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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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Nitric Oxide in Myogenesis and Therapeutic Muscle Repair
Palma, C. D., & Clementi, E. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8311-8 · Cited by 68
“The decrease in mitochondrial size observed in tissues from eNOS null mice [19] is likely to be a morphological correlate of the reduced mitochondrial function.”
BackgroundCalorie restriction and stroke
Manzanero, S., Gelderblom, M., Magnus, T. U., & Arumugam, T. V. (2011) · Experimental & Translational Stroke Medicine · doi:10.1186/2040-7378-3-8 · Cited by 65
“SIRT1 is also activated by NO, another putative target of CR [49].”
BackgroundBereiter‐Hahn, J., & Jendrach, M. (2010) · International review of cytology · doi:10.1016/s1937-6448(10)84001-8 · Cited by 67
Fujii, N., Narita, T., Okita, N., Kobayashi, M., Furuta, Y., Chujo, Y., Sakai, M., Yamada, A., Takeda, K., Konishi, T., et al. (2017) · Aging Cell · doi:10.1111/acel.12576 · Cited by 64
de Lucia, C., Gambino, G., Petraglia, L., Elia, A., Komici, K., Femminella, G. D., D’Amico, M. L., Formisano, R., Borghetti, G., Liccardo, D., et al. (2018) · Circulation Heart Failure · doi:10.1161/circheartfailure.117.004153 · Cited by 64
Chen, J., Shi, X., Padmanabhan, R., Wang, Q., Wu, Z., Stevenson, S. C., Hild, M., Garza, D., & Li, H. (2007) · Genome Research · doi:10.1101/gr.6940108 · Cited by 65
“Guanylyl cyclase was shown to mediate PPARGC1 (PGC-1 ) activation of mitochondrial biogenesis and to be activated by NO (Nisoli et al. 2004, 2005).”
BackgroundBaicalin reduces mitochondrial damage in streptozotocin‐induced diabetic Wistar rats
Waisundara, V. Y., Hsu, A., Tan, B. K., & Huang, D. (2009) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.1005 · Cited by 64
“With increased leptin levels to be a casual factor for reduced calorie consumption [19], the trend in the mitochondrial number is consistent with previous reports showing an increased hepatic mitochondrial number in conditions of restricted calorie intake [22,23].”
ResultMicroRNAs and the metabolic hallmarks of aging
Victoria, B., López, Y. O. N., & Masternak, M. M. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.12.021 · Cited by 64
“, mammalian target of rapamycin (mTOR), insulin/insulin-like growth factor 1 (IGF-1)] as well as by increasing the expression of endothelial nitric oxide synthase [eNOS, involved in mitochondrial biogenesis and sirtuin 1 (SIRT1) expression] (Blagosklonny, 2010; Luigi Fontana, 2009; Nisoli et al., 2005).”
BackgroundMarcu, R., Wiczer, B. M., Neeley, C. K., & Hawkins, B. J. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00068-14 · Cited by 62
“Endothelial SIRT1 targets multiple proteins to effectively modulate nitric oxide production (75, 76), inflammation (47, 77, 78), and vessel growth (79, 80).”
BackgroundMo, L., Wang, Y., Geary, L., Corey, C., Alef, M. J., Beer-Stolz, D., Zuckerbraun, B. S., & Shiva, S. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.07.080 · Cited by 62
“NO is a known stimulator of mitochondrial biogenesis and activator of AMPK [9, 35].”
BackgroundInfluentialBrain response to calorie restriction
Fusco, S., & Pani, G. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1223-y · Cited by 68
“Upregulation of neuronal PGC-1 by dietary restriction may have nitric oxide as an intermediate [108] and occurs through a humoral mechanism, since treatment of cultured neurons with serum of calorie restriction animals induces the expression of nitric oxide synthetases (eNOS and nNOS) and increases mitochondrial mass…”
BackgroundArmour, S. M., Bennett, E. J., Braun, C. R., Zhang, X., McMahon, S. B., Gygi, S. P., Harper, J. W., & Sinclair, D. A. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00971-12 · Cited by 64
“Transcriptional regulation of SIRT1 is altered by stress responses (30–32), metabolic homeostasis (33), as well as calorie restriction, a diet that promotes longevity and disease resistance in a variety of species (12, 34).”
