Cited by 1,107Genetics, Aging, and Longevity in Model OrganismsSirtuins and Resveratrol in MedicineMitochondrial Function and Pathology

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Calorie Restriction Promotes Mitochondrial Biogenesis by Inducing the Expression of eNOS

Nisoli, Enzo, Tonello, Cristina, Cardile, Annalisa, Cozzi, Valeria, Bracale, Renata, Tedesco, Laura, Falcone, Sestina, Valerio, Alessandra, Cantoni, Orazio, Clementi, Emilio, Moncada, Salvador, Carruba, Michele O.·2005·Science

DOI 10.1126/science.1117728

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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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Background
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Background
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“CR increases the expression of eNOS, accompanied by increased mitochondrial biogenesis, mitochondrial respiration and ATP production (Nisoli et al., 2005; Nisoli and Carruba, 2006).”
BackgroundInfluential
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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“Moreover, the upregulation of SIRT-1 and eNOS in response to calorie restriction has been reported [74].”
Background
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“This apparent paradox may be comparable to the finding that restriction of calories, associated with longevity, was found to enhance eNOS-mediated increase in mitochondrial biogenesis [61].”
Result
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“Thus, increase in the deacetylation (29, 30) and phosphorylation (31) by Sirt1 and AMPK, respectively, would lead to the transcriptional activation of PGC-1s, whereas increased NO production by eNOS would enhance the expression of, at least, PGC-1a (25).”
Background
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“Besides, the genesis of nitric oxide (NO), which could facilitate the bioproduction of mitochondrion according to previous studies [39,40], was enhanced by glabridin, indicating phenols ’ potential effect in restoring the activity of mitochondria.”
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Background
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Background
Retracted
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Background
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“For example, an increase in mitochondrial biogenesis is essential for lifespan extension during DR, both in Drosophila(21) and in mouse.(47) Either ROS or a partial inhibition of mitochondrial respiration can promote mitochondrial biogenesis by activating PGC-1α(48) or the AMPK signaling pathway,(49) respectively.”
Background
Metabolic Alterations Due to Caloric Restriction and Every Other Day Feeding in Normal and Growth Hormone Receptor Knockout Mice
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“CR has also been shown to increase mitochondrial biogenesis, adenosine triphosphate production, and VO 2 in vivo (29).”
Background
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“in mitochondrial biogenesis [14].”
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Background
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Berry, 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 23
“(1234567890) models under some conditions [31, 32], however, in other cases mitochondrial mass remains unchanged by DR [33–35], in line with our results.”
Result
Fibroblast Growth Factor‐21 and the Beneficial Effects of Long‐Chain n‐3 Polyunsaturated Fatty Acids
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Background
Do we age because we have mitochondria?
Bereiter‐Hahn, J. (2013) · PROTOPLASMA · doi:10.1007/s00709-013-0515-x · Cited by 25
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“Nitric oxide has also been reported to exert other aspects of mitochondrial function including the prevention of mitochondrial calcium accumulation, activating expression of a number of mitochondrial proteins including PGC1a, increasing the production of mitochondrial DNA or inhibiting the pathway of apoptosis [34–37].”
Background
Calorie restriction (CR) reduces age-dependent decline of non-homologous end joining (NHEJ) activity in rat tissues
Lee, J.-E., Heo, J., Park, S., Kim, J., Kho, Y., Kang, H., Chung, H. Y., Yoon, J. L., & Lee, J. (2011) · Experimental Gerontology · doi:10.1016/j.exger.2011.07.009 · Cited by 25
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Adiponectin reverses β‐Cell damage and impaired insulin secretion induced by obesity
Munhoz, A. C., Serna, J. D. C., Vilas‐Boas, E. A., da Silva, C. C. C., Santos, T. G., Mosele, F. C., Felisbino, S. L., Martins, V. R., & Kowaltowski, A. J. (2023) · Aging Cell · doi:10.1111/acel.13827 · Cited by 23
“Conversely, PEGylated AdipoRon derivatives, capable of overcoming the poor bioavailability of these adiponectin receptor-activating molecules, improve glucose metabolism in mice fed high fat diets (Onodera et al., 2021).”
Background
Chow diet in mouse aging studies: nothing regular about it
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“Caloric restriction (CR), through a reduction in total diet intake, has been demonstrated to extend longevity in rodents [13, 14].”
