Specific training improves skeletal muscle mitochondrial calcium homeostasis after eccentric exercise

Abstract

There is limited understanding of the mitochondrial adaptation following repeated eccentric exercise bouts, a model resulting in muscle adaptation known as the repeat bout effect. It was hypothesized that downhill training would reduce mitochondrial calcium content (MCC) post an acute eccentric bout with concurrent improvements in mitochondrial respiratory function. Thirty-four Sprague-Dawley rats were divided into four groups: control (N), control with acute eccentric exercise (N (ecc)), trained control (X) and trained with acute eccentric exercise (X (ecc)). Training for X and X (ecc) consisted of 30 min per day for five consecutive days of downhill treadmill running. The acute eccentric exercise bout was a -14° treadmill exercise for 90 min performed 2 weeks after the training period. Animals were killed 48 h post-exercise. Isolated mitochondria from the red quadriceps allowed for the measure of mitochondrial respiratory indices and MCC. Calpain activity and heat shock protein 72 expression (HSP72) were also measured. MCC dramatically increased following the acute bout of eccentric exercise in N (ecc) (p < 0.001), but did not change in X (ecc). Mitochondrial respiratory function tended to be slightly depressed in N (ecc) (state 3 respiration, p = 0.053; respiratory control ratio, p = 0.098) and unaltered in X (ecc). Previous training altered the calpain and heat shock protein response to an acute bout of eccentric exercise. The results suggest that downhill exercise training improves mitochondrial calcium homeostasis following an acute bout of prolonged eccentric exercise and may stabilize mitochondrial respiratory function. These improvements coincide with a reduction in calpain activity and heat shock protein upregulation.

Mitochondrial function following downhill and/or uphill exercise training in rats

“…Downhill (DH) running is often used as a model of eccentric exercise in rats to examine skeletal muscle damage/regeneration processes following eccentric‐induced mechanical stress . However, fewer studies have focused on eccentric training‐induced metabolic adaptations in rats, especially on skeletal muscle aerobic energy production in mitochondria . Some studies have used a model of DH exercise training but with no reference to oxygen consumption.…”

L-arginine Supplementation Protects Exercise Performance and Structural Integrity of Muscle Fibers after a Single Bout of Eccentric Exercise in Rats

“…Our experiments showed that exercise performance capacity measured twenty four hours after a single bout of eccentric exercise was higher in L-Arg supplementation rats when compared with control non-treated non-exercised rats. We attributed this finding to the preservation of dystrophin and desmin content after eccentric exercise as well as to adaptive changes in the structure of the sarcomeres related to the previously described post-exercise conditioning of muscle [53], [54] and improved mitochondrial calcium homeostasis [55].…”

Mitochondrial dysfunction and autophagy responses to skeletal muscle stress

“…Mitochondria are appreciated as contributing to the regenerative potential, plasticity, and overall quality of skeletal muscle, and, therefore, investigating the muscle fiber-mitochondrial relationship may produce important targets for rehabilitation and disease prevention. However, there appear to be inconsistencies in the literature regarding what types of muscle stressors elicit mitochondrial dysfunction (20, 30, 31, 33), as well as the extent to which autophagy is necessary for the timely repair of mitochondrial dysfunction after muscle stress (6). Herein, we relied upon oxygen consumption as the marker of mitochondrial function, enzyme activities of succinate dehydrogenase and citrate synthase as markers of mitochondrial content, and a muscle-specific Ulk1 knockout mouse to test the necessity of autophagy for the recovery of mitochondrial function and content.…”

“…Less severe muscle stressors, like eccentric contraction-induced injuries, mainly disrupt excitation-contraction coupling and result in an initial 40%-60% decline in muscle contractility (38). There have been conflicting reports of mitochondrial oxygen consumption rates after downhill treadmill running, a mild and indirect form of eccentric contraction-induced injury in mice with some reporting no changes in mitochondrial respiration and others reporting transient changes immediately and up to 48 hours after the injury (24, 30, 31, 33). Additionally, this injury model is reported to elicit oxidative damage in the form of a greater presence of protein carbonyls and oxidized lipids that could implicate mitochondrial dysfunction (26, 33).…”