BackgroundFiore, D., Gianfrilli, D., Giannetta, E., Galea, N., Panio, G., Dato, C. D., Pofi, R., Pozza, C., Sbardella, E., Carbone, I., et al. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-4252 · Cited by 60
“Interestingly, SIRT1 protein levels in white adipocytes are blunted in endothelial nitric oxide synthase-deficient mice (39), suggesting NO dependency but also a greater response to PDE5i in diabetes, where NO production is defective.”
BackgroundLysine deacetylases and mitochondrial dynamics in neurodegeneration
Guedes-Dias, P., & Oliveira, J. M. A. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.04.005 · Cited by 63
“However, studies reporting increased mitochondrial biogenesis following CR [56–58] were challenged by a recent study showing no increases in mitochondrial structural proteins in several rat tissues including the brain [59].”
BackgroundLidell, M. E., Seifert, E. L., Westergren, R., Heglind, M., Gowing, A., Sukonina, V., Arani, Z., Itkonen, P., Wallin, S., Westberg, F., et al. (2011) · Diabetes · doi:10.2337/db10-0409 · Cited by 64
“Moreover, it has been shown that in WAT of WT mice with enhanced life span because of caloric restriction there is an induced expression of PGC1a, mtTFA, Mfn1, and Mfn2 (33), a response very similar to what we demonstrate in adipocytes with enhanced Foxc2 expression (Figs.”
ResultInfluentialParallel evolution of Nitric Oxide signaling: Diversity of synthesis and memory pathways
Moroz, L. L. (2011) · Frontiers in bioscience · doi:10.2741/3837 · Cited by 59
“Recent data linking NO functions to the biogenesis of mitochondria reveal a novel systemic level of long-term integration of cellular respiration and cell biochemistry (117-126).”
BackgroundYang, Y., & Zhang, L. (2020) · Food & Function · doi:10.1039/c9fo02611h · Cited by 57
Chausse, B., Solon, C., da Silva, C. C. C., dos Reis, I. G. M., Manchado-Gobatto, F. D. B., Gobatto, C. A., Velloso, L. A., & Kowaltowski, A. J. (2014) · Endocrinology · doi:10.1210/en.2013-2057 · Cited by 59
“Other studies (5) have suggested that the control of mitochondrial biogenesis and content may be responsible for changes in energy conversion efficiency observed with dietary interventions.”
BackgroundEffects of caloric restriction on oxidative stress parameters
Stankovic, M. S., Mladenović, D. R., Ninković, M., Vučević, D. B., & Radosavljević, T. S. (2013) · General Physiology and Biophysics · doi:10.4149/gpb_2013027 · Cited by 59
“…of hepatocyte damage were not increased, explanation for NOx increase may be that moderate CR induces endothelial nitric oxide synthase (eNOS) and consequently that low increase in NO level may have protective effect and may prevent age-related changes in blood vessels (Nisoli et al. 2005).”
BackgroundEndothelial nitric oxide synthase, vascular integrity and human exceptional longevity
Puca, A. A., Carrizzo, A., Ferrario, A., Villa, F., & Vecchione, C. (2012) · Immunity & Ageing · doi:10.1186/1742-4933-9-26 · Cited by 59
“These effects were abolished in eNOS mice [15].”
BackgroundRegulation of miRNAs by Natural Antioxidants in Cardiovascular Diseases: Focus on SIRT1 and eNOS
Lee, Y., & Im, E. (2021) · Antioxidants · doi:10.3390/antiox10030377 · Cited by 59
“In cultured adipocytes, NO treatment markedly induced SIRT1 expression [69].”
BackgroundAdaptation of endothelium to exercise training: Insights from experimental studies
Per, M. H. (2007) · Frontiers in bioscience · doi:10.2741/2683 · Cited by 58
“Also, caloric restriction increased mitochondrial biogenesis in wild type, but not eNOS null mice (33).”
BackgroundZheng, J., Chen, L., Zhang, H., Hu, X., Kong, W., & Hu, D. (2011) · Metabolism · doi:10.1016/j.metabol.2011.11.005 · Cited by 60
“[24] Nisoli E, Tonello C, Cardile A, et al.”