Serum levels of cathepsin D, sirtuin1, and endothelial nitric oxide synthase are correlatively reduced in elderly healthy people
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“On the other hand, there are also analyses on various mammalian tissues reporting that a reduction of mitochondrial content leads to an increased ‘workload’ of individual mitochodria which results in a higher inner membrane potential and elevated ROS production [35–38].”
Background
Linking Peroxiredoxin and Vacuolar-ATPase Functions in Calorie Restriction-Mediated Life Span Extension
Molin, M., & Demir, A. B. (2014) · International Journal of Cell Biology · doi:10.1155/2014/913071 · Cited by 25
“Similarly, CR has been observed to increase respiration and mitochondrial ROS production in mice and worms and these increases were reported to be required for the induction of both antioxidant defences and longevity [47, 48].”
Background
Mitogenomic analysis of the genus Pseudois: Evidence of adaptive evolution of morphological variation in the ATP synthase genes
Peng, Q., Tang, L., Tan, S., Li, Z., Wang, J., & Zou, F. (2012) · Mitochondrion · doi:10.1016/j.mito.2012.07.107 · Cited by 24
p66Shc Inactivation Modifies RNS Production, Regulates Sirt3 Activity, and Improves Mitochondrial Homeostasis, Delaying the Aging Process in Mouse Brain
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“High levels are harmful and end in protein oxidation and nitration, leading to loss of mitochondrial and cell function, while controlled levels can induce stress resistance and mitochondrial biogenesis [51].”
Background
Calorie Restriction Improves Physical Performance and Modulates the Antioxidant and Inflammatory Responses to Acute Exercise
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 25
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MicroRNAs mediate metabolic stresses and angiogenesis
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“It has also been found that calorie restriction induces increase of eNOS expression, which is responsible for mitochondrial biogenesis and in part for sirtuin 1 (SIRT1) expression [99].”
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Honeybees and cell lines as models of DNA methylation and aging in response to diet
Ford, D. (2012) · Experimental Gerontology · doi:10.1016/j.exger.2012.07.010 · Cited by 23
The Potential Role of Sirtuins Regarding the Effects of Exercise on Aging- Related Diseases
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Inhibitory effect of paeoniflorin on methylglyoxal-mediated oxidative stress in osteoblastic MC3T3-E1 cells
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“…SIRT1 and its yeast homolog SIR2 appear to be very sensitive to changes in cellular glucose content such as those occurring upon caloric restriction (Lin et al. 2000, Cohen et al. 2004, Nisoli et al. 2005, Civitarese et al. 2007, Chen et al. 2008, Kanfi et al. 2008, Nedachi et al. 2008).”
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Mechanistic Causes of Reduced Cardiorespiratory Fitness in Type 2 Diabetes
Abushamat, L. A., McClatchey, P. M., Scalzo, R. L., Schauer, I. E., Huebschmann, A. G., Nadeau, K. J., Liu, Z., Regensteiner, J. G., & Reusch, J. E. B. (2020) · Journal of the Endocrine Society · doi:10.1210/jendso/bvaa063 · Cited by 23
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“Altering energy metabolism through caloric restriction (Nisoli et al., 2005) is associated with increased mitochondrial biogenesis in the liver, whereas increasing plasma NEFA pharmacologically (Garcia-Roves et al., 2007) or feeding a high fat diet (Hancock et al., 2008) increases mitochondrial…”
Background
Upregulation of Unc-51-Like Kinase 1 by Nitric Oxide Stabilizes SIRT1, Independent of Autophagy
Xing, J., Liu, H., Yang, H., Chen, R., Chen, Y., & Xu, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0116165 · Cited by 23
“For example, when mice are subjected to CR, eNOS expression is increased [21] and is accompanied by increased SIRT1 expression and other changes like increased mitochondrial biogenesis, oxygen consumption, and ATP production.”
Background
Elimination of cardiac arrhythmias using oral taurine with l-arginine with case histories: Hypothesis for nitric oxide stabilization of the sinus node
Eby, G. A., & Halcomb, W. W. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.04.055 · Cited by 24
“With the discovery that caloric restriction, a promising means of life extension, induces NO production [17], interest in nitric oxide and its precursors will likely increase.”
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Gender-specific effects of caloric restriction on the balance of vascular nitric oxide and superoxide radical
Chou, S.-H., Lee, Y.-C., Huang, C.-F., Wang, Y., Yu, H., & Lau, Y. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq095 · Cited by 23
A rare genetic variant of BPIFB4 predisposes to high blood pressure via impairment of nitric oxide signaling
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Midgut Mitochondrial Function as a Gatekeeper for Malaria Parasite Infection and Development in the Mosquito Host
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“stephensi engineered to overexpress activated Akt in the midgut epithelium (Nisoli et al., 2003; Nisoli et al., 2004; Nisoli et al., 2005; Fernandez-Marcos and Auwerx, 2011; Luckhart et al., 2013).”
