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Am J Physiol Endocrinol Metab 287: E834-E841, 2004. First published July 20, 2004; doi:10.1152/ajpendo.00234.2004
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Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle

Ji Li,1 Xiaoyue Hu,1 Pradeepa Selvakumar,1 Raymond R. Russell, III,1 Samuel W. Cushman,2 Geoffrey D. Holman,3 and Lawrence H. Young1

1Section of Cardiovascular Medicine, Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 06520; 2National Institutes of Health, Bethesda, Maryland 20892; and 3Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, United Kingdom

Submitted 1 June 2004 ; accepted in final form 28 June 2004

AMP-activated protein kinase (AMPK) is a serine-threonine kinase that regulates cellular metabolism and has an essential role in activating glucose transport during hypoxia and ischemia. The mechanisms responsible for AMPK stimulation of glucose transport are uncertain, but may involve interaction with other signaling pathways or direct effects on GLUT vesicular trafficking. One potential downstream mediator of AMPK signaling is the nitric oxide pathway. The aim of this study was to examine the extent to which AMPK mediates glucose transport through activation of the nitric oxide (NO)-signaling pathway in isolated heart muscles. Incubation with 1 mM 5-amino-4-imidazole-1-{beta}-carboxamide ribofuranoside (AICAR) activated AMPK (P < 0.01) and stimulated glucose uptake (P < 0.05) and translocation of the cardiomyocyte glucose transporter GLUT4 to the cell surface (P < 0.05). AICAR treatment increased phosphorylation of endothelial NO synthase (eNOS) ~1.8-fold (P < 0.05). eNOS, but not neuronal NOS, coimmunoprecipitated with both the {alpha}2 and {alpha}1 AMPK catalytic subunits in heart muscle. NO donors also increased glucose uptake and GLUT4 translocation (P < 0.05). Inhibition of NOS with N{omega}-nitro-L-arginine and N{omega}-methyl-L-arginine reduced AICAR-stimulated glucose uptake by 21 ± 3% (P < 0.05) and 25 ± 4% (P < 0.05), respectively. Inhibition of guanylate cyclase with ODQ and LY-83583 reduced AICAR-stimulated glucose uptake by 31 ± 4% (P < 0.05) and 22 ± 3% (P < 0.05), respectively, as well as GLUT4 translocation to the cell surface (P < 0.05). Taken together, these results indicate that activation of the NO-guanylate cyclase pathway contributes to, but is not the sole mediator of, AMPK stimulation of glucose uptake and GLUT4 translocation in heart muscle.

nitric oxide synthase; AMP-activated protein kinase; glucose transporter


Address for reprint requests and other correspondence: L. H. Young, Section of Cardiovascular Medicine, TAC S460, Yale Univ. School of Medicine, New Haven, CT 06520 (E-mail: lawrence.young{at}yale.edu)




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