Effects of caloric restriction on mitochondrial function and gene transcripts in rat muscle
Abstract
Rodent skeletal muscle mitochondrial DNA has been shown to be a potential site of oxidative damage during aging. Caloric restriction (CR) is reported to reduce oxidative stress and prolong life expectancy in rodents. Gene expression profiling and measurement of mitochondrial ATP production capacity were performed in skeletal muscle of male rats after feeding them either a control diet or calorie-restricted diet (60% of control diet) for 36 wk to determine the potential mechanism of the beneficial effects of CR. CR enhanced the transcripts of genes involved in reactive oxygen free radical scavenging function, tissue development, and energy metabolism while decreasing expression of those genes involved in signal transduction, stress response, and structural and contractile proteins. Real-time PCR measurments confirmed the changes in transcript levels of cytochrome- c oxidase III, superoxide dismutase (SOD)1, and SOD2 that were noted by the microarray approach. Mitochondrial ATP production and citrate synthase were unaltered by the dietary changes. We conclude that CR alters transcript levels of several genes in skeletal muscle and that mitochondrial function in skeletal muscle remains unaltered by the dietary intervention. Alterations in transcripts of many genes involved in reactive oxygen scavenging function may contribute to the increase in longevity reported with CR.
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Thirty-six weeks of 60% caloric restriction enhances transcription levels of genes involved in ROS scavenger function and energy metabolism without altering mitochondrial function and enzyme activities.
“Similarly, a separate study reports that a 36 weeks of 60% caloric restriction enhances the transcription levels of genes involved in ROS scavenger function and energy metabolism without altering mitochondrial function and enzyme activities [75].”
From Mitochondrial Adaptation in Skeletal Muscle: Impact of Obesity, Caloric Restriction, and Dietary Compounds (2024) · cites this paper as [75]
These responses are not observed in all studies of high-fat feeding.
“However, these responses are not observed in all studies of high-fat feeding; in fact, some studies demonstrate that high-fat feeding is associated with increased numbers of mitochondrial protein and DNA content, potentially mediated by chronic fatty acid activation of PPAR nuclear receptors (130 -132).”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [132]
Some studies demonstrate that high-fat feeding is associated with increased numbers of mitochondrial protein and DNA content, potentially mediated by chronic fatty acid activation of PPAR nuclear receptors.
“However, these responses are not observed in all studies of high-fat feeding; in fact, some studies demonstrate that high-fat feeding is associated with increased numbers of mitochondrial protein and DNA content, potentially mediated by chronic fatty acid activation of PPAR nuclear receptors (130 -132).”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [132]
Cites
Plum, F. (1960) · Archives of Neurology · doi:10.1001/archneur.1960.03840090124020 · Cited by 10,377 · see citing works
Oxidative Stress, Caloric Restriction, and Aging
Sohal, R. S., & Weindruch, R. H. (1996) · Science · doi:10.1126/science.273.5271.59 · Cited by 3,133 · see citing works
Expression monitoring by hybridization to high-density oligonucleotide arrays
Lockhart, D. J., Dong, H., Byrne, M. C., Follettie, M. T., Gallo, M. V., Chee, M. S., Mittmann, M., Wang, C., Kobayashi, M., Norton, H., et al. (1996) · Nature Biotechnology · doi:10.1038/nbt1296-1675 · Cited by 2,841 · see citing works
The retardation of aging and disease by dietary restriction
(1989) · Choice Reviews Online · doi:10.5860/choice.26-5101 · Cited by 1,477 · see citing works
Gene expression profile of aging and its retardation by caloric restriction
Lee, C.-K., Klopp, R. G., Weindruch, R., & Prolla, T. A. (1999) · Science · doi:10.1126/science.285.5432.1390 · Cited by 1,473 · see citing works
Extension of Drosophila lifespan by overexpression of human SOD1 in motorneurons
Parkes, T. L., Elia, A., Dickinson, D., Hilliker, A. J., Phillips, J. P., & Boulianne, G. L. (1998) · Nature Genetics · doi:10.1038/534 · Cited by 862 · see citing works
Energy metabolism in uncoupling protein 3 gene knockout mice
Vidal-Puig, A. J., Grujic, D., Zhang, C.-Y., Hagen, T., Boss, O., Ido, Y., Szczepanik, A., Wade, J., Mootha, V., Cortright, R., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910179199 · Cited by 677 · see citing works
Evans, W. J. (1995) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/50a.special_issue.5 · Cited by 606 · see citing works
Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean
Clapham, J. C., Arch, J. R. S., Chapman, H., Haynes, A., Lister, C., Moore, G. B. T., Piercy, V., Carter, S. A., Lehner, I., Smith, S. A., et al. (2000) · Nature · doi:10.1038/35019082 · Cited by 604 · see citing works
