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J Appl Physiol 90: 1137-1157, 2001;
8750-7587/01 $5.00
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Vol. 90, Issue 3, 1137-1157, March 2001

HIGHLIGHTED TOPICS
Plasticity in Skeletal, Cardiac, and Smooth Muscle
Invited Review: Contractile activity-induced mitochondrial biogenesis in skeletal muscle

David A. Hood

Department of Kinesiology and Health Science and Department of Biology, York University, Toronto, Ontario, Canada M3J 1P3

Chronic contractile activity produces mitochondrial biogenesis in muscle. This adaptation results in a significant shift in adenine nucleotide metabolism, with attendant improvements in fatigue resistance. The vast majority of mitochondrial proteins are derived from the nuclear genome, necessitating the transcription of genes, the translation of mRNA into protein, the targeting of the protein to a mitochondrial compartment via the import machinery, and the assembly of multisubunit enzyme complexes in the respiratory chain or matrix. Putative signals involved in initiating this pathway of gene expression in response to contractile activity likely arise from combinations of accelerations in ATP turnover or imbalances between mitochondrial ATP synthesis and cellular ATP demand, and Ca2+ fluxes. These rapid events are followed by the activation of exercise-responsive kinases, which phosphorylate proteins such as transcription factors, which subsequently bind to upstream regulatory regions in DNA, to alter transcription rates. Contractile activity increases the mRNA levels of nuclear-encoded proteins such as cytochrome c and mitochondrial transcription factor A (Tfam) and mRNA levels of upstream transcription factors like c-jun and nuclear respiratory factor-1 (NRF-1). mRNA level changes are often most evident during the postexercise recovery period, and they can occur as a result of contractile activity-induced increases in transcription or mRNA stability. Tfam is imported into mitochondria and controls the expression of mitochondrial DNA (mtDNA). mtDNA contributes only 13 protein products to the respiratory chain, but they are vital for electron transport and ATP synthesis. Contractile activity increases Tfam expression and accelerates its import into mitochondria, resulting in increased mtDNA transcription and replication. The result of this coordinated expression of the nuclear and the mitochondrial genomes, along with poorly understood changes in phospholipid synthesis, is an expansion of the muscle mitochondrial reticulum. Further understanding of 1) regulation of mtDNA expression, 2) upstream activators of NRF-1 and other transcription factors, 3) the identity of mRNA stabilizing proteins, and 4) potential of contractile activity-induced changes in apoptotic signals are warranted.

muscle gene expression; signal transduction; adaptation; exercise; mitochondrial DNA


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J. Mol. Endocrinol., October 1, 2004; 33(2): 533 - 544.
[Abstract] [Full Text] [PDF]

