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First published online May 26, 2006
Journal of Experimental Biology 209, 2265-2275 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02182
Review Article: Phenotypic Plasticity in Skeletal Muscle |
Coordination of metabolic plasticity in skeletal muscle
1 School of Kinesiology and Health Science, York University, Toronto,
Ontario, M3J 1P3, Canada
2 Department of Biology, York University, Toronto, Ontario, M3J 1P3,
Canada
* Author for correspondence (e-mail: dhood{at}yorku.ca)
Accepted 21 February 2006
Summary
Skeletal muscle is a highly malleable tissue, capable of pronounced
metabolic and morphological adaptations in response to contractile activity
(i.e. exercise). Each bout of contractile activity results in a coordinated
alteration in the expression of a variety of nuclear DNA and mitochondrial DNA
(mtDNA) gene products, leading to phenotypic adaptations. This results in an
increase in muscle mitochondrial volume and changes in organelle composition,
referred to as mitochondrial biogenesis. The functional consequence of this
biogenesis is an improved resistance to fatigue. Signals initiated by the
exercise bout involve changes in intracellular Ca2+ as well as
alterations in energy status (i.e. ATP/ADP ratio) and the consequent
activation of downstream kinases such as AMP kinase and
Ca2+-calmodulin-activated kinases. These kinases activate
transcription factors that bind DNA to affect the transcription of genes, the
most evident manifestation of which occurs during the post-exercise recovery
period when energy metabolism is directed toward anabolism, rather than
contractile activity. An important protein that is affected by exercise is the
transcriptional coactivator PGC-1
, which cooperates with multiple
transcription factors to induce the expression of nuclear genes encoding
mitochondrial proteins. Once translated in the cytosol, these mitochondrially
destined proteins are imported into the mitochondrial outer membrane, inner
membrane or matrix space via specific import machinery transport
components. Contractile activity affects the expression of the import
machinery, as well as the kinetics of import, thus facilitating the entry of
newly synthesized proteins into the expanding organelle. An important set of
proteins that are imported are the mtDNA transcription factors, which
influence the expression and replication of mtDNA. While mtDNA contributes
only 13 proteins to the synthesis of the organelle, these proteins are vital
for the proper assembly of multi-subunit complexes of the respiratory chain,
when combined with nuclear-encoded protein subunits. The expansion of skeletal
muscle mitochondria during organelle biogenesis involves the assembly of an
interconnected network system (i.e. a mitochondrial reticulum). This expansion
of membrane size is influenced by the balance between mitochondrial fusion and
fission. Thus, mitochondrial biogenesis is an adaptive process that requires
the coordination of multiple cellular events, including the transcription of
two genomes, the synthesis of lipids and proteins and the stoichiometric
assembly of multisubunit protein complexes into a functional respiratory
chain. Impairments at any step can lead to defective electron transport, a
subsequent failure of ATP production and an inability to maintain energy
homeostasis.
Key words: mitochondrial biogenesis, transcription factors, reactive oxygen species, calcium signaling, mitochondrial protein import
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