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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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“The Sir2 family members (sirtuins) play important roles in several CR model systems (Lin et al. 2000; Rogina and Helfand 2004; Chen et al. 2005; Nisoli et al. 2005; Wang and Tissenbaum 2006).”
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Obesity-Related Oxidative Stress: the Impact of Physical Activity and Diet Manipulation
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“Consistently, increased intracellular NAD + occur during metabolic stresses such as CR or prolonged fasting (19, 20, 105), and are associated with sirtuin activation in a tissue-specific manner (63, 65).”
Fu, W., Liu, Y., & Yin, H. (2019) · Stem Cells International · doi:10.1155/2019/9757201 · Cited by 165
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“SIRT1 promotes NO bioavailability via the deacetylation of endothelial NO synthase (eNOS) [16] and functions as a free radical repressor by inhibiting the activity of NADPH and upregulating the activities of antioxidant enzymes such as SOD [17, 18].”
BackgroundThe role of mitochondrial respiration in physiological and evolutionary adaptation
Das, J. (2006) · BioEssays · doi:10.1002/bies.20463 · Cited by 158
“The product of eNOS, nitric oxide, and its second messenger, cGMP, activate the PGC-1 pathway to induce mitochondrial proliferation.((59,60)) As a short-term physiological adaptation, quantitative changes in the number of mitochondria may increase lipolysis and b-oxidation (which occurs in the mitochondrial matrix), a…”
BackgroundInfluentialSansbury, B. E., Cummins, T. D., Tang, Y., Hellmann, J., Holden, C. R., Harbeson, M. A., Chen, Y., Patel, R. P., Spite, M., Bhatnagar, A., et al. (2012) · Circulation Research · doi:10.1161/circresaha.112.266395 · Cited by 156
Calorie restriction and the exercise of chromatinPreprint
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“CR in mammalian cells increases mitochondrial biogenesis and energy efficiency through the production of nitric oxide (NO) by endothelial NO synthase (eNOS) (Nisoli et al. 2005; Lopez-Lluch et al. 2006).”
Tipping the metabolic scales towards increased longevity in mammals
Riera, C. E., & Dillin, A. (2015) · Nature Cell Biology · doi:10.1038/ncb3107 · Cited by 153
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Mitochondrial function as a determinant of life span
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“However, the exact opposite appears to be true, evidenced by increases in mitochondrial content and oxygen consumption in response to CR [128].”
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“To determine whether Sirt-1 modulates CREB transcriptional activity, cortical neurons were stimulated with NGF in the presence of sirtuin inhibitor Nicotinamide (34); induction of nNOS and PGC-1α mRNA by NGF was blunted upon inhibition of Sirt-1 deacetylase activity (Fig.”
InfluentialMitochondrial response to nutrient availability and its role in metabolic disease
Gao, A. W., Cantó, C., & Houtkooper, R. H. (2014) · EMBO Molecular Medicine · doi:10.1002/emmm.201303782 · Cited by 148
“Initial evidence indicated that CR enhances mitochondrial content (Nisoli et al , 2005).”
Biological and Potential Therapeutic Roles of Sirtuin Deacetylases
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Biochemical effects of SIRT1 activators
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“At the time when most of these observations were made, no relationship was known between SIRT1 and PPARα or adenosine, and nitric oxide had been shown to function upstream of SIRT1, by increasing expression [63].”
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Lee, J. T., & Gu, W. J. (2013) · Genes & Cancer · doi:10.1177/1947601913484496 · Cited by 151
Maternal cardiac metabolism in pregnancy
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Sánchez-Román, I., & Barja, G. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.02.021 · Cited by 146
SIRT1/eNOS Axis as a Potential Target against Vascular Senescence, Dysfunction and Atherosclerosis
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AMPK Regulates Circadian Rhythms in a Tissue- and Isoform-Specific Manner
Um, J.-H., Pendergast, J. S., Springer, D., Foretz, M., Viollet, B., Brown, A. L., Kim, M. K., Yamazaki, S., & Chung, J. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018450 · Cited by 146
“Since the expression of leptin [55], PGC-1a [56] and Nampt [57] is regulated by food intake, and the feeding rhythm is blunted in both AMPKa12/2 and AMPKa22/2 mice (Fig.”
