Abstract
Preservation of mitochondrial function, which is dependent on mitochondrial homeostasis (biogenesis, dynamics, disposal/recycling), is critical for maintenance of skeletal muscle function. Skeletal muscle performance declines upon aging (sarcopenia) and is accompanied by decreased mitochondrial function in fast-glycolytic muscles. Oxidative metabolism promotes mitochondrial homeostasis, so we investigated whether mitochondrial function is preserved in oxidative muscles. We compared tibialis anterior (predominantly glycolytic) and soleus (oxidative) muscles from young (3 mo) and old (28-29 mo) C57BL/6J mice. Throughout life, the soleus remained more oxidative than the tibialis anterior and expressed higher levels of markers of mitochondrial biogenesis, fission/fusion and autophagy. The respiratory capacity of mitochondria isolated from the tibialis anterior, but not the soleus, declined upon aging. The soleus and tibialis anterior exhibited similar aging-associated changes in mitochondrial biogenesis, fission/fusion, disposal and autophagy marker expression, but opposite changes in fiber composition: the most oxidative fibers declined in the tibialis anterior, while the more glycolytic fibers declined in the soleus. In conclusion, oxidative muscles are protected from mitochondrial aging, probably due to better mitochondrial homeostasis ab initio and aging-associated changes in fiber composition. Exercise training aimed at enriching oxidative fibers may be valuable in preventing mitochondria-related aging and its contribution to sarcopenia.
Highlights
Skeletal muscles comprise fibers with a range of contractile properties and metabolic needs
To determine whether the distinct metabolic nature of the two muscles corresponded to differences in mitochondrial homeostasis, we evaluated the expression of markers of mitochondrial biogenesis (PGC-1α and PGC-1β [2, 15, 26]), fission/fusion (Mfn2, OPA1 [27, 28]), and autophagy (LC3-II/I [29]; APG5 [30])
We evaluated agingassociated changes in mitochondrial function, mitochondrial homeostasis and fiber composition in murine muscles with different contractile functions and metabolic needs by comparing the tibialis anterior, which is strongly enriched in type IIB and IIX fibers, and the soleus, which consists of a mixture of type I and IIA/IIX fibers
Summary
Skeletal muscles comprise fibers with a range of contractile properties and metabolic needs. Slow contractions allow ATP production by mitochondrial oxidative phosphorylation, which is slower, but more efficient. Each muscle comprises a distinct combination of fast-glycolytic, fastwww.aging-us.com oxidative/glycolytic, and slow-oxidative fibers [1, 2]. Mitochondrial function declines in the aged skeletal muscle of several species, including humans [3,4,5,6,7,8,9,10,11]. Mitochondrial biogenesis, dynamics (fission/fusion) and recycling are essential for maintenance of mitochondrial function, and aging is associated with impaired mitochondrial maintenance (reviewed in [6, 12]). Mitochondrial morphology, an indicator of fission/fusion balance, has been shown to change in aged mouse muscles [13], and skeletal muscle aging is associated with altered mitochondrial dynamics and quality control in mice [14]. Improving mitochondrial homeostasis/function has been demonstrated to rejuvenate several tissues in various species, resulting in increased longevity [12]
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