENICILLAMINE; SARCOPLASMIC RETICULUM;

EID: 0034142077     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s002320001022     Document Type: Article

References (40)

1. 2 and dithiothreitol. Am. J. Physiol. 267:H1010-H1016
2. Curello, S., Ceconi, C., Bigoli, C., Ferrari, R., Albertini, A., Guarnieri, C. 1985. Changes in the cardiac glutathione status after ischemia and reperfusion. Experientia 41:42-43
3. 687 and FKBP12. Biophys. J. 77:189-203
4. 2+ and ATP. J. Membrane Biol. 163:9-18
5. Eager, K.R., Dulhunty, A.F. 1999. Cardiac ryanodine receptor activity is altered by oxidizing reagents in either luminal or cytoplasmic solution. J. Membrane Biol. 167:205-214
6. 2+-release channels from sheep myocardium. Am. J. Physiol. 272:C1908-C1918
7. El Dwairi, Q., Guo, Y., Comtois, A., Zhu, E., Greenwood, M.T., Bredt, D.S., Hussain, S.N. 1998. Ontogenesis of nitric oxide synthases in the ventilatory muscles. Am. J. Respir. Cell Mol. Biol. 18:844-852
8. El-Hayek, R., Antoniu, B., Wang, J., Hamilton, S.L., Ikemoto, N. 1995. Identification of calcium release-triggering and blocking regions of the II-III loop of the skeletal muscle dihydropyridine receptor. J. Biol. Chem. 270:22116-22118
9. 2+ release channel from skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 270:25557-25563
10. Franzini-Armstrong, C. 1970. Studies of the triad. 1. Structure of the junction in frog twitch fibers. J. Cell. Biol. 47:488-499
11. Gurrola, G.B., Arevalo, C., Sreekumar, R., Lokuta, A.J., Walker, J.W., Valdivia, H.H. 1999. Activation of ryanodine receptors by imperatoxin A and a peptide segment of the II-III loop of the dihydropyridine receptor. J. Biol. Chem. 274:7879-7886
12. Haarmann, C.S., Fink, R.H.A., Dulhunty, A.F. 1999. Oxidation and reduction of pig skeletal muscle ryanodine receptors. Biophys. J. 77:3010-3022
13. Holmberg, S.R., Cumming, D.V., Kusama, Y., Hearse, D.J., Poole- Wilson, P.A., Shattock, M.J., Williams, A.J. 1991. Reactive oxygen species modify the structure and function of the cardiac sarcoplasmic reticulum calcium-release channel. Cardioscience 2:19-25
14. Kobzik, L., Reid, M.B., Bredt, D.S., Stamler, J.S. 1994. Nitric oxide in skeletal muscle. Nature 372:546-548
15. Kobzik, L., Stringer, B., Balligand, J.L., Reid, M.B., Stamler, J.S. 1995. Endothelial type nitric oxide synthase in skeletal muscle fibers: mitochondrial relationships. Biochem. Biophys. Res. Commun. 211:375-381
16. Koshita, M., Miwa, K., Oba, T. 1993. Sulfhydryl oxidation induces calcium release from fragmented sarcoplasmic reticulum even in the presence of glutathione. Experientia 49:282-284
17. Kourie, J.I., Foster, P.S., Dulhunty, A.F. 1997. Inositol polyphosphates modify the kinetics of a small chloride channel in skeletal muscle sarcoplasmic reticulum. J. Membrane Biol. 157:147-158
18. Laurent, M., Lepoivre, M., Tenu, J.P. 1996. Kinetic modeling of the nitric oxide gradient generated in vitro by adherent cells expressing inducible nitric oxide synthase. Biochem. J. 314:109-113
19. 2+ inhibits the ryanodine receptor from cardiac muscle. J. Membrane Biol. 147:7-22
20. Marengo, J.J., Hidalgo, C., Bull, R. 1998. Sulfhydryl oxidation modifies the calcium dependence of ryanodine-sensitive calcium channels of excitable cells. Biophys. J. 74:1263-1277
