Does calorie restriction induce mitochondrial biogenesis? A reevaluation
Open accessAbstract
It has been reported that 30% calorie restriction (CR) for 3 mo results in large increases in mitochondrial biogenesis in heart, brain, liver, and adipose tissue, with concomitant increases in respiration and ATP synthesis. We found these results surprising, and performed this study to determine whether 30% CR does induce an increase in mitochondria in heart, brain, liver, adipose tissue, and/or skeletal muscle. To this end, we measured the levels of a range of mitochondrial proteins, and mRNAs. With the exception of long-chain acyl-CoA dehydrogenase protein level, which was increased ∼60% in adipose tissue, none of the mitochondrial proteins or mRNAs that we measured were increased in rats subjected to 30% CR for 14 wk. There was also no increase in citrate synthase activity. Because it is not possible to have an increase in mitochondria without any increase in key mitochondrial proteins, we conclude that 30% CR does not induce an increase in mitochondria in heart, brain, liver, adipose tissue, or skeletal muscle in laboratory rodents.
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Long-term caloric restriction does not alter markers of mitochondrial biogenesis.
“Similarly, long-term CR did not alter any markers of mitochondrial biogenesis”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as Hancock et al., 2011
Long-term caloric restriction prevents age-related loss of mitochondrial oxidative capacity and efficiency in isolated mitochondria and in muscle fibres.
“although CR prevented age-related loss of mitochondrial oxidative capacity and efficiency in isolated mitochondria and in muscle fibres”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as Hancock et al., 2011
Hancock et al. could not detect changes in mRNA or protein levels of markers of mitochondrial biogenesis, or citrate synthase activity, in muscle from rats that underwent 30% caloric restriction for 14 weeks.
“Hancock et al. could not detect any changes in mRNA or protein levels of markers of mitochondrial biogenesis, or citrate synthase activity in muscle from rats that underwent 30% CR for 14 weeks (Hancock et al., 2011).”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as Hancock et al., 2011
Long-term caloric restriction reduces oxidative damage.
“and reduced oxidative damage (Hancock et al., 2011).”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as Hancock et al., 2011
The effects of caloric restriction on mitochondrial function are not consistent across studies or across tissues.
“However, this is not consistent across studies or across tissues (Hancock et al., 2011; Lanza et al., 2012; Walsh et al., 2014).”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as Hancock et al., 2011
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PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
A Cold-Inducible Coactivator of Nuclear Receptors Linked to Adaptive Thermogenesis
Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., & Spiegelman, B. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81410-5 · Cited by 3,864 · see citing works
Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging
Kujoth, G. C., Hiona, A., Pugh, T. D., Someya, S., Panzer, K., Wohlgemuth, S. E., Hofer, T., Seo, A. Y., Sullivan, R., Jobling, W. A., et al. (2005) · Science · doi:10.1126/science.1112125 · Cited by 2,165 · see citing works
Metabolic control through the PGC-1 family of transcription coactivators
Lin, J., Handschin, C., & Spiegelman, B. M. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.05.004 · Cited by 2,130 · cited 1× · see citing works
“well established that PGC-1 is responsible for mediating adaptive increases in mitochondria by coactivating the transcription factors that regulate expression of mitochondrial proteins (20, 21).”
