Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 4, 2007, Pages

  Lira, Vitor A ^a   Soltow, Quinlyn A ^a   Long, Jodi H D ^a   Betters, Jenna L ^a   Sellman, Jeff E ^a   Criswell, David S ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

5 aminoimidazole 4 carboxamide 1 D ribofuranoside; Compound C; Glucose transporter 4; Guanosine 3 ,5 cyclic monophosphate; L6 myotubes; N G nitro L arginine methyl ester

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ACETYL COENZYME A CARBOXYLASE; ADENYLATE KINASE; CYCLIC GMP; GLUCOSE TRANSPORTER 4; GUANYLATE CYCLASE INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PENICILLAMINE; S NITROSO N PENICILLAMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENZYME REGULATION; FEMALE; GLUCOSE TRANSPORT; IN VIVO STUDY; MITOCHONDRION; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANTARIS MUSCLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION;

ADENYLATE KINASE; AMINOIMIDAZOLE CARBOXAMIDE; ANIMALS; CELLS, CULTURED; CYCLIC GMP; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORTER TYPE 4; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; RATS; RATS, SPRAGUE-DAWLEY; RIBONUCLEOTIDES; SIGNAL TRANSDUCTION;

EID: 35148827677     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00045.2007     Document Type: Article

References (44)

