Effects of oxidation and cytosolic redox conditions on excitation-contraction coupling in rat skeletal muscle

Posterino, Giuseppe Saverio; Cellini, Maria.; Lamb, Graham D.

doi:10.1111/j.1469-7793.2003.00807.x

Cited by 50 publications

(46 citation statements)

References 45 publications

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“…Moreover, studies performed on isolated muscle fibers indicate that myofilaments are sensitive to direct redox modification and that their function is impaired by exposure to either ROS or NO (Andrade et al, 1998;Posterino et al, 2003). Under our experimental conditions, the results obtained in Triton X-100-skinned fibers show that 1 mM H 2 O 2 slightly decreased the maximal Ca 2ϩ -activated tension without affecting the Ca 2ϩ sensitivity of the contractile proteins; these effects were similar in Bl10 and dystrophic diaphragm.…”

Section: Discussionsupporting

confidence: 60%

Greater Susceptibility of the Sarcoplasmic Reticulum to H₂O₂ Injuries in Diaphragm Muscle from mdx Mice

Lafoux

Divet

Huchet-Cadiou

2006

J Pharmacol Exp Ther

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The aim of the present study was to investigate the direct effects of a reactive oxygen species, H 2 O 2 , on the contractile function and sarcoplasmic reticulum properties of dystrophindeficient diaphragm using chemically skinned fibers and sarcoplasmic reticulum vesicle preparations. The results obtained using Triton X-100-skinned fibers demonstrate that exposure to 1 mM H 2 O 2 had similar effects on the maximal Ca 2ϩ -activated tension and on the Ca 2ϩ sensitivity of the contractile apparatus of diaphragm fibers in Bl10 and mdx mice. The effects of H 2 O 2 were also assessed on sarcoplasmic reticulum function using saponin-skinned fibers and sarcoplasmic reticulum vesicle preparations. We found that H 2 O 2 induced changes in sarcoplasmic reticulum properties, particularly in the Ca 2ϩ pump function. The most important finding was that diaphragm muscle from mdx mice displayed increased sensitivity to the oxidant. Furthermore, in isolated superfused diaphragm muscle from mdx mice, the data demonstrate that the amount of superoxide anion produced under fatiguing conditions was increased. Our study shows that the sarcoplasmic reticulum, and the Ca 2ϩ pump in particular, in dystrophin-deficient muscles display increased susceptibility to H 2 O 2 injuries. This suggests that free radicals might, therefore, be involved in the pathophysiological pathway and dysregulation of Ca 2ϩ homeostasis of muscular dystrophy.

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Section: Discussionsupporting

confidence: 60%

Greater Susceptibility of the Sarcoplasmic Reticulum to H₂O₂ Injuries in Diaphragm Muscle from mdx Mice

Lafoux

Divet

Huchet-Cadiou

2006

J Pharmacol Exp Ther

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“…Following contraction, skeletal muscle fibers appear to release significant amounts of superoxide anion together with nitric oxide into the external medium (56,57,76,77). However, in skinned muscle fibers, exogenous H 2 O 2 stimulates contractions induced by caffeine but not by action potentials (78). Furthermore, H 2 O 2 activates contraction in intact skeletal muscle fibers without an apparent increase in cytoplasmic Ca 2ϩ concentration (79) despite the fact that, as shown here, H 2 O 2 readily activates RyR1-mediated calcium release (see also Ref.…”

Section: Discussionmentioning

confidence: 99%

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

Hidalgo

Pecchi

Barrientos

et al. 2006

Journal of Biological Chemistry

171

147

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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 [ 3 H]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 Ca 2؉ release channels. Possible implications of this putative mechanism for skeletal muscle function are discussed.The NADPH oxidases (NOX) 3 are flavoprotein enzymes that use NADPH as electron donor to mediate the univalent reduction of molecular oxygen to superoxide anion (1), a free radical that by spontaneous or enzymatically catalyzed dismutation is readily converted into H 2 O 2 . The phagocytic NOX isoform (NOX2) was first discovered as a pivotal component of the neutrophil respiratory burst (2, 3). The functional NOX2 enzyme is composed of two integral plasma membrane subunits, gp91 phox and p22phox , which make up cytochrome b 558 , plus three cytosolic regulatory subunits: p40 phox , p47 phox , and p67 phox (2, 4). A variety of tissues, including endothelial cells (5), smooth muscle cells (6), neurons (7-9), and astrocytes (7, 10), possess nonphagocytic NOX homologues (11,12). Several reports indicate that NOX2 and its homologues have a central role in the generation of reactive oxygen species (ROS) in response to diverse physiological extracellular stimuli (13-17). Moreover, membrane depolarization stimulates NOX activity in phagocytes (18) and endothelial cells (19,20). NOX stimulation is also apparent following agonist-induced stimulation of N-methyl-D-aspartate receptors in hippocampal neurons (21). Some N...

