Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide
Abstract
Nitric oxide was found to trigger mitochondrial biogenesis in cells as diverse as brown adipocytes and 3T3-L1, U937, and HeLa cells. This effect of nitric oxide was dependent on guanosine 3',5'-monophosphate (cGMP) and was mediated by the induction of peroxisome proliferator-activated receptor gamma coactivator 1alpha, a master regulator of mitochondrial biogenesis. Moreover, the mitochondrial biogenesis induced by exposure to cold was markedly reduced in brown adipose tissue of endothelial nitric oxide synthase null-mutant (eNOS-/-) mice, which had a reduced metabolic rate and accelerated weight gain as compared to wild-type mice. Thus, a nitric oxide-cGMP-dependent pathway controls mitochondrial biogenesis and body energy balance.
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Chronic exposure to relatively high levels of NO results in mitochondrial biogenesis, which could reprogram a cell or tissue to have a higher metabolic capacity.
“Chronic exposure to relatively high levels of NO results in mitochondrial biogenesis [113-115], which could reprogram a cell or tissue to have a higher metabolic capacity.”
From Regulation of obesity and insulin resistance by nitric oxide (2014) · cites this paper as [114]
Cites
Ford, E. S., Giles, W. H., & Dietz, W. H. (2002) · JAMA · doi:10.1001/jama.287.3.356 · Cited by 6,698 · see citing works
Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)80611-x · Cited by 4,139 · see citing works
A Cold-Inducible Coactivator of Nuclear Receptors Linked to Adaptive Thermogenesis
Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., & Spiegelman, B. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81410-5 · Cited by 3,864 · see citing works
Hypertension in mice lacking the gene for endothelial nitric oxide synthase
Huang, P. L., Huang, Z., Mashimo, H., Bloch, K. D., Moskowitz, M. A., Bevan, J. A., & Fishman, M. C. (1995) · Nature · doi:10.1038/377239a0 · Cited by 2,070 · see citing works
Green, H., & Kehinde, O. (1975) · Cell · doi:10.1016/0092-8674(75)90087-2 · Cited by 1,362 · see citing works
Peroxisome proliferator–activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis
Lehman, J. J., Barger, P. M., Kovacs, A., Saffitz, J. E., Medeiros, D. M., & Kelly, D. P. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10268 · Cited by 1,285 · see citing works
Cleeter, M. W. J., Cooper, J. M., Darley-Usmar, V. M., Moncada, S., & Schapira, A. H. V. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)00424-2 · Cited by 1,241 · see citing works
Self-citationVirbasius, J. V., & Scarpulla, R. C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.4.1309 · Cited by 819 · see citing works
Regulation of mitochondrial biogenesis in skeletal muscle by CaMK
Wu, H., Kanatous, S. B., Thurmond, F. A., Gallardo, T., Isotani, E., Bassel-Duby, R., & Williams, R. S. (2002) · Science · doi:10.1126/science.1071163 · Cited by 684 · see citing works
Lin, J., Puigserver, P., Donovan, J., Tarr, P., & Spiegelman, B. M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c100631200 · Cited by 552 · see citing works
Shankar, R. R., Yu-ling, W., Shen, H.-Q., Zhu, J. S., & Baron, A. (2000) · Diabetes · doi:10.2337/diabetes.49.5.684 · Cited by 297 · see citing works
The adipose organ: morphological perspectives of adipose tissues
Cinti, S. (2001) · Proceedings of The Nutrition Society · doi:10.1079/pns200192 · Cited by 228 · see citing works
Nisoli, E., Clementi, E., Tonello, C., Sciorati, C., Briscini, L., & Carruba, M. O. (1998) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0702131 · Cited by 110 · see citing works
Self-citationEvidence for a functional nitric oxide synthase system in brown adipocyte nucleus
Giordano, A., Tonello, C., Bulbarelli, A., Cozzi, V., Cinti, S., Carruba, M. O., & Nisoli, E. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)02245-7 · Cited by 110 · see citing works
