Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS
Abstract
Calorie restriction extends life span in organisms ranging from yeast to mammals. Here, we report that calorie restriction for either 3 or 12 months induced endothelial nitric oxide synthase (eNOS) expression and 3',5'-cyclic guanosine monophosphate formation in various tissues of male mice. This was accompanied by mitochondrial biogenesis, with increased oxygen consumption and adenosine triphosphate production, and an enhanced expression of sirtuin 1. These effects were strongly attenuated in eNOS null-mutant mice. Thus, nitric oxide plays a fundamental role in the processes induced by calorie restriction and may be involved in the extension of life span in mammals.
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Mitochondrial physiology is involved in the beneficial effects of calorie restriction in budding yeast, C. elegans, and mammals.
“Although the mechanisms behind calorie restriction-driven longevity extension are still poorly understood, mitochondrial physiology is involved in the beneficial effects of calorie restriction in budding yeast11 and Caenorhabditis elegans12, as well as in mammals13.”
From Mitochondrial and metabolic dysfunction in ageing and age-related diseases (2022) · cites this paper as [13]
eNOS is induced by calorie restriction in mice and human muscle.
“eNOS is induced by CR in mice and human muscle”
From Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity (2017) · cites this paper as Nisoli et al., 2005
Calorie-restriction-induced mitochondrial biogenesis in mice increases PGC-1α, Mfn1 and Mfn2 expression levels in several tissues.
“Furthermore, calorie-restriction-induced mitochondrial biogenesis in mice increases PGC-1α, Mfn1 and Mfn2 expression levels in several tissues (Nisoli et al., 2005).”
From New insights into the role of mitochondria in aging: mitochondrial dynamics and more (2010) · cites this paper as Nisoli et al., 2005
Caloric restriction increases mitochondrial biogenesis.
“A number of studies have shown that CR increases mitochondrial biogenesis (Nisoli et al., 2005; Lopez-Lluch et al., 2006)”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as Nisoli et al., 2005
Caloric restriction increases mitochondrial efficiency.
“and mitochondrial efficiency (Nisoli et al., 2005)”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as Nisoli et al., 2005
Cites
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
Negative Control of p53 by Sir2α Promotes Cell Survival under Stress
Luo, J., Nikolaev, A. Y., Imai, S.-I., Chen, D., Su, F., Shiloh, A., Guarente, L., & Gu, W. (2001) · Cell · doi:10.1016/s0092-8674(01)00524-4 · Cited by 2,081 · see citing works
Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-γ
Picard, F., Kurtev, M. V., Chung, N., Topark‐Ngarm, A., Senawong, T., de Oliveira, R. M., Leid, M. E., McBurney, M. W., & Guarente, L. (2004) · Nature · doi:10.1038/nature02583 · Cited by 1,943 · see citing works
Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase
Cohen, H. Y., Miller, C., Bitterman, K. J., Wall, N. R., Hekking, B., Kessler, B., Howitz, K. T., Gorospe, M., de Cabo, R., & Sinclair, D. A. (2004) · Science · doi:10.1126/science.1099196 · Cited by 1,924 · see citing works
Lin, S.-J., Defossez, P.-A., & Guarente, L. (2000) · Science · doi:10.1126/science.289.5487.2126 · Cited by 1,775 · see citing works
Extended Longevity in Mice Lacking the Insulin Receptor in Adipose Tissue
Blüher, M., Kahn, B. B., & Kahn, C. R. (2003) · Science · doi:10.1126/science.1078223 · Cited by 1,348 · 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
Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide
Nisoli, E., Clementi, E., Paolucci, C., Cozzi, V., Tonello, C., Sciorati, C., Bracale, R., Valerio, A., Francolini, M., Moncada, S., et al. (2003) · Science · doi:10.1126/science.1079368 · Cited by 1,243 · see citing works
Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration
Lin, S.-J., Kaeberlein, M., Andalis, A. A., Sturtz, L. A., Defossez, P.-A., Culotta, V. C., Fink, G. R., & Guarente, L. (2002) · Nature · doi:10.1038/nature00829 · Cited by 1,057 · see citing works
Structural Basis of Mitochondrial Tethering by Mitofusin Complexes
Koshiba, T., Detmer, S. A., Kaiser, J. T., Chen, H., McCaffery, J. M., & Chan, D. C. (2004) · Science · doi:10.1126/science.1099793 · Cited by 910 · see citing works
Mitofusin-2 Determines Mitochondrial Network Architecture and Mitochondrial Metabolism
Bach, D., Pich, S., Soriano, F. X., Vega, N., Baumgartner, B., Oriola, J., Daugaard, J. R., Lloberas, J., Camps, M., Zierath, J. R., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212754200 · Cited by 832 · see citing works
Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cerevisiae
Anderson, R. M., Bitterman, K. J., Wood, J. G., Medvedik, O., & Sinclair, D. A. (2003) · Nature · doi:10.1038/nature01578 · Cited by 736 · see citing works
Caloric restriction and aging: an update
Masoro, E. J. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00084-x · Cited by 615 · see citing works
Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals
Nisoli, E., Falcone, S., Tonello, C., Cozzi, V., Palomba, L., Fiorani, M., Pisconti, A., Brunelli, S., Cardile, A., Francolini, M., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405432101 · Cited by 495 · see citing works
Self-citationGoodrick, C. L., Ingram, D. K., Reynolds, M. A., Freeman, J. R., & Cider, N. (1990) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(90)90107-q · Cited by 279 · see citing works
Action of food restriction in delaying the aging process
Masoro, E. J., Yu, B. P., & Bertrand, H. A. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.13.4239 · Cited by 247 · see citing works
Development of Calorie Restriction Mimetics as a Prolongevity Strategy
Ingram, D. K., Anson, R. M., de Cabo, R., Mamczarz, J., Zhu, M., Mattison, J. A., Lane, M. A., & Roth, G. S. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1297.074 · Cited by 194 · see citing works
Higami, Y., Pugh, T. D., Page, G. P., Allison, D. B., Prolla, T. A., & Weindruch, R. (2004) · The FASEB Journal · doi:10.1096/fj.03-0678fje · Cited by 173 · see citing works
Clustering of cardiovascular risk factors mimicking the human metabolic syndrome X in eNOS null mice
Egli, M., Vollenweider, P., Burcelin, R., Nicod, P., & Thorens, B. (2003) · Swiss Medical Weekly · doi:10.4414/smw.2003.10239 · Cited by 161 · see citing works
No reduction of metabolic rate in food restricted Caenorhabditis elegans
Houthoofd, K., Braeckman, B. P., Lenaerts, I., Brys, K., Vreese, A. D., Eygen, S. V., & Vanfleteren, J. R. (2002) · Experimental Gerontology · doi:10.1016/s0531-5565(02)00172-9 · Cited by 129 · see citing works
Effect of a C/EBP gene replacement on mitochondrial biogenesis in fat cellsPreprint
Chiu, C., Lin, W., Huang, S.-Y., & Lee, Y.-H. (2004) · Genes & Development · doi:10.1101/gad.1213104 · Cited by 96 · see citing works
Miwa, S., Riyahi, K., Partridge, L., & Brand, M. D. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1297.069 · Cited by 89 · see citing works
Cloning and mRNA tissue distribution of human PPARγ coactivator-1
Larrouy, D., Vidal, H., Andréelli, F., Laville, M., & Langin, D. (1999) · International Journal of Obesity · doi:10.1038/sj.ijo.0801106 · Cited by 84 · see citing works
Dessı̀-Fulgheri, P., Sarzani, R., Serenelli, M., Tamburrini, P., Spagnolo, D., Giantomassi, L., Espinosa, E., & RAPPELLI, A. (1999) · Hypertension · doi:10.1161/01.hyp.33.2.658 · Cited by 71 · see citing works
Dere, E., Silva, M. A. D. S., Topic, B., Fiorillo, C., Li, J., Sadile, A. G., Frisch, C. M., & Huston, J. P. (2002) · Genes Brain & Behavior · doi:10.1034/j.1601-183x.2002.10402.x · Cited by 35 · see citing works