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Dietary restriction.; mitochondrial function and aging: From yeast to humans
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“Two important previous studies differ in their conclusions of mitochondrial biogenesis (Nisoli et al., 2005; Hancock et al., 2011).”
BackgroundInfluentialType 2 diabetes mellitus and exercise impairment
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“In middle-aged rats, CR has been reported to increase the expression of SIRT1 protein in brain, fat, kidney and liver (Cohen et al. 2004, Nisoli et al. 2005).”
Fuel economy in food‐deprived skeletal muscle: signaling pathways and regulatory mechanisms
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“Very recently, it has been shown that SIRT1 deacetylates PGC-1 under low glucose conditions in skeletal muscle cells (with concomitant elevation of NAD levels), inducing a metabolic gene transcription program of mitochondrial fatty acid oxidation (73), although the authors did not address the involvement of NO-mediate…”
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“in skeletal muscle of rodents and humans [46–48].”
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Kinugawa, S., Takada, S., Matsushima, S., Okita, K., & Tsutsui, H. (2015) · International Heart Journal · doi:10.1536/ihj.15-108 · Cited by 140
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Mitochondrial mechanisms of sepsis-induced organ failure.
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Hoffmann, E. C., Wald, J., Lavu, S., Roberts, J., Beaumont, C., Haddad, J., Elliott, P. J., Westphal, C. H., & Jacobson, E. W. (2012) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.2012.04340.x · Cited by 139
Crosstalk between mitochondrial (dys)function and mitochondrial abundance
Michel, S., Wanet, A., Pauw, A. D., Rommelaere, G., Arnould, T., & Renard, P. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.23021 · Cited by 138
Natriuretic peptides and cGMP signaling control of energy homeostasis
Moro, C., & Lafontan, M. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00704.2012 · Cited by 134
The Efficacy of Edaravone (Radicut), a Free Radical Scavenger, for Cardiovascular Disease
Kikuchi, K., Tancharoen, S., Takeshige, N., Yoshitomi, M., Morioka, M., Murai, Y., & Tanaka, E. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140713909 · Cited by 134
“The supplementation of antioxidant, superoxide dismutase, has also been shown to improve endothelium dependent vasodilatation of coronary arteries [70].”
BackgroundDoes calorie restriction induce mitochondrial biogenesis? A reevaluation
Hancock, C. R., Han, D., Higashida, K., Kim, S. H., & Holloszy, J. O. (2011) · The FASEB Journal · doi:10.1096/fj.10-170415 · Cited by 131
“cept that CR induces an increase in mitochondria (1, 2)”
BackgroundInfluentialEccleston, H. B., Andringa, K. K., Betancourt, A. M., King, A. L., Mantena, S. K., Swain, T. M., Tinsley, H. N., Nolte, R. N., Nagy, T. R., Abrams, G. A., et al. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3395 · Cited by 142
“Indeed, eNOS-derived NO has been shown to activate the master regulator of mitochondrial biogenesis, peroxisome proliferator-activated receptor coactivator 1a, which stimulates expression of mitochondrial transcription factors initiating expression of genes encoding mitochondrial proteins (31, 33).”
VEGF stimulation of mitochondrial biogenesis: requirement of AKT3 kinase
Wright, G. L., Maroulakou, I. G., Eldridge, J. D., Liby, T. L., Sridharan, V., Tsichlis, P. N., & Muise‐Helmericks, R. C. (2008) · The FASEB Journal · doi:10.1096/fj.08-106468 · Cited by 138
“PGC-1 activity can be regulated by changes in its expression via nitric oxide (37, 38), calmodulin-dependent protein kinase (CaMK) (39) and oxidative stress (40).”