BackgroundSrere, P. A. (1969) · Methods in Enzymology · doi:10.1016/0076-6879(69)13005-0 · Cited by 2,005 · see citing works
Adaptations of skeletal muscle to endurance exercise and their metabolic consequences
Holloszy, J. O., & Coyle, E. F. (1984) · Journal of Applied Physiology · doi:10.1152/jappl.1984.56.4.831 · Cited by 1,985 · see citing works
Self-citationDecline in skeletal muscle mitochondrial function with aging in humans
Short, K. R., Bigelow, M. L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., & Nair, K. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501559102 · Cited by 1,333 · see citing works
Peroxisome-Proliferator-Activated Receptor δ Activates Fat Metabolism to Prevent Obesity
Wang, Y.-X., Lee, C.-H., Tiep, S., Yu, R. T., Ham, J., Kang, H., & Evans, R. M. (2003) · Cell · doi:10.1016/s0092-8674(03)00269-1 · Cited by 1,296 · see citing works
Peroxisome proliferator–activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis
Lehman, J. J., Barger, P. M., Kovacs, A., Saffitz, J. E., Medeiros, D. M., & Kelly, D. P. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10268 · Cited by 1,285 · see citing works
Transcriptional regulatory circuits controlling mitochondrial biogenesis and function
Kelly, D. P., & Scarpulla, R. C. (2004) · Genes & Development · doi:10.1101/gad.1177604 · Cited by 1,243 · see citing works
Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS
Nisoli, E., Tonello, C., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Falcone, S., Valerio, A., Cantoni, O., Clementi, E., et al. (2005) · Science · doi:10.1126/science.1117728 · Cited by 1,107 · see citing works
Overview of caloric restriction and ageing
Masoro, E. J. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2005.03.012 · Cited by 1,054 · see citing works
Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1
Baar, K., Wende, A. R., Jones, T. E., Marison, M., Nolte, L. A., Chen, M., Kelly, D. P., & Holloszy, J. O. (2002) · The FASEB Journal · doi:10.1096/fj.02-0367com · Cited by 1,020 · see citing works
Self-citationKraytsberg, Y., Kudryavtseva, E., McKee, A. C., Geula, C., Kowall, N. W., & Khrapko, K. (2006) · Nature Genetics · doi:10.1038/ng1778 · Cited by 884 · see citing works
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
Does oxidative damage to DNA increase with age?
Hamilton, M. L., Van Remmen, H., Drake, J. A., Yang, H., Guo, Z. M., Kewitt, K., Walter, C. A., & Richardson, A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171202698 · Cited by 768 · see citing works
Michael, L. F., Wu, Z., Cheatham, R. B., Puigserver, P., Adelmant, G., Lehman, J. J., Kelly, D. P., & Spiegelman, B. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.061035098 · Cited by 663 · see citing works
PPAR : a dagger in the heart of the metabolic syndrome
Barish, G. D. (2006) · Journal of Clinical Investigation · doi:10.1172/jci27955 · Cited by 641 · see citing works
Cao, W., Daniel, K. W., Robidoux, J., Puigserver, P., Medvedev, A. V., Bai, X., Floering, L. M., Spiegelman, B. M., & Collins, S. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.7.3057-3067.2004 · Cited by 605 · see citing works
Mitochondria—A Nexus for Aging, Calorie Restriction, and Sirtuins?
Guarente, L. (2008) · Cell · doi:10.1016/j.cell.2008.01.007 · Cited by 513 · see citing works
Russell, L. K., Mansfield, C. M., Lehman, J. J., Kovacs, A., Courtois, M., Saffitz, J. E., Medeiros, D. M., Valencik, M. L., McDonald, J. A., & Kelly, D. P. (2004) · Circulation Research · doi:10.1161/01.res.0000117088.36577.eb · Cited by 402 · see citing works
WANAGAT, J., CAO, Z., PATHARE, P., & AIKEN, J. M. (2001) · The FASEB Journal · doi:10.1096/fj.00-0320com · Cited by 378 · 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
Drew, B., Phaneuf, S., Dirks, A. J., Selman, C., Gredilla, R., Lezza, A. M. S., Barja, G., & Leeuwenburgh, C. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00455.2002 · Cited by 287 · see citing works
Lass, A., Sohal, B. H., Weindruch, R. H., Forster, M. J., & Sohal, R. S. (1998) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(98)00144-0 · Cited by 251 · see citing works
Garcia-Roves, P., Huss, J. M., Han, D.-H., Hancock, C. R., Iglesias-Gutierrez, E., Chen, M., & Holloszy, J. O. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704024104 · Cited by 246 · see citing works
Self-citationSarcopenia of aging: Underlying cellular mechanisms and protection by calorie restriction
Marzetti, E., Lees, H. A., Wohlgemuth, S. E., & Leeuwenburgh, C. (2009) · BioFactors · doi:10.1002/biof.5 · Cited by 182 · see citing works
Mitochondrial death effectors: Relevance to sarcopenia and disuse muscle atrophy
Marzetti, E., Hwang, J. C. Y., Lees, H. A., Wohlgemuth, S. E., Dupont-Versteegden, E. E., Carter, C. S., Bernabei, R., & Leeuwenburgh, C. (2010) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.05.007 · Cited by 174 · see citing works