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V. Ljubicic, P. J. Adhihetty, and D. A. Hood
Role of UCP3 in state 4 respiration during contractile activity-induced mitochondrial biogenesis
J Appl Physiol, September 1, 2004; 97(3): 976 - 983.
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 Exp PhysiolHome page
C. M. Stary, O. Mathieu-Costello, and M. C. Hogan
Resistance to fatigue of individual Xenopus single skeletal muscle fibres is correlated with mitochondrial volume density
Exp Physiol, September 1, 2004; 89(5): 617 - 621.
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P. J. LeBlanc, S. J. Peters, R. J. Tunstall, D. Cameron-Smith, and G. J. F. Heigenhauser
Effects of aerobic training on pyruvate dehydrogenase and pyruvate dehydrogenase kinase in human skeletal muscle
J. Physiol., June 1, 2004; 557(2): 559 - 570.
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 Am. J. Physiol. Endocrinol. Metab.Home page
T. E. Sheehan, P. A. Kumar, and D. A. Hood
Tissue-specific regulation of cytochrome c oxidase subunit expression by thyroid hormone
Am J Physiol Endocrinol Metab, June 1, 2004; 286(6): E968 - E974.
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 Am. J. Physiol. Cell Physiol.Home page
D. Freyssenet, I. Irrcher, M. K. Connor, M. Di Carlo, and D. A. Hood
Calcium-regulated changes in mitochondrial phenotype in skeletal muscle cells
Am J Physiol Cell Physiol, May 1, 2004; 286(5): C1053 - C1061.
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 Am. J. Physiol. Endocrinol. Metab.Home page
S. Terada and I. Tabata
Effects of acute bouts of running and swimming exercise on PGC-1{alpha} protein expression in rat epitrochlearis and soleus muscle
Am J Physiol Endocrinol Metab, February 1, 2004; 286(2): E208 - E216.
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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
M. Lucassen, A. Schmidt, L. G. Eckerle, and H.-O. Portner
Mitochondrial proliferation in the permanent vs. temporary cold: enzyme activities and mRNA levels in Antarctic and temperate zoarcid fish
Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2003; 285(6): R1410 - R1420.
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 Am. J. Physiol. Endocrinol. Metab.Home page
A. L. Hildebrandt, H. Pilegaard, and P. D. Neufer
Differential transcriptional activation of select metabolic genes in response to variations in exercise intensity and duration
Am J Physiol Endocrinol Metab, November 1, 2003; 285(5): E1021 - E1027.
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 FASEB J.Home page
K. BAAR, Z. SONG, C. F. SEMENKOVICH, T. E. JONES, D.-H. HAN, L. A. NOLTE, E. O. OJUKA, M. CHEN, and J. O. HOLLOSZY
Skeletal muscle overexpression of nuclear respiratory factor 1 increases glucose transport capacity
FASEB J, September 1, 2003; 17(12): 1666 - 1673.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
C. R. Bruce, A. L. Carey, J. A. Hawley, and M. A. Febbraio
Intramuscular Heat Shock Protein 72 and Heme Oxygenase-1 mRNA Are Reduced in Patients With Type 2 Diabetes: Evidence That Insulin Resistance Is Associated With a Disturbed Antioxidant Defense Mechanism
Diabetes, September 1, 2003; 52(9): 2338 - 2345.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
C. Handschin, J. Rhee, J. Lin, P. T. Tarr, and B. M. Spiegelman
An autoregulatory loop controls peroxisome proliferator-activated receptor {gamma} coactivator 1{alpha} expression in muscle
PNAS, June 10, 2003; 100(12): 7111 - 7116.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
I. Irrcher, P. J. Adhihetty, T. Sheehan, A.-M. Joseph, and D. A. Hood
PPARgamma coactivator-1alpha expression during thyroid hormone- and contractile activity-induced mitochondrial adaptations
Am J Physiol Cell Physiol, June 1, 2003; 284(6): C1669 - C1677.
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S. Welle, K. Bhatt, B. Shah, N. Needler, J. M. Delehanty, and C. A. Thornton
Reduced amount of mitochondrial DNA in aged human muscle
J Appl Physiol, April 1, 2003; 94(4): 1479 - 1484.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
S. L. McGee, K. F. Howlett, R. L. Starkie, D. Cameron-Smith, B. E. Kemp, and M. Hargreaves
Exercise Increases Nuclear AMPK {alpha}2 in Human Skeletal Muscle
Diabetes, April 1, 2003; 52(4): 926 - 928.
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 J. Physiol.Home page
H. Pilegaard, B. Saltin, and P D. Neufer
Exercise induces transient transcriptional activation of the PGC-1{alpha} gene in human skeletal muscle
J. Physiol., February 1, 2003; 546(3): 851 - 858.
