Mitochondrial biogenesis in mammals: The role of endogenous nitric oxide

Enzo Nisoli; Emilio Clementi; Clara Paolucci; Valeria Cozzi; Cristina Tonello; Clara Sciorati; Renata Bracale; Alessandra Valerio; Maura Francolini; Salvador Moncada; Michele O. Carruba

doi:10.1126/science.1079368

Mitochondrial biogenesis in mammals: The role of endogenous nitric oxide

Enzo Nisoli, Emilio Clementi, Clara Paolucci, Valeria Cozzi, Cristina Tonello, Clara Sciorati, Renata Bracale, Alessandra Valerio, Maura Francolini, Salvador Moncada, Michele O. Carruba

Research output: Contribution to journal › Article › peer-review

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 γ coactivator 1α, 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.

Original language	English
Pages (from-to)	896-899
Number of pages	3
Journal	Science
Volume	299
Issue number	5608
DOIs	https://doi.org/10.1126/science.1079368
Publication status	Published - 7 Feb 2003

Keywords

3T3 Cells
8-Bromo Cyclic Adenosine Monophosphate/pharmacology
Adipocytes/*metabolism/ultrastructure
Adipose Tissue, Brown/cytology/metabolism/ultrastructure
Animals
Cold Temperature
Cyclic GMP/metabolism
DNA, Mitochondrial/metabolism
DNA-Binding Proteins/metabolism
Eating
Energy Metabolism
Female
HeLa Cells
High Mobility Group Proteins
Humans
Male
Mice
Mice, Knockout
Mitochondria/*metabolism/ultrastructure
*Mitochondrial Proteins
Motor Activity
NF-E2-Related Factor 1
Nitric Oxide/*physiology
Nitric Oxide Synthase/genetics/*metabolism
Nitric Oxide Synthase Type II
Nitric Oxide Synthase Type III
Nuclear Proteins/metabolism
Nuclear Respiratory Factors
Oligonucleotides, Antisense/pharmacology
Oxadiazoles/pharmacology
Oxygen Consumption
Penicillamine/*analogs & derivatives/pharmacology
Quinoxalines/pharmacology
RNA, Messenger/genetics/metabolism
Rats
Signal Transduction
Trans-Activators/metabolism
Transcription Factors/metabolism
U937 Cells
Weight Gain

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10.1126/science.1079368

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title = "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 γ coactivator 1α, 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.",

keywords = "3T3 Cells, 8-Bromo Cyclic Adenosine Monophosphate/pharmacology, Adipocytes/*metabolism/ultrastructure, Adipose Tissue, Brown/cytology/metabolism/ultrastructure, Animals, Cold Temperature, Cyclic GMP/metabolism, DNA, Mitochondrial/metabolism, DNA-Binding Proteins/metabolism, Eating, Energy Metabolism, Female, HeLa Cells, High Mobility Group Proteins, Humans, Male, Mice, Mice, Knockout, Mitochondria/*metabolism/ultrastructure, *Mitochondrial Proteins, Motor Activity, NF-E2-Related Factor 1, Nitric Oxide/*physiology, Nitric Oxide Synthase/genetics/*metabolism, Nitric Oxide Synthase Type II, Nitric Oxide Synthase Type III, Nuclear Proteins/metabolism, Nuclear Respiratory Factors, Oligonucleotides, Antisense/pharmacology, Oxadiazoles/pharmacology, Oxygen Consumption, Penicillamine/*analogs & derivatives/pharmacology, Quinoxalines/pharmacology, RNA, Messenger/genetics/metabolism, Rats, Signal Transduction, Trans-Activators/metabolism, Transcription Factors/metabolism, U937 Cells, Weight Gain",

author = "Enzo Nisoli and Emilio Clementi and Clara Paolucci and Valeria Cozzi and Cristina Tonello and Clara Sciorati and Renata Bracale and Alessandra Valerio and Maura Francolini and Salvador Moncada and Carruba, {Michele O.}",

note = "Nisoli, Enzo Clementi, Emilio Paolucci, Clara Cozzi, Valeria Tonello, Cristina Sciorati, Clara Bracale, Renata Valerio, Alessandra Francolini, Maura Moncada, Salvador Carruba, Michele O New York, N.Y. Science. 2003 Feb 7;299(5608):896-9.",

year = "2003",

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doi = "10.1126/science.1079368",

language = "English",

volume = "299",

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T1 - Mitochondrial biogenesis in mammals: The role of endogenous nitric oxide

AU - Nisoli, Enzo

AU - Clementi, Emilio

AU - Paolucci, Clara

AU - Cozzi, Valeria

AU - Tonello, Cristina

AU - Sciorati, Clara

AU - Bracale, Renata

AU - Valerio, Alessandra

AU - Francolini, Maura

AU - Moncada, Salvador

AU - Carruba, Michele O.

N1 - Nisoli, Enzo Clementi, Emilio Paolucci, Clara Cozzi, Valeria Tonello, Cristina Sciorati, Clara Bracale, Renata Valerio, Alessandra Francolini, Maura Moncada, Salvador Carruba, Michele O New York, N.Y. Science. 2003 Feb 7;299(5608):896-9.

PY - 2003/2/7

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N2 - 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 γ coactivator 1α, 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.

AB - 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 γ coactivator 1α, 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.

KW - 3T3 Cells

KW - 8-Bromo Cyclic Adenosine Monophosphate/pharmacology

KW - Adipocytes/metabolism/ultrastructure

KW - Adipose Tissue, Brown/cytology/metabolism/ultrastructure

KW - Animals

KW - Cold Temperature

KW - Cyclic GMP/metabolism

KW - DNA, Mitochondrial/metabolism

KW - DNA-Binding Proteins/metabolism

KW - Eating

KW - Energy Metabolism

KW - Female

KW - HeLa Cells

KW - High Mobility Group Proteins

KW - Humans

KW - Male

KW - Mice

KW - Mice, Knockout

KW - Mitochondria/metabolism/ultrastructure

KW - Mitochondrial Proteins

KW - Motor Activity

KW - NF-E2-Related Factor 1

KW - Nitric Oxide/physiology

KW - Nitric Oxide Synthase/genetics/metabolism

KW - Nitric Oxide Synthase Type II

KW - Nitric Oxide Synthase Type III

KW - Nuclear Proteins/metabolism

KW - Nuclear Respiratory Factors

KW - Oligonucleotides, Antisense/pharmacology

KW - Oxadiazoles/pharmacology

KW - Oxygen Consumption

KW - Penicillamine/analogs & derivatives/pharmacology

KW - Quinoxalines/pharmacology

KW - RNA, Messenger/genetics/metabolism

KW - Rats

KW - Signal Transduction

KW - Trans-Activators/metabolism

KW - Transcription Factors/metabolism

KW - U937 Cells

KW - Weight Gain

U2 - 10.1126/science.1079368

DO - 10.1126/science.1079368

M3 - Article

VL - 299

SP - 896

EP - 899

JO - Science

JF - Science

SN - 0036-8075

IS - 5608

ER -

Mitochondrial biogenesis in mammals: The role of endogenous nitric oxide

Abstract

Keywords

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