Cookies Notification

We use cookies to improve your website experience. To learn about our use of cookies and how you can manage your cookie settings, please see our Cookie Policy.
×

Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle

Publication: Applied Physiology, Nutrition, and Metabolism
12 May 2009

Abstract

Acute exercise initiates rapid cellular signals, leading to the subsequent activation of proteins that increase gene transcription. The result is a higher level of mRNA expression, often observed during the recovery period following exercise. These molecules are translated into precursor proteins for import into preexisting mitochondria. Once inside the organelle, the protein is processed to its mature form and either activates mitochondrial DNA gene expression, serves as a single subunit enzyme, or is incorporated into multi-subunit complexes of the respiratory chain devoted to electron transport and substrate oxidation. The result of this exercise-induced sequence of events is the expansion of the mitochondrial network within muscle cells and the capacity for aerobic ATP provision. An understanding of the molecular processes involved in this complex pathway of organelle synthesis is important for therapeutic purposes, and is a primary research undertaking in laboratories involved in the study of mitochondrial biogenesis. This pathway in muscle becomes impaired with chronic inactivity and aging, which leads to a reduced muscle aerobic capacity and an increased tendency for mitochondrially mediated apoptosis, a situation that can contribute to muscle atrophy. The resumption, or adoption, of an active lifestyle can ameliorate this metabolic dysfunction, improve endurance, and help maintain muscle mass.

Résumé

Une séance d’exercice déclenche une série rapide de signaux cellulaires aboutissant à l’activation de protéines, ce qui accroît la transcription génique. Il s’ensuit un plus haut degré d’expression d’ARNm, souvent observée au cours de la récupération consécutive à un exercice physique. Ces molécules donnent lieu à des précurseurs protéiques à importer dans la mitochondrie déjà en place. Une fois à l’intérieur de l’organelle, la protéine évolue jusqu’à maturité et stimule l’expression d’un gène dans la mitochondrie ou sert de simple module enzymatique ou est intégré dans un complexe multimodulaire de la chaîne respiratoire dédiée au transport d’électrons et à l’oxydation des substrats. Le résultat de cette séquence d’événements déclenchée par l’exercice physique contribue à augmenter le réseau mitochondrial dans la cellule musculaire et à accroître la production aérobie d’ATP. La compréhension des processus moléculaires impliqués dans la voie complexe de la synthèse d’un organelle est importante au plan thérapeutique et doit faire l’objet d’études fondamentales dans les laboratoires consacrés à l’étude de la biogenèse des mitochondries. Cette voie est entravée par l’inactivité chronique et le vieillissement ce qui entraîne une diminution de la capacité aérobie du muscle et une augmentation de la tendance à l’apoptose médiée par la mitochondrie, d’où la possibilité d’atrophie musculaire. L’adoption ou le retour à un mode de vie actif peut contribuer à contrer cette dysfonction métabolique, à améliorer l’endurance et à maintenir la masse musculaire.

Get full access to this article

View all available purchase options and get full access to this article.