Self-citationNadai, C. D., Sestili, P., Cantoni, O., Lièvremont, J.-P., Sciorati, C., Barsacchi, R., Moncada, S., Meldolesi, J., & Clementi, E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.070062397 · Cited by 109 · see citing works
Self-citationHimms‐Hagen, J. (1995) · Experimental Biology and Medicine · doi:10.3181/00379727-208-43847a · Cited by 106 · see citing works
Nicholls, D. G. (2001) · Biochemical Society Transactions · doi:10.1042/bst0290751 · Cited by 102 · see citing works
Boss, O., Bachman, E. S., Vidal‐Puig, A., Zhang, C., Peroni, O. D., & Lowell, B. B. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1145 · Cited by 100 · see citing works
Activation of the Endothelial Nitric-oxide Synthase by Tumor Necrosis Factor-α
Bulotta, S., Barsacchi, R., Rotiroti, D., Borgese, N., & Clementi, E. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m006535200 · Cited by 92 · see citing works
Self-citationDevelopment of brown fat cells in monolayer culture
Néchad, M. (1983) · Experimental Cell Research · doi:10.1016/0014-4827(83)90385-3 · Cited by 47 · see citing works
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Transcriptional paradigms in mammalian mitochondrial biogenesis and function
Scarpulla, R. C. (2008) · Physiological Reviews · doi:10.1152/physrev.00025.2007 · Cited by 1,666 · see citing works
Cancer metabolism: a therapeutic perspective
Martinez-Outschoorn, U. E., Peiris-Pagés, M., Pestell, R. G., Sotgia, F., & Lisanti, M. P. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2016.60 · Cited by 1,505 · see citing works
Transcriptional regulatory circuits controlling mitochondrial biogenesis and function
Kelly, D. P., & Scarpulla, R. C. (2004) · Genes & Development · doi:10.1101/gad.1177604 · Cited by 1,243 · see citing works
Regulation of pgc-1α, a nodal regulator of mitochondrial biogenesis
Fernandez-Marcos, P. J., & Auwerx, J. (2011) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.001917 · Cited by 1,237 · see citing works
Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS
Nisoli, E., Tonello, C., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Falcone, S., Valerio, A., Cantoni, O., Clementi, E., et al. (2005) · Science · doi:10.1126/science.1117728 · Cited by 1,107 · see citing works
Role of Mitochondrial Dysfunction in Insulin Resistance
Kim, J.-A., Wei, Y., & Sowers, J. R. (2008) · Circulation Research · doi:10.1161/circresaha.107.165472 · Cited by 1,103 · see citing works
Handschin, C., & Spiegelman, B. M. (2006) · Endocrine Reviews · doi:10.1210/er.2006-0037 · Cited by 1,090 · see citing works
Transcriptional 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 · see citing works
Bordicchia, M., Liu, D., Amri, E.-Z., Ailhaud, G., Dessì-Fulgheri, P., Zhang, C., Takahashi, N., Sarzani, R., & Collins, S. (2012) · Journal of Clinical Investigation · doi:10.1172/jci59701 · Cited by 872 · see citing works
Butow, R. A., & Avadhani, N. G. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00179-0 · Cited by 882 · see citing works
The discovery of nitric oxide and its role in vascular biology
Moncada, S., & Higgs, E. A. (2006) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706458 · Cited by 863 · see citing works
Self-citationTranscriptional integration of mitochondrial biogenesis
Scarpulla, R. C., Vega, R. B., & Kelly, D. P. (2012) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2012.06.006 · Cited by 798 · see citing works
Calorie Restriction Increases Muscle Mitochondrial Biogenesis in Healthy Humans
Civitarese, A. E., Carling, S., Heilbronn, L. K., Hulver, M. H., Ukropcova, B., Deutsch, W. A., Smith, S. R., & Ravussin, E. (2007) · PLoS Medicine · doi:10.1371/journal.pmed.0040076 · Cited by 790 · see citing works
Sivitz, W. I., & Yorek, M. A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2531 · Cited by 742 · see citing works
Dietary Inorganic Nitrate Improves Mitochondrial Efficiency in Humans
Larsen, F. J., Schiffer, T. A., Borniquel, S., Sahlin, K., Ekblom, B., Lundberg, J. O., & Weitzberg, E. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.01.004 · Cited by 689 · see citing works
