Adaptation of motor unit contractile properties in rat medial gastrocnemius to treadmill endurance training: Relationship to muscle mitochondrial biogenesis

This study aimed at investigating the effects of 2, 4 and 8 weeks of endurance training on the contractile properties of slow (S), fast fatigue resistant (FR) and fast fatigable (FF) motor units (MUs) in rat medial gastrocnemius (MG) in relation to the changes in muscle mitochondrial biogenesis. The properties of functionally isolated MUs were examined in vivo. Mitochondrial biogenesis was judged based on the changes in mitochondrial DNA copy number (mtDNA), the content of the electron transport chain (ETC) proteins and PGC-1α in the MG. Moreover, the markers of mitochondria remodeling mitofusins (Mfn1, Mfn2) and dynamin-like protein (Opa1) were studied using qPCR. A proportion of FR MUs increased from 37.9% to 50.8% and a proportion of FF units decreased from 44.7% to 26.6% after 8 weeks of training. The increased fatigue resistance, shortened twitch duration, and increased ability to potentiate force were found as early as after 2 weeks of endurance training, predominantly in FR MUs. Moreover, just after 2 weeks of the training an enhancement of the mitochondrial network remodeling was present as judged by an increase in expression of Mfn1, Opa1 and an increase in PGC-1α in the slow part of MG. Interestingly, no signs of intensification of mitochondrial biogenesis assessed by ETC proteins content and mtDNA in slow and fast parts of gastrocnemius were found at this stage of the training. Nevertheless, after 8 weeks of training an increase in the ETC protein content was observed, but mainly in the slow part of gastrocnemius. Concluding, the functional changes in MUs’ contractile properties leading to the enhancement of muscle performance accompanied by an activation of signalling that controls the muscle mitochondrial network reorganisation and mitochondrial biogenesis belong to an early muscle adaptive responses that precede an increase in mitochondrial ETC protein content.本研究旨在探究2周、4周及8周耐力训练对大鼠腓肠肌内侧头(medial gastrocnemius, MG)内慢收缩型(S)、抗快速疲劳型(FR)及快速疲劳型(FF)运动单位(motor units, MUs)收缩特性的影响，并分析其与肌肉线粒体生物发生(mitochondrial biogenesis)变化的关联。本研究在体检测了功能性分离运动单位的各项特性。线粒体生物发生的评价指标包括线粒体DNA拷贝数(mtDNA)、电子传递链(electron transport chain, ETC)蛋白含量及过氧化物酶体增殖物激活受体γ辅激活因子1α(PGC-1α)的变化。此外，本研究还通过实时定量聚合酶链式反应(qPCR)检测了线粒体重塑相关标志物：线粒体融合蛋白(mitofusins, Mfn1、Mfn2)及动力样蛋白(dynamin-like protein, Opa1)的表达水平。8周耐力训练后，FR运动单位的占比从37.9%提升至50.8%，FF运动单位的占比则从44.7%降至26.6%。早在训练2周后，即可在FR运动单位中观察到抗疲劳能力增强、抽搐时程缩短及肌力强化能力提升。同时，训练仅2周时，腓肠肌内侧头慢收缩肌部分的Mfn1、Opa1表达上调，PGC-1α水平升高，提示线粒体网络重塑过程增强。值得注意的是，此训练阶段未在腓肠肌快慢收缩肌部分观察到电子传递链蛋白含量及mtDNA水平升高，即未出现线粒体生物发生增强的迹象。训练8周后，仅在慢收缩肌部分观察到电子传递链蛋白含量升高。综上，运动单位收缩特性的功能变化可提升肌肉运动表现，同时伴随调控肌肉线粒体网络重塑及线粒体生物发生的信号通路激活，这类变化属于早期肌肉适应性应答，其发生早于线粒体电子传递链蛋白含量的提升。