References

Adhihetty, P.J., Ljubicic, V., Menzies, K.J., and Hood, D.A. 2005. Differential susceptibility of subsarcolemmal and intermyofibrillar mitochondria to apoptotic stimuli. Am. J. Physiol. Cell Physiol. 289: C994–C1001.
Adhihetty, P.J., Ljubicic, V., and Hood, D.A. 2007. Effect of chronic contractile activity on SS and IMF mitochondrial apoptotic susceptibility in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 292: E748–E755.
Akimoto, T., Sorg, B.S., and Yan, Z. 2004. Real-time imaging of peroxisome proliferator-activated receptor-gamma coactivator-1alpha promoter activity in skeletal muscles of living mice. Am. J. Physiol. Cell Physiol. 287: C790–C796.
Akimoto, T., Pohnert, S.C., Li, P., Zhang, M., Gumbs, C., Rosenberg, P.B., et al. 2005. Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J. Biol. Chem. 280: 19587–19593.
Ames, B.N., Shigenaga, M.K., and Hagen, T.M. 1993. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U.S.A. 90: 7915–7922.
Arany, Z. 2008. PGC-1 coactivators and skeletal muscle adaptations in health and disease. Curr. Opin. Genet. Dev. 18: 426–434.
Baar, K., Wende, A.R., Jones, T.E., Marison, M., Nolte, L.A., Chen, M., et al. 2002. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J. 16: 1879–1886.
Babij, P., and Booth, F.W. 1988. Alpha-actin and cytochrome c mRNAs in atrophied adult rat skeletal muscle. Am. J. Physiol. 254: C651–C656.
Bengtsson, J., Gustafsson, T., Widegren, U., Jansson, E., and Sundberg, C.J. 2001. Mitochondrial transcription factor A and respiratory complex IV increase in response to exercise training in humans. Pflugers Arch. 443: 61–66.
Bolender, N., Sickmann, A., Wagner, R., Meisinger, C., and Pfanner, N. 2008. Multiple pathways for sorting mitochondrial precursor proteins. EMBO Rep. 9: 42–49.
Brierley, E.J., Johnson, M.A., James, O.F., and Turnbull, D.M. 1996. Effects of physical activity and age on mitochondrial function. Q. J. Med. 89: 251–258.
Bua, E.A., McKiernan, S.H., Wanagat, J., McKenzie, D., and Aiken, J.M. 2002. Mitochondrial abnormalities are more frequent in muscles undergoing sarcopenia. J. Appl. Physiol. 92: 2617–2624.
Calvo, J.A., Daniels, T.G., Wang, X., Paul, A., Lin, J., Spiegelman, B.M., et al. 2008. Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J. Appl. Physiol. 104: 1304–1312.
Chabi, B., Adhihetty, P.J., Ljubicic, V., and Hood, D.A. 2005. How is mitochondrial biogenesis affected in mitochondrial disease? Med. Sci. Sports Exerc. 37: 2102–2110.
Chabi, B., Ljubicic, V., Menzies, K.J., Huang, J.H., Saleem, A., and Hood, D.A. 2008. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell, 7: 2–12.
Coggan, A.R., Spina, R.J., King, D.S., Rogers, M.A., Brown, M., Nemeth, P.M., and Holloszy, J.O. 1992. Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J. Appl. Physiol. 72: 1780–1786.
Conley, K.E., Marcinek, D.J., and Villarin, J. 2007. Mitochondrial dysfunction and age. Curr. Opin. Clin. Nutr. Metab. Care. 10: 688–692.
Gordon, J.W., Rungi, A.A., Inagaki, H., and Hood, D.A. 2001. Effects of contractile activity on mitochondrial transcription factor A expression in skeletal muscle. J. Appl. Physiol. 90: 389–396.
Handschin, C., Rhee, J., Lin, J., Tarr, P.T., and Spiegelman, B.M. 2003. An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc. Natl. Acad. Sci. U.S.A. 100: 7111–7116.
