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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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“Notably, the anti-aging effect of calorie restriction and the beneficial adaptations of the heart to exercise depend on the eNOS-mediated induction of mitochondrial biogenesis (Nisoli et al., 2005; Vettor et al., 2014).”
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“Although in vitro study using carotid reported that longevity and endothelial function preservation does not correlate with maximal sensitivity to Ach [51], many studies on various organisms ranging from yeasts to mammals have shown that longevity is correlated to NO pathway preservation [14,52] and eNOS function [53,…”
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“Notably, we reported that an intermittent fasting protocol reducing calorie intake (CR by every-other-day feeding), promotes mitochondrial biogenesis through increased eNOS expression and NO production in several tissues, including fat, skeletal muscle, and the brain of male mice [36].”
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“Little is known about the effects of CR on mitochondrial function and its link to adiponectin, speci fi cally in the bone, but increased mitochondrial biogenesis is well established and described in many tissues, including the brain, liver, heart, and brown adipose tissue upon CR (47).”
BackgroundClinical Nutrition University: Muscle physiology and bioenergetics
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“NO enhances mitochondriogenesis and BAT thermogenic activity [66,67], and the NO second messenger cGMP promotes WAT browning [68].”
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“These effects were dramatically reduced in mice mutant at eNOS [146].”
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“Caloric restriction induces endothelial NO synthetase (eNOS) expression which increases nitric oxide (NO) production and ultimately mitochondrial biogenesis [8].”
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“…in body weight and waist circumference, preferential loss of visceral fat, improvements in insulin sensitivity and lipid parameters, and attenuation of low-grade inflammation (e.g., CRP/IL-6/TNF-α trajectories consistent with the adipose signaling noted above) [ 38 – 41 , 44 , 45, 52, 53].”
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“Actually, CR efects on mitochondrial biogenesis are reduced in eNOS knock out animals (Nisoli et al., 2005).”
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“Recent reports also have found increases in mitochondrial biogenesis and mitochondrial bioenergetic efficiency [ 72 , 73], decreases in cellular steady-state ROS levels [73] and lack of changes or even increases in O 2 consumption [72, 74–76] in CR models, including mammals, nematodes, and yeast.”
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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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