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The cannabinoid type 1 (CB 1 ) receptor is widely distributed in the brain and peripheral organs where it regulates cellular functions and metabolism. In the brain, CB 1  is mainly localized on presynaptic axon terminals but is also found on mitochondria (mtCB 1 ), where it regulates cellular respiration and energy production. Likewise, CB 1  is localized on muscle mitochondria, but very little is known about it. The aim of this study was to further investigate in detail the distribution and functional role of mtCB 1  in three different striated muscles. Immunoelectron microscopy for CB 1  was used in skeletal muscles (gastrocnemius and rectus abdominis) and myocardium from wild-type and  CB   1  -KO mice. Functional assessments were performed in mitochondria purified from the heart of the mice and the mitochondrial oxygen consumption upon application of different acute delta-9-tetrahydrocannabinol (Δ 9 -THC) concentrations (100 nM or 200 nM) was monitored. About 26% of the mitochondrial profiles in gastrocnemius, 22% in the rectus abdominis and 17% in the myocardium expressed CB 1 . Furthermore, the proportion of mtCB1 versus total CB 1  immunoparticles was about 60% in the gastrocnemius, 55% in the rectus abdominis and 78% in the myocardium. Importantly, the CB 1  immunolabeling pattern disappeared in muscles of  CB   1  -KO mice. Functionally, acute 100 nM or 200 nM THC treatment specifically decreased mitochondria coupled respiration between 12 and 15% in wild-type isolated mitochondria of myocardial muscles but no significant difference was noticed between THC treated and vehicle in mitochondria isolated from  CB   1  -KO heart. Furthermore, gene expression of key enzymes involved in pyruvate synthesis, tricarboxylic acid (TCA) cycle and mitochondrial respiratory chain was evaluated in the striated muscle of  CB   1  -WT and  CB   1  -KO.  CB   1  -KO showed an increase in the gene expression of  Eno3, Pkm2 , and  Pdha1 , suggesting an increased production of pyruvate. In contrast, no significant difference was observed in the  Sdha  and  Cox4i1  expression, between  CB   1  -WT and  CB   1  -KO. In conclusion, CB 1  receptors in skeletal and myocardial muscles are predominantly localized in mitochondria. The activation of mtCB 1  receptors may participate in the mitochondrial regulation of the oxidative activity probably through the relevant enzymes implicated in the pyruvate metabolism, a main substrate for TCA activity.

Cannabinoid CB1 Receptors Are Localized in Striated Muscle Mitochondria and Regulate Mitochondrial Respiration