Aging and oxidative stress: Modulation by dietary restriction
Yu, B. P. (1996) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(96)00162-1 · Cited by 443 · see citing works
Gong, D., Monemdjou, S., Gavrilova, O., Leon, L. R., Marcus‐Samuels, B., Chou, C. J., Everett, C. A., Kozak, L. P., Li, C., Deng, C., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910177199 · Cited by 385 · see citing works
Barazzoni, R., Short, K. R., & Nair, K. S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.5.3343 · Cited by 367 · see citing works
Self-citationOverexpression of human copper,zinc-superoxide dismutase (SOD1) prevents postischemic injury
Wang, P., Chen, H., Qin, H., Sankarapandi, S., Bêcher, M. W., Wong, P. C., & Zweier, J. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4556 · Cited by 258 · see citing works
Age effect on transcript levels and synthesis rate of muscle MHC and response to resistance exercise
Balagopal, P., Coenen-Schimke, J. M., Ades, P. A., Adey, D., & Nair, K. S. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.280.2.e203 · Cited by 248 · see citing works
Self-citationAn Emerging Hypothesis: Synergistic Induction of Aging by Free Radicals and Maillard Reactions
Kristal, B. S., & Yu, B. P. (1992) · Journal of Gerontology · doi:10.1093/geronj/47.4.b107 · Cited by 223 · see citing works
A high-density probe array sample preparation method using 10- to 100-fold fewer cells
Mahadevappa, M., & Warrington, J. A. (1999) · Nature Biotechnology · doi:10.1038/15124 · Cited by 158 · see citing works
Nelson, J. F., Karelus, K., Bergman, M. D., & Felicio, L. S. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)00072-m · Cited by 139 · see citing works
Short, K. R., Nygren, J., Barazzoni, R., Levine, J. A., & Nair, K. S. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.280.5.e761 · Cited by 90 · see citing works
Self-citationGene Expression and Protein Degradation
Remmen, H. V., Ward, W. F., Sabia, R. V., & Richardson, A. G. (1995) · Comprehensive physiology · doi:10.1002/cphy.cp110109 · Cited by 83 · see citing works
Interventions Based on the Possibility That Oxidative Stress Contributes to Sarcopenia
Schwartz, R. S., & Weindruch, R. H. (1995) · The Journals of Gerontology Series A · doi:10.1093/gerona/50a.special_issue.157 · Cited by 80 · see citing works
A sensitive method for measuring ATP-formation in rat muscle mitochondria
Wibom, R., Lundin, A., & Hultman, E. (1990) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365519009089146 · Cited by 74 · see citing works
Walford, R. L., & Spindler, S. R. (1997) · The Journals of Gerontology Series A · doi:10.1093/gerona/52a.4.b179 · Cited by 68 · see citing works
Changes in uncoupling protein-2 and -3 expression in aging rat skeletal muscle, liver, and heart
Barazzoni, R., & Nair, K. S. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.280.3.e413 · Cited by 64 · see citing works
Self-citationAge-related changes in skeletal muscle function
McCarter, R. (1990) · Aging Clinical and Experimental Research · doi:10.1007/bf03323892 · Cited by 33 · see citing works
Short, K. R., Nygren, J., Barazzoni, R., Levine, J. A., & Nair, K. S. (2001) · Cited by 19 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Calorie Restriction Increases Muscle Mitochondrial Biogenesis in Healthy Humans
Civitarese, A. E., Carling, S., Heilbronn, L. K., Hulver, M. H., Ukropcova, B., Deutsch, W. A., Smith, S. R., & Ravussin, E. (2007) · PLoS Medicine · doi:10.1371/journal.pmed.0040076 · Cited by 790 · see citing works
Calorie restriction–the SIR2 connection
Guarente, L., & Picard, F. (2005) · Cell · doi:10.1016/j.cell.2005.01.029 · Cited by 793 · see citing works
Ristow, M., & Zarse, K. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.03.014 · Cited by 789 · see citing works
The role of mitochondria in the pathogenesis of type 2 diabetes
Patti, M.-E., & Corvera, S. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0027 · Cited by 551 · see citing works
Aging, adiposity, and calorie restriction
Fontana, L. (2007) · JAMA · doi:10.1001/jama.297.9.986 · Cited by 526 · see citing works
Mitohormesis: Promoting Health and Lifespan by Increased Levels of Reactive Oxygen Species (ROS)
Ristow, M., & Schmeisser, K. (2014) · Dose-Response · doi:10.2203/dose-response.13-035.ristow · Cited by 534 · see citing works
Mitochondria and ageing: Role in heart, skeletal muscle and adipose tissue
Boengler, K., Kosiol, M., Mayr, M., Schulz, R., & Rohrbach, S. (2017) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12178 · Cited by 421 · see citing works
Mitochondrial dysfunction in cardiovascular disease
Ballinger, S. W. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.02.014 · Cited by 405 · see citing works
Calorie Restriction: Is AMPK a Key Sensor and Effector
Cantó, C., & Auwerx, J. (2011) · Physiology · doi:10.1152/physiol.00010.2011 · Cited by 282 · see citing works