Weight Loss and Race Modulate Nitric Oxide Metabolism in Overweight Women
Fenster, C. P., Darley-Usmar, V. M., Landar, A. L., Gower, B. A., Weinsier, R. L., Hunter, G. R., & Patel, R. P. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.05.021 · Cited by 23 · see citing works
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Baur, J. A., Pearson, K. J., Price, N. L., Jamieson, H. A., Lerin, C., Kalra, A., Prabhu, V. V., Allard, J. S., Lopez-Lluch, G., Lewis, K., et al. (2006) · Nature · doi:10.1038/nature05354 · Cited by 4,290 · see citing works
Therapeutic potential of resveratrol: the in vivo evidence
Baur, J. A., & Sinclair, D. A. (2006) · Nature Reviews Drug Discovery · doi:10.1038/nrd2060 · Cited by 3,958 · see citing works
Mammalian Sirtuins: Biological Insights and Disease Relevance
Haigis, M. C., & Sinclair, D. A. (2010) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev.pathol.4.110807.092250 · Cited by 2,085 · see citing works
Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes
Milne, J. C., Lambert, P. D., Schenk, S., Carney, D. P., Smith, J. J., Gagne, D. J., Jin, L., Boss, O., Perni, R. B., Vu, C. B., et al. (2007) · Nature · doi:10.1038/nature06261 · Cited by 1,707 · see citing works
Cancer metabolism: a therapeutic perspective
Martinez-Outschoorn, U. E., Peiris-Pagés, M., Pestell, R. G., Sotgia, F., & Lisanti, M. P. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2016.60 · Cited by 1,505 · see citing works
Recent progress in the biology and physiology of sirtuins
Finkel, T., Deng, C., & Mostoslavsky, R. (2009) · Nature · doi:10.1038/nature08197 · Cited by 1,484 · see citing works
Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals?
Giorgio, M., Trinei, M., Migliaccio, E., & Pelicci, P. G. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2240 · Cited by 1,450 · see citing works
Mitochondrial energetics in the kidney
Bhargava, P., & Schnellmann, R. G. (2017) · Nature Reviews Nephrology · doi:10.1038/nrneph.2017.107 · Cited by 1,363 · see citing works
Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation
Qiu, X., Brown, K., Hirschey, M. D., Verdin, E., & Chen, D. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.11.015 · Cited by 1,310 · see citing works
Mammalian sirtuins—emerging roles in physiology, aging, and calorie restriction
Haigis, M. C., & Guarente, L. P. (2006) · Genes & Development · doi:10.1101/gad.1467506 · Cited by 1,295 · see citing works
Mitochondria and reactive oxygen species
Kowaltowski, A. J., de Souza-Pinto, N. C., Castilho, R. F., & Vercesi, A. E. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.05.004 · Cited by 1,162 · see citing works
Role of Mitochondrial Dysfunction in Insulin Resistance
Kim, J.-A., Wei, Y., & Sowers, J. R. (2008) · Circulation Research · doi:10.1161/circresaha.107.165472 · Cited by 1,103 · see citing works
The role of mitochondria in aging
Bratic, A., & Larsson, N.-G. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64125 · Cited by 1,087 · see citing works
Mitochondrial and metabolic dysfunction in ageing and age-related diseases
Amorim, J. A., Coppotelli, G., Rolo, A. P., Palmeira, C. M., Ross, J. M., & Sinclair, D. A. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-021-00626-7 · Cited by 990 · see citing works
Mitochondrial Dynamics in Mammalian Health and Disease
Liesa, M., Palacín, M., & Zorzano, A. (2009) · Physiological Reviews · doi:10.1152/physrev.00030.2008 · Cited by 953 · see citing works
Transcriptional control of mitochondrial biogenesis: the central role of PGC-1
Ventura-Clapier, R., Garnier, A., & Veksler, V. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn098 · Cited by 932 · see citing works
Ungvari, Z., Tarantini, S., Donato, A. J., Galvan, V., & Csiszar, A. (2018) · Circulation Research · doi:10.1161/circresaha.118.311378 · Cited by 919 · see citing works
AMPK and SIRT1: a long-standing partnership?