Effects of caloric restriction on mitochondrial function and gene transcripts in rat muscle
Sreekumar, R., Unnikrishnan, J., Fu, A., Nygren, J., Short, K. R., Schimke, J., Barazzoni, R., & Nair, K. S. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00387.2001 · Cited by 170 · see citing works
Muscle Plasticity: Energy Demand and Supply Processes
Booth, F. W., & Baldwin, K. M. (1996) · Comprehensive physiology · doi:10.1002/cphy.cp120124 · Cited by 165 · see citing works
Cardiac mitochondrial bioenergetics, oxidative stress, and aging
Judge, S., & Leeuwenburgh, C. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00285.2006 · Cited by 141 · see citing works
Energy metabolism in contracting rat skeletal muscle: adaptation to exercise training
Constable, S. H., Favier, R. J., McLane, J. A., Fell, R. D., Chen, M., & Holloszy, J. O. (1987) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1987.253.2.c316 · Cited by 140 · cited 1× · see citing works
“For example, a 2-fold adaptive increase in muscle mitochondria induced by exercise training has no effect on resting oxygen consumption or ATP concentration (12).”
BackgroundSelf-citationWard, W. F., Qi, W., Remmen, H. V., Zackert, W. E., Roberts, L. J., & Richardson, A. G. (2005) · The Journals of Gerontology Series A · doi:10.1093/gerona/60.7.847 · Cited by 118 · see citing works
Skeletal muscle overexpression of nuclear respiratory factor 1 increases glucose transport capacity
Baar, K., Song, Z., Semenkovich, C. F., Jones, T. E., Han, D.-H., Nolte, L. A., Ojuka, E. O., Chen, M. W., & Holloszy, J. O. (2003) · The FASEB Journal · doi:10.1096/fj.03-0049com · Cited by 106 · see citing works
Self-citationTaffet, G. E., Pham, T. T. T., & Hartley, C. J. (1997) · The Journals of Gerontology Series A · doi:10.1093/gerona/52a.6.b285 · Cited by 101 · 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
Rabøl, R., Svendsen, P. F., Skovbro, M., Boushel, R., Haugaard, S. B., Schjerling, P., Schrauwen, P., Hesselink, M. K. C., Nilas, L., Madsbad, S., et al. (2009) · Metabolism · doi:10.1016/j.metabol.2009.03.014 · Cited by 75 · see citing works
Calpain System Regulates Muscle Mass and Glucose Transporter GLUT4 Turnover
Otani, K., Han, D.-H., Ford, E. L., Garcia-Roves, P. M., Ye, H., Horikawa, Y., Bell, G. I., Holloszy, J. O., & Polonsky, K. S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400213200 · Cited by 67 · see citing works
Self-citationHuang, J. H., & Hood, D. A. (2009) · IUBMB Life · doi:10.1002/iub.164 · Cited by 66 · see citing works
McKiernan, S. H., Tuen, V. C., Baldwin, K. R., Wanagat, J., Djamali, A., & Aiken, J. M. (2007) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00307.2006 · Cited by 63 · see citing works
Lee, C. M., Aspnes, L. E., Chung, S. S., Weindruch, R. H., & Aiken, J. M. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09901.x · Cited by 52 · see citing works
Cartier, L.-J., Ohira, Y., Chen, M., Cuddihee, R. W., & Holloszy, J. O. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)67094-2 · Cited by 39 · see citing works
Self-citationPPARδ activator GW-501516 has no acute effect on glucose transport in skeletal muscle
Terada, S., Wicke, S., Holloszy, J. O., & Han, D. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00430.2005 · Cited by 32 · see citing works
Self-citationTime course of the T3- and T4-induced increase in rat soleus muscle mitochondria
Winder, W. W. (1979) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1979.236.3.c132 · Cited by 32 · see citing works
Mulligan, J. D., Stewart, A. M., & Saupe, K. W. (2007) · Experimental Gerontology · doi:10.1016/j.exger.2007.10.011 · Cited by 31 · see citing works
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Correia‐Melo, C., Marques, F. D., Anderson, R., Hewitt, G., Hewitt, R., Cole, J., Carroll, B. M., Miwa, S., Birch, J., Merz, A., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201592862 · Cited by 796 · see citing works
Speakman, J. R., & Mitchell, S. E. (2011) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2011.07.001 · Cited by 769 · see citing works
Luen Tang, B. (2016) · Molecules and Cells · doi:10.14348/molcells.2016.2318 · Cited by 740 · see citing works
Diet and depression: Exploring the biological mechanisms of action
Marx, W., Lane, M., Hockey, M., Aslam, H., Berk, M., Walder, K., Borsini, A., Firth, J., Pariante, C. M., Berding, K., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00925-x · Cited by 685 · see citing works
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Kulkarni, S. S., & Cantó, C. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.10.005 · Cited by 477 · see citing works
“Similarly, Rsv, but not SIRT1 overexpression or CR, leads to a dramatic increase in skeletal muscle mitochondrial content [44,56,58].”