Hood, D.A., Irrcher, I., Ljubicic, V., and Joseph, A.M. 2006. Coordination of metabolic plasticity in skeletal muscle. J. Exp. Biol. 209: 2265–2275.
Huang, J.H., and Hood, D.A. 2009. Age-associated mitochondrial dysfunction in skeletal muscle: contributing factors and suggestions for long-term interventions. IUBMB Life. 61: 201–214.
Irrcher, I., Adhihetty, P.J., Sheehan, T., Joseph, A.M., and Hood, D.A. 2003. PPARgamma coactivator-1alpha expression during thyroid hormone- and contractile activity-induced mitochondrial adaptations. Am. J. Physiol. Cell Physiol. 284: C1669–C1677.
Irrcher, I., Ljubicic, V., Kirwan, A.F., and Hood, D.A. 2008. AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells. PLoS One. 3: e3614.
Irrcher, I., Ljubicic, V., and Hood, D.A. 2009. Interactions between ROS and AMP kinase activity in the regulation of PGC-1alpha transcription in skeletal muscle cells. Am. J. Physiol. Cell Physiol. 296: C116–C123.
Judge, S., Jang, Y.M., Smith, A., Selman, C., Phillips, T., Speakman, J.R., et al. 2005. Exercise by lifelong voluntary wheel running reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289: R1564–R1572.
Kent-Braun, J.A. 2009. Skeletal muscle fatigue in old age: whose advantage? Exerc. Sport Sci. Rev. 37: 3–9.
Koulmann, N., and Bigard, A.X. 2006. Interaction between signalling pathways involved in skeletal muscle responses to endurance exercise. Pflugers Arch. 452: 125–139.
Krieger, D.A., Tate, C.A., Millin-Wood, J., and Booth, F.W. 1980. Populations of rat skeletal muscle mitochondria after exercise and immobilization. J. Appl. Physiol. 48: 23–28.
Larsson, N.G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., Lewandoski, M., et al. 1998. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 18: 231–236.
Leick, L., Wojtaszewski, J.F., Johansen, S.T., Kiilerich, K., Comes, G., Hellsten, Y., et al. 2008. PGC-1alpha is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 294: E463–E474.
Leone, T.C., Lehman, J.J., Finck, B.N., Schaeffer, P.J., Wende, A.R., Boudina, S., et al. 2005. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3: e101.
Lin, J., Wu, H., Tarr, P.T., Zhang, C.Y., Wu, Z., Boss, O., et al. 2002. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature. 418: 797–801.
Lin, J., Handschin, C., and Spiegelman, B.M. 2005. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1: 361–370.
Ljubicic, V., and Hood, D.A. 2008. Kinase-specific responsiveness to incremental contractile activity in skeletal muscle with low and high mitochondrial content. Am. J. Physiol. Endocrinol. Metab. 295: E195–E204.
McArdle, A., van der Meulen, J., Close, G.L., Pattwell, D., Van Remmen, H., Huang, T.T., et al. 2004. Role of mitochondrial superoxide dismutase in contraction-induced generation of reactive oxygen species in skeletal muscle extracellular space. Am. J. Physiol. Cell Physiol. 286: C1152–C1158.
Neupert, W., and Herrmann, J.M. 2007. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76: 723–749.
Norrbom, J., Sundberg, C.J., Ameln, H., Kraus, W.E., Jansson, E., and Gustafsson, T. 2004. PGC-1alpha mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. J. Appl. Physiol. 96: 189–194.
Orlander, J., and Aniansson, A. 1980. Effect of physical training on skeletal muscle metabolism and ultrastructure in 70 to 75-year-old men. Acta Physiol. Scand. 109: 149–154.
Pattwell, D.M., McArdle, A., Morgan, J.E., Patridge, T.A., and Jackson, M.J. 2004. Release of reactive oxygen and nitrogen species from contracting skeletal muscle cells. Free Radic. Biol. Med. 37: 1064–1072.