Shiva, S., Huang, Z., Grubina, R., Sun, J., Ringwood, L. A., MacArthur, P. H., Xu, X., Murphy, E., Darley-Usmar, V. M., & Gladwin, M. T. (2007) · Circulation Research · doi:10.1161/01.res.0000260171.52224.6b · Cited by 599 · see citing works
D'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 · see citing works
Self-citationShiva, S., Sack, M. N., Greer, J. J., Duranski, M., Ringwood, L. A., Burwell, L., Wang, X., MacArthur, P. H., Shoja, A., Raghavachari, N., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070198 · Cited by 555 · see citing works
Mitochondria and Endothelial Function
Kluge, M. A., Fetterman, J. L., & Vita, J. A. (2013) · Circulation Research · doi:10.1161/circresaha.111.300233 · Cited by 508 · see citing works
Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals
Nisoli, E., Falcone, S., Tonello, C., Cozzi, V., Palomba, L., Fiorani, M., Pisconti, A., Brunelli, S., Cardile, A., Francolini, M., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405432101 · Cited by 495 · see citing works
Self-citationTargeting Sirtuin 1 to Improve Metabolism: All You Need Is NAD+?
Cantó, C., & Auwerx, J. (2012) · Pharmacological Reviews · doi:10.1124/pr.110.003905 · Cited by 433 · see citing works
Thomas, S. R., Witting, P. K., & Drummond, G. R. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2027 · Cited by 383 · see citing works
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 · see citing works
McKnight, J. R., Satterfield, M. C., Jobgen, W. S., Smith, S. B., Spencer, T. E., Meininger, C. J., McNeal, C. J., & Wu, G. (2010) · Amino Acids · doi:10.1007/s00726-010-0598-z · Cited by 376 · see citing works
Kim, F., Pham, M., Maloney, E., Rizzo, N. O., Morton, G. J., Wisse, B. E., Kirk, E. A., Chait, A., & Schwartz, M. W. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.169722 · Cited by 364 · see citing works
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 · see citing works
Roles of dietary inorganic nitrate in cardiovascular health and disease
Lundberg, J. O., Carlström, M., Larsen, F. J., & Weitzberg, E. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvq325 · Cited by 355 · see citing works
Dietary L-arginine supplementation reduces fat mass in Zucker diabetic fatty rats
Fu, W. J., Haynes, T. E., Kohli, R., Hu, J., Shi, W., Spencer, T. E., Carroll, R. J., Meininger, C. J., & Wu, G. (2005) · The Journal of Nutrition · doi:10.1093/jn/135.4.714 · Cited by 353 · see citing works
TNF- downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents
Valerio, A. (2006) · Journal of Clinical Investigation · doi:10.1172/jci28570 · Cited by 327 · see citing works
Self-citationGoossens, G. H., Bizzarri, A., Venteclef, N., Essers, Y., Cleutjens, J. P., Konings, E., Jocken, J. W. E., Čajlaković, M., Ribitsch, V., Clément, K., et al. (2011) · Circulation · doi:10.1161/circulationaha.111.027813 · Cited by 324 · see citing works
The secretory function of adipocytes in the physiology of white adipose tissue
Wang, P., Mariman, E., Renes, J., & Keijer, J. (2008) · Journal of Cellular Physiology · doi:10.1002/jcp.21386 · Cited by 318 · see citing works
The functional nitrite reductase activity of the heme-globins
Gladwin, M. T., & Kim-Shapiro, D. B. (2008) · Blood · doi:10.1182/blood-2008-01-115261 · Cited by 293 · see citing works
Jobgen, W., Meininger, C. J., Jobgen, S. C., Li, P., Lee, M.-J., Smith, S. B., Spencer, T. E., Fried, S. K., & Wu, G. (2009) · The Journal of Nutrition · doi:10.3945/jn.108.096362 · Cited by 288 · see citing works
Carbon monoxide, reactive oxygen signaling, and oxidative stress
Piantadosi, C. A. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.05.013 · Cited by 281 · see citing works
Regulation of obesity and insulin resistance by nitric oxide
Sansbury, B. E., & Hill, B. G. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.05.016 · Cited by 274 · see citing works
“Chronic exposure to relatively high levels of NO results in mitochondrial biogenesis [113–115], which”
BackgroundNitrite in nitric oxide biology: Cause or consequence?