Ruderman, N. B., Julia Xu, X., Nelson, L., Cacicedo, J. M., Saha, A. K., Lan, F., & Ido, Y. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00745.2009 · Cited by 903 · see citing works
Mattagajasingh, I., Kim, C.-S., Naqvi, A., Yamamori, T., Hoffman, T. A., Jung, S.-B., DeRicco, J., Kasuno, K., & Irani, K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704329104 · Cited by 881 · see citing works
Cardiovascular Actions of Insulin
Muniyappa, R., Montagnani, M., Koh, K. K., & Quon, M. J. (2007) · Endocrine Reviews · doi:10.1210/er.2007-0006 · Cited by 873 · see citing works
Nitric oxide signaling in health and disease
Lundberg, J. O., & Weitzberg, E. (2022) · Cell · doi:10.1016/j.cell.2022.06.010 · Cited by 850 · see citing works
Nitric oxide signalling in cardiovascular health and disease
Farah, C., Michel, L. Y. M., & Balligand, J.-L. (2018) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.224 · Cited by 779 · 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
Mitochondria are required for pro-ageing features of the senescent phenotype
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
Ristow, M., & Zarse, K. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.03.014 · Cited by 789 · 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
Molecular mechanisms of dietary restriction promoting health and longevity
Green, C. L., Lamming, D. W., & Fontana, L. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00411-4 · Cited by 714 · see citing works
Luen Tang, B. (2016) · Molecules and Cells · doi:10.14348/molcells.2016.2318 · Cited by 740 · see citing works
Resveratrol stimulates AMP kinase activity in neurons
Dasgupta, B., & Milbrandt, J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610068104 · Cited by 723 · see citing works
Translational Regulation of Gene Expression during Conditions of Cell Stress
Spriggs, K. A., Bushell, M., & Willis, A. E. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.028 · Cited by 721 · see citing works
SIRT1 transgenic mice show phenotypes resembling calorie restriction
Bordone, L., Cohen, D., Robinson, A., Motta, M. C., Van Veen, E., Czopik, A., Steele, A. D., Crowe, H., Marmor, S., Luo, J., et al. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00335.x · Cited by 722 · see citing works
Extending life span by increasing oxidative stress
Ristow, M., & Schmeisser, S. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.05.010 · Cited by 718 · see citing works
Transcriptional Control of Mitochondrial Biogenesis and Function
Hock, M. B., & Kralli, A. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163119 · Cited by 616 · see citing works
Barger, J. L., Kayo, T., Vann, J. M., Arias, E. B., Wang, J., Hacker, T. A., Wang, Y., Raederstorff, D., Morrow, J. D., Leeuwenburgh, C., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002264 · Cited by 580 · see citing works
Endothelial dysfunction in diabetes mellitus: Molecular mechanisms and clinical implications
Tabit, C. E., Chung, W. B., Hamburg, N. M., & Vita, J. A. (2010) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-010-9134-4 · Cited by 584 · see citing works
Oxidative stress and vascular inflammation in aging
Assar, M. E., Angulo, J., & Rodríguez‐Mañas, L. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.07.003 · Cited by 576 · see citing works
The neuroprotective properties of calorie restriction, the ketogenic diet, and ketone bodies
Maalouf, M., Rho, J. M., & Mattson, M. P. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.09.002 · Cited by 575 · see citing works
D'Antona, G., Ragni, M., Cardile, A., Tedesco, L., Dossena, M., Bruttini, F., Caliaro, F., Corsetti, G., Bottinelli, R., Carruba, M. O., et al. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.08.016 · Cited by 568 · see citing works
Self-citationTissue-specific regulation of SIRT1 by calorie restriction
Chen, D., Bruno, J., Easlon, E., Lin, S.-J., Cheng, H.-L., Alt, F. W., & Guarente, L. (2008) · Genes & Development · doi:10.1101/gad.1650608 · Cited by 567 · see citing works
Adipokines as novel biomarkers and regulators of the metabolic syndrome
Deng, Y., & Scherer, P. E. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05875.x · Cited by 558 · see citing works
4E-BP Extends Lifespan upon Dietary Restriction by Enhancing Mitochondrial Activity in Drosophila