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“…The EDL and soleus muscles were excised, immersed under paraffin oil, and kept on ice. Under a dissecting microscope, single fibers were isolated from whole muscle and mechanically skinned with a pair of fine forceps (14,23,25). A single fiber was then mounted between a force transducer (2 kHz resonance frequency; AME801, SensoNor, Horten, Norway) and stationary pin and stretched to 120% of its resting length.…”

Section: Muscle Preparationmentioning

confidence: 99%

Sequential effects of GSNO and H₂O₂ on the Ca²⁺ sensitivity of the contractile apparatus of fast- and slow-twitch skeletal muscle fibers from the rat

Spencer

Posterino²

2009

American Journal of Physiology-Cell Physiology

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Spencer T, Posterino GS. Sequential effects of GSNO and H2O2 on the Ca 2ϩ sensitivity of the contractile apparatus of fast-and slow-twitch skeletal muscle fibers from the rat. Am J Physiol Cell Physiol 296: C1015-C1023, 2009. First published February 18, 2009 doi:10.1152/ajpcell.00251.2008.-Reactive oxygen species (ROS), such as hydrogen peroxide (H2O2) and nitric oxide (NO), have been shown to differentially alter the Ca 2ϩ sensitivity of the contractile apparatus of fast-twitch skeletal muscle, leading to the proposal that normal muscle function is controlled by perturbations in the amounts of these two groups of molecules (28). However, no previous studies have examined whether these opposing actions are retained when the contractile apparatus is subjected to both molecule types. Using mechanically skinned fast-and slow-twitch skeletal muscle fibers of the rat, we compared the effects of sequential addition of nitrosoglutathione (GSNO), a NO donor, and H2O2 on the Ca 2ϩ sensitivity of the contractile apparatus. As expected from previous reports in fast-twitch fibers, when added separately, GSNO (1 mM) reduced the Ca 2ϩ sensitivity of the contractile apparatus, whereas H2O2 (10 mM; added during contractions) increased the Ca 2ϩ sensitivity of the contractile apparatus. When added sequentially to the same fiber, such that the oxidation by one molecule (e.g., GSNO) preceded the oxidation by the other (e.g., H2O2), and vice versa, the individual effects of both molecules on the Ca 2ϩ sensitivity were retained. Interestingly, neither molecule had any effect on the Ca 2ϩ sensitivity of slow-twitch skeletal muscle. The data show that H 2O2 and GSNO retain the capacity to independently affect the contractile apparatus to modulate force. Furthermore, the absence of effects in slow-twitch muscle may further explain why this fiber type is relatively insensitive to fatigue. nitric oxide; reactive oxygen species; nitrosoglutathione; hydrogen peroxide THE REDOX STATE OF A SKELETAL muscle cell has been hypothesized to affect the force output in a similar fashion to other homeostatic variables such as pH and temperature (28). Skeletal muscle is known to produce a number of reactive oxygen species (termed ROS) as well as a variety of nitrogen-based compounds that include nitric oxide (NO) (see review in Ref. 29) that contribute to the redox state of the cell. The production of both ROS and NO occurs at varying rates during both rest and activity (29) as a by-product of oxidative metabolism (5). Reid et al. (28) had proposed a model depicting a biphasic effect of changes in cellular redox state on isometric force. The model predicted that basal (resting) levels of ROS (and/or NO) in muscle normally maintain a suboptimal performance level that can be modified by activity that results in deviations in contractile force output both potentially increasing and decreasing force. To date, there have been a number of studies in both intact muscle and skinned muscle fibers examining the effects of both ROS and NO on contractile a...

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Effects of oxidation and cytosolic redox conditions on excitation-contraction coupling in rat skeletal muscle

Cited by 50 publications

References 45 publications

Greater Susceptibility of the Sarcoplasmic Reticulum to H₂O₂ Injuries in Diaphragm Muscle from mdx Mice

Greater Susceptibility of the Sarcoplasmic Reticulum to H₂O₂ Injuries in Diaphragm Muscle from mdx Mice

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

Sequential effects of GSNO and H₂O₂ on the Ca²⁺ sensitivity of the contractile apparatus of fast- and slow-twitch skeletal muscle fibers from the rat

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Effects of oxidation and cytosolic redox conditions on excitation-contraction coupling in rat skeletal muscle

Cited by 50 publications

References 45 publications

Greater Susceptibility of the Sarcoplasmic Reticulum to H2O2 Injuries in Diaphragm Muscle from mdx Mice

Greater Susceptibility of the Sarcoplasmic Reticulum to H2O2 Injuries in Diaphragm Muscle from mdx Mice

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

Sequential effects of GSNO and H2O2 on the Ca2+ sensitivity of the contractile apparatus of fast- and slow-twitch skeletal muscle fibers from the rat

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Greater Susceptibility of the Sarcoplasmic Reticulum to H₂O₂ Injuries in Diaphragm Muscle from mdx Mice

Greater Susceptibility of the Sarcoplasmic Reticulum to H₂O₂ Injuries in Diaphragm Muscle from mdx Mice

Sequential effects of GSNO and H₂O₂ on the Ca²⁺ sensitivity of the contractile apparatus of fast- and slow-twitch skeletal muscle fibers from the rat