Bryan, N. S. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2006.05.019 · Cited by 260 · see citing works
Mitochondrial Dysfunction in Alzheimer’s Disease and the Rationale for Bioenergetics Based Therapies
Onyango, I. G., Dennis, J., & Khan, S. M. (2016) · Aging and Disease · doi:10.14336/ad.2015.1007 · Cited by 260 · see citing works
Merry, T. L., & Ristow, M. (2016) · The Journal of Physiology · doi:10.1113/jp271957 · Cited by 246 · see citing works
Ayala, J. E., Bracy, D. P., Julien, B. M., Rottman, J. N., Fueger, P. T., & Wasserman, D. H. (2007) · Diabetes · doi:10.2337/db06-0883 · Cited by 237 · see citing works
The autocrine and paracrine roles of adipokines
Karastergiou, K., & Mohamed-Ali, V. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.11.011 · Cited by 233 · see citing works
Piccoli, C., Ria, R., Scrima, R., Cela, O., D'Aprile, A., Boffoli, D., Falzetti, F., Tabilio, A., & Capitanio, N. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m500047200 · Cited by 209 · see citing works
(–)-Epicatechin enhances fatigue resistance and oxidative capacity in mouse muscle
Nogueira, L., Ramirez‐Sanchez, I., Perkins, G. A., Murphy, A., Taub, P. R., Ceballos, G., Villarreal, F. J., Hogan, M. C., & Malek, M. H. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.209924 · Cited by 205 · see citing works
Biology of nitrogen oxides in the gastrointestinal tract
Lundberg, J. O., & Weitzberg, E. (2013) · Gut · doi:10.1136/gutjnl-2011-301649 · Cited by 200 · see citing works
Branched-chain amino acids, mitochondrial biogenesis, and healthspan: an evolutionary perspective
Valerio, A., D'Antona, G., & Nisoli, E. (2011) · Aging · doi:10.18632/aging.100322 · Cited by 196 · see citing works
Self-citationMusclin is an activity-stimulated myokine that enhances physical endurance
Subbotina, E., Sierra, A., Zhu, Z., Gao, Z., Koganti, S. R. K., Reyes, S., Stepniak, E., Walsh, S. A., Acevedo, M. R., Perez-Terzic, C. M., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514250112 · Cited by 198 · see citing works
Placental mitochondrial content and function in intrauterine growth restriction and preeclampsia
Mandò, C., De Palma, C., Stampalija, T., Anelli, G. M., Figus, M., Novielli, C., Parisi, F., Clementi, E., Ferrazzi, E., & Cetin, I. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00426.2013 · Cited by 196 · see citing works
Self-citationKim, S.-J., Nian, C., Karunakaran, S., Clee, S. M., Isales, C. M., & McIntosh, C. H. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040156 · Cited by 182 · see citing works
Regulatory circuits controlling white versus brown adipocyte differentiation
Hansen, J. B., & Kristiansen, K. (2006) · Biochemical Journal · doi:10.1042/bj20060402 · Cited by 178 · see citing works
Insulin says NO to cardiovascular disease
Yu, Q., Gao, F., & Ma, X. L. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvq349 · Cited by 172 · see citing works
Signaling of Mitochondrial Biogenesis following Oxidant Injury
Rasbach, K. A., & Schnellmann, R. G. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m608009200 · Cited by 168 · see citing works
The Role of Mitochondria in the Pathophysiology of Skeletal Muscle Insulin Resistance
Pagel-Langenickel, I., Bao, J., Pang, L., & Sack, M. N. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0003 · Cited by 154 · see citing works
Turn up the power - pharmacological activation of mitochondrial biogenesis in mouse models
Komen, J. C., & Thorburn, D. R. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12413 · Cited by 149 · see citing works
Sutherland, L. N., Capozzi, L. C., Turchinsky, N. J., Bell, R. C., & Wright, D. C. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90408.2008 · Cited by 147 · see citing works
