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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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“These conditions include exercise in muscle and caloric restriction in brain, heart, liver, and white and brown adipose tissue (which also increase mitochondrial biogenesis) (44, 219).”
BackgroundTranscriptional control of mitochondrial biogenesis: the central role of PGC-1
Ventura-Clapier, R., Garnier, A., & Veksler, V. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn098 · Cited by 932
“Interestingly, caloric restriction-induced mitochondrial biogenesis in heart is accompanied by increased SIRT1 expression in wild-type but not eNOS mice.(49) These results again indicate that mitochondrial biogenesis is strictly controlled in the heart.”
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Calorie Restriction Increases Muscle Mitochondrial Biogenesis in Healthy Humans
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BackgroundResultInfluentialMitochondria are required for pro-ageing features of the senescent phenotype
Correia‐Melo, C., Marques, F. D., Anderson, R., Hewitt, G., Hewitt, R., Cole, J., Carroll, B. M., Miwa, S., Birch, J., Merz, A., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201592862 · Cited by 796
“This latter study, together with other more recent reports (Hancock et al , 2011; Lanza et al , 2012; Price et al , 2012), has questioned early associations between CR and enhanced mitochondrial content (Nisoli et al , 2005).”
Ristow, M., & Zarse, K. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.03.014 · Cited by 789
“Similarly, however analyzing global CR (and not specifically glucose restriction), it was shown that food deprivation promotes mitochondrial biogenesis and OxPhos in rodents (Nisoli et al., 2005).”
BackgroundSpeakman, J. R., & Mitchell, S. E. (2011) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2011.07.001 · Cited by 797
“A second signaling system implicated in the immediate activity response is the orexin (hypocretin) system (Novak et al., 2005).”
BackgroundInfluentialMolecular mechanisms of dietary restriction promoting health and longevity
Green, C. L., Lamming, D. W., & Fontana, L. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00411-4 · Cited by 714
Luen Tang, B. (2016) · Molecules and Cells · doi:10.14348/molcells.2016.2318 · Cited by 740
“CR has been shown to significantly increase mitochondrial biogenesis in multiple tissues in mice (Nisoli et al., 2005) and in human muscles (Civitarese et al., 2007).”
BackgroundResveratrol stimulates AMP kinase activity in neurons
Dasgupta, B., & Milbrandt, J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610068104 · Cited by 723
Translational Regulation of Gene Expression during Conditions of Cell Stress
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“, 2007), and under nutrient depletion in mammals there is an increase in mitochondrial biogenesis (Nisoli et al., 2005).”
BackgroundSIRT1 transgenic mice show phenotypes resembling calorie restriction
Bordone, L., Cohen, D., Robinson, A., Motta, M. C., Van Veen, E., Czopik, A., Steele, A. D., Crowe, H., Marmor, S., Luo, J., et al. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00335.x · Cited by 722
Extending life span by increasing oxidative stress
Ristow, M., & Schmeisser, S. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.05.010 · Cited by 737
“Furthermore, CR promotes mitochondria biogenesis and OxPhos in rodents as well as enhancement of respiratory capacity in mammalian cells [114,115].”
BackgroundTranscriptional Control of Mitochondrial Biogenesis and Function
Hock, M. B., & Kralli, A. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163119 · Cited by 626
“Mice lacking eNOS, an NO-producing enzyme that is induced by caloric restriction, show mitochondrial defects in multiple tissues (135).”
BackgroundBarger, J. L., Kayo, T., Vann, J. M., Arias, E. B., Wang, J., Hacker, T. A., Wang, Y., Raederstorff, D., Morrow, J. D., Leeuwenburgh, C., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002264 · Cited by 580
“Previous studies in rats [23] and humans [24] suggest that CR induces SIRT1 in these species, but the only study in mice that addressed this issue used an ‘‘every other day’’ feeding protocol, and therefore does not represent CR [31].”
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Tabit, C. E., Chung, W. B., Hamburg, N. M., & Vita, J. A. (2010) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-010-9134-4 · Cited by 594
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“…this discrepancy can be explained by the fact that calorie restriction also promotes mitochondrial biogenesis, thereby maintaining total metabolic output per cell while decreasing mitochondrial production of ROS (Diano et al., 2003; Nisoli et al., 2005; Civitarese et al., 2007; Valle et al., 2008).”