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Klotho and SIRT1 changes from pre-diabetes to diabetes and pre-hypertension to hypertension
Yeganeh‐Hajahmadi, M., Najafipour, H., Rostamzadeh, F., & Naghibzadeh‐Tahami, A. (2021) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-021-00736-2 · Cited by 22
“After the first report showing that SIRT1 activates eNOS [13], several studies using mutated rats showed that SIRT1 has protective effects against atherosclerosis [11–14].”
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Sustained hypoxia modulates mitochondrial DNA content in the neonatal rat brain
Lee, H. M., Greeley, G. H., & Englander, E. W. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.11.005 · Cited by 22
“The role of NO in mitochondrial biogenesis was further corroborated by demonstrating that caloric restriction (CR) can induce mitochondrial biogenesis in an eNOS dependent manner [21] and that mitochondrial biogenesis is diminished in both, eNOS lacking mutant mice [21] and in obese rodents where endogenous eNOS level…”
BackgroundResultInfluential
Serum from Calorie-Restricted Rats Activates Vascular Cell eNOS through Enhanced Insulin Signaling Mediated by Adiponectin
Cerqueira, F. M., Brandizzi, L. I., da Cunha, F. M., Laurindo, F. R. M., & Kowaltowski, A. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031155 · Cited by 22
“induced the expression of eNOS through Akt [5,13,17,19,20].”
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Regulation of mitochondrial function and endoplasmic reticulum stress by nitric oxide in pluripotent stem cells
Caballano‐Infantes, E., Bautista, J., Beltrán-Povea, A., Cahuana, G. M., Soria, B., Hajji, N., Bedoya, F. J., & Tejedo, J. R. (2017) · World Journal of Stem Cells · doi:10.4252/wjsc.v9.i2.26 · Cited by 22
The signaling pathways that mediate the anti-cancer effects of caloric restriction
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On the comparative biology of Nitric Oxide (NO) synthetic pathways: Parallel evolution of NO-mediated signaling
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Alternate day fasting impacts the brain insulin‐signaling pathway of young adult male C57BL/6 mice
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“Because of the study of Nisoli et al. (2005), which found RFR does induce brain mitochondrial biogenesis in mice, and the study of Schulz et al. (2007), which found antioxidants mitigate increased respiration in 2-deoxyglucosetreated C. elegans, we included a DR group that was cotreated with an…”
BackgroundInfluential
Sciadopitysin alleviates methylglyoxal-mediated glycation in osteoblastic MC3T3-E1 cells by enhancing glyoxalase system and mitochondrial biogenesis
Choi, E. M., Suh, K. S., Rhee, S. Y., & Kim, Y. S. (2014) · Free Radical Research · doi:10.3109/10715762.2014.903562 · Cited by 21
“Treatment with NO donors also increased mitochondrial mass in various cell types [13,57,58].”
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Signalling processes in endothelial ageing in relation to chronic oxidative stress and their potential therapeutic implications in humans
van der Loo, B., Schildknecht, S., Zee, R. S., & Bachschmid, M. M. (2008) · Experimental Physiology · doi:10.1113/expphysiol.2008.043315 · Cited by 22
“Interestingly, calorie restriction was also recently shown to induce eNOS expression in various mouse tissues, accompanied by a promotion of mitochondrial biogenesis, increased mtDNA content and SIRT1 expression, dependent on eNOS-derived ·NO (Nisoli et al. 2005).”
Limonene protects osteoblasts against methylglyoxal-derived adduct formation by regulating glyoxalase, oxidative stress, and mitochondrial function
Suh, K. S., Chon, S., & Choi, E. M. (2017) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2017.10.001 · Cited by 24
Do the Effects of Resveratrol on Thermogenic and Oxidative Capacities in IBAT and Skeletal Muscle Depend on Feeding Conditions?