Pesce, V., Cormio, A., Fracasso, F., Lezza, A.M., Cantatore, P., and Gadaleta, M.N. 2005. Age-related changes of mitochondrial DNA content and mitochondrial genotypic and phenotypic alterations in rat hind-limb skeletal muscles. J. Gerontol. A Biol. Sci. Med. Sci. 60: 715–723.
Pilegaard, H., Saltin, B., and Neufer, P.D. 2003. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J. Physiol. 546: 851–858.
Radak, Z., Naito, H., Kaneko, T., Tahara, S., Nakamoto, H., Takahashi, R., et al. 2002. Exercise training decreases DNA damage and increases DNA repair and resistance against oxidative stress of proteins in aged rat skeletal muscle. Pflugers Arch. 445: 273–278.
Rifenberick, D.H., Gamble, J.G., and Max, S.R. 1973. Response of mitochondrial enzymes to decreased muscular activity. Am. J. Physiol. 225: 1295–1299.
Rodgers, J.T., Lerin, C., Haas, W., Gygi, S.P., Spiegelman, B.M., and Puigserver, P. 2005. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature. 434: 113–118.
Sakamoto, K., and Goodyear, L.J. 2002. Invited review: intracellular signaling in contracting skeletal muscle. J. Appl. Physiol. 93: 369–383.
Saleem, A., Adhihetty, P.J., and Hood, D.A. 2009. Role of p53 in mitochondrial biogenesis and apoptosis in skeletal muscle. Physiol. Genomics. 37: 58–66.
Short, K.R., Vittone, J.L., Bigelow, M.L., Proctor, D.N., Rizza, R.A., Coenen-Schimke, J.M., and Nair, K.S. 2003. Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes. 52: 1888–1896.
Stephens, T.J., Chen, Z.P., Canny, B.J., Michell, B.J., Kemp, B.E., and McConell, G.K. 2002. Progressive increase in human skeletal muscle AMPKalpha2 activity and ACC phosphorylation during exercise. Am. J. Physiol. Endocrinol. Metab. 282: E688–E694.
Suliman, H.B., Carraway, M.S., Welty-Wolf, K.E., Whorton, A.R., and Piantadosi, C.A. 2003. Lipopolysaccharide stimulates mitochondrial biogenesis via activation of nuclear respiratory factor-1. J. Biol. Chem. 278: 41510–41518.
Taivassalo, T., Shoubridge, E.A., Chen, J., Kennaway, N.G., DiMauro, S., Arnold, D.L., and Haller, R.G. 2001. Aerobic conditioning in patients with mitochondrial myopathies: physiological, biochemical, and genetic effects. Ann. Neurol. 50: 133–141.
Takahashi, M., Chesley, A., Freyssenet, D., and Hood, D.A. 1998. Contractile activity-induced adaptations in the mitochondrial protein import system. Am. J. Physiol. 274: C1380–C1387.
Taylor, E.B., Lamb, J.D., Hurst, R.W., Chesser, D.G., Ellingson, W.J., Greenwood, L.J., et al. 2005. Endurance training increases skeletal muscle LKB1 and PGC-1alpha protein abundance: effects of time and intensity. Am. J. Physiol. Endocrinol. Metab. 289: E960–E968.
Wicks, K.L., and Hood, D.A. 1991. Mitochondrial adaptations in denervated muscle: relationship to muscle performance. Am. J. Physiol. 260: C841–C850.
Winder, W.W., Holmes, B.F., Rubink, D.S., Jensen, E.B., Chen, M., and Holloszy, J.O. 2000. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol. 88: 2219–2226.
Yan, Z., Li, P., and Akimoto, T. 2007. Transcriptional control of the Pgc-1alpha gene in skeletal muscle in vivo. Exerc. Sport Sci. Rev. 35: 97–101.
Zong, H., Ren, J.M., Young, L.H., Pypaert, M., Mu, J., Birnbaum, M.J., and Shulman, G.I. 2002. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc. Natl. Acad. Sci. U.S.A. 99: 15983–15987.

