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J. Biol. Chem., Vol. 278, Issue 44, 42927-42935, October 31, 2003

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S-Glutathionylation Decreases Mg²⁺ Inhibition and S-Nitrosylation Enhances Ca²⁺ Activation of RyR1 Channels^*

Paula Aracena, Gina Sánchez, Paulina Donoso, Susan L. Hamilton¶, and Cecilia Hidalgo||

From the Centro Fondo de Investigación Avanzada en Areas Prioritarias de Estudios Moleculares de la Célula, Facultad de Medicina, Universidad de Chile, Casilla 70005, Santiago 7, Chile, the Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Casilla 70005, Santiago 7, Chile, and the ^¶Department of Molecular Physiology and Biophysics, Baylor College of Medicine, Houston, Texas 77030

We have analyzed the effects of the endogenous redoxactive agents S-nitrosoglutathione and glutathione disulfide, and the NO donor NOR-3, on calcium release kinetics mediated by ryanodine receptor channels. Incubation of triad-enriched sarcoplasmic reticulum vesicles isolated from mammalian skeletal muscle with these three agents elicits different responses. Glutathione disulfide significantly reduces the inhibitory effect of Mg²⁺ without altering Ca²⁺ activation of release kinetics, whereas NOR-3 enhances Ca²⁺ activation of release kinetics without altering Mg²⁺ inhibition. Incubation with S-nitrosoglutathione produces both effects; it significantly enhances Ca²⁺ activation of release kinetics and diminishes the inhibitory effect of Mg²⁺ on this process. Triad incubation with [³⁵S]nitrosoglutathione at pCa 5 promoted ³⁵S incorporation into 2.5 cysteine residues per channel monomer; this incorporation decreased significantly at pCa 9. These findings indicate that S-nitrosoglutathione supports S-glutathionylation as well as the reported S-nitrosylation of ryanodine receptor channels (Sun, J., Xu, L., Eu, J. P., Stamler, J. S., and Meissner, G. (2003) J. Biol. Chem. 278, 8184–8189). The combined results suggest that S-glutathionylation of specific cysteine residues can modulate channel inhibition by Mg²⁺, whereas S-nitrosylation of different cysteines can modulate the activation of the channel by Ca²⁺. Possible physiological and pathological implications of the activation of skeletal Ca²⁺ release channels by endogenous redox species are discussed.

Received for publication, June 30, 2003 , and in revised form, August 5, 2003.

^* This work was supported by FONDAP Center for Molecular Studies of the Cell, Fondo Nacional de Investigación Científica y Tecnológica (Chile) Grant 15010006 and by National Institutes of Health Grants AR41802 and AR44864. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| To whom correspondence should be addressed: Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Casilla 70005, Santiago 7, Chile. Tel.: 56-2-678-6510; Fax: 56-2-777-6916; E-mail: chidalgo{at}machi.med.uchile.cl.

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