Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: tailoring the organelle for optimal function

Abstract

Picard M, Hepple RT, Burelle Y. Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: tailoring the organelle for optimal function. Am J Physiol Cell Physiol 302: C629 -C641, 2012. First published October 26, 2011; doi:10.1152/ajpcell.00368.2011In skeletal muscle, two major types of muscle fibers exist: slow-twitch oxidative (type I) fibers designed for low-intensity long-lasting contractions, and fast-twitch glycolytic (type II) fibers designed for high-intensity short-duration contractions. Such a wide range of capabilities has emerged through the selection across fiber types of a narrow set of molecular characteristics suitable to achieve a specific contractile phenotype. In this article we review evidence supporting the existence of distinct functional phenotypes in mitochondria from slow and fast fibers that may be required to ensure optimal muscle function. This includes differences with respect to energy substrate preferences, regulation of oxidative phosphorylation, dynamics of reactive oxygen species, handling of Ca 2ϩ , and regulation of cell death. The potential physiological implications on muscle function and the putative mechanisms responsible for establishing and maintaining distinct mitochondrial phenotype across fiber types are also discussed. mitochondria; reactive oxygen species; calcium retention capacity; oxidative capacity SKELETAL MUSCLE FIBERS are fantastic molecular and metabolic machines that have developed through evolution a large scope of contractile properties, ranging from slow contracting, lowpowered fibers designed for endurance, to fast contracting, high-powered fibers designed for short bursts of high-intensity work. Such a wide range of functional specialization has emerged through the selection across fiber types of optimal cytoarchitectural configurations, and expression of specific isoforms for most molecular components of myofibers including, among others, sarcomeres, excitation-contraction coupling machinery, and energy metabolism pathways. Importantly, in this process, evolution seems to have favored coadaptation whereby only a very narrow combination of molecular characteristics appear suitable to achieve a specific contractile phenotype (42).At the level of energy metabolism, one of the classical and distinctive features differentiating fiber types is mitochondrial volume density, slow twitch type I fibers typically displaying a two-to threefold higher mitochondrial density and substantially lower capacity for nonoxidative ATP synthesis compared with fast twitch type II fibers. While this difference in mitochondrial quantity was for a long time considered the main factor that varied substantially across fiber types, studies demonstrating the existence of fiber type-specific differences in mitochondrial respiratory properties, and in mechanisms coupling mitochondria to sites of ATP consumption, have progressively contributed to change this view.More recently, studies from our laboratory (79) and others (2) have shown that marked differences...

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