BackgroundD'Antona, G., Ragni, M., Cardile, A., Tedesco, L., Dossena, M., Bruttini, F., Caliaro, F., Corsetti, G., Bottinelli, R., Carruba, M. O., et al. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.08.016 · Cited by 568
“…of sirtuin 1 (SIRT1, a member of the sirtuin family linked to life span extension, enhanced mitochondrial biogenesis, and decreased ROS production), thus reducing oxidative damage in metabolically active tissues of mice and humans (Civitarese et al., 2007; Nisoli et al., 2005; Ristow et al., 2009).”
BackgroundResultInfluentialSelf-citationTissue-specific regulation of SIRT1 by calorie restriction
Chen, D., Bruno, J., Easlon, E., Lin, S.-J., Cheng, H.-L., Alt, F. W., & Guarente, L. (2008) · Genes & Development · doi:10.1101/gad.1650608 · Cited by 567
“The levels of SIRT1 have been reported to increase in rodent and human tissues in response to CR (Cohen et al. 2004; Nisoli et al. 2005; Civitarese et al. 2007), and this increase is proposed to cause favorable changes in metabolism and stress tolerance triggered by this diet.”
BackgroundResultAdipokines as novel biomarkers and regulators of the metabolic syndrome
Deng, Y., & Scherer, P. E. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05875.x · Cited by 578
4E-BP Extends Lifespan upon Dietary Restriction by Enhancing Mitochondrial Activity in Drosophila
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“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript Mitochondrial biogenesis and efficiency have been suggested to increase under DR in mammals (Lopez-Lluch et al., 2006; Nisoli et al., 2005).”
Mitohormesis: Promoting Health and Lifespan by Increased Levels of Reactive Oxygen Species (ROS)
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“Chronic exposure of mammalian cells to NO has been shown to result in cGMP-mediated activation of regulatory protein sirtuin (SIRT1), which upregulates transcriptional factors and nuclear respiratory factors involved in the coordination of mitochondrial fusion and fission events (24, 35, 36).”
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“, 2006) and endothelial nitric oxide synthase (eNOS) (Nisoli et al., 2005).”
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Seo, A. Y., Joseph, A.-M., Dutta, D., Hwang, J. C. Y., Aris, J. P., & Leeuwenburgh, C. (2010) · Journal of Cell Science · doi:10.1242/jcs.070490 · Cited by 522
“Furthermore, calorie-restriction-induced mitochondrial biogenesis in mice increases PGC-1, Mfn1 and Mfn2 expression levels in several tissues (Nisoli et al., 2005).”
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Guarente, L. (2008) · Cell · doi:10.1016/j.cell.2008.01.007 · Cited by 513
“Second, CR increases respiration as well as mitochondrial number per cell in mice (Nisoli et al., 2005) (see Figure 1).”
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“NRF1 is a transcription factor, and its expression is regulated by CR (Mahishi and Usdin, 2006; Nisoli et al., 2005).”
Mitochondria and Endothelial Function
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“The first line of defense against mitochondrial superoxide is MnSOD.”
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Hwang, J.-W., Yao, H., Caito, S., Sundar, I. K., & Rahman, I. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.03.015 · Cited by 503
“cGMP and eNOS are elevated in tissues of calorie restricted mice, and the production of NO increases SIRT1 expression, which was blunted in eNOS-deficient mice [137].”
Mitofusins, from Mitochondria to Metabolism
Schrepfer, E., & Scorrano, L. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.022 · Cited by 504
Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog
Rera, M., Bahadorani, S., Cho, J., Koehler, C. L., Ulgherait, M., Hur, J. H., Ansari, W. S., Lo, T., Jones, D. L., & Walker, D. W. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.09.013 · Cited by 472
“Cell M humans (Bishop and Guarente, 2007; Civitarese et al., 2007; Lin et al., 2002; López-Lluch et al., 2006; Nisoli et al., 2005; Zid et al., 2009).”
Terman, A., Kurz, T., Navratil, M., Arriaga, E. A., & Brunk, U. T. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2598 · Cited by 490
“Direct regulation by NO occurs through upregulation of transcription factors by cyclic GMP, which in turn leads to the expression of sirtuins [silent information regulation 2 (Sir2) proteins] that deacetylate PGC-1 a , making it more active (24, 172).”
