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PMID: 20200137 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Endothelial nitric oxide synthase is central to skeletal muscle metabolic regulation and enzymatic signaling during exercise in vivo.

Lee-Young RS, Ayala JE, Hunley CF, James FD, Bracy DP, Kang L, Wasserman DH

Abstract

Endothelial nitric oxide synthase (eNOS) is associated with a number of physiological functions involved in the regulation of metabolism; however, the functional role of eNOS is poorly understood. We tested the hypothesis that eNOS is critical to muscle cell signaling and fuel usage during exercise in vivo, using 16-wk-old catheterized (carotid artery and jugular vein) C57BL/6J mice with wild-type (WT), partial (+/-), or no expression (-/-) of eNOS. Quantitative reductions in eNOS expression ( approximately 40%) elicited many of the phenotypic effects observed in enos(-/-) mice under fasted, sedentary conditions, with expression of oxidative phosphorylation complexes I to V and ATP levels being decreased, and total NOS activity and Ca(2+)/CaM kinase II Thr(286) phosphorylation being increased in skeletal muscle. Despite these alterations, exercise tolerance was markedly impaired in enos(-/-) mice during an acute 30-min bout of exercise. An eNOS-dependent effect was observed with regard to AMP-activated protein kinase signaling and muscle perfusion. Muscle glucose and long-chain fatty acid uptake, and hepatic and skeletal muscle glycogenolysis during the exercise bout was markedly accelerated in enos(-/-) mice compared with enos(+/-) and WT mice. Correspondingly, enos(-/-) mice exhibited hypoglycemia during exercise. Thus, the ablation of eNOS alters a number of physiological processes that result in impaired exercise capacity in vivo. The finding that a partial reduction in eNOS expression is sufficient to induce many of the changes associated with ablation of eNOS has implications for chronic metabolic diseases, such as obesity and insulin resistance, which are associated with reduced eNOS expression.

MeSH Terms
AMP-Activated Protein Kinases/metabolism Animals Body Composition/physiology Body Weight/physiology Calorimetry, Indirect Energy Metabolism/physiology Female Gluconeogenesis/physiology Glycogen/metabolism Hypoglycemia/metabolism,physiopathology Insulin/blood Male Mice Mice, Inbred C57BL Mice, Mutant Strains Mitochondria/physiology Muscle, Skeletal/blood supply,enzymology Nitric Oxide Synthase Type III/genetics,metabolism Oxidative Phosphorylation Photoperiod Physical Conditioning, Animal/physiology Physical Exertion/physiology Pregnancy Regional Blood Flow/physiology Signal Transduction/physiology
Chemicals
Insulin Glycogen Nitric Oxide Synthase Type III Nos3 protein, mouse AMPK alpha1 subunit, mouse AMP-Activated Protein Kinases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Lee-Young Robert S
Department of Molecular Physiology and Biophysics, Vanderbilt University, School of Medicine, 2200 Pierce Ave., Nashville, TN 37232, U.S.A. robert.s.lee-young@vanderbilt.edu
Ayala Julio E
Hunley Charles F
James Freyja D
Bracy Deanna P
Kang Li
Wasserman David H
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Article Info
Journal
American journal of physiology. Regulatory, integrative and comparative physiology
Abbr.
Am J Physiol Regul Integr Comp Physiol
ISSN
1522-1490
Published
2010-05-00
Epub
2010-00-03
Pages
R1399-408
Language
English
Region
United States
NLM ID
100901230
PMCID
PMC2867517
Subset
IM
Grants
NIDDK NIH HHS · R01 DK-54902 · United States
NIDDK NIH HHS · U24 DK-59637 · United States
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