BackgroundResultWakeling, L. A., Ions, L. J., & Ford, D. (2009) · AGE · doi:10.1007/s11357-009-9104-5 · Cited by 63
“In rats and mice, DR increased Sirt1 expression in several tissues, including liver (Cohen et al. 2004; Nisoli et al. 2005), and in human subjects DR increased Sirt1 mRNA in skeletal muscle (Civitarese et al.”
BackgroundCsiszár, A., Sosnowska, D., Tucsek, Z., Gautam, T., Toth, P. P., Losonczy, G., Colman, R. J., Weindruch, R. H., Anderson, R. M., Sonntag, W. E., et al. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls158 · Cited by 58
“Because CR in vivo was shown to significantly increase endothelial NO production by upregulating eNOS (28,29,109), we anticipated that this effect would be recapitulated in vitro by treatment of CAECs with sera derived from caloric-restricted M mulatta.”
BackgroundColleoni, F., Lattuada, D., Garretto, A., Massari, M., Mandò, C., Somigliana, E., & Cetin, I. (2010) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2010.05.027 · Cited by 60
S-Nitrosylation in Tumor Microenvironment
Sharma, V., Fernando, V., Letson, J., Walia, Y., Zheng, X., Fackelman, D., & Furuta, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094600 · Cited by 59
Kobayashi, M., Deguchi, Y., Nozaki, Y., & Higami, Y. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22116025 · Cited by 63
“Nisoli and colleagues reported that CR increased Pgc-1α and mtDNA levels in WAT [92].”
BackgroundVascular Ageing: Mechanisms, Risk Factors, and Treatment Strategies
Ya, J., & Bayraktutan, U. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411538 · Cited by 57
“Attenuation of the lifespan extension in the eNOS knockout mouse model pinpoints the significance of the eNOS/NO pathway in calorie restriction-mediated organismal benefits [77].”
BackgroundDietary restriction in cerebral bioenergetics and redox state
Amigo, I., & Kowaltowski, A. J. (2014) · Redox Biology · doi:10.1016/j.redox.2013.12.021 · Cited by 59
“[78] showed that IF could induce mitochondrial biogenesis in several mouse tissues, including brain, through a mechanism that requires eNOS.”
BackgroundMethylglyoxal induces oxidative stress and mitochondrial dysfunction in osteoblastic MC3T3-E1 cells
Suh, K. S., Choi, E. M., Rhee, S. Y., & Kim, Y. S. (2013) · Free Radical Research · doi:10.3109/10715762.2013.859387 · Cited by 57
Kim, Y. S., Lee, Y., Park, J., Lee, S., & Kim, E. (2010) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22858 · Cited by 57
“The present study demonstrated that HMGB1 increases SIRT1 mRNA and protein expression in hPDLCs, as has been shown in various other cell types [Nisoli et al., 2005; Rodgers et al., 2005; Kim et al., 2007].”
BackgroundMetabolism Regulation and Redox State: Insight into the Role of Superoxide Dismutase 1
Damiano, S., Sozio, C., Rosa, G. L., Guida, B., Faraonio, R., Santillo, M., & Mondola, P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186606 · Cited by 59
“For example, nutrient deprivation induces a metabolic switch from glycolysis to oxidative phosphorylation, a more efficient process in terms of energy production [46–48] that, however, is associated with increased ROS generation [49].”
BackgroundMechanisms Underlying Brain Aging Under Normal and Pathological Conditions
Jin, M., & Cai, S. (2022) · Neuroscience Bulletin · doi:10.1007/s12264-022-00969-9 · Cited by 61
Okita, N., Hayashida, Y., Kojima, Y., Fukushima, M., Yuguchi, K., Mikami, K., Yamauchi, A., Watanabe, K., Noguchi, M., Nakamura, M., et al. (2012) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2012.02.003 · Cited by 57
“Thus, CR activates various mitochondrial metabolic processes (Anderson and Prolla, 2009; Higami et al., 2004; Nisoli et al., 2005).”
BackgroundResultMitochondrial sirtuins and metabolic homeostasis
Pirinen, E., Sasso, G. L., & Auwerx, J. H. (2012) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2012.05.001 · Cited by 57
Mitochondrial dysfunction in metabolism and ageing: shared mechanisms and outcomes?