Zid, B. M., Rogers, A. N., Katewa, S. D., Vargas, M. A., Kolipinski, M., Lu, T. A., Benzer, S., & Kapahi, P. (2009) · Cell · doi:10.1016/j.cell.2009.07.034 · Cited by 541 · 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
Mechanisms of Vascular Aging: New Perspectives
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Vanhatalo, A., Bailey, S. J., Blackwell, J. R., DiMenna, F. J., Pavey, T. G., Wilkerson, D. P., Benjamin, N., Winyard, P. G., & Jones, A. M. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00206.2010 · Cited by 529 · see citing works
Haigis, M. C., & Yankner, B. A. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.10.002 · Cited by 525 · see citing works
New insights into the role of mitochondria in aging: mitochondrial dynamics and more
Seo, A. Y., Joseph, A.-M., Dutta, D., Hwang, J. C. Y., Aris, J. P., & Leeuwenburgh, C. (2010) · Journal of Cell Science · doi:10.1242/jcs.070490 · Cited by 522 · 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
Guarente, L. (2011) · New England Journal of Medicine · doi:10.1056/nejmra1100831 · Cited by 510 · see citing works
(2010) · doi:10.1016/j.cmet.2010.06.009 · Cited by 512 · see citing works
Mitochondria and Endothelial Function
Kluge, M. A., Fetterman, J. L., & Vita, J. A. (2013) · Circulation Research · doi:10.1161/circresaha.111.300233 · Cited by 508 · see citing works
Redox regulation of SIRT1 in inflammation and cellular senescence
Hwang, J.-W., Yao, H., Caito, S., Sundar, I. K., & Rahman, I. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.03.015 · Cited by 503 · see citing works
Mitofusins, from Mitochondria to Metabolism
Schrepfer, E., & Scorrano, L. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.022 · Cited by 490 · see citing works
Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog
Rera, M., Bahadorani, S., Cho, J., Koehler, C. L., Ulgherait, M., Hur, J. H., Ansari, W. S., Lo, T., Jones, D. L., & Walker, D. W. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.09.013 · Cited by 472 · see citing works
Terman, A., Kurz, T., Navratil, M., Arriaga, E. A., & Brunk, U. T. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2598 · Cited by 490 · see citing works
Insulin resistance and atherosclerosis
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Mechanisms of Disease: endothelial dysfunction in insulin resistance and diabetes
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Sirtuins as potential targets for metabolic syndrome
Guarente, L. (2006) · Nature · doi:10.1038/nature05486 · Cited by 468 · see citing works
Maalouf, M., Sullivan, P. G., Davis, L. M., Kim, D., & Rho, J. M. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.11.065 · Cited by 477 · see citing works
Calorie restriction and sirtuins revisited
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Nitric oxide and atherosclerosis: An update
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Mitochondria and Reactive Oxygen Species in Aging and Age-Related Diseases
Giorgi, C., Marchi, S., Simões, I. C. M., Ren, Z., Morciano, G., Perrone, M., Patalas‐Krawczyk, P., Borchard, S., Jędrak, P., Pierzynowska, K., et al. (2018) · International review of cytology · doi:10.1016/bs.ircmb.2018.05.006 · Cited by 467 · see citing works
Effects of Sex, Strain, and Energy Intake on Hallmarks of Aging in Mice
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SIRT3 deacetylates FOXO3 to protect mitochondria against oxidative damage.
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Resveratrol induces mitochondrial biogenesis in endothelial cells
Csiszár, A., Labinskyy, N., Pinto, J. T., Ballabh, P., Zhang, H., Losonczy, G., Pearson, K. J., de Cabo, R., Pacher, P., Zhang, C., et al. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00368.2009 · Cited by 450 · see citing works
Protective effects of sirtuins in cardiovascular diseases: from bench to bedside
Winnik, S. H., Auwerx, J. H., Sinclair, D. A., & Matter, C. M. (2015) · European Heart Journal · doi:10.1093/eurheartj/ehv290 · Cited by 443 · see citing works
Mitochondria and Cardiovascular Aging
Dai, D., Rabinovitch, P. S., & Ungvari, Z. I. (2012) · Circulation Research · doi:10.1161/circresaha.111.246140 · Cited by 435 · see citing works
Targeting Sirtuin 1 to Improve Metabolism: All You Need Is NAD+?