Preiser, J. (2012) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607111434963 · Cited by 236 · see citing works
Lanza, I. R., Zabielski, P., Klaus, K. A., Morse, D. M., Heppelmann, C. J., Bergen, H. R., Dasari, S., Walrand, S., Short, K. R., Johnson, M. L., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.11.003 · Cited by 227 · see citing works
Self-citationThe effects of dietary restriction on oxidative stress in rodents
Walsh, M. E., Shi, Y., & Van Remmen, H. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.05.037 · Cited by 181 · see citing works
Gene expression profiling of aging reveals activation of a p53-mediated transcriptional program
Edwards, M. G., Anderson, R. M., Yuan, M., Kendziorski, C. M., Weindruch, R., & Prolla, T. A. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-80 · Cited by 174 · see citing works
Yao, J., Chen, S., Mao, Z., Cadenas, E., & Brinton, R. D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021788 · Cited by 169 · see citing works
Preston, C. C., Oberlin, A. S., Holmuhamedov, E. L., Gupta, A., Sagar, S., Syed, R. H. K., Siddiqui, S. A., Raghavakaimal, S., Terzic, A., & Jahangir, A. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.02.010 · Cited by 136 · see citing works
Does calorie restriction induce mitochondrial biogenesis? A reevaluation
Hancock, C. R., Han, D., Higashida, K., Kim, S. H., & Holloszy, J. O. (2011) · The FASEB Journal · doi:10.1096/fj.10-170415 · Cited by 131 · see citing works
Marzetti, E., Lawler, J. M., Hiona, A., Manini, T., Seo, A. Y., & Leeuwenburgh, C. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.05.028 · Cited by 113 · see citing works
Colom, B., Alcolea, M., Valle, A., Oliver, J., Roca, P., & García-Palmer, F. (2007) · Cellular Physiology and Biochemistry · doi:10.1159/000099208 · Cited by 89 · see citing works
Baker, D. J., Betik, A. C., Krause, D. J., & Hepple, R. T. (2006) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/61.7.675 · Cited by 89 · see citing works
Long-term caloric restriction abrogates the age-related decline in skeletal muscle aerobic function
Hepple, R. T., Baker, D. J., Kaczor, J. J., & Krause, D. J. (2005) · The FASEB Journal · doi:10.1096/fj.04-3535fje · Cited by 80 · see citing works
Age-Related Deficit in Load-Induced Skeletal Muscle Growth
Hwee, D. T., & Bodine, S. C. (2009) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glp026 · Cited by 74 · see citing works
Nutrition modulation of human aging: The calorie restriction paradigm
Das, S. K., Balasubramanian, P., & Weerasekara, Y. K. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.04.011 · Cited by 51 · see citing works
Hempenstall, S., Page, M. M., Wallen, K. R., & Selman, C. (2012) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2011.12.002 · Cited by 47 · see citing works
Stamerra, C. A., Di Giosia, P., Giorgini, P., Ferri, C., Sukhorukov, V. N., & Sahebkar, A. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/9530007 · Cited by 48 · see citing works
RetractedJun, L., Tao, Y.-X., Geetha, T., & Babu, J. R. (2024) · Current Nutrition Reports · doi:10.1007/s13668-024-00555-7 · Cited by 27 · see citing works
- Authors
- Sreekumar, R., Unnikrishnan, J., Fu, A., Nygren, J., Short, K. R., Schimke, J., Barazzoni, R., & Nair, K. S.
- Affiliations
- Mayo Clinic (US)
- Venue
- American Journal of Physiology-Endocrinology and Metabolism
- Publisher
- American Physiological Society
- Published
- 2002-07-01
- Volume
- 283
- Issue
- 1
- Pages
- E38-E43
- ISSN
- 0193-1849 (ISSN-L)
- 1522-1555
- OpenAlex
- W2161680769
- Cited by
- 170
- References
- 25
- Citations by year
- 2025: 1 · 2024: 3 · 2023: 4 · 2022: 3 · 2021: 1 · 2020: 1 · 2019: 2 · 2018: 1 · 2017: 4 · 2016: 1 · 2015: 4 · 2014: 5 · 2013: 4 · 2012: 13
- FWCI
- 3.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
- PubMed (publishedVersion)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion)
- Funders
- National Institute on Aging (R01‐AG09531, R01AG009531)
- National Institute of Diabetes and Digestive and Kidney Diseases (T32-DK-07352, T32DK007352)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Keywords
- caloric restriction, skeletal muscle, mitochondrial function, gene expression, oxidative stress, reactive oxygen species scavenging, superoxide dismutase, citrate synthase, mitochondrial ATP production, longevity, aging, oxidative damage
- MeSH terms
- Uncoupling Protein 2, Uncoupling Protein 3, Superoxide Dismutase-1, Superoxide Dismutase 2, Adenosine Triphosphate, Animals, Body Weight, Energy Intake, Carrier Proteins, Citrate (si)-Synthase, Electron Transport Complex IV, Ion Channels, Male, Mitochondria, Proteins, RNA, Messenger, Superoxide Dismutase, Blotting, Northern, Polymerase Chain Reaction, Rats, Sprague-Dawley, Muscle, Skeletal, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mitochondrial Proteins, Membrane Transport Proteins, Rats
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