López‐Lluch, G., Hernández‐Camacho, J. D., Fernández‐Ayala, D. J. M., & Navas, P. (2018) · Biogerontology · doi:10.1007/s10522-018-9768-2 · Cited by 60
Wilson, K. A., Chamoli, M., Hilsabeck, T. A. U., Pandey, M., Bansal, S., Chawla, G., & Kapahi, P. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.08.018 · Cited by 57
Lifestyle effects on aging and CVD: A spotlight on the nutrient-sensing network
Yang, K., Hou, R., Zhao, J., Wang, X., Wei, J., Pan, X., & Zhu, X. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102121 · Cited by 59
“…in the regulation of CVD via the NSN. Hypertension is a risk factor for numerous CVDs, and a large number of studies have shown that CR ameliorates hypertension (Gorostegi-Anduaga et al., 2018; Kord-Varkaneh et al., 2020) and is strongly associated with an increase in eNOS (Nisoli et al., 2005).”
BackgroundSIRT1 and caloric restriction: an insight into possible trade-offs between robustness and frailty
Imai, S. (2009) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32832c932d · Cited by 55
Role of Sirtuin 1 in metabolic regulation
Silva, J. P., & Wahlestedt, C. (2010) · Drug Discovery Today · doi:10.1016/j.drudis.2010.07.001 · Cited by 55
The role of nNOS and PGC-1α in skeletal muscle cells
Baldelli, S., Lettieri‐Barbato, D., Tatulli, G., Aquilano, K., & Ciriolo, M. R. (2014) · Journal of Cell Science · doi:10.1242/jcs.154229 · Cited by 62
“In particular, caloric restriction increases both eNOS and nNOS activity (Nisoli et al., 2005; Fusco et al., 2012).”
BackgroundVink, R., Roumans, N. J. T., Fazelzadeh, P., Tareen, S. H. K., Boekschoten, M. V., van Baak, M. A., & Mariman, E. C. M. (2016) · International Journal of Obesity · doi:10.1038/ijo.2016.201 · Cited by 55
eNOS deletion impairs mitochondrial quality control and exacerbates Western diet-induced NASH
Sheldon, R. D., Meers, G. M.-E., Morris, E. M., Linden, M. A., Cunningham, R. P., Ibdah, J. A., Thyfault, J. P., Laughlin, M. H., & Rector, R. S. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00096.2019 · Cited by 55
Bioenergetics of aging and calorie restriction
Hunt, N. D., Hyun, D., Allard, J. S., Minor, R. K., Mattson, M. P., Ingram, D. K., & de Cabo, R. (2006) · Ageing Research Reviews · doi:10.1016/j.arr.2006.03.006 · Cited by 55
Fusco, S., Maulucci, G., & Pani, G. (2012) · Cell Cycle · doi:10.4161/cc.22074 · Cited by 54
“Calorie restriction increases Sirt1 immunoreactivity in several rodent tissues, including brain, kidney, white fat and liver.(20,21,119) Initial observations revealed such increases to be inhibited by the insulin/IGF signaling cascade,(20) to occur concomitantly with mitochondrial biogenesis and to depend on the expre…”
Caro, P., Gómez, J., Sánchez-Román, I., García-Martín, R., Lopez‐Torres, M., Naudí, A., Portero‐Otín, M., Pamplona, R., & Barja, G. (2008) · Biogerontology · doi:10.1007/s10522-008-9200-4 · Cited by 54
“Since previous studies have shown that changes in mitROS generation can be due in part to variations in the amounts of respiratory complexes, the levels of complexes I to IV were also studied, as well as the factors controlling mitochondrial biogenesis PPARc coactivator 1a (PGC-1a) and nuclear respiratory factor-2 (NR…”
BackgroundMethodYe, L., Widlund, A. L., Sims, C. A., Lamming, D. W., Guan, Y., Davis, J. G., Sabatini, D. M., Harrison, D. E., Vang, O., & Baur, J. A. (2013) · Aging · doi:10.18632/aging.100576 · Cited by 56
Claudio Napoli, A., Williams‐Ignarro, S., de Nigris, F., Lerman, L. O., D’Armiento, F. P., Crimi, E., Byrns, R. E., Casamassimi, A., Lanza, A., Gombos, F., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602774103 · Cited by 56
Merlin, J., Evans, B. A., Dehvari, N., Sato, M., Bengtsson, T., & Hutchinson, D. S. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500251 · Cited by 56
“NO upregulation (by induction of endothelial NO synthase expression through calorie restriction) upregulates PGC-1 and other brown adipocyte genes, activates mitochondrial biogenesis, and increases respiration in mouse eWAT [216].”