BackgroundSergi, D., Naumovski, N., Heilbronn, L. K., Abeywardena, M., O’Callaghan, N., Lionetti, L., & Luscombe-Marsh, N. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00532 · Cited by 347 · see citing works
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Peterson, C. M., Johannsen, D. L., & Ravussin, É. (2012) · Journal of Aging Research · doi:10.1155/2012/194821 · Cited by 318 · see citing works
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Cantó, C., & Auwerx, J. (2011) · Physiology · doi:10.1152/physiol.00010.2011 · Cited by 282 · see citing works
Effects of Resveratrol and SIRT1 on PGC-1α Activity and Mitochondrial Biogenesis: A Reevaluation
Higashida, K., Kim, S. H., Jung, S. R., Asaka, M., Holloszy, J. O., & Han, D.-H. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001603 · Cited by 228 · see citing works
Self-citationLanza, 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
Contribution of Impaired Mitochondrial Autophagy to Cardiac Aging
Dutta, D., Calvani, R., Bernabei, R., Leeuwenburgh, C., & Marzetti, E. (2012) · Circulation Research · doi:10.1161/circresaha.111.246108 · Cited by 221 · see citing works
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Marzetti, E., Csiszár, A., Dutta, D., Balagopal, G., Calvani, R., & Leeuwenburgh, C. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00936.2012 · Cited by 197 · see citing works
Lane, N. J. (2011) · BioEssays · doi:10.1002/bies.201100051 · Cited by 177 · see citing works
Flachs, P., Rossmeisl, M., Kuda, O., & Kopecký, J. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2013.02.003 · Cited by 149 · see citing works
Testa, G., Biasi, F., Poli, G., & Chiarpotto, E. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113196660699 · Cited by 148 · see citing works
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Koh, J., Hancock, C. R., Terada, S., Higashida, K., Holloszy, J. O., & Han, D.-H. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.04.029 · Cited by 95 · see citing works
Self-citationAmigo, I., Menezes‐Filho, S. L., Luévano‐Martínez, L. A., Chausse, B., & Kowaltowski, A. J. (2017) · Aging Cell · doi:10.1111/acel.12527 · Cited by 95 · see citing works
Sin, T. K., Yu, A. P., Yung, B. Y., Yip, S. P., Chan, L., Wong, S. C. C., Ying, M. T. C., Rudd, J. A., & Siu, P. M. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.271387 · Cited by 94 · see citing works
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Miller, B. F., & Hamilton, K. L. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00578.2011 · Cited by 86 · see citing works
Price, J. C., Khambatta, C. F., Li, K. W., Bruss, M. D., Shankaran, M., Dalidd, M., Floreani, N. A., Roberts, L. S., Turner, S., Holmes, W. E., et al. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m112.021204 · Cited by 84 · see citing works
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Cabiscol, E., Tamarit, J., & Ros, J. (2013) · Mass Spectrometry Reviews · doi:10.1002/mas.21375 · Cited by 81 · see citing works
Duszka, K., Gregor, A., Guillou, H., König, J. S., & Wahli, W. (2020) · Cells · doi:10.3390/cells9071708 · Cited by 82 · see citing works
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“content in aged skeletal muscle is in line with recent studies from the Hollozy and Nair research groups, which have shown that CR does not increase mitochondrial content in rodent skeletal muscle (Hancock et al., 2011;Lanza et al., 2012).”