BackgroundDerbré, F., Gómez‐Cabrera, M. C., Nascimento, A. L. R., Sanchis‐Gomar, F., Martinez-Bello, V. E., Tresguerres, J. A. F., Fuentes, T., Gratas‐Delamarche, A., Monsalve, M., & Viña, J. (2011) · AGE · doi:10.1007/s11357-011-9264-y · Cited by 135
“Calorie restriction has been shown to activate PGC-1α (Nisoli et al. 2005; Anderson et al. 2008; Anderson and Weindruch 2009) and it may be an effective strategy in delaying aging-induced cellular phenotypes in skeletal muscle (McKiernan et al.”
BackgroundRole of mitochondria in liver metabolic health and diseases
Morio, B., Panthu, B., Bassot, A., & Rieusset, J. (2020) · Cell Calcium · doi:10.1016/j.ceca.2020.102336 · Cited by 136
Mitochondrial Protection by Resveratrol
Ungvari, Z. I., Sonntag, W. E., de Cabo, R., Baur, J. A., & Csiszár, A. (2011) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3182141f80 · Cited by 131
“In a similar situation, although SIRT1 can activate eNOS, there is evidence that SIRT1 induction also is a downstream effect of NO production (21).”
BackgroundThe Role of Chronic Inflammation in Obesity-Associated Cancers
Ramos‐Niño, M. E. (2013) · ISRN Oncology · doi:10.1155/2013/697521 · Cited by 137
Molecular and Cellular Basis for Diastolic Dysfunction
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“Interestingly, mitochondrial biogenesis is stimulated in response to increased myocardial NO bioavailability and cGMP levels [72].”
BackgroundPamplona, R., & Barja, G. (2007) · Ageing Research Reviews · doi:10.1016/j.arr.2007.06.002 · Cited by 128
Kondo, M., Shibata, R., Miura, R., Shimano, M., Kondo, K., Li, P., Ohashi, T., Kihara, S., Maeda, N., Walsh, K., et al. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m805301200 · Cited by 124
The many roles of PGC-1α in muscle — recent developments
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“Increase in PGC-1α was first observed in brain, liver, heart and brown adipose tissue with CR [73].”
BackgroundMitochondrial Sirtuins in the Regulation of Mitochondrial Activity and Metabolic Adaptation
Lombard, D. B., Tishkoff, D. X., & Bao, J. (2011) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-21631-2_8 · Cited by 128
“In mammals, CR induces mitochondrial biogenesis in a tissue-specific manner, at least in part through increased expression and activity of endothelial nitric oxide synthase and PGC-1α (Anderson et al. 2008a; Civitarese et al. 2007; Lambert et al. 2004; Lopez-Lluch et al. 2006; Nisoli et al. 2005).”
BackgroundInfluentialCaloric restriction: Beneficial effects on brain aging and Alzheimer’s disease
Van Cauwenberghe, C., Vandendriessche, C., Libert, C., & Vandenbroucke, R. E. (2016) · Mammalian Genome · doi:10.1007/s00335-016-9647-6 · Cited by 121
“These findings point to an important role of nitric oxide (NO), generated by eNOS, in response to CR (Nisoli et al. 2005).”
BackgroundNadtochiy, S. M., & Redman, E. (2011) · Nutrition · doi:10.1016/j.nut.2010.12.006 · Cited by 125
“Furthermore, SIRT1 can be upregulated and activated by NO• [183], forming a positive feed-back loop which enhances NO• availability.”
BackgroundShinmura, K., Tamaki, K., & Bolli, R. (2008) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00602.2008 · Cited by 122
Kang, N., Cao, S., Chatterjee, S., Yao, J. Z., Egan, L. J., Semela, D., Mukhopadhyay, D., & Shah, V. H. (2007) · Journal of Cell Science · doi:10.1242/jcs.03361 · Cited by 121
“Complementary NO donor compounds were used for various assays described below, at doses that did not exceed 100 M, a concentration threshold commonly used for in vitro studies (Nisoli et al., 2005).”