BackgroundTargeting Sirtuin-1 in Huntington’s Disease: Rationale and Current Status
Duan, W. (2013) · CNS Drugs · doi:10.1007/s40263-013-0055-0 · Cited by 54
“Calorie restriction increases mitochondrial biogenesis by inducing endothelial nitric oxide synthase (eNOS), and nitric oxide (NO) can activate the sirtuin 1 (SIRT1) gene [23, 24] which is the mammalian ortholog of yeast Sir2, and a highly conserved NAD-dependent protein deacetylase.”
BackgroundSkeletal Muscle Nucleo-Mitochondrial Crosstalk in Obesity and Type 2 Diabetes
Devarshi, P. P., McNabney, S. M., & Henagan, T. M. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040831 · Cited by 55
Does eating less make you live longer and better? An update on calorie restriction
Picca, A., Pesce, V., & Lezza, A. M. S. (2017) · Clinical Interventions in Aging · doi:10.2147/cia.s126458 · Cited by 57
“The CR-related induction of NOS in mice and human muscle 45,83 is very relevant for the sequential activation of mitochondrial biogenesis.”
Essential amino acid formulations to prevent mitochondrial dysfunction and oxidative stress
Ruocco, C., Segala, A., Valerio, A., & Nisoli, E. (2020) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000704 · Cited by 56
“Significantly, the eNOS-PGC-1a-mediated mitochondrial renewal mechanisms are at the basis of the beneficial effects of calorie restriction, exercise, and BCAA supplementation [2,14,15].”
BackgroundDiabetes, stroke, and neuroresilience: looking beyond hyperglycemia
Krinock, M. J., & Singhal, N. S. (2021) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14583 · Cited by 56
Easlon, E. J., Tsang, F. A., Dilova, I., Wang, C., Lu, S.-P., Skinner, C., & Lin, S.-J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m607661200 · Cited by 55
Exercise improves vascular health: Role of mitochondria
Zhang, X., & Gao, F. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.11.002 · Cited by 52
The Multifaceted Role of Endothelial Sirt1 in Vascular Aging: An Update
Campagna, R., Mazzanti, L., Pompei, V., Alia, S., Vignini, A., & Emanuelli, M. (2024) · Cells · doi:10.3390/cells13171469 · Cited by 59
“…However, in eNOS-knockout mice, calorie restriction-induced expression of Sirt1 was diminished, suggesting a mutual regulatory loop involving the two enzymes in the endothelium [93]. against endothelial dysfunction are still far from being fully elucidated, thus requiring deeper insights.”
BackgroundDietary Polyphenols as Anti-Aging Agents: Targeting the Hallmarks of Aging
Liu, Y., Fang, M., Tu, X., Mo, X., Zhang, L., Yang, B., Wang, F., Kim, Y., Huang, C., Chen, L., et al. (2024) · Nutrients · doi:10.3390/nu16193305 · Cited by 62
“Experiments have proved that resveratrol, a stilbene abundantly present in grapes, can increase the number of mitochondria and citrate synthase activity [33].”
BackgroundMitochondrial response to controlled nutrition in health and disease
Schiff, M., Bénit, P., Coulibaly, A., Loublier, S., El‐Khoury, R., & Rustin, P. (2011) · Nutrition Reviews · doi:10.1111/j.1753-4887.2010.00363.x · Cited by 53
Khraiwesh, H. M., Lopez-Dominguez, J. A., López‐Lluch, G., Navas, P., de Cabo, R., Ramsey, J. J., Villalba, J. M., & González-Reyes, J. A. (2013) · The Journals of Gerontology Series A · doi:10.1093/gerona/glt006 · Cited by 54
“Therefore, in spite of the objection recently reported (56,57), our results showing significant increases of Fis1 and Drp1 expression and the mean number of mitochondria per hepatocyte in CR-fed animals clearly support the idea of increased mitochondrial biogenesis under CR conditions (23,54).”
