A single muscle contusion promotes an immediate alteration in mitochondrial bioenergetics response in skeletal muscle fibres with different metabolism

Abstract

Skeletal muscle is the most abundant tissue in the human body and mechanical injuries are common; these are frequently of mechanical origins, such as contusion. However, the immediate mitochondrial response to injury and energetic substrate utilisation is still unclear. We evaluated the acute response in mitochondrial function after a single muscle contusion, either in fast twitch fibres (glycolytic metabolism), fast and slow twitch (oxidative and glycolytic metabolism), or slow twitch fibres (oxidative metabolism). Rats were assigned to two groups: control and Lesion (muscle contusion). We collected the gastrocnemius and soleus muscles. The fibres were analysed for mitochondrial respiration, lactate dehydrogenase (LDH), citrate synthase (CS) activity, Ca²⁺ uptake, and H₂O₂ production. We found that muscle injury was able to increase ATP synthesis-dependent and OXPHOS oxygen flux in the oxidative fibres when stimulated by complex I + II substrates. On the other hand, the muscle injury increased hydrogen peroxide (H₂O₂) production when compared to control fibres, and reduced citrate synthase activity; however, it did not change Ca²⁺ uptake. Surprisingly, injury in mixed fibres increased the OXPHOS and ATP synthesis oxygen consumption, and H₂O₂ production, but it reduced Ca²⁺ uptake. The injury in glycolytic fibres did not affect oxygen flux coupled to ATP synthesis, citrate synthase, and lactate dehydrogenase activity, but did reduce Ca²⁺ uptake. Finally, we demonstrated distinct mitochondrial responses between the different muscle fibres, indicating that the mitochondrial dynamics is related to flexibilities in metabolism, and that reactive oxygen species directly affect physiology and normal function.

Keywords:

• Bioenergetics
• contusion injury
• high-resolution respirometry
• mitochondrial function
• ROS production
• skeletal muscle fibres

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

Financial support for this study was provided by Fundação de Amparo à pesquisa do Estado do RS (FAPERGS), Brazilian National Council of Technological and Scientific Development (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazilian National Institute for Science and Technology (INCT), “Programa de Apoio a Núcleos Emergentes” (PRONEM) and MCTI/CNPq [grant numbers 472669/2011-7, 475896/2012-2]. Programa de excelência acadêmica (PROEX) process number 88 882.182135/2018-01.