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Science 299 (5608): 896-899

Copyright © 2003 by the American Association for the Advancement of Science

Mitochondrial Biogenesis in Mammals: The Role of Endogenous Nitric Oxide

Enzo Nisoli,12*dagger Emilio Clementi,34* Clara Paolucci,3 Valeria Cozzi,1 Cristina Tonello,1 Clara Sciorati,3 Renata Bracale,1 Alessandra Valerio,5 Maura Francolini,6 Salvador Moncada,7 Michele O. Carruba12

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.

1 Department of Preclinical Sciences, Center for Study and Research on Obesity, Luigi Sacco Hospital, University of Milan, Milan 20157, Italy.
2 Istituto Auxologico Italiano, Milan 20149, Italy.
3 DIBIT-H San Raffaele Institute, Milan 20132, Italy.
4 Department of Pharmaco-Biology, University of Calabria, Rende 87036, Italy.
5 Department of Biomedical Sciences and Biotechnology, University of Brescia, Brescia 25123, Italy.
6 Consiglio Nazionale delle Ricerche Institute of Neuroscience, Cellular and Molecular Pharmacology Section, Milan 20129, Italy.
7 The Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, UK.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed. E-mail: enzo.nisoli{at}

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F. Kim, M. Pham, E. Maloney, N. O. Rizzo, G. J. Morton, B. E. Wisse, E. A. Kirk, A. Chait, and M. W. Schwartz (2008)
Arterioscler Thromb Vasc Biol 28, 1982-1988
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Time course of high-fat diet-induced reductions in adipose tissue mitochondrial proteins: potential mechanisms and the relationship to glucose intolerance.
L. N. Sutherland, L. C. Capozzi, N. J. Turchinsky, R. C. Bell, and D. C. Wright (2008)
Am J Physiol Endocrinol Metab 295, E1076-E1083
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Identification of Nitric Oxide as an Endogenous Activator of the AMP-activated Protein Kinase in Vascular Endothelial Cells.
J. Zhang, Z. Xie, Y. Dong, S. Wang, C. Liu, and M.-H. Zou (2008)
J. Biol. Chem. 283, 27452-27461
   Abstract »    Full Text »    PDF »
The functional nitrite reductase activity of the heme-globins.
M. T. Gladwin and D. B. Kim-Shapiro (2008)
Blood 112, 2636-2647
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Suppression of the JNK Pathway by Induction of a Metabolic Stress Response Prevents Vascular Injury and Dysfunction.
E. Schulz, J. Dopheide, S. Schuhmacher, S. R. Thomas, K. Chen, A. Daiber, P. Wenzel, T. Munzel, and J. F. Keaney Jr (2008)
Circulation 118, 1347-1357
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Time course of regression of the protection conferred by simulated high altitude to rat myocardium: correlation with mtNOS.
P. La Padula, J. Bustamante, A. Czerniczyniec, and L. E. Costa (2008)
J Appl Physiol 105, 951-957
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High mitochondrial densities in the hearts of Antarctic icefishes are maintained by an increase in mitochondrial size rather than mitochondrial biogenesis.
M. R. Urschel and K. M. O'Brien (2008)
J. Exp. Biol. 211, 2638-2646
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Cannabinoid Type 1 Receptor Blockade Promotes Mitochondrial Biogenesis Through Endothelial Nitric Oxide Synthase Expression in White Adipocytes.
L. Tedesco, A. Valerio, C. Cervino, A. Cardile, C. Pagano, R. Vettor, R. Pasquali, M. O. Carruba, G. Marsicano, B. Lutz, et al. (2008)
Diabetes 57, 2028-2036
   Abstract »    Full Text »    PDF »
Transcriptional control of mitochondrial biogenesis: the central role of PGC-1{alpha}.
R. Ventura-Clapier, A. Garnier, and V. Veksler (2008)
Cardiovasc Res 79, 208-217
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The nitric oxide-donating derivative of acetylsalicylic acid, NCX 4016, stimulates glucose transport and glucose transporters translocation in 3T3-L1 adipocytes.
V. Kaddai, T. Gonzalez, M. Bolla, Y. Le Marchand-Brustel, and M. Cormont (2008)
Am J Physiol Endocrinol Metab 295, E162-E169
   Abstract »    Full Text »    PDF »

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