MethodMulti-site control and regulation of mitochondrial energy production
Bénard, G., Bellancé, N., José, C., Melser, S., Nouette‐Gaulain, K., & Rossignol, R. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.02.030 · Cited by 126
“Alternatively, the activation of CREB was shown to induce the expression of endothelial nitric oxide synthase (eNOS) [103], and intracellular nitric oxide (NO) generation stimulates mitochondrial biogenesis [104–106].”
BackgroundDifferential Modulation of Nitric Oxide Synthases in Aging: Therapeutic Opportunities
Cáu, S. B. D. A., Carneiro, F. S., & Tostes, R. C. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00218 · Cited by 131
Caloric restriction and its mimetics
Lee, S.-H., & Min, K.-J. (2013) · BMB Reports · doi:10.5483/bmbrep.2013.46.4.033 · Cited by 119
“environments, the expression and activity of Sirtuin is increased in many tissues, including adipose and brain tissue (50).”
BackgroundTraba, J., Geiger, S. S., Osei, M. A., Han, K., Ra, O. H., Siegel, R. M., Gius, D. R., & Sack, M. N. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.791715 · Cited by 120
Mitochondrial Biogenesis in Health and Disease. Molecular and Therapeutic Approaches
Sanchis‐Gomar, F., García‐Giménez, J. L., Gómez‐Cabrera, M. C., & Pallardó, F. V. (2014) · Current Pharmaceutical Design · doi:10.2174/1381612820666140306095106 · Cited by 120
“The role of RONS in the regulation of MB has been suggested by different research groups [14, 47-49].”
MethodHigh glucose downregulates endothelial progenitor cell number via SIRT1
Balestrieri, M. L., Rienzo, M., Felice, F., Rossiello, R., Grimaldi, V., Milone, L., Casamassimi, A., Servillo, L., Farzati, B., Giovane, A., et al. (2008) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2008.03.004 · Cited by 117
“Mammalian SIRT1 NAD+-dependent protein deacetylase, the closest homolog of Sir2, mediates many of the effects of calorie restriction (CR) on organism lifespan and metabolic pathways [ 3 ,4] as it regulates cell cycle, premature senescence, apoptosis and metabolism by interacting with a number of molecules, including,…”
BackgroundJoseph, A.-M., Joanisse, D. R., Baillot, R. G., & Hood, D. A. (2011) · Experimental Diabetes Research · doi:10.1155/2012/642038 · Cited by 119
SIRT1 is a positive regulator of in vivo bone mass and a therapeutic target for osteoporosis
Zainabadi, K., Liu, C. J., Caldwell, A. L. M., & Guarente, L. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185236 · Cited by 118
The Role of Sirtuin1 in Regulating Endothelial Function, Arterial Remodeling and Vascular Aging
Man, A. W. C., Li, H., & Xia, N. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01173 · Cited by 123
Selman, C., Kerrison, N. D., Cooray, A., Piper, M. D. W., Lingard, S. J., Barton, R. H., Schuster, E. F., Blanc, E., Gems, D., Nicholson, J. K., et al. (2006) · Physiological Genomics · doi:10.1152/physiolgenomics.00084.2006 · Cited by 117
“It has recently been shown that CR (3 or 12 months duration) promotes mitochondrial biogenesis in several tissues via endothelial nitric oxide synthase (eNOS) induction, leading to elevated oxygen consumption, increased mitochondrial DNA levels (marker of mitochondrial content) and ATP production (45).”
BackgroundBiochemical Genetic Pathways that Modulate Aging in Multiple Species: Figure 1.Preprint
Bitto, A., Wang, A. M., Bennett, C. F., & Kaeberlein, M. R. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a025114 · Cited by 122
“…are increased in response to DR (Lin et al. 2002), and similar effects have been reported in some tissues of mice and in cultured mammalian cells (Nisoli et al. 2005; Lopez-Lluch et al. 2006), further supporting the idea that mitochondrial inhibition extends life span by a mechanism distinct…”
BackgroundBaldelli, S., Aquilano, K., & Ciriolo, M. R. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.04.006 · Cited by 120
“CR elicits the increase of PGC-1α mRNA levels in different tissues and in cellular model of CR [114, 118].”
