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Nitric oxide and AMPK cooperatively regulate PGC-1 alpha in skeletal muscle cells
Journal article   Open access   Peer reviewed

Nitric oxide and AMPK cooperatively regulate PGC-1 alpha in skeletal muscle cells

Vitor A. Lira, Dana L. Brown, Ana K. Lira, Andreas N. Kavazis, Quinlyn A. Soltow, Elizabeth H. Zeanah and David S. Criswell
The Journal of physiology, Vol.588(18), pp.3551-3566
09/15/2010
DOI: 10.1113/jphysiol.2010.194035
PMCID: PMC2988518
PMID: 20643772
url
https://doi.org/10.1113/jphysiol.2010.194035View
Published (Version of record) Open Access

Abstract

Nitric oxide (NO) induces mitochondrial biogenesis in skeletal muscle cells via upregulation of the peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha). Further, we have shown that nitric oxide interacts with the metabolic sensor enzyme, AMPK. Therefore, we tested the hypothesis that nitric oxide and AMPK act synergistically to upregulate PGC-1 alpha mRNA expression and stimulate mitochondrial biogenesis in culture. L6 myotubes treated with nitric oxide donors, S-nitroso-N-penicillamine (SNAP, 25 mu m) or diethylenetriamine-NONO (DETA-NO, 50 mu m), exhibited elevated AMPK phosphorylation, PGC-1 alpha mRNA and protein, and basal and uncoupled mitochondrial respiration (P < 0.05). Pre-treatment of cultures with the AMPK inhibitor, Compound C, prevented these effects. Knockdown of AMPK alpha 1 in L6 myotubes using siRNA reduced AMPK alpha protein content and prevented upregulation of PGC-1 alpha mRNA by DETA-NO. Meanwhile, siRNA knockdown of AMPK alpha 2 had no effect on total AMPK alpha protein content or PGC-1 alpha mRNA. These results suggest that NO effects on PGC-1 alpha expression are mediated by AMPK alpha 1. Paradoxically, we found that the AMPK-activating compound, AICAR, induced NO release from L6 myotubes, and that AICAR-induced upregulation of PGC-1 alpha mRNA was prevented by inhibition of NOS with NG-nitro-l-arginine methyl ester (l-NAME, 1 mm). Additionally, incubation of isolated mouse extensor digitorum longus (EDL) muscles with 2 mm AICAR for 20 min or electrical stimulation (10 Hz, 13 V) for 10 min induced phosphorylation of AMPK alpha (P < 0.05), which was completely prevented by pre-treatment with the NOS inhibitor, l-NG-monomethyl arginine (l-NMMA, 1 mm). These data identify the AMPK alpha 1 isoform as the mediator of NO-induced effects in skeletal muscle cells. Further, this study supports a proposed model of synergistic interaction between AMPK and NOS that is critical for maintenance of metabolic function in skeletal muscle cells.
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