Effects of exercise on mitochondrial content and function in aging human skeletal muscle
Elizabeth V Menshikova, Vladimir B Ritov, Liane Fairfull, Robert E Ferrell, David E Kelley, Bret H Goodpaster, Elizabeth V Menshikova, Vladimir B Ritov, Liane Fairfull, Robert E Ferrell, David E Kelley, Bret H Goodpaster
Abstract
Skeletal muscle mitochondria are implicated with age-related loss of function and insulin resistance. We examined the effects of exercise on skeletal muscle mitochondria in older (age = 67.3 +/- 0.6 years) men (n = 5) and women (n = 3). Similar increases in (p <.01) cardiolipin (88.2 +/- 9.0 to 130.6 +/- 7.5 microg/mU creatine kinase activity [CK]) and the total mitochondrial DNA (1264 +/- 170 to 1895 +/- 273 copies per diploid of nuclear genome) reflected increased mitochondria content. Succinate oxidase activity, complexes 2-4 of the electron transport chain (ETC), increased from 0.13 +/- 0.02 to 0.20 +/- 0.02 U/mU CK (p <.01). This improvement was more pronounced (p <.05) in subsarcolemmal (127 +/- 48%) compared to intermyofibrillar (56 +/- 12%) mitochondria. NADH oxidase activity, representing total ETC activity, increased from 0.51 +/- 0.09 to 1.00 +/- 0.09 U/mU CK (p <.01). In conclusion, exercise enhances mitochondria ETC activity in older human skeletal muscle, particularly in subsarcolemmal mitochondria, which is likely related to the concomitant increases in mitochondrial biogenesis.
Figures
mtDNA copy number in total mitochondria fraction relative to diploid nuclear genome before (gray bars) and after (black bars) exercise training; * denotes significant (P Figure 2. Effects of exercise on skeletal muscle cardiolipin content in sub-sarcolemmal (SS) and inter-myofibrillar (IMF1 and IMF2) mitochondrial fractions
Figure 2. Effects of exercise on skeletal…
Figure 2. Effects of exercise on skeletal muscle cardiolipin content in sub-sarcolemmal (SS) and inter-myofibrillar…
Cardiolipin content before (gray bars) and after (black bars) exercise training; * denotes significant (P Figure 3. Effects of exercise on total mitochondrial electron transport chain activity
Figure 3. Effects of exercise on total…
Figure 3. Effects of exercise on total mitochondrial electron transport chain activity
Total skeletal muscle…
Total skeletal muscle NADH oxidase activity before (gray bars) and after (black bars) exercise training; Data are presented as means ± standard error of the mean; n=5; CK, activity of creatine kinase; * denotes significant change from Pre-intervention assessed by paired t-test, P Figure 4
Figure 4
Effects of exercise on electron…
Figure 4
Effects of exercise on electron transport chain activity in sub-sarcolemmal (SS) and inter-myofibrillar…
Effects of exercise on electron transport chain activity in sub-sarcolemmal (SS) and inter-myofibrillar (IMF1 and IMF2) mitochondrial fractions. Skeletal muscle succinate oxidase activity in SS and IMF fractions of skeletal muscle before (gray bars) and after (black bars) exercise. Data are presented as means ± standard error of the mean; n=8; SS; CK, activity of creatine kinase; * denotes significant change from Pre-intervention assessed by paired t-test, P
Similar articles
- Characteristics of skeletal muscle mitochondrial biogenesis induced by moderate-intensity exercise and weight loss in obesity.Menshikova EV, Ritov VB, Ferrell RE, Azuma K, Goodpaster BH, Kelley DE. Menshikova EV, et al. J Appl Physiol (1985). 2007 Jul;103(1):21-7. doi: 10.1152/japplphysiol.01228.2006. Epub 2007 Mar 1. J Appl Physiol (1985). 2007. PMID: 17332268 Clinical Trial.
- Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity.Menshikova EV, Ritov VB, Toledo FG, Ferrell RE, Goodpaster BH, Kelley DE. Menshikova EV, et al. Am J Physiol Endocrinol Metab. 2005 Apr;288(4):E818-25. doi: 10.1152/ajpendo.00322.2004. Epub 2004 Dec 7. Am J Physiol Endocrinol Metab. 2005. PMID: 15585590
- Calorie Restriction-induced Weight Loss and Exercise Have Differential Effects on Skeletal Muscle Mitochondria Despite Similar Effects on Insulin Sensitivity.Menshikova EV, Ritov VB, Dube JJ, Amati F, Stefanovic-Racic M, Toledo FGS, Coen PM, Goodpaster BH. Menshikova EV, et al. J Gerontol A Biol Sci Med Sci. 2017 Dec 12;73(1):81-87. doi: 10.1093/gerona/glw328. J Gerontol A Biol Sci Med Sci. 2017. PMID: 28158621 Free PMC article.