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
“Thus, while some authors have reported that the maintenance of a 30% energy restriction for a period of 3 months effectively induces mitochondrial biogenesis and function (increased respiration and expression of genes important for oxidative function), others have found no such effects under similar experimental condi…”
Background
Intermittent fasting promotes anxiolytic-like effects unrelated to synaptic mitochondrial function and BDNF support
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
The non-modifiable factors age, gender, and genetics influence resistance exercise
Viecelli, C., & Ewald, C. Y. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.1005848 · Cited by 26
Insights into the Therapeutic and Pharmacological Properties of Resveratrol as a Nutraceutical Antioxidant Polyphenol in Health Promotion and Disease Prevention
Mohammadi, S., Moghadam, M. D., Nasiriasl, M., Akhzari, M., & Barazesh, M. (2024) · Current Clinical Pharmacology · doi:10.2174/0127724328268507231218051058 · Cited by 22
Emerging phosphodiesterase inhibitors for treatment of neurodegenerative diseases
Xiang, Y., Naik, S. G., Zhao, L., Shi, J., & Ke, H. (2024) · Medicinal Research Reviews · doi:10.1002/med.22017 · Cited by 21
“109 In addition, PGC1 α promotes the transcription of antioxidant genes, and regulates glutathione peroxidase 1 110 and the genes involved in oxidative respiration 111,112 and fatty acid β ‐ oxidation.”
Background
Effects of Aging and Cardiovascular Disease Risk Factors on the Expression of Sirtuins in the Human Corpus Cavernosum
Freitas, M., Rodrigues, A. R., Tomada, N., Fonseca, J., Magalhães, A. L., Gouveia, A., & Neves, D. (2015) · The Journal of Sexual Medicine · doi:10.1111/jsm.13035 · Cited by 20
Quantitative proteomics of rat livers shows that unrestricted feeding is stressful for proteostasis with implications on life span
Gat‐Yablonski, G., Finka, A., Pinto, G., Quadroni, M., Shtaif, B., & Goloubinoff, P. (2016) · Aging · doi:10.18632/aging.101009 · Cited by 21
“We found that although the very slow growing RES liver cells massively accumulated specific mitochondrial proteins [25-27], they did not necessitate high levels of HSP chaperones to carry out optimal folding and warrant optimal life span.”
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Cellular Respiration and Carcinogenesis
Sarangarajan, R., & Apte, S. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-435-3 · Cited by 20
A Low-Glycemic, Mediterranean Diet and Lifestyle Modification Program with Targeted Nutraceuticals Reduces Body Weight, Improves Cardiometabolic Variables and Longevity Biomarkers in Overweight Subjects: A 13-Week Observational Trial
Tripp, M. L., Dahlberg, C. J., Eliason, S., Lamb, J. J., Ou, J. J., Gao, W., Bhandari, J., Graham, D., Dudleenamjil, E., & Babish, J. G. (2019) · Journal of Medicinal Food · doi:10.1089/jmf.2018.0063 · Cited by 22
“44 In addition, CR may function to induce endothelial NO synthase resulting in increased fasting levels of plasma NO 45–47 and work in concert with our low-glycemic load Mediterranean diet, as well as polyphenol and probiotic supplementation.”
Vasodilatory and vascular mitochondrial respiratory function with advancing age: evidence of a free radically mediated link in the human vasculature
Park, S. H., Kwon, O. S., Park, S., Weavil, J. C., Hydren, J. R., Reese, V. R., Andtbacka, R. H. I., Hyngstrom, J. R., & Richardson, R. S. (2020) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00268.2019 · Cited by 21
Oxidative Stress: Noxious but Also Vital
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Mitochondrial Dysfunction Increases Arrhythmic Triggers and Substrates; Potential Anti-arrhythmic Pharmacological Targets
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Mitochondria: A Potential Rejuvenation Tool against Aging
Phua, Q. H., Ng, S., & Soh, B.-S. (2023) · Aging and Disease · doi:10.14336/ad.2023.0712 · Cited by 21
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“[51] Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L et al (2005).”
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Life-history Constraints on the Mechanisms that Control the Rate of ROS Production
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“Such conclusions were based on measuring PGC-1α protein level and RNA expression, increased mitochondrial DNA, cytochrome c, and cytochrome oxidase subunit IV in cells [94, 95].”

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: Nisoli, Enzo
Bracale, Renata
Tedesco, Laura
Falcone, Sestina
Valerio, Alessandra
Cantoni, Orazio
Clementi, Emilio
Moncada, Salvador
Carruba, Michele O.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2005-10-14
Volume: 310
Issue: 5746
Pages: 314-317
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1117728
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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Calorie Restriction Promotes Mitochondrial Biogenesis by Inducing the Expression of eNOS

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