Tedesco, L., Valerio, A., Cervino, C., Cardile, A., Pagano, C., Vettor, R., Pasquali, R., Carruba, M. O., Marsicano, G., Lutz, B., et al. (2008) · Diabetes · doi:10.2337/db07-1623 · Cited by 145 · see citing works
Self-citationPreston, C. C., Oberlin, A. S., Holmuhamedov, E. L., Gupta, A., Sagar, S., Syed, R. H. K., Siddiqui, S. A., Raghavakaimal, S., Terzic, A., & Jahangir, A. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.02.010 · Cited by 136 · see citing works
L-Arginine as a Potential Ergogenic Aid in Healthy Subjects
Álvares, T. S., Meirelles, C. M., Bhambhani, Y. N., Paschoalin, V. M. F., & Gomes, P. S. C. (2011) · Sports Medicine · doi:10.2165/11538590-000000000-00000 · Cited by 138 · see citing works
Sankaran, V. G., Orkin, & Walkley, C. R. (2008) · Genes & Development · doi:10.1101/gad.1627208 · Cited by 133 · see citing works
Vettor, R., Valerio, A., Ragni, M., Trevellin, E., Granzotto, M., Olivieri, M., Tedesco, L., Ruocco, C., Fossati, A., Fabris, R., et al. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00617.2013 · Cited by 132 · see citing works
Self-citationNitric Oxide-Dependent Mitochondrial Biogenesis Generates Ca2+ Signaling Profile of Lupus T Cells
Nagy, G., Barcza, M., Gonchoroff, N., Phillips, P. E., & Perl, A. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.6.3676 · Cited by 132 · see citing works
Endothelial Nitric Oxide Synthase (eNOS) Knockout Mice Have Defective Mitochondrial β-Oxidation
Gouill, E. L., Jimenez, M., Binnert, C., Jayet, P.-Y., Thalmann, S., Nicod, P., Scherrer, U., & Vollenweider, P. (2007) · Diabetes · doi:10.2337/db06-1228 · Cited by 130 · see citing works
Campbell, B., Roberts, M., Kerksick, C., Wilborn, C., Marcello, B., Taylor, L., Nassar, E., Leutholtz, B., Bowden, R., Rasmussen, C., et al. (2006) · Nutrition · doi:10.1016/j.nut.2006.06.003 · Cited by 128 · see citing works
Sano, M., Tokudome, S., Shimizu, N., Yoshikawa, N., Ogawa, C., Shirakawa, K., Endo, J., Katayama, T., Yuasa, S., Ieda, M., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m703634200 · Cited by 114 · see citing works
Nitric Oxide in Skeletal Muscle: Role on Mitochondrial Biogenesis and Function
Tengan, C., Rodrigues, G., & Godinho, R. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms131217160 · Cited by 123 · see citing works
West, M. B., Rokosh, G., Obal, D., Velayutham, M., Xuan, Y.-T., Hill, B. G., Keith, R. J., Schrader, J., Guo, Y., Conklin, D. J., et al. (2008) · Circulation · doi:10.1161/circulationaha.108.791533 · Cited by 121 · see citing works
Fulford, J., Winyard, P. G., Vanhatalo, A., Bailey, S. J., Blackwell, J. R., & Jones, A. M. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1220-5 · Cited by 118 · see citing works
The role of iNOS in alcohol-dependent hepatotoxicity and mitochondrial dysfunction in mice
Venkatraman, A., Shiva, S., Wigley, A., Ulasova, E., Chhieng, D., Bailey, S. M., & Darley-Usmar, V. M. (2004) · Hepatology · doi:10.1002/hep.20326 · Cited by 117 · see citing works
Shiva, S., Oh, J.-Y., Landar, A. L., Ulasova, E., Venkatraman, A., Bailey, S. M., & Darley-Usmar, V. M. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.10.037 · Cited by 112 · see citing works
Corton, J. C., & Brown-Borg, H. M. (2005) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/60.12.1494 · Cited by 106 · see citing works
Diani, A. R., Sawada, G., Wyse, B., Murray, F. T., & Khan, M. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00331.2003 · Cited by 100 · see citing works
Martin, L. J., Adams, N. A., Pan, Y., Price, A., & Wong, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2225-10.2011 · Cited by 96 · see citing works
Colom, B., Alcolea, M., Valle, A., Oliver, J., Roca, P., & García-Palmer, F. (2007) · Cellular Physiology and Biochemistry · doi:10.1159/000099208 · Cited by 89 · see citing works