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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
B. Drew, S. Phaneuf, A. Dirks, C. Selman, R. Gredilla, A. Lezza, G. Barja, and C. Leeuwenburgh
Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart
Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2003; 284(2): R474 - R480.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
H. Zong, J. M. Ren, L. H. Young, M. Pypaert, J. Mu, M. J. Birnbaum, and G. I. Shulman
AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation
PNAS, December 10, 2002; 99(25): 15983 - 15987.
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 FASEB J.Home page
K. BAAR, A. R. WENDE, T. E. JONES, M. MARISON, L. A. NOLTE, M. CHEN, D. P. KELLY, and J. O. HOLLOSZY
Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1
FASEB J, December 1, 2002; 16(14): 1879 - 1886.
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M. A Febbraio, P. Ott, H. B. Nielsen, A. Steensberg, C. Keller, P. Krustrup, N. H Secher, and B. K. Pedersen
Exercise induces hepatosplanchnic release of heat shock protein 72 in humans
J. Physiol., November 1, 2002; 544(3): 957 - 962.
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 Am. J. Physiol. Endocrinol. Metab.Home page
B. F. Miller, J. A. Fattor, K. A. Jacobs, M. A. Horning, S.-H. Suh, F. Navazio, and G. A. Brooks
Metabolic and cardiorespiratory responses to "the lactate clamp"
Am J Physiol Endocrinol Metab, November 1, 2002; 283(5): E889 - E898.
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F. W Booth, M. V Chakravarthy, and E. E Spangenburg
Exercise and gene expression: physiological regulation of the human genome through physical activity
J. Physiol., September 1, 2002; 543(2): 399 - 411.
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J Zoll, H Sanchez, B N'Guessan, F Ribera, E Lampert, X Bigard, B Serrurier, D Fortin, B Geny, V Veksler, et al.
Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle
J. Physiol., August 15, 2002; 543(1): 191 - 200.
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H. Hoppeler and M. Fluck
Normal mammalian skeletal muscle and its phenotypic plasticity
J. Exp. Biol., August 1, 2002; 205(15): 2143 - 2152.
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 J. Appl. Physiol.Home page
F. W. Booth, M. V. Chakravarthy, S. E. Gordon, and E. E. Spangenburg
Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy
J Appl Physiol, July 1, 2002; 93(1): 3 - 30.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
R. J. Tunstall, K. A. Mehan, G. D. Wadley, G. R. Collier, A. Bonen, M. Hargreaves, and D. Cameron-Smith
Exercise training increases lipid metabolism gene expression in human skeletal muscle
Am J Physiol Endocrinol Metab, July 1, 2002; 283(1): E66 - E72.
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 J. Physiol.Home page
K. Sahlin, M. Fernstrom, M. Svensson, and M. Tonkonogi
No evidence of an intracellular lactate shuttle in rat skeletal muscle
J. Physiol., June 1, 2002; 541(2): 569 - 574.
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 ScienceHome page
H. Wu, S. B. Kanatous, F. A. Thurmond, T. Gallardo, E. Isotani, R. Bassel-Duby, and R. S. Williams
Regulation of Mitochondrial Biogenesis in Skeletal Muscle by CaMK
Science, April 12, 2002; 296(5566): 349 - 352.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
S. Duguez, L. Feasson, C. Denis, and D. Freyssenet
Mitochondrial biogenesis during skeletal muscle regeneration
Am J Physiol Endocrinol Metab, April 1, 2002; 282(4): E802 - E809.
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M. A Febbraio, A. Steensberg, R. Walsh, I. Koukoulas, G. van Hall, B. Saltin, and B. K. Pedersen
Reduced glycogen availability is associated with an elevation in HSP72 in contracting human skeletal muscle
J. Physiol., February 1, 2002; 538(3): 911 - 917.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
W. W. Winder
Energy-sensing and signaling by AMP-activated protein kinase in skeletal muscle
J Appl Physiol, September 1, 2001; 91(3): 1017 - 1028.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
G. B. McClelland and G. A. Brooks
Changes in MCT 1, MCT 4, and LDH expression are tissue specific in rats after long-term hypobaric hypoxia
J Appl Physiol, April 1, 2002; 92(4): 1573 - 1584.
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M. K. Connor, I. Irrcher, and D. A. Hood
Contractile Activity-induced Transcriptional Activation of Cytochrome c Involves Sp1 and Is Proportional to Mitochondrial ATP Synthesis in C2C12 Muscle Cells
J. Biol. Chem., May 4, 2001; 276(19): 15898 - 15904.
[Abstract] [Full Text] [PDF]


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