Information & Authors

Information

Published In

cover image Applied Physiology, Nutrition, and Metabolism
Applied Physiology, Nutrition, and Metabolism
Volume 34Number 3June 2009
Pages: 465 - 472

History

Received: 10 March 2009
Accepted: 10 March 2009
Version of record online: 12 May 2009

Notes

This paper is one of a selection of papers published in this Special Issue, entitled 14th International Biochemistry of Exercise Conference – Muscles as Molecular and Metabolic Machines, and has undergone the Journal’s usual peer review process.

Permissions

Request permissions for this article.

Key Words

  1. PGC-1α
  2. mitochondrial transcription factor A
  3. reactive oxygen species
  4. AMP kinase
  5. aging
  6. muscle disuse

Mots-clés

  1. PGC-1α
  2. facteur A de transcription mitochondriale
  3. espèces oxygénées radicalaires
  4. AMP kinase
  5. vieillissement
  6. inactivité musculaire

Authors

Affiliations

School of Kinesiology and Health Science, and Muscle Health Research Centre, York University, Rm. 302, Farquharson Life Science Bldg, 4700 Keele Street, Toronto, ON M3J 1P3, Canada (e-mail: (email: [email protected])).

Metrics & Citations

Metrics

Other Metrics

Citations

Cite As

Export Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

1. Advancing cancer cachexia diagnosis with -omics technology and exercise as molecular medicine
2. Morphological, radiographic, three-dimensional computed tomographic, and histological features of the primary upstroke and downstroke muscles and bones in the domestic duck (Anas platyrhynchos domesticus) and the cattle egret (Bubulcus ibis, Linnaeus, 1758), reflecting the evolutionary transition towards the irreversible flightlessness
3. Mouse skeletal muscle adaptations to different durations of treadmill exercise after the cessation of FOLFOX chemotherapy
4. THE EFFECT OF HIGH-INTENSITY INTERVAL TRAINING WITH SODIUM CITRATE ON THE EXPRESSION OF PGC-1Α AND NRF2 IN SOLEUS MUSCLE OF RATS
5. Exercise, mitochondrial dysfunction and inflammasomes in skeletal muscle
6. Changes in mitochondrial function parallel life history transitions between flight and reproduction in wing polymorphic field crickets
7. A Scoping Review Investigating the “Gene-Dosage Theory” of Mitochondrial DNA in the Healthy Skeletal Muscle
8. The COVID ‐19 vaccine did not affect the basal immune response and menstruation in female athletes
9. Molekulare Anpassungen an kombiniertes Ausdauer- und Krafttraining
10. Structural functionality of skeletal muscle mitochondria and its correlation with metabolic diseases
11. Differential Effects of Amount, Intensity, and Mode of Exercise Training on Insulin Sensitivity and Glucose Homeostasis: A Narrative Review
12. The Effect of a 12 Week Mixed-Modality Training Intervention on the Cardio-Metabolic Health of Rotational Shift Workers
13. Is there a mitochondrial DNA haplogroup connection between osteoarthritis and elite athletes? A narrative review
14. Localized Heat Therapy Improves Mitochondrial Respiratory Capacity but Not Fatty Acid Oxidation
15. The Role of Exercise Training in Delaying Kidney Function Decline in Non-Dialysis-Dependent Chronic Kidney Disease
16. Time course and fibre type‐dependent nature of calcium‐handling protein responses to sprint interval exercise in human skeletal muscle
17. Conserved and convergent mechanisms underlying performance–life-history trade-offs
18. Skeletal muscle metabolic responses to physical activity are muscle type specific in a rat model of chronic kidney disease
19. Exercise improves vascular health: Role of mitochondria
20. Oxidative Stress, Mitochondrial Function and Adaptation to Exercise: New Perspectives in Nutrition
21. The Impact of Vegan and Vegetarian Diets on Physical Performance and Molecular Signaling in Skeletal Muscle
22. Changes in foraging mode caused by a decline in prey size have major bioenergetic consequences for a small pelagic fish
23. Aerobic Exercise Induces Alternative Splicing of Neurexins in Frontal Cortex
24. Running and Swimming Differently Adapt the BDNF/TrkB Pathway to a Slow Molecular Pattern at the NMJ
25. Blood‐flow‐restricted exercise: Strategies for enhancing muscle adaptation and performance in the endurance‐trained athlete
26. Effect of the protein hydrolysate of rice syrup meal on the endurance exercise performance of BALB/c mice
27. Exercise and mitochondrial health
28. Mitochondrial biogenesis and mitophagy
29. Linking mitochondrial dysfunction to sarcopenia
30. β2-Adrenergic Signaling Modulates Mitochondrial Function and Morphology in Skeletal Muscle in Response to Aerobic Exercise
31. Effects of concomitant use of hydrogen water and photobiomodulation on Parkinson disease