Handa, P., Tateya, S., Rizzo, N. O., Cheng, A. M., Morgan-Stevenson, V., Han, C.-Y., Clowes, A. W., Daum, G., O'Brien, K. D., Schwartz, M. W., et al. (2011) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.111.236554 · Cited by 86 · see citing works
Hsieh, Y.-C., Yang, S., Choudhry, M. A., Yu, H.-P., Rue, L. W., Bland, K. I., & Chaudry, I. H. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00682.2005 · Cited by 84 · see citing works
Effects of nitrite on modulating ROS generation following ischemia and reperfusion
Raat, N. J. H., Shiva, S., & Gladwin, M. T. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.02.002 · Cited by 79 · see citing works
Kou, G., Li, Z., Wu, C., Liu, Y., Hu, Y., Guo, L., Xu, X., & Zhou, Z. (2018) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.8b04124 · Cited by 78 · see citing works
Emerging Roles of Endothelial Nitric Oxide in Preservation of Cognitive Health
Katusic, Z. S., d’Uscio, L. V., & He, T. (2023) · Stroke · doi:10.1161/strokeaha.122.041444 · Cited by 73 · see citing works
Mitochondrial adaptations in skeletal muscle to hindlimb unloading
Wagatsuma, A., Kotake, N., Kawachi, T., Shiozuka, M., Yamada, S., & Matsuda, R. (2011) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-010-0677-1 · Cited by 70 · see citing works
Nitric oxide is the primary mediator of cytotoxicity induced by GSH depletion in neuronal cells
Aquilano, K., Baldelli, S., Cardaci, S., Rotilio, G., & Ciriolo, M. R. (2011) · Journal of Cell Science · doi:10.1242/jcs.077149 · Cited by 67 · see citing works
Chen, J., Wong, H. S., Leong, P. K., Leung, H. Y., Chan, W. M., & Ko, K. M. (2017) · Food & Function · doi:10.1039/c7fo00127d · Cited by 67 · see citing works
Roberts, L. D., Ashmore, T., McNally, B. D., Murfitt, S. A., Fernandez, B. O., Feelisch, M., Lindsay, R., Siervo, M., Williams, E. A., Murray, A. J., et al. (2017) · Diabetes · doi:10.2337/db16-0843 · Cited by 57 · see citing works
Nitrite as a mediator of ischemic preconditioning and cytoprotection
Murillo, D., Kamga, C., Mo, L., & Shiva, S. (2011) · Nitric Oxide · doi:10.1016/j.niox.2011.01.003 · Cited by 57 · see citing works
Thompson, C., Wylie, L. J., Blackwell, J. R., Fulford, J., Black, M. I., Kelly, J., McDonagh, S. T. J., Carter, J., Bailey, S. J., Vanhatalo, A., et al. (2017) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00909.2016 · Cited by 51 · see citing works
Shen, W., Hao, J., Feng, Z., Tian, C., Chen, W., Packer, L., Shi, X., Zang, W., & Liu, J. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.01134.x · Cited by 52 · see citing works
Kemper, M. F., Stirone, C., Krause, D. N., Duckles, S. P., & Procaccio, V. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.11.009 · Cited by 42 · see citing works
Savoia, C., Volpe, M., Alonzo, A., Rossi, C., & Rubattu, S. (2010) · Clinical Science · doi:10.1042/cs20090204 · Cited by 35 · see citing works
Thompson, C., Vanhatalo, A., Kadach, S., Wylie, L. J., Fulford, J., Ferguson, S. K., Blackwell, J. R., Bailey, S. J., & Jones, A. M. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00047.2018 · Cited by 32 · see citing works
Nitric oxide in exercise physiology: past and present perspectives
Mueller, B. J., Roberts, M. D., Mobley, C. B., Judd, R. L., & Kavazis, A. N. (2025) · Frontiers in Physiology · doi:10.3389/fphys.2024.1504978 · Cited by 32 · see citing works
De Toni, L., Strapazzon, G., Gianesello, L., Caretta, N., Pilon, C., Bruttocao, A., & Foresta, C. (2011) · Journal of Endocrinological Investigation · doi:10.1007/bf03346724 · Cited by 25 · see citing works
Nitric Oxide as a Determinant of Human Longevity and Health Span
Poeggeler, B., Singh, K. S., Sambamurti, K., & Pappolla, M. A. (2023) · doi:10.20944/preprints202309.0213.v1 · Cited by 20 · see citing works
Can dietary nitrates enhance the efficiency of mitochondria?