ResultSands, B. E., Joshi, S., Haddad, J., Freudenberg, J., Oommen, D. E., Hoffmann, E. C., McCallum, S. W., & Jacobson, E. W. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000597 · Cited by 53
Valle, A., Guevara, R., García-Palmer, F., Roca, P., & Oliver, J. (2008) · Rejuvenation Research · doi:10.1089/rej.2007.0626 · Cited by 54
“13,15,16 This improvement in mitochondrial functionality may prevent the age-associated decrease in adenosine triphosphate (ATP) production and, therefore, may be a reasonable mechanism in the amelioration of organ function and the extension of lifespan in old restricted animals.”
Nutrition modulation of human aging: The calorie restriction paradigm
Das, S. K., Balasubramanian, P., & Weerasekara, Y. K. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.04.011 · Cited by 51
“The effects of CR on mitochondrial biogenesis is controversial (Civitarese et al., 2007; Hancock et al., 2010; Nisoli et al., 2005), however it is well established that CR promotes mitochondrial efficiency where the mitochondria consumes less oxygen and generates less reactive oxygen species (ROS) while maintaining AT…”
BackgroundLeón, B. E., Kang, S., Franca-Solomon, G., Shang, P., & Choi, D. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.778456 · Cited by 56
“Importantly, the bioenergetics and dynamics of mitochondria are subject to extrinsic factors such as diet (Nisoli et al., 2005) and hormones (Cioffi et al.”
BackgroundCaloric restriction and heart function: is there a sensible link?
Han, X., & Ren, J. T. (2010) · Acta Pharmacologica Sinica · doi:10.1038/aps.2010.146 · Cited by 51
SIRT1 in metabolic syndrome: Where to target matters
Wang, Y., Xu, C., Liang, Y., & Vanhoutte, P. M. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.08.009 · Cited by 51
Diet, energy metabolism and mitochondrial biogenesis
Civitarese, A. E., Smith, S. R., & Ravussin, É. (2007) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e3282f0ecd2 · Cited by 52
Nutrient availability links mitochondria, apoptosis, and obesity
Pintus, F., Floris, G., & Rufini, A. (2012) · Aging · doi:10.18632/aging.100505 · Cited by 51
“Highly metabolic tissues (such as muscle) show increased fusion, stimulated by PGC-1 -mediated increase of Mfn2 expression.”
BackgroundInfluentialTherapeutic potential of activators and inhibitors of sirtuins
Balcerczyk, A., & Pirola, L. (2010) · BioFactors · doi:10.1002/biof.112 · Cited by 49
Sharma, P. K., Agrawal, V., & Roy, N. (2010) · AGE · doi:10.1007/s11357-010-9169-1 · Cited by 50
“It has been reported that calorie restriction affects mitochondria biogenesis in rats and humans (Civitarese et al. 2007; Nisoli et al. 2005).”
BackgroundResultA specific amino acid formula prevents alcoholic liver disease in rodents
Tedesco, L., Corsetti, G., Ruocco, C., Ragni, M., Rossi, F., Carruba, M. O., Valerio, A., & Nisoli, E. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00231.2017 · Cited by 51
Targeting mitochondrial fitness as a strategy for healthy vascular aging
Rossman, M. J., Gioscia‐Ryan, R. A., Clayton, Z. S., Murphy, M. P., & Seals, D. R. (2020) · Clinical Science · doi:10.1042/cs20190559 · Cited by 51
Resveratrol relieves ischemia‑induced oxidative stress in the hippocampus by activating SIRT1
Meng, Z., Li, J., Zhao, H., Liu, H., Zhang, G., Wang, L., Hu, H., Li, D., Liu, M., Bi, F.-L., et al. (2015) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2015.2555 · Cited by 49
“Another study demonstrated that SIRT1-dependent pathways, in addition to nitric oxide (NO)-dependent mechanisms, contribute to the beneficial mitochondrial and cellular effects of dietary restriction (39).”