ResultBjedov, I., Cochemé, H. M., Foley, A., Wieser, D., Woodling, N. S., Castillo-Quan, J. I., Norvaišas, P., Lujan, C., Regan, J. C., Toivonen, J. M., et al. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1009083 · Cited by 68 · see citing works
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Khraiwesh, H., López-Domínguez, J., López-Lluch, G., Navas, P., de Cabo, R., Ramsey, J., Villalba, J., & González-Reyes, J. (2013) · The journals of gerontology. Series A, Biological sciences and medical sciences · doi:10.1093/gerona/glt006 · Cited by 51 · see citing works
Nutrition modulation of human aging: The calorie restriction paradigm
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Abiri, B., & Vafa, M. (2017) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2017.1412940 · Cited by 51 · see citing works
Biphasic Modeling of Mitochondrial Metabolism Dysregulation during Aging
Baker, D. J., & Peleg, S. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.06.005 · Cited by 48 · see citing works
The role of SirT1 in muscle mitochondrial turnover
Menzies, K. J., & Hood, D. A. (2011) · Mitochondrion · doi:10.1016/j.mito.2011.03.001 · Cited by 48 · see citing works
Duivenvoorde, L. P. M., van Schothorst, E. M., Bunschoten, A., & Keijer, J. (2011) · Journal of Molecular Endocrinology · doi:10.1530/jme-11-0001 · Cited by 48 · 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
Energy restriction and potential energy restriction mimetics
Nikolai, S., Pallauf, K., Huebbe, P., & Rimbach, G. H. (2015) · Nutrition Research Reviews · doi:10.1017/s0954422415000062 · Cited by 43 · see citing works
Kitaoka, Y., Nakazato, K., & Ogasawara, R. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00465.2016 · Cited by 43 · see citing works
Mitochondrial form, function and signalling in aging
Amigo, I., da Cunha, F. M., Forni, M. F., Garcia-Neto, W., Kakimoto, P. A., Luévano‐Martínez, L. A., Macedo, F. P., Menezes‐Filho, S. L., Peloggia, J., & Kowaltowski, A. J. (2016) · Biochemical Journal · doi:10.1042/bcj20160451 · Cited by 42 · see citing works
Facts and controversies in our understanding of how caloric restriction impacts the mitochondrion
Gouspillou, G., & Hepple, R. T. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.03.004 · Cited by 42 · see citing works
SIRT1 Gain of Function Does Not Mimic or Enhance the Adaptations to Intermittent Fasting
Boutant, M., Kulkarni, S. S., Joffraud, M., Raymond, F., Métairon, S., Descombes, P., & Cantó, C. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.02.007 · Cited by 42 · see citing works
Gesing, A., Masternak, M. M., Wang, F., Joseph, A.-M., Leeuwenburgh, C., Westbrook, R., Lewiñski, A., Karbownik‐Lewińska, M., & Bartke, A. (2011) · The Journals of Gerontology Series A · doi:10.1093/gerona/glr080 · Cited by 40 · see citing works
Targeting mitochondrial function and proteostasis to mitigate dynapenia
Musci, R. V., Hamilton, K. L., & Miller, B. F. (2017) · European Journal of Applied Physiology · doi:10.1007/s00421-017-3730-x · Cited by 38 · see citing works
Nitric oxide, interorganelle communication, and energy flow: a novel route to slow aging
Valerio, A., & Nisoli, E. (2015) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2015.00006 · Cited by 37 · see citing works