- Does aging adversely affect muscle mitochondrial function?Short KR, Nair KS. Short KR, et al. Exerc Sport Sci Rev. 2001 Jul;29(3):118-23. doi: 10.1097/00003677-200107000-00006. Exerc Sport Sci Rev. 2001. PMID: 11474959 Review.
- Assembly of the cellular powerhouse: current issues in muscle mitochondrial biogenesis.Hood DA, Takahashi M, Connor MK, Freyssenet D. Hood DA, et al. Exerc Sport Sci Rev. 2000 Apr;28(2):68-73. Exerc Sport Sci Rev. 2000. PMID: 10902088 Review.
Cited by
- The impact of mild hypoxia exposure on myokine secretion in human obesity.van Meijel RLJ, Vliex LMM, Hartwig S, Lehr S, Al-Hasani H, Blaak EE, Goossens GH. van Meijel RLJ, et al. Int J Obes (Lond). 2023 Mar 30. doi: 10.1038/s41366-023-01294-5. Online ahead of print. Int J Obes (Lond). 2023. PMID: 36997723
- Increasing skeletal muscle carnitine content in older individuals increases whole-body fat oxidation during moderate-intensity exercise.Chee C, Shannon CE, Burns A, Selby AL, Wilkinson D, Smith K, Greenhaff PL, Stephens FB. Chee C, et al. Aging Cell. 2021 Feb;20(2):e13303. doi: 10.1111/acel.13303. Epub 2021 Jan 19. Aging Cell. 2021. PMID: 33464721 Free PMC article.
Publication types
- Comparative Study
- Research Support, N.I.H., Extramural
MeSH terms
- Aged
- Aging / physiology*
- Biopsy
- Cardiolipins / metabolism
- Chromatography, High Pressure Liquid
- Creatine Kinase / metabolism
- DNA, Mitochondrial / metabolism
- Exercise / physiology*
- Exercise Test
- Female
- Follow-Up Studies
- Humans
- Male
- Mitochondria, Muscle / metabolism*
- Muscle Contraction / physiology*
- Muscle, Skeletal / cytology
- Muscle, Skeletal / physiology*
- Oxidoreductases / metabolism
- Spectrophotometry
Substances
- Cardiolipins
- DNA, Mitochondrial
- Oxidoreductases
- succinate oxidase
- Creatine Kinase
Related information
Grant support
Show all 7 grants
LinkOut - more resources
- Full Text Sources
- Medical
- Research Materials
Full text links [x]
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Send To [x]
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
Follow NCBI
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
Cardiolipin content before (gray bars) and after (black bars) exercise training; * denotes significant (P Figure 3. Effects of exercise on total mitochondrial electron transport chain activity
Figure 3. Effects of exercise on total…
Figure 3. Effects of exercise on total mitochondrial electron transport chain activity
Total skeletal muscle…
Total skeletal muscle NADH oxidase activity before (gray bars) and after (black bars) exercise training; Data are presented as means ± standard error of the mean; n=5; CK, activity of creatine kinase; * denotes significant change from Pre-intervention assessed by paired t-test, P Figure 4
Figure 4
Effects of exercise on electron…
Figure 4
Effects of exercise on electron transport chain activity in sub-sarcolemmal (SS) and inter-myofibrillar…
Effects of exercise on electron transport chain activity in sub-sarcolemmal (SS) and inter-myofibrillar (IMF1 and IMF2) mitochondrial fractions. Skeletal muscle succinate oxidase activity in SS and IMF fractions of skeletal muscle before (gray bars) and after (black bars) exercise. Data are presented as means ± standard error of the mean; n=8; SS; CK, activity of creatine kinase; * denotes significant change from Pre-intervention assessed by paired t-test, P
Similar articles
- Characteristics of skeletal muscle mitochondrial biogenesis induced by moderate-intensity exercise and weight loss in obesity.Menshikova EV, Ritov VB, Ferrell RE, Azuma K, Goodpaster BH, Kelley DE. Menshikova EV, et al. J Appl Physiol (1985). 2007 Jul;103(1):21-7. doi: 10.1152/japplphysiol.01228.2006. Epub 2007 Mar 1. J Appl Physiol (1985). 2007. PMID: 17332268 Clinical Trial.
- Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity.Menshikova EV, Ritov VB, Toledo FG, Ferrell RE, Goodpaster BH, Kelley DE. Menshikova EV, et al. Am J Physiol Endocrinol Metab. 2005 Apr;288(4):E818-25. doi: 10.1152/ajpendo.00322.2004. Epub 2004 Dec 7. Am J Physiol Endocrinol Metab. 2005. PMID: 15585590
- Calorie Restriction-induced Weight Loss and Exercise Have Differential Effects on Skeletal Muscle Mitochondria Despite Similar Effects on Insulin Sensitivity.Menshikova EV, Ritov VB, Dube JJ, Amati F, Stefanovic-Racic M, Toledo FGS, Coen PM, Goodpaster BH. Menshikova EV, et al. J Gerontol A Biol Sci Med Sci. 2017 Dec 12;73(1):81-87. doi: 10.1093/gerona/glw328. J Gerontol A Biol Sci Med Sci. 2017. PMID: 28158621 Free PMC article.
- Does aging adversely affect muscle mitochondrial function?Short KR, Nair KS. Short KR, et al. Exerc Sport Sci Rev. 2001 Jul;29(3):118-23. doi: 10.1097/00003677-200107000-00006. Exerc Sport Sci Rev. 2001. PMID: 11474959 Review.
- Assembly of the cellular powerhouse: current issues in muscle mitochondrial biogenesis.Hood DA, Takahashi M, Connor MK, Freyssenet D. Hood DA, et al. Exerc Sport Sci Rev. 2000 Apr;28(2):68-73. Exerc Sport Sci Rev. 2000. PMID: 10902088 Review.
Cited by
- The impact of mild hypoxia exposure on myokine secretion in human obesity.van Meijel RLJ, Vliex LMM, Hartwig S, Lehr S, Al-Hasani H, Blaak EE, Goossens GH. van Meijel RLJ, et al. Int J Obes (Lond). 2023 Mar 30. doi: 10.1038/s41366-023-01294-5. Online ahead of print. Int J Obes (Lond). 2023. PMID: 36997723
- Increasing skeletal muscle carnitine content in older individuals increases whole-body fat oxidation during moderate-intensity exercise.Chee C, Shannon CE, Burns A, Selby AL, Wilkinson D, Smith K, Greenhaff PL, Stephens FB. Chee C, et al. Aging Cell. 2021 Feb;20(2):e13303. doi: 10.1111/acel.13303. Epub 2021 Jan 19. Aging Cell. 2021. PMID: 33464721 Free PMC article.
Publication types
- Comparative Study
- Research Support, N.I.H., Extramural
MeSH terms
- Aged
- Aging / physiology*
- Biopsy
- Cardiolipins / metabolism
- Chromatography, High Pressure Liquid
- Creatine Kinase / metabolism
- DNA, Mitochondrial / metabolism
- Exercise / physiology*
- Exercise Test
- Female
- Follow-Up Studies
- Humans
- Male
- Mitochondria, Muscle / metabolism*
- Muscle Contraction / physiology*
- Muscle, Skeletal / cytology
- Muscle, Skeletal / physiology*
- Oxidoreductases / metabolism
- Spectrophotometry
Substances
- Cardiolipins
- DNA, Mitochondrial
- Oxidoreductases
- succinate oxidase
- Creatine Kinase
Related information
Grant support
Show all 7 grants
LinkOut - more resources
- Full Text Sources
- Medical
- Research Materials
Full text links [x]
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Send To [x]
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
Follow NCBI
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
Total skeletal muscle NADH oxidase activity before (gray bars) and after (black bars) exercise training; Data are presented as means ± standard error of the mean; n=5; CK, activity of creatine kinase; * denotes significant change from Pre-intervention assessed by paired t-test, P Figure 4
Figure 4
Effects of exercise on electron…
Figure 4
Effects of exercise on electron transport chain activity in sub-sarcolemmal (SS) and inter-myofibrillar…
Effects of exercise on electron transport chain activity in sub-sarcolemmal (SS) and inter-myofibrillar (IMF1 and IMF2) mitochondrial fractions. Skeletal muscle succinate oxidase activity in SS and IMF fractions of skeletal muscle before (gray bars) and after (black bars) exercise. Data are presented as means ± standard error of the mean; n=8; SS; CK, activity of creatine kinase; * denotes significant change from Pre-intervention assessed by paired t-test, P
Similar articles
- Characteristics of skeletal muscle mitochondrial biogenesis induced by moderate-intensity exercise and weight loss in obesity.Menshikova EV, Ritov VB, Ferrell RE, Azuma K, Goodpaster BH, Kelley DE. Menshikova EV, et al. J Appl Physiol (1985). 2007 Jul;103(1):21-7. doi: 10.1152/japplphysiol.01228.2006. Epub 2007 Mar 1. J Appl Physiol (1985). 2007. PMID: 17332268 Clinical Trial.
- Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity.Menshikova EV, Ritov VB, Toledo FG, Ferrell RE, Goodpaster BH, Kelley DE. Menshikova EV, et al. Am J Physiol Endocrinol Metab. 2005 Apr;288(4):E818-25. doi: 10.1152/ajpendo.00322.2004. Epub 2004 Dec 7. Am J Physiol Endocrinol Metab. 2005. PMID: 15585590
- Calorie Restriction-induced Weight Loss and Exercise Have Differential Effects on Skeletal Muscle Mitochondria Despite Similar Effects on Insulin Sensitivity.Menshikova EV, Ritov VB, Dube JJ, Amati F, Stefanovic-Racic M, Toledo FGS, Coen PM, Goodpaster BH. Menshikova EV, et al. J Gerontol A Biol Sci Med Sci. 2017 Dec 12;73(1):81-87. doi: 10.1093/gerona/glw328. J Gerontol A Biol Sci Med Sci. 2017. PMID: 28158621 Free PMC article.
- Does aging adversely affect muscle mitochondrial function?Short KR, Nair KS. Short KR, et al. Exerc Sport Sci Rev. 2001 Jul;29(3):118-23. doi: 10.1097/00003677-200107000-00006. Exerc Sport Sci Rev. 2001. PMID: 11474959 Review.
- Assembly of the cellular powerhouse: current issues in muscle mitochondrial biogenesis.Hood DA, Takahashi M, Connor MK, Freyssenet D. Hood DA, et al. Exerc Sport Sci Rev. 2000 Apr;28(2):68-73. Exerc Sport Sci Rev. 2000. PMID: 10902088 Review.
Cited by
- The impact of mild hypoxia exposure on myokine secretion in human obesity.van Meijel RLJ, Vliex LMM, Hartwig S, Lehr S, Al-Hasani H, Blaak EE, Goossens GH. van Meijel RLJ, et al. Int J Obes (Lond). 2023 Mar 30. doi: 10.1038/s41366-023-01294-5. Online ahead of print. Int J Obes (Lond). 2023. PMID: 36997723
- Increasing skeletal muscle carnitine content in older individuals increases whole-body fat oxidation during moderate-intensity exercise.Chee C, Shannon CE, Burns A, Selby AL, Wilkinson D, Smith K, Greenhaff PL, Stephens FB. Chee C, et al. Aging Cell. 2021 Feb;20(2):e13303. doi: 10.1111/acel.13303. Epub 2021 Jan 19. Aging Cell. 2021. PMID: 33464721 Free PMC article.
Publication types
- Comparative Study
- Research Support, N.I.H., Extramural
MeSH terms
- Aged
- Aging / physiology*
- Biopsy
- Cardiolipins / metabolism
- Chromatography, High Pressure Liquid
- Creatine Kinase / metabolism
- DNA, Mitochondrial / metabolism
- Exercise / physiology*
- Exercise Test
- Female
- Follow-Up Studies
- Humans
- Male
- Mitochondria, Muscle / metabolism*
- Muscle Contraction / physiology*
- Muscle, Skeletal / cytology
- Muscle, Skeletal / physiology*
- Oxidoreductases / metabolism
- Spectrophotometry
Substances
- Cardiolipins
- DNA, Mitochondrial
- Oxidoreductases
- succinate oxidase
- Creatine Kinase
Related information
Grant support
Show all 7 grants
LinkOut - more resources
- Full Text Sources
- Medical
- Research Materials
Full text links [x]
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Send To [x]
Effects of exercise on electron transport chain activity in sub-sarcolemmal (SS) and inter-myofibrillar (IMF1 and IMF2) mitochondrial fractions. Skeletal muscle succinate oxidase activity in SS and IMF fractions of skeletal muscle before (gray bars) and after (black bars) exercise. Data are presented as means ± standard error of the mean; n=8; SS; CK, activity of creatine kinase; * denotes significant change from Pre-intervention assessed by paired t-test, P
Source: PubMed