Su, M., Zhao, W., Xu, S., & Weng, J. (2022) · Antioxidants · doi:10.3390/antiox11061085 · Cited by 121
Robich, M. P., Osipov, R. M., Nezafat, R., Feng, J., Clements, R., Bianchi, C. F., Boodhwani, M., Coady, M. A., Laham, R. J., & Sellke, F. W. (2010) · Circulation · doi:10.1161/circulationaha.109.920132 · Cited by 112
Karamanlidis, G., Bautista‐Hernández, V., Fynn‐Thompson, F., del Nido, P. J., & Tian, R. (2011) · Circulation Heart Failure · doi:10.1161/circheartfailure.111.961474 · Cited by 112
Nutrition and Healthy Ageing: Calorie Restriction or Polyphenol-Rich “MediterrAsian” Diet?
Pallauf, K., Giller, K., Huebbe, P., & Rimbach, G. H. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/707421 · Cited by 116
“Mice (C57BLK/6×SV127 F1 hybrid) 10 30–40% White adipose tissue Sirt1 ↑ (protein) [36]”
BackgroundSanders, O. D., & Rajagopal, L. (2020) · Journal of Alzheimer s Disease Reports · doi:10.3233/adr-200191 · Cited by 117
Recent advances in calorie restriction research on aging
Chung, K. W., Kim, D. H., Park, M. H., Choi, Y. J., Kim, N. D., Lee, J., Yu, B. P., & Chung, H. Y. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2012.11.007 · Cited by 108
“CR increases the expression of SIRT1 in liver, adipose tissue, brain, and kidney (Nisoli et al., 2005).”
BackgroundImpaired quality control of mitochondria: Aging from a new perspective
Weber, T. A., & Reichert, A. S. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.03.018 · Cited by 112
“In general, CR increases the amount of ATP generated via respiration, stimulates mitochondrial biogenesis, and leads to reduced levels of ROS (Nisoli et al. 2005; Guarente 2008).”
BackgroundMechanisms of obesity-induced metabolic and vascular dysfunctions
Caldwell, R. W. (2019) · Frontiers in bioscience · doi:10.2741/4758 · Cited by 112
“Other studies have demonstrated that eNOS expression and activity are tightly regulated in adipose tissue and muscle, and that eNOS is necessary for caloric restriction-induced upregulation of SIRT1, a protein involved in promotion of insulin sensitivity and amplification of eNOS activity (235, 304, 305).”
Flachs, P., Rühl, R., Hensler, M., Janovská, P., Zouhar, P., Kůs, V., Jílková, Z. M., Papp, E., Kuda, O., Svobodová, M., et al. (2011) · Diabetologia · doi:10.1007/s00125-011-2233-2 · Cited by 111
“The metabolic changes induced by both calorie restriction and LC n-3 PUFA include induction of mitochondrial biogenesis and lipid catabolism in WAT [3, 13].”
BackgroundDNA Replication Stress Is a Determinant of Chronological Lifespan in Budding Yeast
Weinberger, M., Li, F., Paul, A., Smith, D. L., Hontz, R. D., Smith, J. S., Vujcic, M., Singh, K. K., Huberman, J. A., & Burhans, W. C. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000748 · Cited by 110
“In mammals (including humans), caloric restriction stimulates mitochondrial biogenesis [34,35,36].”
BackgroundLugus, J. J., Ngoh, G. A., Bachschmid, M. M., & Walsh, K. X. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2011.07.023 · Cited by 114
“Lastly, Mfn2, but not Mfn1, has been linked to cellular functions including oxidative metabolism [44] and is induced by caloric restriction [45] and repressed in obese and diabetic individuals [46,47].”