1. Balon TW, Jasman AP. Acute exposure to AICAR increases glucose transport in mouse EDL and soleus muscle. Biochem Biophys Res Commun 282: 1008-1011, 2001.
2. Balon TW, Nadler JL. Nitric oxide release is present from incubated skeletal muscle preparations. J Appl Physiol 77: 2519-2521, 1994.
3. Bedard S, Marcotte B, Marette A. Cytokines modulate glucose transport in skeletal muscle by inducing the expression of inducible nitric oxide synthase. Biochem J 325: 487-493, 1997.
4. Bustin SA. Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29: 23-39, 2002.
5. Chen ZP, McConell GK, Michell BJ, Snow RJ, Canny BJ, Kemp BE. AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation. Am J Physiol Endocrinol Metab 279: E1202-E1206, 2000.
6. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano PR, Kemp BE. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 443: 285-289, 1999.
7. Chen ZP, Stephens TJ, Murthy S, Canny BJ, Hargreaves M, Witters LA, Kemp BE, McConell GK. Effect of exercise intensity on skeletal muscle AMPK signaling in humans. Diabetes 52: 2205-2212, 2003.
8. Cleeter MW, Cooper JM, Darley-Usmar VM, Moncada S, Schapira AH. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett 345: 50-54, 1994.
9. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30: 1000-1007, 1981.
10. Devlin JT, Hishman M, Horton ED, Horton ES. Enhanced peripheral and splanchnic insulin sensitivityin NIDDM men after single bout of exercise. Diabetes 36: 434-439, 1987.
11. Friebe A, Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circ Res 93: 96-105, 2003.
12. Fryer LG, Hajduch E, Rencurel F, Salt IP, Hundal HS, Hardie DG, Carling D. Activation of glucose transport by AMP-activated protein kinase via stimulation of nitric oxide synthase. Diabetes 49: 1978-1985, 2000.
13. Fujii N, Jessen N, Goodyear LJ. AMP-activated protein kinase and the regulation of glucose transport. Am J Physiol Endocrinol Metab 291: E867-E877, 2006.
14. Gaidhu MP, Fediuc S, Ceddia RB. 5-Aminoimidazole-1-β-D- ribofuranoside-induced AMP-activated protein kinase phosphorylation inhibits basal and insulin-stimulated glucose uptake, lipid synthesis, and fatty acid oxidation in isolated rat adipocytes. J Biol Chem 281: 25956-25964, 2006.
15. Goodyear LJ, Hirshman MF, Valyou PM, Horton ES. Glucose transporter number, function, and subcellular distribution in rat skeletal muscle after exercise training. Diabetes 41: 1091-1099, 1992.
16. Gross WL, Bak MI, Ingwall JS, Arstall MA, Smith TW, Balligand JL, Kelly RA. Nitric oxide inhibits creatine kinase and regulates rat heart contractile reserve. Proc Natl Acad Sci USA 93: 5604-5609, 1996.
17. Hardie DG, Carling D, Carlson M. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensor of eukaryotic cell? Annu Rev Biochem 67: 821-855, 1998.
18. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR, Hardie DG. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade (Abstract). J Biol 2: 28, 2003.
19. Higaki Y, Hirshamn MF, Fujii N, Goodyear LJ. Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle. Diabetes 50: 241-247, 2001.
20. Hirota Y, Ishida H, Genka C, Obama R, Matsuyama S, Nakazawa H. Physiological concentration of nitric oxide induces positive inotropic effects through cGMP pathway in isolated rat ventricular myocytes. Jpn J Physiol 51: 455-461, 2001.
21. Holmes BF, Sparling DP, Olson AL, Winder WW, Dohm GL. Regulation of muscle GLUT4 enhancer factor and myocyte enhancer factor 2 by AMP-activated protein kinase. Am J Physiol Endocrinol Metab 289: E071-E1076, 2005.
22. Ivy JL, Holloszy JO. Persistent increase in glucose uptake by rat skeletal muscle following exercise. Am J Physiol Cell Physiol 241: C200-C203, 1981.
23. Ji LL, Gomez-Cabrera MC, Vina J. Exercise and hormesis: activation of cellular antioxidant signaling pathway. Ann NY Acad Sci 1067: 425-435, 2006.
24. Katz LD, Glickman MG, Rapoport S, Ferrannini E, DeFronzo RA. Splanchnic and peripheral disposal of oral glucose in man. Diabetes 32: 675-679, 1983.
25. Larsen JJS, Dela F, Kjaer M, Galbo H. The effect of moderate exercise on post prandial glucose homeostasis in NIDDM patients. Diabetologia 40: 447-453, 1997.
26. Lau KS, Grange RW, Isotani E, Sarelius IH, Kamm KE, Stull JT. nNOS and eNOS modulate cGMP formation and vascular response in contracting fast-twitch skeletal muscle. Physiol Genomics 2: 21-27, 2000.
27. Long JH, Lira VA, Soltow QA, Betters JL, Sellman JE, Criswell DS. Arginine supplementation induces myoblast fusion via augmentation of nitric oxide production. J Muscle Res Cell Motil 27: 577-584, 2006.
28. Michael LF, Wu Z, Cheatham RB, Puigserver P, Adelmant G, Lehman JJ, Kelly DP, Spiegelman BM. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc Natl Acad Sci USA 98: 3820-3825, 2001.
29. Neufer PD, Shinebarger MH, Dohm GL. Effect of training and detraining on skeletal muscle glucose transporter (GLUT4) content in rats. Can J Physiol Pharmacol 70: 1286-1290, 1992.
30. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C, Bracale R, Valerio A, Francolini M, Moncada S, Carruba MO. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299: 896-899, 2003.
31. Nisoli E, Falcone S, Tonello C, Cozzi V, Palomba L, Fiorani M, Pisconti A, Brunelli S, Cardile A, Francolini M, Cantoni O, Carruba MO, Moncada S, Clementi E. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc Natl Acad Sci USA 101: 16507-16512, 2004.
32. 2+. Am J Physiol Endocrinol Metab 282: E1008-E1013, 2002.
33. Patwell DM, McArdle A, Mogan JE, Patridge TA, Jackson MJ. Release of reactive oxygen and nitrogen species from contracting skeletal muscle cells. Free Rad Biol Med 37: 1064-1072, 2004.
34. Pilon G, Dallaire P, Marette A. Inhibition of inducible nitric oxide synthase by activators of AMP-activated protein kinase: a new mechanism of action of insulin-sensitizing drugs. J Biol Chem 279: 20767-20774, 2004.
35. Reid MB. Role of nitric oxide in skeletal muscle: synthesis, distribution and functional importance. Acta Physiol Scand 162: 401-409, 1998.
36. Silveira LR, Pereira-Da-Silva L, Juel C, Hellsten Y. Formation of hydrogen peroxide and nitric oxide in rat skeletal muscle cells during contractions. Free Radic Biol Med 35: 455-464, 2003.
37. Smith AC, Bruce CR, Dyck DJ. AMP-kinase activation with AICAR simultaneously increases fatty acid and glucose oxidation in resting rat soleus muscle. J Physiol 565: 547-553, 2005.
38. Stamler JS, Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol Rev 81: 209-237, 2001.
39. Stoppani J, Hildebrandt AL, Sakamoto K, Cameron-Smith D, Goodyear LJ, Neufer PD. AMP-activated protein kinase activates transcription of the UCP3 and HKII genes in rat skeletal muscle. Am J Physiol Endocrinol Metab 283: E1239-E1248, 2002.
40. Sugita H, Fujimoto M, Yasukawa T, Shimizu N, Sugita M, Yasuhara S, Jeevendra Martyn JA, Kaneki M. Inducible nitric-oxide synthase and NO donor induce insulin receptor substrate-1 degradation in skeletal muscle cells. J Biol Chem 280: 14203-14211, 2005.
41. Winder WW, Hardie DG. AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am J Physiol Endocrinol Metab 277: E1-E10, 1999.
42. Winder WW, Holmes BF, Rubink DS, Jensen EB, Chen M, Holloszy JO. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol 88: 2219-2226, 2000.
43. Zheng D, MacLean PS, Pohnert SC, Knight JB, Olson AL, Winder WW, Dohm GL. Regulation of muscle GLUT-4 transcription by AMP-activated protein kinase. J Appl Physiol 91: 1073-1083, 2001.
44. Zong H, Ren JM, Young LH, Pypaert M, Mu J, Birnbaum MJ, Shulman GI. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci USA 99: 15983-15987, 2002.