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Mitochondria and Neuroplasticity
Cheng, A., Hou, Y., & Mattson, M. P. (2010) · ASN NEURO · doi:10.1042/an20100019 · Cited by 433 · 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 Biogenesis and Proteome Remodeling Promote One-Carbon Metabolism for T Cell Activation
Ron-Harel, N., Santos, D., Ghergurovich, J. M., Sage, P. T., Reddy, A., Lovitch, S. B., Dephoure, N., Satterstrom, F. K., Sheffer, M., Spinelli, J. B., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.06.007 · Cited by 429 · see citing works
Sirtuins — novel therapeutic targets to treat age-associated diseases
Lavu, S., Boss, O., Elliott, P. J., & Lambert, P. (2008) · Nature Reviews Drug Discovery · doi:10.1038/nrd2665 · Cited by 425 · see citing works
Genetic links between diet and lifespan: shared mechanisms from yeast to humans
Bishop, N. A., & Guarente, L. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2188 · Cited by 421 · see citing works
Figueira, T. R., de Barros, M. H., Camargo, A. A., Castilho, R. F., Ferreira, J. C. B., Kowaltowski, A. J., Sluse, F. E., de Souza-Pinto, N. C., & Vercesi, A. E. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4729 · Cited by 417 · see citing works
Conserved Metabolic Regulatory Functions of Sirtuins
Schwer, B., & Verdin, E. M. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.006 · Cited by 415 · see citing works
Monda, M., Messina, G., Scognamiglio, I., Lombardi, A., Martin, G., Sperlongano, P., Porcelli, M., Caraglia, M., & Stiuso, P. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/131024 · Cited by 411 · see citing works
Nitric Oxide and the Vascular Endothelium
Moncada, S., & Higgs, E. A. (2006) · Springer eBooks · doi:10.1007/3-540-32967-6_7 · Cited by 408 · see citing works
Villena, J. A. (2014) · FEBS Journal · doi:10.1111/febs.13175 · Cited by 404 · see citing works
Sirtuins: The ‘ <i>magnificent seven</i> ’, function, metabolism and longevity
Dali‐Youcef, N., Lagouge, M., Froelich, S., Koehl, C., Schoonjans, K., & Auwerx, J. (2007) · Annals of Medicine · doi:10.1080/07853890701408194 · Cited by 402 · see citing works
Caloric restriction, SIRT1 and longevity
Cantó, C., & Auwerx, J. (2009) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2009.03.008 · Cited by 395 · see citing works
SIRT1 and SIRT6 Signaling Pathways in Cardiovascular Disease Protection
D’Onofrio, N., Servillo, L., & Balestrieri, M. L. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7178 · Cited by 389 · see citing works
Ten years of NAD-dependent SIR2 family deacetylases: implications for metabolic diseases
Imai, S., & Guarente, L. (2010) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.02.003 · Cited by 387 · see citing works
Zhang, Q., Wang, Z., Chen, H., Zhou, S., Zheng, W., Liu, G., Wei, Y.-S., Cai, H. “., Liu, D., & Liang, C. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn224 · Cited by 388 · see citing works
Thomas, S. R., Witting, P. K., & Drummond, G. R. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2027 · Cited by 383 · see citing works
Carlström, M., Larsen, F. J., Nyström, T., Hezel, M., Borniquel, S., Weitzberg, E., & Lundberg, J. O. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008872107 · Cited by 382 · see citing works
Mitochondrial dysfunction as a cause of ageing
Trifunović, A., & Larsson, N. (2008) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2007.01905.x · Cited by 375 · see citing works
Seven sirtuins for seven deadly diseases ofaging
Morris, B. J. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.10.525 · Cited by 380 · see citing works
Sirtuins in Aging and DiseasePreprint
Guarente, L. (2007) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2007.72.024 · Cited by 371 · see citing works
Mitochondrial biogenesis and healthy aging
López-Lluch, G., Irusta, P. M., Navas, P., & de Cabo, R. (2008) · Experimental Gerontology · doi:10.1016/j.exger.2008.06.014 · Cited by 364 · see citing works
