Enhanced activity of eccentric contraction induces alterations in <i>in vitro</i> sarcoplasmic reticulum Ca²⁺ handling in rat hindlimb muscles

Abstract

In order to investigate factors that contribute to eccentric contraction (ECC)-induced loss of tetanic force, Ca 2+ uptake, Ca 2+ release, and Ca 2+ -ATPase activity of the sarcoplasmic reticulum (SR) and sarcolemmal Na + -K + -ATPase activity were examined in rat fast-twitch skeletal muscles that underwent in situ ECC or isometric contraction (ISC) for up to 500 repetitions. The tetanic force at 60 Hz was more depressed in ECC-treated muscles than in ISC-treated muscles. SR Ca 2+ -ATPase activity displayed biphasic changes in response to ECC; after a temporary increase (up to 200 ECC repetitions), the activity decreased. With ECC, SR Ca 2+ release rate and Na + -K + -ATPase activity decreased during the first 100 repetitions and remained almost constant thereafter. In contrast, the investigated variables (Ca 2+ -ATPase activity, Ca 2+ release rate, and Na + -K + -ATPase activity) were unaltered in ISC-treated muscles. These results indicate that a more pronounced reduction in force output in ECC-treated muscles than in ISC-treated muscles might be attributable, at least in part, to impaired function of the SR Ca 2+ release channel and/or Na + -K + -ATPase.

Effect of Dietary Nitrate on Force Production and Sarcoplasmic Reticulum Ca&lt;sup&gt;2+&lt;/sup&gt; Handling in Rat Fast-Twitch Muscles Following Eccentric Contraction

“…ECC results in an inability to produce the desired force characterized by triad deformation [36], sarcomere inhomogeneity [37], increased membrane permeability [38], inflammation [39], and proteolysis [21] release rate in rat fast-twitch muscles. We noted that loss of ECC-induced contractile activity can be attributed to a failure of SR Ca 2+ release [11]. Nitrate ingestion enhanced SR Ca 2+ release and tetanic force production via modifications of the cellular Ca 2+ handling components in mouse fast-twitch muscle [20].…”

“…Throughout the experiment, the rats were deeply anesthetized with an intraperitoneal injection of a mixture of medetomidine (0.4 mg kg body wt −1 ), midazolam (2.0 mg kg body wt −1 ), and butorphanol (2.5 mg kg body wt −1 ). ECC was performed as described previously [11]. Briefly, an animal was placed in the supine position on a supporting platform, with the left foot secured in a foot holder attached to the rim of a servomotor.…”

“…The TA muscle pieces were diluted in a ratio of 1:9 (mass vol −1 ) in ice-cold homogenizing buffer (pH 7.4) composed of 300 mM sucrose, 20 mM MOPS/KOH, 0.0014 mM pepstatin, 0.83 mM benzamidine, 0.0022 mM leupeptin, and 0.2 mM phenylmethanesulfonyl fluoride [11]. They were mechanically homogenized thrice with a hand-held glass homogenizer (Asone, Osaka, Japan) at 5000 rpm for 30-s bursts separated by 30-s breaks.…”

“…Reportedly, impaired excitation-contraction coupling occurs in eccentrically damaged mammalian muscles [8]. It has been suggested that sarcomeres within myofibrils, transverse tubules (t-tubules), and SR are susceptible to damage in the overstretched regions, possibly marking the basis of excitation-contraction coupling damage [11].…”

Pre-exercise nitric oxide donor supplementation attenuates decline in muscle contractile force and ryanodine receptor proteolysis following eccentric contraction

“…This is primarily due to muscle damage, characterized by swelling 2) , inflammation 3) , triad deformation 4,5) , increased membrane permeability 6) , proteolysis 7) , or a combination of these. It has been suggested that sarcomeres within myofibrils, transverse tubules, and the sarcoplasmic reticulum (SR) are susceptible to damage in overstretched regions, which may be the basis of impairment to excitation-contraction coupling 8) .…”