BackgroundSirtuin regulation in calorie restriction
Qiu, X., Brown, K. V., Moran, Y., & Chen, D. (2009) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2009.09.015 · Cited by 50
Limited predictive value of TFAM in mitochondrial biogenesis
Kozhukhar, N., & ALEXEYEV, M. F. (2019) · Mitochondrion · doi:10.1016/j.mito.2019.08.001 · Cited by 52
Resveratrol: A Multifunctional Compound Improving Endothelial Function
Li, H., & Förstermann, U. (2009) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-009-6209-0 · Cited by 51
“Calorie restriction leads to the enhanced expression of SIRT1 and eNOS upregulation [21]; the endothelium-specific overexpression of SIRT1 results in an increase in eNOS expression in mice [22].”
BackgroundImpairment of endothelial nitric oxide synthase causes abnormal fat and glycogen deposition in liver
Schild, L., Dombrowski, F., Lendeckel, U., Schulz, C., Gardemann, A., & Keilhoff, G. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2007.12.007 · Cited by 49
“This conclusion was based on the finding that long term caloric restriction causes increase of eNOS protein as well as the mitochondrial proteins cytochrome c oxidase subunit IV and cytochrome c in WT mice but not in eNOS-KO mice [19].”
Hempenstall, S., Page, M. M., Wallen, K. R., & Selman, C. (2012) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2011.12.002 · Cited by 47
“, 2004a), and total oxygen (O2) consumption was elevated in several tissues in DR mice (Nisoli et al., 2005).”
InfluentialAfzaal, A., Rehman, K., Kamal, S., & Akash, M. S. H. (2022) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.23047 · Cited by 49
Targeting PGC-1α to control energy homeostasis
Wu, Z., & Boss, O. (2007) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.11.10.1329 · Cited by 50
“In addition, nitric oxide increases PGC-1 α level and increases mitochondrial biogenesis through the cGMP pathway [45,46] .”
BackgroundThe role of SirT1 in muscle mitochondrial turnover
Menzies, K. J., & Hood, D. A. (2011) · Mitochondrion · doi:10.1016/j.mito.2011.03.001 · Cited by 49
Mitochondrial function and diabetes: consequences for skeletal and cardiac muscle metabolism
Schrauwen-Hinderling, V. B., Kooi, M. E., & Schrauwen, P. (2016) · Antioxidants & Redox Signaling · doi:10.1089/ars.2015.6291 · Cited by 47
“In mice, CR was shown to induce mitochondrial biogenesis by upregulating PGC-1 a , NRF-1, and TFAM (74).”
Hormesis in Aging and Neurodegeneration—A Prodigy Awaiting Dissection
Mao, L., & Franke, J. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140713109 · Cited by 47
“mechanism [72,73].”
Mitochondrial Therapeutics for Cardioprotection
Carreira, R., Lee, P. P. W., & Gottlieb, R. A. (2011) · Current Pharmaceutical Design · doi:10.2174/138161211796904777 · Cited by 48
“This increase in mitochondrial biogenesis has been proposed to be critical for the beneficial effects of CR [250, 251, 254, 255].”
BackgroundInfluentialcGMP rescues mitochondrial dysfunction induced by glucose and insulin in myocytes
Mitsuishi, M., Miyashita, K., & Itoh, H. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.01.017 · Cited by 48
Liu, Z., Gan, L., Liu, G., Chen, Y., Wu, T., Feng, F., & Sun, C. (2016) · Journal of Lipid Research · doi:10.1194/jlr.m063537 · Cited by 47
“logical functions of many key metabolic tissues (37, 38).”
BackgroundLi, Y., Meng, X., Wang, W., Liu, F., Hao, Z.-R., Yang, Y., Zhao, J., Yin, W., Xu, L., Zhao, R., et al. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00394 · Cited by 47
“SIRT1 activates endothelial nitric oxide synthase and protects vascular smooth muscle cells against DNA damage, medial degeneration, and atherosclerosis (Nisoli et al., 2005; Gorenne et al., 2013).”