32. An Examination and Critique of Current Methods to Determine Exercise Intensity
33. Association between muscle aerobic capacity and whole-body peak oxygen uptake
34. Acute and chronic effects of resistance training on skeletal muscle markers of mitochondrial remodeling in older adults
35. Exercise and High-Fat Diet in Obesity: Functional Genomics Perspectives of Two Energy Homeostasis Pillars
36. Protective effects of endurance exercise on skeletal muscle remodeling against doxorubicin-induced myotoxicity in mice
37. Acute hypertrophic but not maximal strength loading transiently enhances the kynurenine pathway towards kynurenic acid
38. Androgenic modulation of extraordinary muscle speed creates a performance trade-off with endurance
39. The Role of Nutri(epi)genomics in Achieving the Body’s Full Potential in Physical Activity
40. Exercise training protects the heart against ischemia-reperfusion injury: A central role for mitochondria?
41. Skeletal-Muscle Metabolic Reprogramming in ALS-SOD1G93A Mice Predates Disease Onset and Is A Promising Therapeutic Target
42. Inter-Day Reliability and Changes of Surface Electromyography on Two Postural Muscles Throughout 12 Weeks of Hippotherapy on Patients with Cerebral Palsy: A Pilot Study
43. What is effective, may be effective, and is not effective for improvement of biochemical markers on muscle damage and inflammation, and muscle recovery? A Systematic Review of PubMed’s Database
44. Forty high-intensity interval training sessions blunt exercise-induced changes in the nuclear protein content of PGC-1α and p53 in human skeletal muscle
45. Metabolic Syndrome, Hormones, and Exercise
46.
47. Mitophagy Regulation in Skeletal Muscle: Effect of Endurance Exercise and Age
48. The Effect of either Aerobic Exercise Training or Chrysin Supplementation on Mitochondrial Biogenesis in Skeletal Muscle of High Fat Diet-Induced Obese Mice
49. Mechanisms of exercise‐induced survival motor neuron expression in the skeletal muscle of spinal muscular atrophy‐like mice
50. Effects of Treadmill Training on Muscle Oxidative Capacity and Endurance in People with Multiple Sclerosis with Significant Walking Limitations
51. N-acetyl-L-cysteine Prevents Lactate-Mediated PGC1-alpha Expression in C2C12 Myotubes
52. Skeletal muscle excitation-metabolism coupling
53. Changes in Redox Signaling in the Skeletal Muscle with Aging
54. Molecular Adaptations to Concurrent Strength and Endurance Training
55. Biochemie: Grundlage Ihrer Gesundheit und Leistungsfähigkeit
56. The Evolving Concept of Mitochondrial Dynamics in Heart: Interventional Opportunities
57. Antioxidants and Polyphenols Mediate Mitochondrial Mediated Muscle Death Signaling in Sarcopenia
58. Impact of Lifestyle and Clinical Interventions on Mitochondrial Function in Obesity and Type 2 Diabetes
59. The Evolution of Skeletal Muscle Plasticity in Response to Physical Activity and Inactivity
60. Comparative studies on the effects of high-fat diet, endurance training and obesity on Ucp1 expression in male C57BL/6 mice
61. Sarcopenic obesity in older adults: aetiology, epidemiology and treatment strategies
62. Training-Induced Changes in Mitochondrial Content and Respiratory Function in Human Skeletal Muscle
63. Principles of Exercise Prescription, and How They Influence Exercise-Induced Changes of Transcription Factors and Other Regulators of Mitochondrial Biogenesis
64. Protein Availability and Satellite Cell Dynamics in Skeletal Muscle
65. Myoblast mitochondrial respiration is decreased in chronic binge alcohol administered simian immunodeficiency virus-infected antiretroviral-treated rhesus macaques
66. Mimicking exercise in three‐dimensional bioengineered skeletal muscle to investigate cellular and molecular mechanisms of physiological adaptation
67. Low-fat diet, and medium-fat diets containing coconut oil and soybean oil exert different metabolic effects in untrained and treadmill-trained mice
68. Dynapenia: Term, causes and consequences
69. Submaximal exercise training improves mitochondrial efficiency in the gluteus medius but not in the triceps brachii of young equine athletes
70. Mitochondrial Abnormality Facilitates Cyst Formation in Autosomal Dominant Polycystic Kidney Disease
71. The Role of gp130 in Basal and Exercise Trained Skeletal Muscle Mitochondrial Quality Control
72. The role of androgens in the regulation of muscle oxidative capacity following aerobic exercise training
73. The effects of exercise and cold exposure on mitochondrial biogenesis in skeletal muscle and white adipose tissue
74. PPARβ Is Essential for Maintaining Normal Levels of PGC-1α and Mitochondria and for the Increase in Muscle Mitochondria Induced by Exercise
75. Concurrent exercise training: do opposites distract?