Insulin resistance and atherosclerosis
Semenkovich, C. F. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29024 · Cited by 481
Mechanisms of Disease: endothelial dysfunction in insulin resistance and diabetes
Rask‐Madsen, C., & King, G. L. (2006) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0366 · Cited by 490
“NO derived from eNOS is an important regulator of mitochondrial number and function during caloric restriction”
BackgroundMaalouf, M., Sullivan, P. G., Davis, L. M., Kim, D., & Rho, J. M. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.11.065 · Cited by 477
Sirtuins as potential targets for metabolic syndrome
Guarente, L. (2006) · Nature · doi:10.1038/nature05486 · Cited by 468
“Indeed, SIRT1 protein levels have been shown to increase during CR in the brain, white adipose tissue, muscles, liver and kidney”
BackgroundCalorie restriction and sirtuins revisited
Guarente, L. (2013) · Genes & Development · doi:10.1101/gad.227439.113 · Cited by 464
“Importantly, eNOS / mice do not show the induction of mitochondria by CR (Nisoli et al. 2005).”
BackgroundNitric oxide and atherosclerosis: An update
Claudio Napoli, A., de Nigris, F., Williams‐Ignarro, S., Pignalosa, O., Sica, V., & Ignarro, L. J. (2006) · Nitric Oxide · doi:10.1016/j.niox.2006.03.011 · Cited by 471
“In a very recent study, calorie restriction for either 3 or 12 months induced eNOS expression and 3 ,5 -cyclic guanosine monophosphate formation in various tissues of male mice [108].”
BackgroundMitochondria and Reactive Oxygen Species in Aging and Age-Related Diseases
Giorgi, C., Marchi, S., Simões, I. C. M., Ren, Z., Morciano, G., Perrone, M., Patalas‐Krawczyk, P., Borchard, S., Jędrak, P., Pierzynowska, K., et al. (2018) · International review of cytology · doi:10.1016/bs.ircmb.2018.05.006 · Cited by 484
Effects of Sex, Strain, and Energy Intake on Hallmarks of Aging in Mice
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“, 2013), enhanced mitochondrial function (López-Lluch et al., 2006; Nisoli et al., 2005), improved proteostasis and autophagy (Cuervo, 2008; Hansen et al.”
BackgroundSIRT3 deacetylates FOXO3 to protect mitochondria against oxidative damage
Tseng, A. H.-H., Shieh, S.-S., & Wang, D. L. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.05.002 · Cited by 458
“Our results demonstrate that SIRT3–FOXO3 upregulate PGC1α and TFAM to promote mitochondrial biogenesis; induce Drp1, Fis1, and Mfn2 to coordinate mitochondrial fission/fusion; and increase Bnip3, Nix, and LC3-II/LC3-I to execute mitophagy under oxidative stress.”
BackgroundInfluentialResveratrol induces mitochondrial biogenesis in endothelial cells
Csiszár, A., Labinskyy, N., Pinto, J. T., Ballabh, P., Zhang, H., Losonczy, G., Pearson, K. J., de Cabo, R., Pacher, P., Zhang, C., et al. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00368.2009 · Cited by 459
“Previous studies also suggest that expression of mitochondrial biogenesis factors may be directly regulated by bioavailability of NO (2, 31).”
BackgroundProtective effects of sirtuins in cardiovascular diseases: from bench to bedside
Winnik, S., Auwerx, J., Sinclair, D. A., & Matter, C. M. (2015) · European Heart Journal · doi:10.1093/eurheartj/ehv290 · Cited by 422
“First evidence of a connection between Sirt1 and endothelial cells was that Sirt1 activates endothelial nitric oxide synthase (eNOS).(11) Later on, studies”
BackgroundMitochondria and Cardiovascular Aging
Dai, D., Rabinovitch, P. S., & Ungvari, Z. I. (2012) · Circulation Research · doi:10.1161/circresaha.111.246140 · Cited by 446
Targeting Sirtuin 1 to Improve Metabolism: All You Need Is NAD+?
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“It is noteworthy that impaired eNOS function has major consequences on whole-body metabolism, since it affects peripheral glucose uptake (Kapur et al., 1997; Li et al., 2004) and mitochondrial biogenesis (Nisoli et al., 2003; Nisoli et al., 2005; Le Gouill et al., 2007).”
BackgroundMitochondria and Neuroplasticity
Cheng, A., Hou, Y., & Mattson, M. P. (2010) · ASN NEURO · doi:10.1042/an20100019 · Cited by 446
“CR (caloric restriction) and exercise stimulate mitochondrial biogenesis in muscle and nerve cells by a PGC1a-mediated mechanism (Puigserver et al., 1998; Yoon et al., 2001; Baar et al., 2002; Lin et al., 2004; Norrbom et al., 2004; Nisoli et al., 2005; López-Lluch et al., 2006).”