Dynamic Adaptation of Liver Mitochondria to Chronic Alcohol Feeding in Mice
Han, D., Ybanez, M. D., Johnson, H. S., McDonald, J. N., Mesropyan, L., Sancheti, H., Martin, G. G., Martin, A. M., Lim, A. M., Dara, L., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.377374 · Cited by 109
The role of SIRT1 in ocular aging
Mimura, T., Kaji, Y., Noma, H., Funatsu, H., & Okamoto, S. (2013) · Experimental Eye Research · doi:10.1016/j.exer.2013.07.017 · Cited by 114
Su, J.-L., Yang, C., Zhao, M., Kuo, M., & Yen, M. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702452200 · Cited by 110
NF-κB pathway activators as potential ageing biomarkers: targets for new therapeutic strategies
Balistreri, C. R., Candore, G., Accardi, G., Colonna‐Romano, G., & Lio, D. (2013) · Immunity & Ageing · doi:10.1186/1742-4933-10-24 · Cited by 111
“chondrial biogenesis, as evidenced by changes in mtDNA levels, and protein levels [77].”
Wang, Y., Li, X., Guo, Y., Chan, L., & Guan, X. (2009) · Metabolism · doi:10.1016/j.metabol.2009.10.018 · Cited by 106
“We note that caloric restriction has been shown to increase longevity and mitochondrial biogenesis [40].”
Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity
López-Lluch, G. (2017) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.12.005 · Cited by 103
“Further, it has been demonstrated that eNOS is induced by CR in mice and human muscle (Civitarese et al., 2007; Nisoli et al., 2005) being essential in the CR-induced mitochondrial biogenesis since in eNOS-/- mice this induction is blocked (Nisoli et al., 2005).”
BackgroundMitochondrial Metabolic Reprogramming Induced by Calorie Restriction
Martín‐Montalvo, A., & de Cabo, R. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4866 · Cited by 106
“Increases in cGMP levels have also been related to the expression of the deacetylase SIRT1 (71). eNOS gene expression is increased in humans under CR and CR plus exercise.”
Sirtuins' control of autophagy and mitophagy in cancer
Aventaggiato, M., Vernucci, E., Barreca, F., Russo, M. A., & Tafani, M. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107748 · Cited by 103
Neuroprotective effects of dietary restriction: Evidence and mechanisms
Pani, G. (2015) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2015.03.004 · Cited by 103
Mitochondria and aging in the vascular system
Ungvari, Z., Sonntag, W. E., & Csiszar, A. (2010) · Journal of Molecular Medicine · doi:10.1007/s00109-010-0667-5 · Cited by 103
“Studies on animal models with genetic depletion of eNOS [34] and treated with pharmacological inhibitors of NO synthesis [35] support this model.”
Jokinen, R., Pirnes-Karhu, S., Pietiläinen, K. H., & Pirinen, E. (2017) · Redox Biology · doi:10.1016/j.redox.2017.02.011 · Cited by 103
Natural products, PGC-1 , and Duchenne muscular dystrophy
Süntar, I. P., Sureda, A., Belwal, T., Sanches-Silva, A. T., Vacca, R. A., Tewari, D., Sobarzo‐Sánchez, E., Nabavi, S. F., Shirooie, S., Dehpour, A. R., et al. (2020) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2020.01.001 · Cited by 103
Finley, L. W. S., Lee, J., Souza, A., Desquiret-Dumas, V., Bullock, K., Rowe, G. C., Procaccio, V., Clish, C. B., Arany, Z., & Haigis, M. C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115813109 · Cited by 102
“CR increases mitochondrial DNA content in several mouse tissues (4).”
BackgroundCancer cell metabolism and the modulating effects of nitric oxide
Chang, C.-F., Diers, A. R., & Hogg, N. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.11.012 · Cited by 103
Nutrient Sensing and the Oxidative Stress Response
Luo, H., Chiang, H.-H., Louw, M., Susanto, A., & Chen, D. (2017) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2017.02.008 · Cited by 107
“This metabolic switch requires cells to be reliant on increased mitochondrial activity, which is associated with increased ROS production [18].”
BackgroundArterial Stiffness Assessed by Cardio-Ankle Vascular Index
Namba, T., Masaki, N., Takase, B., & Adachi, T. K. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153664 · Cited by 103
“SIRT-1 protects against high fat, high sucrose induced arterial stiffness [34], and caloric restriction activates SIRT-1 and increases eNOS expression [35].”
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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