Calcaterra, V., Rossi, V., Magenes, V. C., Baldassarre, P., Grazi, R., Loiodice, M., Fabiano, V., & Zuccotti, G. (2024) · Frontiers in Pediatrics · doi:10.3389/fped.2024.1368283 · Cited by 40 · see citing works
Hamilton, K. L., & Miller, B. F. (2017) · The Journal of Physiology · doi:10.1113/jp274335 · Cited by 35 · see citing works
Kim, S.-E., Mori, R., Komatsu, T., Chiba, T., Hayashi, H., Park, S., Sugawa, M. D., Dencher, N. A., & Shimokawa, I. (2015) · AGE · doi:10.1007/s11357-015-9787-8 · Cited by 34 · see citing works
Self-citationThe role of lipids in aging-related metabolic changes
de Diego, I., Peleg, S., & Fuchs, B. (2019) · Chemistry and Physics of Lipids · doi:10.1016/j.chemphyslip.2019.05.005 · Cited by 34 · see citing works
Chujo, Y., Fujii, N., Okita, N., Konishi, T., Narita, T., Yamada, A., Haruyama, Y., Tashiro, K., Chiba, T., Shimokawa, I., et al. (2012) · AGE · doi:10.1007/s11357-012-9439-1 · Cited by 33 · see citing works
Hoevenaars, F. P. M., Keijer, J., Herreman, L., Palm, I. F., Hegeman, M. A., Swarts, H. J. M., & van Schothorst, E. M. (2014) · Genes & Nutrition · doi:10.1007/s12263-014-0391-9 · Cited by 31 · see citing works
Rohrbach, S., Aslam, M., Niemann, B., & Schulz, R. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12650 · Cited by 30 · see citing works
Hagopian, K., Chen, Y., Domer, K. S., Hoo, R. S., Bentley, T., McDonald, R. B., & Ramsey, J. J. (2011) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-011-9353-8 · Cited by 29 · see citing works
Pardo, R., Vilà, M., Cervela, L., de Marco, M., Gama-Pérez, P., González-Franquesa, A., Statuto, L., Vilallonga, R., Simó, R., Garcia-Roves, P. M., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201800310r · Cited by 27 · see citing works
PGC‐1α mediates a rapid, exercise‐induced downregulation of glycogenolysis in rat skeletal muscle
Kim, S. H., Koh, J., Higashida, K., Jung, S. R., Holloszy, J. O., & Han, D. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.283820 · Cited by 26 · see citing works
Self-citationPark, J.-S., Holloszy, J. O., Kim, K., & Koh, J. (2020) · Nutrients · doi:10.3390/nu12030652 · Cited by 26 · see citing works
Self-citationBerry, B. J., Mjelde, E., Carreno, F., Gilham, K., Hanson, E. J., Na, E., & Kaeberlein, M. R. (2023) · GeroScience · doi:10.1007/s11357-023-00766-w · Cited by 25 · see citing works
Wang, H., Sharma, N., Arias, E. B., & Cartee, G. D. (2015) · The Journals of Gerontology Series A · doi:10.1093/gerona/glv142 · Cited by 24 · see citing works
Capó, X., Martorell, M., Ferrer, M. D., Sureda, A., Pons, V., Domingo, J. C., Drobnic, F., Martínez-Rodríguez, A., Leyva-Vela, B., Sarabia, J. M., et al. (2020) · Nutrients · doi:10.3390/nu12040930 · Cited by 23 · see citing works
Prezotto, L. D., Lemley, C. O., Camacho, L. E., Doscher, F. E., Meyer, A. M., Caton, J. S., Awda, B. J., Vonnahme, K. A., & Swanson, K. C. (2013) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/jpn.12142 · Cited by 23 · see citing works
Malcomson, F. C., & Mathers, J. C. (2018) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-981-13-2835-0_13 · Cited by 21 · see citing works
Milton‐Laskibar, I., Aguirre, L., Etxeberría, U., Milagro, F. I., Martínez, J. A., & Portillo, M. P. (2018) · Nutrients · doi:10.3390/nu10101446 · Cited by 21 · see citing works