21. Meister, A., Anderson, M.E. 1983. Glutathione. Annu. Rev. Biochem. 52:711-760
22. Mészáros, L.G., Minarovic, I., Zahradníková, A. 1996. Inhibition of the skeletal muscle ryanodine receptor calcium release channel by nitric oxide. FEBS Lett. 380:49-52
23. 2+-induced fusion of fragmented sarcoplasmic reticulum with artificial planar bilayers. J. Membrane Biol. 9:283-300
24. Moncada, S., Higgs, A. 1993. The L-arginine nitric oxide pathway. N. Engl. J. Med. 329:2002-2012
25. Murrant, C.L., Barclay, J.K. 1995. Endothelial cell products alter mammalian skeletal muscle function in vitro. Can. J. Physiol. Pharmacol. 73:736-741
26. Murrant, C.L., Woodley, N.E., Barclay, J.K. 1994. Effect of nitroprus-side and endothelium-derived products on slow-twitch skeletal muscle function in vitro. Can. J. Physiol. Pharmacol. 72:1089-1093
27. 2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J. Biol. Chem. 265:13472-13483
28. Perkins, W.J., Han, Y.S., Sieck, G.C. 1997. Skeletal muscle force and actomyosin ATPase activity reduced by nitric oxide donor. J. Appl. Physiol. 83:1326-1332
29. Reid, M.B. 1998. Role of nitric oxide in skeletal muscle: synthesis, distribution and functional importance. Acta Physiol. Scand. 162:401-409
30. Saito, A., Seiler, S., Chu, A., Fleischer, S. 1984. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. J. Cell. Biol. 99:875-885
31. Sies, H., Gerstenecker, C., Menzel, H., Flohe, L. 1972. Oxidation in the NADP system and release of GSSG from hemoglobin-free perfused rat liver during peroxidatic oxidation of glutathione by hydroperoxides. FEBS Lett. 27:171-175
32. Simon, D.I., Mullins, M.E., Jia, L., Gaston, B., Singel, D.J., Stamler, J.S. 1996. Polynitrosylated proteins: characterization, bioactivity and functional consequences. Proc. Natl. Acad. Sci. USA 93:4736-4741
33. Simonsen, U., Wadsworth, R.M., Buus, N.H., Mulvany, M.J. 1999. In vitro simultaneous measurements of relaxation and nitric oxide concentration in rat superior mesenteric artery. J. Physiol. 516:271-282
34. Sirsjö, A., Årstrand, K., Kågedal, B., Nylander, G., Gidlöf, A. 1996. In situ microdialysis for monitoring of extracellular glutathione levels in normal, ischemic and post-ischemic skeletal muscle. Free Rad. Res. 25:385-391
35. Steare, S.E., Yellon, D.M. 1995. The potential for endogenous myocardial antioxidants to protect the myocardium against ischaemia- reperfusion injury: Refreshing the parts exogenous antioxidants cannot reach? J. Mol. Cell Cardiol. 27:65-74
36. Stoyanovsky, D., Murphy, T., Anno, P.R., Kim, Y.M., Salama, G. 1997. Nitric oxide activates skeletal and cardiac ryanodine receptors. Cell Calcium 21:19-29
37. Tanabe, T., Beam, K.G., Adams, B.A., Niidome, T., Numa, S. 1990. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature 346:567-569
38. Williams, G., Brown, T., Becker, M., Prager, M., Giroir, B.P. 1994. Cytokine-induced expression of nitric oxide synthase in C2C12 skeletal muscle myocytes. Am. J. Physiol. 267:R1020-R1025
39. Xu, L., Eu, J.P., Meissner, G., Stamler, J.S. 1998. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S- Nitrosylation. Science 279:234-237
40. Zahradníková, A., Minarovic, I., Venema, R.C., Mészáros, L.G. 1997. Inactivation of the cardiac ryanodine receptor calcium release channel by nitric oxide. Cell Calcium 22:447-454