The DOI matches its Crossref record; 26 of the 26 references it cites were found in a registry or an index.
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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In the citing paper
“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
Citations
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
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
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
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
Lin, S.-J., Defossez, P.-A., & Guarente, L. (2000) · Science · doi:10.1126/science.289.5487.2126 · Cited by 1,775
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
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
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 1,155
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
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
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
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
Caloric restriction and aging: an update
Masoro, E. J. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00084-x · Cited by 615
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
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
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
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
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
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 156
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
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 97
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
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
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
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
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
Flagged first, then by citations
Research works printed but not linked: 2
- Y. Higami et al., FASEB J.18, 415 (2004).
- S. Cook et al., Swiss Med. Wkly.133, 360 (2003).
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Therapeutic potential of resveratrol: the in vivo evidence
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“, which is consistent with observations in calorie-restricted animal”
ResultMammalian 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
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
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
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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