BackgroundPolonsky, K. S., & Burant, C. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-29738-7.00031-9 · Cited by 53
Zhang, L., Zhou, Y., Yang, Z., Jiang, L., Yan, X., Zhu, W., Shen, Y., Wang, B., Li, J., & Song, J. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03334-5 · Cited by 54
The anti-aging effects of Ludwigia octovalvis on Drosophila melanogaster and SAMP8 mice
Lin, W., Chen, J., Wang, J.-C., Chen, L.-Y., Lin, C.-H., Hsieh, T.-R., Wang, M.-F., Fu, T., & Wang, P. (2013) · AGE · doi:10.1007/s11357-013-9606-z · Cited by 47
“DR has been shown to increase mitochondrial activity (Nisoli et al. 2005; Lopez-Lluch et al. 2006), but to delay or reduce oxidative stress and damage in flies (Zheng et al.”
BackgroundThe measurement of protein synthesis for assessing proteostasis in studies of slowed aging
Miller, B. F., Drake, J. C., Naylor, B. C., Price, J. C., & Hamilton, K. L. (2014) · Ageing Research Reviews · doi:10.1016/j.arr.2014.09.005 · Cited by 47
“1 Caloric restriction—CR is a fascinating aging intervention because some evidence suggests that mitochondrial biogenesis is maintained or increased during CR (Nisoli, 2005), while others have speculated that decreased protein synthesis leads to lifespan extension (Kapahi, 2010; Tavernarakis, 2008).”
BackgroundMontesanto, A., Crocco, P., Tallaro, F., Pisani, F., Mazzei, B., Mari, V., Corsonello, A., Lattanzio, F., Passarino, G., & Rose, G. (2013) · Biogerontology · doi:10.1007/s10522-013-9421-z · Cited by 47
“Moreover, a reduction in survival rate of about 50 %, and an attenuation of caloric restriction-induced life extension has been observed in nos3 knockout mice (Dere et al. 2002; Nisoli et al. 2005).”
BackgroundChoi, E. M., Suh, K. S., Kim, Y., Hong, S. M., Park, S. Y., & Chon, S. (2015) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5b05157 · Cited by 46
Das, U. N. (2007) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2007.01.002 · Cited by 46
Erratum to: Resveratrol and red wine, healthy heart and longevity
Das, D. K., Mukherjee, S., & Ray, D. (2011) · Heart Failure Reviews · doi:10.1007/s10741-011-9234-6 · Cited by 49
“4 mg/kg/day) along with the high-fat diets extended the life span by inducing Sirt1 similar to calorie-restricted animals with greater SIRT1 coexpression [71].”
Milan, M., Brown, J., O’Reilly, C. L., Bubak, M. P., Negri, S., Balasubramanian, P., Dhanekula, A., Pharaoh, G. A., Reyff, Z., Ballard, C., et al. (2024) · Redox Biology · doi:10.1016/j.redox.2024.103189 · Cited by 47
Crosstalk between nitric oxide and hypoxia-inducible factor signaling pathways: an update
Poyton, R., & Hendrickson, M. (2015) · Research and Reports in Biochemistry · doi:10.2147/rrbc.s58280 · Cited by 45
“increased lifespan under nonrestricted diets, but when calorically restricted (CR), loss of HIF-1 decreased the lifespan extension typically conferred by CR, indicating HIF-1 may play an important role in the mitohormesis necessary for CR-dependent lifespan elongation.(120) How does NO then relate to HIF-1 and aging?…”
Regulation and protection of mitochondrial physiology by sirtuins
Pereira, C. V., Lebiedzińska, M., Wieckowski, M. R., & Oliveira, P. J. (2011) · Mitochondrion · doi:10.1016/j.mito.2011.07.003 · Cited by 46
The roles of FoxOs in modulation of aging by calorie restriction
Kim, D. H., Park, M. H., Lee, E. K., Choi, Y. J., Chung, K. W., Moon, K. M., Kim, M. J., An, H. J., Park, J. W., Kim, N. D., et al. (2014) · Biogerontology · doi:10.1007/s10522-014-9519-y · Cited by 47
“CR increases SIRT1 expression in liver, adipose tissue, brain, and kidney (Nisoli et al. 2005), and SIRT1-dependent deacetylation promotes the nuclear trapping of FoxO1 and upregulates the expressions of its downstream genes (Frescas et al. 2005; Kobayashi et al. 2005).”
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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