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Originally published In Press as doi:10.1074/jbc.M100083200 on February 16, 2001

J. Biol. Chem., Vol. 276, Issue 19, 15625-15630, May 11, 2001
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Classes of Thiols That Influence the Activity of the Skeletal Muscle Calcium Release Channel*

Junhui SunDagger , Le XuDagger , Jerry P. Eu§, Jonathan S. Stamler§, and Gerhard MeissnerDagger

From the Dagger  Departments of Biochemistry and Biophysics and Cell and Molecular Physiology, University of North Carolina, Chapel Hill, North Carolina 27599-7260 and the § Howard Hughes Medical Institute, Department of Medicine, Divisions of Pulmonary and Cardiovascular Medicine, and Department of Biochemistry, Duke University Medical Center, Durham, North Carolina 27710

The skeletal muscle Ca2+ release channel/ryanodine receptor (RyR1) is a prototypic redox-responsive ion channel. Nearly half of the 101 cysteines per RyR1 subunit are kept in a reduced (free thiol) state under conditions comparable with resting muscle. Here we assessed the effects of physiological determinants of cellular redox state (oxygen tension, reduced (GSH) or oxidized (GSSG) glutathione, and NO/O&cjs1138;2 (released by 3-morpholinosydnonimine)) on RyR1 redox state and activity. Oxidation of ~10 RyR1 thiols (from ~48 to ~38 thiols/RyR1 subunit) had little effect on channel activity. Channel activity increased reversibly as the number of thiols was further reduced to ~23/subunit, whereas more extensive oxidation (to ~13 thiols/subunit) inactivated the channel irreversibly. Neither S-nitrosylation nor tyrosine nitration contributed to these effects. The results identify at least three functional classes of RyR1 thiols and suggest that 1) the channel may be protected from oxidation by a large reservoir of functionally inert thiols, 2) the channel may be designed to respond to moderate oxidative stress by a change in activation setpoint, and 3) the channel is susceptible to oxidative injury under more extensive conditions.

* The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.This

work was supported by National Institutes of Health Grants HL04053 (to J. P. E.); HL52529, ES-09206, and HL59130 (to J. J. S.); and AR18687 and HL27430 (to G. M.).

To whom correspondence should be addressed: Dept. of Biochemistry and Biophysics, University of North Carolina, Chapel Hill, NC 27599-7260. Tel.: 919-966-5021; Fax: 919-966-2852; E-mail: meissner@med.unc.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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