BackgroundMitochondria and ageing: Role in heart, skeletal muscle and adipose tissue
Boengler, K., Kosiol, M., Mayr, M., Schulz, R., & Rohrbach, S. (2017) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12178 · Cited by 421
“in mice after CR, a condition with chronically low nutrients.(181) The mechanistic target of rapamycin (mTOR) complex 1 (mTORC1) signalling pathway is also critically”
BackgroundMitochondrial Biogenesis and Proteome Remodeling Promote One-Carbon Metabolism for T Cell Activation
Ron-Harel, N., Santos, D., Ghergurovich, J. M., Sage, P. T., Reddy, A., Lovitch, S. B., Dephoure, N., Satterstrom, F. K., Sheffer, M., Spinelli, J. B., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.06.007 · Cited by 429
“Mitochondrial biogenesis has been observed in a number of models, including brown fat activation, exercise, and calorie restriction (Finley et al., 2012; Freyssenet et al., 1996; Martin-Montalvo and de Cabo, 2013; Nisoli et al., 2005).”
BackgroundSirtuins — novel therapeutic targets to treat age-associated diseases
Lavu, S., Boss, O., Elliott, P. J., & Lambert, P. (2008) · Nature Reviews Drug Discovery · doi:10.1038/nrd2665 · Cited by 427
“The expression level of SIRT1 increases upon calorie restriction in several rodent and human tissues such as white adipose, liver, skeletal muscle, brain and kidne”
BackgroundGenetic links between diet and lifespan: shared mechanisms from yeast to humans
Bishop, N. A., & Guarente, L. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2188 · Cited by 426
Figueira, T. R., de Barros, M. H., Camargo, A. A., Castilho, R. F., Ferreira, J. C. B., Kowaltowski, A. J., Sluse, F. E., de Souza-Pinto, N. C., & Vercesi, A. E. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4729 · Cited by 430
“Interestingly, calorie restriction increases mitochondrial content (88, 109, 326, 387), but decreases ROS release, possibly due to mitochondrial uncoupling (88, 277, 296).”
Conserved Metabolic Regulatory Functions of Sirtuins
Schwer, B., & Verdin, E. M. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.006 · Cited by 422
Monda, M., Messina, G., Scognamiglio, I., Lombardi, A., Martin, G. A., Sperlongano, P., Porcelli, M., Caraglia, M., & Stiuso, P. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/131024 · Cited by 178
Nitric Oxide and the Vascular Endothelium
Moncada, S., & Higgs, E. A. (2006) · Springer eBooks · doi:10.1007/3-540-32967-6_7 · Cited by 419
“Thus, NO plays a role in the processes induced by calorie restriction andmaybe involved in the extensionof lifespan inmammals (Nisoli et al. 2005).”
BackgroundVillena, J. A. (2014) · FEBS Journal · doi:10.1111/febs.13175 · Cited by 413
Sirtuins: The ‘ magnificent seven ’, function, metabolism and longevity
Dali‐Youcef, N., Lagouge, M., Froelich, S., Koehl, C., Schoonjans, K., & Auwerx, J. (2007) · Annals of Medicine · doi:10.1080/07853890701408194 · Cited by 402
“Interestingly, these effects were completely inhibited in eNOS animals in which life span was significantly reduced (55).”
BackgroundCaloric restriction, SIRT1 and longevity
Cantó, C., & Auwerx, J. (2009) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2009.03.008 · Cited by 395
“In line with this, SIRT1 protein levels are increased in response to CR in many key metabolic tissues [46-50].”
SIRT1 and SIRT6 Signaling Pathways in Cardiovascular Disease Protection
D’Onofrio, N., Servillo, L., & Balestrieri, M. L. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7178 · Cited by 396
“The enhanced SIRT1 expression observed during the increased eNOS expression and cGMP formation in mice at 3–12 months of calorie restriction is consistent with the key regulatory role of this protein in mammal survival in response to stress (133).”
BackgroundTen years of NAD-dependent SIR2 family deacetylases: implications for metabolic diseases
Imai, S., & Guarente, L. (2010) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.02.003 · Cited by 394
Zhang, Q.-J., Wang, Z., Chen, H.-Z., Zhou, S., Zheng, W., Liu, G., Wei, Y.-S., Cai, H., Liu, D.-P., & Liang, C.-C. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn224 · Cited by 349
“Former research found that CR induces eNOS expression and mitochondrial biogenesis.(26) Here we give direct evidence that SIRT1 is a regulator of eNOS expression in vitro and in vivo.”