Carteri, R. B., Menegassi, L. N., Feldmann, M., Kopczynski, A., Rodolphi, M. S., Strogulski, N. R., Almeida, A. S., Marques, D. M., Porciúncula, L. O., & Portela, L. V. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113163 · Cited by 21 · see citing works
Gat‐Yablonski, G., Finka, A., Pinto, G., Quadroni, M., Shtaif, B., & Goloubinoff, P. (2016) · Aging · doi:10.18632/aging.101009 · Cited by 21 · see citing works
Wang, D., Wu, M., Li, S., Gao, Q., & Zeng, Q.-P. (2015) · Science China Life Sciences · doi:10.1007/s11427-014-4736-9 · Cited by 20 · see citing works
Wang, R., Santos, J. M., Dufour, J. M., Stephens, E. R., Miranda, J. M., Washburn, R. L., Hibler, T., Kaur, G., Lin, D., & Shen, C. (2022) · Nutrients · doi:10.3390/nu14204384 · Cited by 20 · see citing works
Resemblance and differences in dietary restriction nephroprotective mechanisms in young and old rats
Andrianova, N. V., Zorova, L. D., Pevzner, I. B., Popkov, V. A., Chernikov, V. P., Silachev, D. N., Plotnikov, E. Y., & Zorov, D. B. (2020) · Aging · doi:10.18632/aging.103960 · Cited by 20 · see citing works
Sato, T., Yasuzawa, T., Uesaka, A., Izumi, Y., Kamiya, A., Tsuchiya, K., Kobayashi, Y., Kuwahata, M., & Kido, Y. (2014) · Nutrition Research · doi:10.1016/j.nutres.2014.04.013 · Cited by 19 · see citing works
Storoschuk, K. L., Lesiuk, D., Nuttall, J., LeBouedec, M. A., Khansari, A., Islam, H., & Gurd, B. J. (2023) · Metabolism · doi:10.1016/j.metabol.2023.155768 · Cited by 20 · see citing works
β-Adrenergic stimulation does not activate p38 MAP kinase or induce PGC-1α in skeletal muscle
Kim, S. H., Asaka, M., Higashida, K., Takahashi, Y., Holloszy, J. O., & Han, D.-H. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00581.2012 · Cited by 19 · see citing works
Self-citationGesing, A., Bartke, A., Wang, F., Karbownik‐Lewińska, M., & Masternak, M. M. (2011) · Cell Biochemistry and Function · doi:10.1002/cbf.1773 · Cited by 19 · see citing works
Wang, H., Arias, E. B., Yu, C. S., Verkerke, A. R. P., & Cartee, G. D. (2017) · The Journals of Gerontology Series A · doi:10.1093/gerona/glx099 · Cited by 18 · see citing works
Epigenetics and Effects on the Neonate That May Impact Feed Efficiency
Meyer, A. M., Caton, J. S. S., Hess, B. W., Ford, S. P., & Reynolds, L. P. (2012) · doi:10.1002/9781118392331.ch13 · Cited by 18 · see citing works
Neuroprotective Effects of Intermittent Fasting in the Aging Brain
Dong, H., Wang, S., Hu, C., Wang, M., Zhou, T., & Zhou, Y. (2024) · Annals of Nutrition and Metabolism · doi:10.1159/000538782 · Cited by 19 · see citing works
Delic, V., Brownlow, M. L., Joly‐Amado, A., Zivkovic, S., Noble, K. V., Phan, T.-A., Ta, Y., Zhang, Y., Bell, S. D., Kurien, C., et al. (2015) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2015.06.001 · Cited by 17 · see citing works
Mulvey, L., Sands, W. A., Salin, K., Carr, A. E., & Selman, C. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.09.001 · Cited by 16 · see citing works
The Roles of White Adipose Tissue and Liver NADPH in Dietary Restriction-Induced Longevity
Jamerson, L. E., & Bradshaw, P. C. (2024) · Antioxidants · doi:10.3390/antiox13070820 · Cited by 18 · see citing works
Milton‐Laskibar, I., Aguirre, L., Fernández‐Quintela, A., Rolo, A. P., Teodoro, J. S., Palmeira, C. M., & Portillo, M. P. (2017) · Nutrients · doi:10.3390/nu9070737 · Cited by 16 · see citing works
Molecular Mechanisms of Intermittent Fasting-induced Ischemic Tolerance.