Oxidative Stress as a Mediator of Cardiovascular Disease
Elahi, M. M., Kong, Y. X. G., & Matata, B. M. (2009) · Oxidative Medicine and Cellular Longevity · doi:10.4161/oxim.2.5.9441 · Cited by 362 · see citing works
Madamanchi, C., Alhosaini, H., Sumida, A., & Runge, M. S. (2014) · International Journal of Cardiology · doi:10.1016/j.ijcard.2014.08.007 · Cited by 357 · see citing works
Metabolic Effects of Dietary Nitrate in Health and Disease
Lundberg, J. O., Carlström, M., & Weitzberg, E. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.06.007 · Cited by 374 · see citing works
eNOS, metabolic syndrome and cardiovascular disease
Huang, P. L. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.03.005 · Cited by 357 · see citing works
Mitochondrial Quality Control and Disease: Insights into Ischemia-Reperfusion Injury
Anzell, A. R., Maizy, R., Przyklenk, K., & Sanderson, T. H. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0503-9 · Cited by 350 · see citing works
Ungvari, Z. I., Orosz, Z. Z., Labinskyy, N., Rivera, A., Xiangmin, Z., Smith, K. E., & Csiszár, A. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01346.2006 · Cited by 347 · see citing works
Sirtuins mediate mammalian metabolic responses to nutrient availability
Chalkiadaki, A., & Guarente, L. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.225 · Cited by 342 · see citing works
Mitochondria, endothelial cell function, and vascular diseases
Tang, X., Luo, Y., Chen, H., & Liu, D. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00175 · Cited by 345 · see citing works
Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity
da Silva, C. C. C., Cerqueira, F. M., Barbosa, L. F., de Medeiros, M. H. G., & Kowaltowski, A. J. (2008) · Aging Cell · doi:10.1111/j.1474-9726.2008.00407.x · Cited by 346 · see citing works
Lu, Q., Zhu, Y., Deng, C., Liang, Z., Chen, J., Chen, Y., Wang, X., Liu, Y., Tian, Y., & Yang, Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01756-w · Cited by 360 · see citing works
Sergi, 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
Resveratrol—A boon for treating Alzheimer's disease?
Anekonda, T. S. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.04.004 · Cited by 341 · see citing works
- Authors
- Nisoli, E., Tonello, C., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Falcone, S., Valerio, A., Cantoni, O., Clementi, E., Moncada, S., & Carruba, M. O.
- Affiliations
- University of Milan (IT)
- Corresponding author
- Nisoli, Enzo
- ORCID
- Venue
- Science
- Published
- 2005-10-14
- Volume
- 310
- Issue
- 5746
- Pages
- 314-317
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2162306102
- Cited by
- 1,107
- References
- 26
- Citations by year
- 2026: 11 · 2025: 23 · 2024: 28 · 2023: 36 · 2022: 32 · 2021: 44 · 2020: 48 · 2019: 46 · 2018: 37 · 2017: 49 · 2016: 42 · 2015: 70 · 2014: 72 · 2013: 83 · 2012: 103
- FWCI
- 15.75
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Institutional Research Information System (Università degli Studi di Brescia) (submittedVersion)
- Archivio Istituzionale della Ricerca - Università degli Studi del Molise (submittedVersion)
- CINECA IRIS Institutional Research information system (University of Urbino) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Geriatrics and Gerontology › Sirtuins and Resveratrol in Medicine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- caloric restriction, mitochondrial biogenesis, endothelial nitric oxide synthase, nitric oxide, SIRT1, cyclic GMP, lifespan extension, oxygen consumption, ATP production
- MeSH terms
- Adipose Tissue, Animals, DNA, Mitochondrial, Enzyme Induction, Female, Life Expectancy, Male, Mice, Inbred C57BL, Mitochondria, Nitric Oxide, Oxygen Consumption, Protein Biosynthesis, Nitric Oxide Synthase, GTP Phosphohydrolases, Caloric Restriction, Sirtuins, Mice, Nitric Oxide Synthase Type II, Nitric Oxide Synthase Type III, Sirtuin 1
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