BackgroundThomas, S. R., Witting, P. K., & Drummond, G. R. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2027 · Cited by 383
“For example, eNOS-derived NO signals for mitochondrial biogenesis in response to calorie restriction, which may be important for extension of the mammalian life span (373, 374).”
Carlström, M., Larsen, F. J., Nyström, T., Hezel, M., Borniquel, S., Weitzberg, E., & Lundberg, J. O. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008872107 · Cited by 382
Mitochondrial dysfunction as a cause of ageing
Trifunović, A., & Larsson, N. (2008) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2007.01905.x · Cited by 384
Seven sirtuins for seven deadly diseases ofaging
Morris, B. J. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.10.525 · Cited by 386
“Moreover, during calorie restriction NO derived from eNOS increases and stimulates SIRT1 expression [355].”
BackgroundSirtuins in Aging and DiseasePreprint
Guarente, L. (2007) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2007.72.024 · Cited by 376
Mitochondrial biogenesis and healthy aging
López-Lluch, G., Irusta, P. M., Navas, P., & de Cabo, R. (2008) · Experimental Gerontology · doi:10.1016/j.exger.2008.06.014 · Cited by 364
“In fact, resveratrol is completely unable to modulate PGC1-α function in SIRT1 −/− MEFs.”
BackgroundInfluentialOxidative Stress as a Mediator of Cardiovascular Disease
Elahi, M. M., Kong, Y. X. G., & Matata, B. M. (2009) · Oxidative Medicine and Cellular Longevity · doi:10.4161/oxim.2.5.9441 · Cited by 364
Madamanchi, C., Alhosaini, H., Sumida, A., & Runge, M. S. (2014) · International Journal of Cardiology · doi:10.1016/j.ijcard.2014.08.007 · Cited by 357
“In this context, it is of interest to note that calorie restriction promotes muscle mitochondrial biogenesis in rodents [106] as well as humans [107] by increasing the levels of nitric oxide, the upstream activator of cGMP/cGK1 pathway.”
BackgroundMetabolic Effects of Dietary Nitrate in Health and Disease
Lundberg, J. O., Carlström, M., & Weitzberg, E. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.06.007 · Cited by 374
eNOS, metabolic syndrome and cardiovascular disease
Huang, P. L. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.03.005 · Cited by 365
“eNOS-knockout mice also fail to show mitochondrial biogenesis in response to exercise or caloric restriction [87].”
BackgroundMitochondrial Quality Control and Disease: Insights into Ischemia-Reperfusion Injury
Anzell, A. R., Maizy, R., Przyklenk, K., & Sanderson, T. H. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0503-9 · Cited by 359
Ungvari, Z. I., Orosz, Z. Z., Labinskyy, N., Rivera, A., Xiangmin, Z., Smith, K. E., & Csiszár, A. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01346.2006 · Cited by 352
Sirtuins mediate mammalian metabolic responses to nutrient availability
Chalkiadaki, A., & Guarente, L. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.225 · Cited by 344
Mitochondria, endothelial cell function, and vascular diseases
Tang, X., Luo, Y., Chen, H., & Liu, D. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00175 · Cited by 361
Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity
Caldeira da Silva, C. C., Cerqueira, F. M., Barbosa, L. F., Medeiros, M. H. G., & Kowaltowski, A. J. (2008) · Aging Cell · doi:10.1111/j.1474-9726.2008.00407.x · Cited by 306
“Lower insulin levels in calorie-restricted animals may induce nitric oxide synthase (Nisoli et al., 2005) and increase uncoupling protein expression (Nisoli et al., 2003).”
BackgroundInfluentialLu, Q., Zhu, Y., Deng, C., Liang, Z., Chen, J., Chen, Y., Wang, X., Liu, Y., Tian, Y., & Yang, Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01756-w · Cited by 391
Sergi, D., Naumovski, N., Heilbronn, L. K., Abeywardena, M., O’Callaghan, N., Lionetti, L., & Luscombe-Marsh, N. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00532 · Cited by 347
Resveratrol—A boon for treating Alzheimer's disease?
Anekonda, T. S. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.04.004 · Cited by 343
“This increased expression was associated with increased SIRT1, mitochondrial biogenesis, increased oxygen consumption, and increased ATP production (Nisoli 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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