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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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“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]
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
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“These enzymes are signalling nexuses pivotal to endothelial cell homeostasis and are linked to each other by a positive feedback loop, where eNOS stimulates the expression of SIRT-1 (Nisoli et al., 2005) and SIRT-1 activates eNOS (Mattagajasingh et al.”
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“This forms a very interesting positive regulatory loop (Nisoli et al. 2005).”
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Nunn, A. V. W., Bell, J. D., & Guy, G. W. (2009) · Nutrition & Metabolism · doi:10.1186/1743-7075-6-16 · Cited by 77
Gu, Q., Yang, X., Li, L., Li, S., Li, Q., Zhong, S., Peng, J., & Cui, Z. (2014) · Hepatology · doi:10.1002/hep.27356 · Cited by 77
“Previous studies have demonstrated that physiological amounts of NO can positively affect mitochondrial function and participate in mitochondrial biogenesis.(6,7) In addition, NO is shown to induce”
BackgroundNAD+ Homeostasis and NAD+-Consuming Enzymes: Implications for Vascular Health
Campagna, R., & Vignini, A. (2023) · Antioxidants · doi:10.3390/antiox12020376 · Cited by 76
“While the upregulation of SIRT1, consequent to caloric restriction, is reduced in eNOS knockout mice, the overexpression of human SIRT1 displays a protective effect against age-related adverse arterial remodeling of eNOS-deficient mice, thus indicating a complex reciprocal regulation in the endothelium [70].”
BackgroundPatel, B. P., Safdar, A., Raha, S., Tarnopolsky, M. A., & Hamadeh, M. J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009386 · Cited by 76
“cy in both animals and humans [26–28].”
Emerging Roles of Endothelial Nitric Oxide in Preservation of Cognitive Health
Katusic, Z. S., d’Uscio, L. V., & He, T. (2023) · Stroke · doi:10.1161/strokeaha.122.041444 · Cited by 73
Nitric oxide regulates vascular adaptive mitochondrial dynamics
Miller, M. W., Knaub, L. A., Olivera-Fragoso, L. F., Keller, A. C., Balasubramaniam, V., Watson, P. A., & Reusch, J. E. B. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00987.2012 · Cited by 71
Midlife gene expressions identify modulators of aging through dietary interventions
Zhou, B., Liu, Y., Li, S., Huang, J., Chen, H., Hou, L., Wang, J., Green, C. D., Yan, Z., Huang, X., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119304109 · Cited by 72
Aging Fits the Disease Criteria of the International Classification of Diseases
Khaltourina, D. A., Matveyev, Y., Alekseev, A., Cortese, F., & Ioviţă, A. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111230 · Cited by 78
Park, S., Mori, R., & Shimokawa, I. (2013) · Molecules and Cells · doi:10.1007/s10059-013-0130-x · Cited by 75
“CR and resveratrol increase endothelial-derived nitric oxide (NO) (Csiszar et al., 2009; Nisoli et al., 2005), an important regulator of vascular relaxation and endothelial senescence (Oemar et al., 1998).”
BackgroundDeletion of the Mitochondrial Chaperone TRAP-1 Uncovers Global Reprogramming of Metabolic Networks
Lisanti, S., Tavecchio, M., Chae, Y. C., Liu, Q., Brice, A. K., Thakur, M. L., Languino, L. R., & Altieri, D. C. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.06.061 · Cited by 69
“However, increased mitochondrial respiration, as paradoxically induced as compensation for TRAP-1 loss (this study), has been associatedwith extended lifespan in model organisms (Guarente, 2008), potentially contributing to the increased longevity afforded by calorie restriction (Nisoli et al., 2005).”
BackgroundO'Donnell, E., Goodman, J., & Harvey, P. (2011) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2011-1223 · Cited by 2
Impact of nitric oxide on metabolism in health and age‐related disease
Knott, A. B., & Bossy‐Wetzel, E. (2010) · Diabetes Obesity and Metabolism · doi:10.1111/j.1463-1326.2010.01267.x · Cited by 73
“eNOS is required for CR mitochondrial benefits and SIRT1 induction as eNOS null mice do not show the same effects [53].”
BackgroundInfluentialRan, J., Li, H., Fu, J., Liu, L., Xing, Y., Li, X., Shen, H., Chen, Y., Jiang, X., Li, H., et al. (2013) · BMC Systems Biology · doi:10.1186/1752-0509-7-32 · Cited by 70
“A recent study has shown that production of NO, stimulated by caloric restriction, increases SIRT1 expression; this study suggests that eNOS may be involved in regulation of the expression of SIRT1 in murine white adipocytes [17].”
BackgroundAnti-aging molecule, Sirt1: a novel therapeutic target for diabetic nephropathy
Kume, S., Kitada, M., Kanasaki, K., Maegawa, H., & Koya, D. (2013) · Archives of Pharmacal Research · doi:10.1007/s12272-013-0019-4 · Cited by 71
“2004), nitric oxide (NO) (Nisoli et al. 2005), and aldosterone (Fan et al.”
BackgroundNRF2 and the Phase II Response in Acute Stress Resistance Induced by Dietary Restriction
Hine, C. (2012) · Journal of Clinical & Experimental Pathology · doi:10.4172/2161-0681.s4-004 · Cited by 69
“elegans [46], flies [50] and rodents [51] points to increased rates of oxidative phosphorylation often accompanied by increased mitochondrial biogenesis.”