Vemuganti, R., & Arumugam, T. V. (2020) · PubMed · Cited by 16 · see citing works
Effects of maternal dietary olive oil on pathways involved in diabetic embryopathy
Higa, R., Roberti, S. L., Musikant, D., Mazzucco, M. B., White, V., & Jawerbaum, A. (2014) · Reproductive Toxicology · doi:10.1016/j.reprotox.2014.09.004 · Cited by 16 · see citing works
Qi, Z., & Ding, S. (2012) · PPAR Research · doi:10.1155/2012/348245 · Cited by 16 · see citing works
The Role of Nutrition in Attenuating Age-Related Skeletal Muscle Atrophy
Abiri, B., & Vafa, M. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-42667-5_12 · Cited by 14 · see citing works
Gesing, A., Masternak, M. M., Lewiñski, A., Karbownik‐Lewińska, M., Kopchick, J. J., & Bartke, A. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls231 · Cited by 14 · see citing works
Mitochondrial energetics in liver and skeletal muscle after energy restriction in young rats
Crescenzo, R., Bianco, F., Falcone, I., Coppola, P., Dulloo, A. G., Liverini, G., & Iossa, S. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511005903 · Cited by 14 · see citing works
Sex Specific Differences in Response to Calorie Restriction in Skeletal Muscle of Young Rats
Torrens‐Mas, M., Navas-Enamorado, C., Wahl, D., Sánchez-Polo, A., Picca, A., Oliver, J., Roca, P., & González‐Freire, M. (2022) · Nutrients · doi:10.3390/nu14214535 · Cited by 13 · see citing works
Estey, C., Seifert, E. L., Aguer, C., Moffat, C., & Harper, M. (2012) · Experimental Gerontology · doi:10.1016/j.exger.2012.02.008 · Cited by 13 · see citing works
Keeping the beat against time: Mitochondrial fitness in the aging heart
Mendoza, A., & Karch, J. M. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.951417 · Cited by 13 · see citing works
D’Aquila, P., Rango, F. D., Guarasci, F., Mandalà, M., Corsonello, A., Bellizzi, D., & Passarino, G. (2020) · Nutrients · doi:10.3390/nu12020460 · Cited by 12 · see citing works
Torma, F., Bori, Z., Koltai, E., Felszeghy, K., Vácz, G., Koch, L. G., Britton, S. L., Boldogh, I. R., & Radak, Z. O. (2014) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2014.07.003 · Cited by 11 · see citing works
Food restriction modifies ultrastructure of hippocampal synapses
Babits, R., Szőke, B., Sótonyi, P., & Rácz, B. (2015) · Hippocampus · doi:10.1002/hipo.22533 · Cited by 10 · see citing works
Mitochondria: Master Regulator of Metabolism, Homeostasis, Stress, Aging and Epigenetics
Meiliana, A., Dewi, N. M., & Wijaya, A. (2021) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v13i3.1616 · Cited by 7 · see citing works
Lim, V. J. T., Tabassum, N. I., Orian, J. M., Arumugam, T. V., & Weng, E. F.-J. (2025) · Progress in brain research · doi:10.1016/bs.pbr.2025.05.003 · Cited by 7 · see citing works
- Authors
- Hancock, C. R., Han, D., Higashida, K., Kim, S. H., & Holloszy, J. O.
- Affiliations
- Washington University in St. Louis (US)
- Corresponding author
- Holloszy, John O.
- Venue
- The FASEB Journal
- Publisher
- Wiley
- Published
- 2010-11-03
- Volume
- 25
- Issue
- 2
- Pages
- 785-791
- ISSN
- 0892-6638 (ISSN-L)
- 1530-6860
- PMC
- PMC3023396
- OpenAlex
- W2058512647
- Cited by
- 131
- References
- 45
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 3 · 2022: 6 · 2021: 3 · 2020: 9 · 2019: 6 · 2018: 3 · 2017: 15 · 2016: 8 · 2015: 14 · 2014: 15 · 2013: 12 · 2012: 13
- FWCI
- 5.21
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The FASEB Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (AG00425)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- caloric restriction, mitochondrial biogenesis, mitochondrial proteins, mitochondrial mRNA, citrate synthase, long-chain acyl-CoA dehydrogenase, heart, brain, liver, adipose tissue, skeletal muscle, mitochondrial respiration, ATP production, rats
- MeSH terms
- Adipose Tissue, Animals, Brain, Gene Expression Regulation, Liver, Male, Mitochondria, Myocardium, RNA, Messenger, Rats, Wistar, Muscle, Skeletal, Mitochondrial Proteins, Caloric Restriction, Rats
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