76. Mitochondria Initiate and Regulate Sarcopenia
77. Nutrition and Training Influences on the Regulation of Mitochondrial Adenosine Diphosphate Sensitivity and Bioenergetics
78. Mitochondrial Adaptations in Aged Skeletal Muscle: Effect of Exercise Training
79. Exercise-Induced Mitochondrial Adaptations in Addressing Heart Failure
80. Changes in Myofibrillar and Mitochondrial Compartments during Increased Activity: Dependance from Oxidative Capacity of Muscle
81. Role of metabolic stress for enhancing muscle adaptations: Practical applications
82. Physical exercise during muscle regeneration improves recovery of the slow/oxidative phenotype
83. Hyperinsulinemia and Insulin Resistance: Scope of the Problem
84. Resveratrol primes the effects of physical activity in old mice
85. Muscle fiber type diversification during exercise and regeneration
86. Function of specialized regulatory proteins and signaling pathways in exercise-induced muscle mitochondrial biogenesis
87. Conjugated linoleic acid (CLA) influences muscle metabolism via stimulating mitochondrial biogenesis signaling in adult‐onset inactivity induced obese mice
88. NOX2 Inhibition Impairs Early Muscle Gene Expression Induced by a Single Exercise Bout
89. Intense Resistance Exercise Promotes the Acute and Transient Nuclear Translocation of Small Ubiquitin-Related Modifier (SUMO)-1 in Human Myofibres
90. Social Inequalities and the Road to Allostatic Load: From Vulnerability to Resilience
91. Training intensity modulates changes in PGC‐1α and p53 protein content and mitochondrial respiration, but not markers of mitochondrial content in human skeletal muscle
92. AMPK agonist AICAR delays the initial decline in lifetime-apex V̇ o2 peak , while voluntary wheel running fails to delay its initial decline in female rats
93. Citrus flavonoid, naringenin, increases locomotor activity and reduces diacylglycerol accumulation in skeletal muscle of obese ovariectomized mice
94. Influence of exercise training with resveratrol supplementation on skeletal muscle mitochondrial capacity
95. Effects of skeletal muscle energy availability on protein turnover responses to exercise
96. Skeletal muscle mass and composition during mammalian hibernation
97. Effects of Postweaning Administration of Conjugated Linoleic Acid on Development of Obesity in Nescient Basic Helix–Loop–Helix 2 Knockout Mice
98. iTRAQ-based quantitative proteomic analysis of longissimus muscle from growing pigs with dietary supplementation of non-starch polysaccharide enzymes
99. Role of PGC-1α during acute exercise-induced autophagy and mitophagy in skeletal muscle
100. Exercise improves mitochondrial and redox-regulated stress responses in the elderly: better late than never!
101. The Role of Oxidative, Inflammatory and Neuroendocrinological Systems During Exercise Stress in Athletes: Implications of Antioxidant Supplementation on Physiological Adaptation During Intensified Physical Training
102. Conjugated Linoleic Acid (CLA) Stimulates Mitochondrial Biogenesis Signaling by the Upregulation of PPARγ Coactivator 1α (PGC‐1α) in C2C12 Cells
103. Perivascular adipose tissue and vascular responses in healthy trained rats
104. Altering the redox state of skeletal muscle by glutathione depletion increases the exercise-activation of PGC-1 α
105. Effect of endurance training on skeletal muscle myokine expression in obese men: identification of apelin as a novel myokine
106. Mitochondrial function in metabolic health: A genetic and environmental tug of war
107. Vitamin C and Physical Performance in the Elderly
108. Effect of near-infrared light exposure on mitochondrial signaling in C2C12 muscle cells
109. Activity-Induced Changes in Skeletal Muscle Metabolism Measured with Optical Spectroscopy
110. Exercise training increases the expression and nuclear localization of mRNA destabilizing proteins in skeletal muscle
111. Oxygen control of intracellular distribution of mitochondria in muscle fibers
112. Mammalian target of rapamycin pathway is up-regulated by both acute endurance exercise and chronic muscle contraction in rat skeletal muscle
113. Protein ingestion does not impair exercise-induced AMPK signalling when in a glycogen-depleted state: implications for train-low compete-high
114. Endurance training ameliorates the metabolic and performance characteristics of circadian Clock mutant mice
115. Skeletal Muscle Function during Exercise—Fine-Tuning of Diverse Subsystems by Nitric Oxide
116. Bone Remodeling and Energy Metabolism: New Perspectives
117. Mitochondrial morphology transitions and functions: implications for retrograde signaling?
118. The rs12594956 polymorphism in the NRF-2 gene is associated with top-level Spanish athlete's performance status
