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J. Biol. Chem., Vol. 281, Issue 36, 26473-26482, September 8, 2006

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A Transverse Tubule NADPH Oxidase Activity Stimulates Calcium Release from Isolated Triads via Ryanodine Receptor Type 1 S -Glutathionylation^*

Cecilia Hidalgo¹, Gina Sánchez^¶, Genaro Barrientos, and Paula Aracena-Parks²

From the Centro FONDAP de Estudios Moleculares de la Célula, Facultad de Medicina, Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas, Facultad de Medicina, and ^¶Programa de Patología, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Casilla 70005, Santiago 7, Chile

We report here the presence of an NADPH oxidase (NOX) activity both in intact and in isolated transverse tubules and in triads isolated from mammalian skeletal muscle, as established by immunochemical, enzymatic, and pharmacological criteria. Immunohistochemical determinations with NOX antibodies showed that the gp91^phox membrane subunit and the cytoplasmic regulatory p47^phox subunit co-localized in transverse tubules of adult mice fibers with the _1s subunit of dihydropyridine receptors. Western blot analysis revealed that isolated triads contained the integral membrane subunits gp91^phox and p22^phox, which were markedly enriched in isolated transverse tubules but absent from junctional sarcoplasmic reticulum vesicles. Isolated triads and transverse tubules, but not junctional sarcoplasmic reticulum, also contained varying amounts of the cytoplasmic NOX regulatory subunits p47^phox and p67^phox. NADPH or NADH elicited superoxide anion and hydrogen peroxide generation by isolated triads; both activities were inhibited by NOX inhibitors but not by rotenone. NADH diminished the total thiol content of triads by one-third; catalase or apocynin, a NOX inhibitor, prevented this effect. NADPH enhanced the activity of ryanodine receptor type 1 (RyR1) in triads, measured through [³H]ryanodine binding and calcium release kinetics, and increased significantly RyR1 S-glutathionylation over basal levels. Preincubation with reducing agents or NOX inhibitors abolished the enhancement of RyR1 activity produced by NADPH and prevented NADPH-induced RyR1 S-glutathionylation. We propose that reactive oxygen species generated by the transverse tubule NOX activate via redox modification the neighboring RyR1 Ca²⁺ release channels. Possible implications of this putative mechanism for skeletal muscle function are discussed.

Received for publication, January 17, 2006 , and in revised form, June 6, 2006.

^* This study was supported by Fondo de Investigación Avanzada enÁ_reas Prioritarias (FONDAP) Project 15600001. 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.

² Recipient of a Comisión Nacional de Investigación Científica y Tecnológica de Chile (CONICYT) Ph.D. scholarship during this work. Present address: Dept. of Molecular Physiology and Biophysics, Baylor College of Medicine, Houston, TX 77030.

¹ To whom correspondence should be addressed: ICBM, 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}med.uchile.cl.

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