BackgroundContribution of mitochondrial oxidative stress to hypertension
Dikalov, S., & Dikalova, A. (2015) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0000000000000198 · Cited by 71
“All rights rese PHYSICAL ACTIVITY AND MITOCHONDRIA Physical activity affects mitochondrial function through multiple pathways, which include shear stress stimulation of NO-mediated mitochondrial biogenesis [60,67], metabolic regulations [68 && ], increased antioxidant expression [69], and NADþ”
BackgroundMitochondrial Abnormalities in Alzheimer’s Disease
Silva, D. F., Selfridge, J. E., Lu, J., E, L., Cardoso, S. M., & Swerdlow, R. H. (2012) · Advances in Pharmacology · doi:10.1016/b978-0-12-394816-8.00003-9 · Cited by 86
“Caloric restriction shifts the liver’s redox balance towards a more oxidized state, and this is associated with mitochondrial biogenesis at least in the liver (Civitarese et al., 2007; Lambert et al., 2004; Lopez-Lluch et al., 2006)and also perhaps in the brain (Nisoli et al., 2005).”
BackgroundThe Spectrum of Fundamental Basic Science Discoveries Contributing to Organismal Aging
Farr, J. N., & Almeida, M. (2018) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3564 · Cited by 70
“The beneficial effects of caloric restriction on bone mass are associated with a twofold induction of Sirt1 expression in bone, as seen in other tissues.((115,116)) Importantly, long-term administration of Sirt1 activators or overexpression of Sirt1 attenuates the loss of bone mass with aging.”
BackgroundCerqueira, F. M., da Cunha, F. M., Laurindo, F. R. M., & Kowaltowski, A. J. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.01.011 · Cited by 71
Sanchez-Roman, I., Gómez, A., Pérez, I., Sanchez, C., Suarez, H., Naudí, A., Jové, M., Lopez-Torres, M., Pamplona, R., & Barja, G. (2012) · Biogerontology · doi:10.1007/s10522-012-9384-5 · Cited by 66
Kaptan, Z., Akgün‐Dar, K., Kapucu, A., Dedeakayoğulları, H., Batu, Ş., & Üzüm, G. (2015) · Brain Research · doi:10.1016/j.brainres.2015.05.041 · Cited by 72
“This situation may increases production of ROS in hippocampus and oxidative damage.”
Meydani, M., Das, S. K., Band, M., Epstein, S., & Roberts, S. B. (2011) · The journal of nutrition health & aging · doi:10.1007/s12603-011-0002-z · Cited by 67
“In addition, CR can induce the expression of eNOS and nitric oxide production (33), which in turn upregulates GPx (34).”
BackgroundMitochondria and Oxidative Stress in the Cardiorenal Metabolic Syndrome
Aroor, A. R., Mandavia, C. H., Ren, J. T., Sowers, J. R., & Pulakat, L. (2012) · Cardiorenal Medicine · doi:10.1159/000335675 · Cited by 67
Karpe, P. A., & Tikoo, K. (2013) · Diabetes · doi:10.2337/db13-1267 · Cited by 70
“As far as the stress response is concerned, calorie restriction or exercise training has also been shown to increase eNOS expression and NO bioavailability, which are implicated in mitochondrial biogenesis (22).”
BackgroundSirtuin-1 and Its Relevance in Vascular Calcification
Lu, C., Liao, M.-T., Hou, Y., Fang, Y.-W., Zheng, C., Liu, W.-C., Chao, C., Lu, K., & Ng, Y.-Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051593 · Cited by 67
“CR is a dietary regimen that induces eNOS expression and is accompanied by enhanced Sirt1 levels, which is considered a link to delay aging and extend the lifespan in mammals [53].”
BackgroundShinmura, K. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/528935 · Cited by 67
Luckhart, S., Giulivi, C., Drexler, A., Antonova‐Koch, Y., Sakaguchi, D., Napoli, E., Wong, S., Price, M. S., Eigenheer, R. A., Phinney, B. S., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003180 · Cited by 68
“PGC-1a expression [82–84].”
Arunachalam, G., Sundar, I. K., Hwang, J., Yao, H., & Rahman, I. (2010) · Journal of Inflammation · doi:10.1186/1476-9255-7-34 · Cited by 66
“Recently, we and others have shown that eNOS is regulated by acetylation/deacetylation via SIRT1 deacetylase or calorie restriction [34,39,40].”
BackgroundRole of sirtuins, calorie restriction and physical activity in aging
Corbi, G. (2011) · Frontiers in Bioscience-Elite · doi:10.2741/417 · Cited by 66
Shalwala, M., Zhu, S., Das, A., Salloum, F. N., Xi, L., & Kukreja, R. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086977 · Cited by 65
“Based on the reported NO-dependence of SIRT1 induction and cardioprotection by caloric restriction [13,19], we hypothesized that SIRT1 activation may be necessary for the cardioprotective effect of SIL, which is also mediated by NO signaling [2,4].”
Bahadorani, S., Cho, J., Lo, T., Contreras, H. L., Lawal, H. O., Krantz, D. E., Bradley, T. J., & Walker, D. W. (2010) · Aging Cell · doi:10.1111/j.1474-9726.2010.00546.x · Cited by 66
“Previous studies in mammalian model systems have reported a positive correlation between increased respiratory chain activity and longevity (Speakman et al., 2004; Nisoli et al., 2005; Katic et al., 2007; Caldeira da Silva et al., 2008).”
BackgroundGalkin, A. S., Higgs, A., & Moncada, S. (2007) · Essays in Biochemistry · doi:10.1042/bse0430029 · Cited by 66
“We have also shown that mitochondrial biogenesis is reduced in eNOS / mice following either exposure to cold or calorie restriction, thus providing further evidence that a NO/cGMP-dependent pathway plays a signifi cant role in the control of mitochondrial biogenesis and the body energy balance [56].”
Background
Metadata
- 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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