119. Co-ingestion of carbohydrate and whey protein isolates enhance PGC-1α mRNA expression: a randomised, single blind, cross over study
120. The impact of antioxidant supplements and endurance exercise on genes of the carbohydrate and lipid metabolism in skeletal muscle of mice
121. Muscle damage and regeneration: Response to exercise training
122. Adaptation of Cardiac and Skeletal Muscle Mitochondria to Endurance Training: Implications for Cardiac Protection
123. Muscle weakness in the elderly: role of sarcopenia, dynapenia, and possibilities for rehabilitation
124. Exercise Training and Peripheral Arterial Disease
125. Denervation-induced mitochondrial dysfunction and autophagy in skeletal muscle of apoptosis-deficient animals
126. Exercise tames the wild side of the Myc network: a hypothesis
127. Mild mitochondrial uncoupling does not affect mitochondrial biogenesis but downregulates pyruvate carboxylase in adipocytes: role for triglyceride content reduction
128. Early Exercise Affects Mitochondrial Transcription Factors Expression after Cerebral Ischemia in Rats
129. Mitochondrial Abnormalities in Alzheimer’s Disease
130. Antioxidant Supplementation Reduces Skeletal Muscle Mitochondrial Biogenesis
131. Role of Exercise Therapy in Prevention of Decline in Aging Muscle Function: Glucocorticoid Myopathy and Unloading
132. Impact of exercise on mitochondrial transcription factor expression and damage in the striatum of a chronic mouse model of Parkinson's disease
133. Skeletal muscle apoptotic response to physical activity: potential mechanisms for protection
134. Energy metabolism, proteotoxic stress and age-related dysfunction – Protection by carnosine
135. Regulation of glucose metabolism and the skeleton
136. The champions' mitochondria: is it genetically determined? A review on mitochondrial DNA and elite athletic performance
137. Molecular Mechanisms of Muscle Plasticity with Exercise
138. An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1α and activates mitochondrial biogenesis in human skeletal muscle
139. Antioxidant Supplementation Reduces Skeletal Muscle Mitochondrial Biogenesis
140. Mitochondrial dynamic remodeling in strenuous exercise-induced muscle and mitochondrial dysfunction: Regulatory effects of hydroxytyrosol
141. Regulation of Mitochondrial Biogenesis and GLUT4 Expression by Exercise
142. Striated muscle activator of Rho signalling (STARS) is a PGC‐1α/oestrogen‐related receptor‐α target gene and is upregulated in human skeletal muscle after endurance exercise
143. Aging and Apoptosis in Muscle
144. Energy metabolism in amyotrophic lateral sclerosis
145. Mitochondrial biogenesis related endurance genotype score and sports performance in athletes
146. Effects of a 300 mT static magnetic field on human umbilical vein endothelial cells
147. Age‐related anabolic resistance after endurance‐type exercise in healthy humans
148. Asymmetric superoxide release inside and outside the mitochondria in skeletal muscle under conditions of aging and disuse
149. Mitochondrial metabolism and diabetes
150. Chronic AMP-activated protein kinase activation and a high-fat diet have an additive effect on mitochondria in rat skeletal muscle
151. Effect of chronic contractile activity on mRNA stability in skeletal muscle
152. NAD+ and metabolic regulation of age-related proteoxicity: A possible role for methylglyoxal?
153. Peroxisome Proliferator–Activated Receptor-γ Coactivator-1α Overexpression Increases Lipid Oxidation in Myocytes From Extremely Obese Individuals
154. MuRF1 is a muscle fiber-type II associated factor and together with MuRF2 regulates type-II fiber trophicity and maintenance
155. Research in the Exercise Sciences
156. Mitochondrial Dysfunction, Proteotoxicity, and Aging
157. Modulation of Muscle Atrophy, Fatigue and MLC Phosphorylation by MuRF1 as Indicated by Hindlimb Suspension Studies on MuRF1-KO Mice
158. Integrative Physiology: Defined Novel Metabolic Roles of Osteocalcin
159. Adenine Nucleotide Translocator as a Regulator of Mitochondrial Function: Implication in the Pathogenesis of Metabolic Syndrome
160. Mitochondrial Medicine and the Neurodegenerative Mitochondriopathies

View Options

Get Access

Login options

Check if you access through your login credentials or your institution to get full access on this article.

Subscribe

Click on the button below to subscribe to Applied Physiology, Nutrition, and Metabolism

Purchase options

Purchase this article to get full access to it.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

View options

PDF

View PDF

Full Text

View Full Text

Media

Media

Other

Tables

Share Options

Share

Share the article link

Share on social media