Nair, K. S., Irving, B. A., & Lanza, I. R. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.01.013 · Cited by 13 · see citing works
Lee, W. J., Kim, H. S., Park, H.-S., Kim, M.-O., Kim, M., Yun, J.-Y., Kim, E. H., Lee, S. A., Lee, S. H., Koh, E. H., et al. (2009) · Korean Diabetes Journal · doi:10.4093/kdj.2009.33.3.198 · Cited by 4 · see citing works
Mitochondrial Function and Neurodegenerative Diseases
Wilkins, H. M., Weidling, I., Koppel, S., Wang, X., von Schulze, A., & Swerdlow, R. H. (2018) · The Molecular and Cellular Basis of Neurodegenerative Diseases · doi:10.1016/b978-0-12-811304-2.00013-4 · Cited by 2 · see citing works
- Authors
- Nisoli, E., Clementi, E., Paolucci, C., Cozzi, V., Tonello, C., Sciorati, C., Bracale, R., Valerio, A., Francolini, M., Moncada, S., & Carruba, M. O.
- Affiliations
- University of Milan (IT)
- University of Calabria (IT)
- DIBIT-H San Raffaele Institute, Milan 20132, Italy.
- University of Brescia (IT)
- National Research Council (IT)
- University College London (GB)
- Corresponding author
- Nisoli, Enzo
- Clementi, Emilio
- ORCID
- Venue
- Science
- Published
- 2003-02-07
- Volume
- 299
- Issue
- 5608
- Pages
- 896-899
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2169001678
- Cited by
- 1,243
- References
- 20
- Citations by year
- 2026: 16 · 2025: 26 · 2024: 30 · 2023: 28 · 2022: 45 · 2021: 40 · 2020: 51 · 2019: 46 · 2018: 51 · 2017: 48 · 2016: 49 · 2015: 62 · 2014: 73 · 2013: 65 · 2012: 88
- FWCI
- 33.73
- 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)
- Research Explorer (The University of Manchester) (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- mitochondrial biogenesis, nitric oxide, cGMP signaling, PGC-1α, brown adipose tissue, cold exposure, endothelial nitric oxide synthase, energy balance, brown adipocytes, 3T3-L1 cells, U937 cells, HeLa cells
- MeSH terms
- Animals, Adipose Tissue, Brown, Cold Temperature, DNA-Binding Proteins, DNA, Mitochondrial, Eating, Energy Metabolism, Female, Cyclic GMP, HeLa Cells, High Mobility Group Proteins, Humans, Male, Mitochondria, Motor Activity, Nitric Oxide, Nuclear Proteins, Oxadiazoles, Oxygen Consumption, Penicillamine, Quinoxalines, RNA, Messenger, Transcription Factors, 8-Bromo Cyclic Adenosine Monophosphate, Signal Transduction, Weight Gain, Trans-Activators, Oligonucleotides, Antisense, 3T3 Cells, Adipocytes, Mice, Knockout, Nitric Oxide Synthase, U937 Cells, Mitochondrial Proteins, Nuclear Respiratory Factors, NF-E2-Related Factor 1, Mice, Rats, Nitric Oxide Synthase Type II, Nitric Oxide Synthase Type III
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