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Science 7 February 2003:
Vol. 299. no. 5608, pp. 896 - 899
DOI: 10.1126/science.1079368
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Reports

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}unimi.it

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T. Zaobornyj, L. B. Valdez, P. La Padula, L. E. Costa, and A. Boveris (2005)
J Appl Physiol 98, 2370-2375
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Dietary L-Arginine Supplementation Reduces Fat Mass in Zucker Diabetic Fatty Rats.
W. J. Fu, T. E. Haynes, R. Kohli, J. Hu, W. Shi, T. E. Spencer, R. J. Carroll, C. J. Meininger, and G. Wu (2005)
J. Nutr. 135, 714-721
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Effects of all-trans retinoic acid on orphan receptor APJ signaling in spontaneously hypertensive rats.
J.-C. Zhong, D.-Y. Huang, G.-F. Liu, H.-Y. Jin, Y.-M. Yang, Y.-F. Li, X.-H. Song, and K. Du (2005)
Cardiovasc Res 65, 743-750
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Amyloid {beta}-induced Changes in Nitric Oxide Production and Mitochondrial Activity Lead to Apoptosis.
U. Keil, A. Bonert, C. A. Marques, I. Scherping, J. Weyermann, J. B. Strosznajder, F. Muller-Spahn, C. Haass, C. Czech, L. Pradier, et al. (2004)
J. Biol. Chem. 279, 50310-50320
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Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals.
E. Nisoli, S. Falcone, C. Tonello, V. Cozzi, L. Palomba, M. Fiorani, A. Pisconti, S. Brunelli, A. Cardile, M. Francolini, et al. (2004)
PNAS 101, 16507-16512
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Activation of the AMP-activated Protein Kinase by the Anti-diabetic Drug Metformin in Vivo: ROLE OF MITOCHONDRIAL REACTIVE NITROGEN SPECIES.
M.-H. Zou, S. S. Kirkpatrick, B. J. Davis, J. S. Nelson, W. G. Wiles IV, U. Schlattner, D. Neumann, M. Brownlee, M. B. Freeman, and M. H. Goldman (2004)
J. Biol. Chem. 279, 43940-43951
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Nuclear Receptor Signaling and Cardiac Energetics.
J. M. Huss and D. P. Kelly (2004)
Circ. Res. 95, 568-578
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Changes in the Mitochondrial Proteome during the Anoxia to Air Transition in Rice Focus around Cytochrome-containing Respiratory Complexes.
A. H. Millar, A. E. Trend, and J. L. Heazlewood (2004)
J. Biol. Chem. 279, 39471-39478
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Nitric Oxide-Dependent Mitochondrial Biogenesis Generates Ca2+ Signaling Profile of Lupus T Cells.
G. Nagy, M. Barcza, N. Gonchoroff, P. E. Phillips, and A. Perl (2004)
J. Immunol. 173, 3676-3683
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Real-time imaging of peroxisome proliferator-activated receptor-{gamma} coactivator-1{alpha} promoter activity in skeletal muscles of living mice.
T. Akimoto, B. S. Sorg, and Z. Yan (2004)
Am J Physiol Cell Physiol 287, C790-C796
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Voluntary physical activity alterations in endothelial nitric oxide synthase knockout mice.
I. Momken, P. Lechene, R. Ventura-Clapier, and V. Veksler (2004)
Am J Physiol Heart Circ Physiol 287, H914-H920
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Genetically Modified Animals in Endocrinology.
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Endocr. Rev. 25, 512-519
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Formation of Protein Tyrosine ortho-Semiquinone Radical and Nitrotyrosine from Cytochrome c-derived Tyrosyl Radical.
Y.-R. Chen, C.-L. Chen, W. Chen, J. L. Zweier, O. Augusto, R. Radi, and R. P. Mason (2004)
J. Biol. Chem. 279, 18054-18062
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