Skeletal muscle neuronal nitric oxide synthase μ protein is reduced in people with impaired glucose homeostasis and is not normalized by exercise training

Metabolism: Clinical and Experimental

Volumn 56, Issue 10, 2007, Pages 1405-1411

  Bradley, Scott J ^a,b,c   Kingwell, Bronwyn A ^a,b,c   Canny, Benedict J ^a,b,c   McConell, Glenn K ^a,b,c  

^a MONASH UNIVERSITY   (Australia)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

NEURONAL NITRIC OXIDE SYNTHASE;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; EXERCISE; FEMALE; GLUCOSE HOMEOSTASIS; HOMEOSTASIS; HUMAN; HUMAN TISSUE; IMPAIRED GLUCOSE TOLERANCE; INSULIN SENSITIVITY; MALE; MUSCLE BIOPSY; NON INSULIN DEPENDENT DIABETES MELLITUS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE;

ADULT; BLOOD GLUCOSE; BLOOD PRESSURE; BODY MASS INDEX; CHOLESTEROL; FEMALE; GLUCOSE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; HUMANS; INSULIN RESISTANCE; MALE; MIDDLE AGED; MUSCLE, SKELETAL; NITRIC OXIDE SYNTHASE TYPE II; OXYGEN CONSUMPTION; PHYSICAL FITNESS; TRIGLYCERIDES;

EID: 34548628793     PISSN: 00260495     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.metabol.2007.06.003     Document Type: Article

References (41)

1. Eriksson J., Taimela S., and Koivisto V.A. Exercise and the metabolic syndrome. Diabetologia 40 (1997) 125-135
2. Richter E.A., Derave W., and Wojtaszewski J.F. Glucose, exercise and insulin: emerging concepts. J Physiol 535 (2001) 313-322
3. Bradley S.J., Kingwell B.A., and McConell G.K. Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans. [published erratum appears in Diabetes 1999 Dec;48(12):2480]. Diabetes 48 (1999) 1815-1821
4. Kingwell B., Formosa M., Muhlmann M., Bradley S., and McConell G. Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects. Diabetes 51 (2002) 2572-2580
5. Baron A.D., Steinberg H.O., Chaker H., Leaming R., Johnson A., and Brechtel G. Insulin-mediated skeletal muscle vasodilation contributes to both insulin sensitivity and responsiveness in lean humans. J Clin Invest 96 (1995) 786-792
6. Baron A.D., Brechtel-Hook G., Johnson A., Cronin J., Leaming R., and Steinberg H.O. Effect of perfusion rate on the time course of insulin-mediated skeletal muscle glucose uptake. Am J Physiol 271 (1996) E1067-E1072
7. Vincent M.A., Barrett E.J., Lindner J.R., Clark M.G., and Rattigan S. Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. Am J Physiol Endocrinol Metab 285 (2003) E123-E129
8. Roy D., Perreault M., and Marette A. Insulin stimulation of glucose uptake in skeletal muscles and adipose tissues in vivo is NO dependent. Am J Physiol 274 (1998) E692-E699
9. Rudnick J., Puttmann B., Tesch P.A., Alkner B., Schoser B.G., Salanova M., et al. Differential expression of nitric oxide synthases (NOS 1-3) in human skeletal muscle following exercise countermeasure during 12 weeks of bed rest. Faseb J 18 (2004) 1228-1230
10. Frandsen U., Lopez-Figueroa M., and Hellsten Y. Localization of nitric oxide synthase in human skeletal muscle. Biochem Biophys Res Commun 227 (1996) 88-93
11. Torres S.H., De Sanctis J.B., de L.B.M., Hernandez N., and Finol H.J. Inflammation and nitric oxide production in skeletal muscle of type 2 diabetic patients. J Endocrinol 181 (2004) 419-427
12. Shankar R.R., Wu Y., Shen H.Q., Zhu J.S., and Baron A.D. Mice with gene disruption of both endothelial and neuronal nitric oxide synthase exhibit insulin resistance. Diabetes 49 (2000) 684-687
13. Balon T.W., and Nadler J.L. Evidence that nitric oxide increases glucose transport in skeletal muscle. J Appl Physiol 82 (1997) 359-363
14. Tatchum-Talom R., Schulz R., McNeill J.R., and Khadour F.H. Upregulation of neuronal nitric oxide synthase in skeletal muscle by swim training. Am J Physiol 279 (2000) H1757-H1766
15. Vassilakopoulos T., Deckman G., Kebbewar M., Rallis G., Harfouche R., and Hussain S.N. Regulation of nitric oxide production in limb and ventilatory muscles during chronic exercise training. Am J Physiol Lung Cell Mol Physiol 284 (2003) L452-L457
16. Frandsen U., Hoffner L., Betak A., Saltin B., Bangsbo J., and Hellsten Y. Endurance training does not alter the level of neuronal nitric oxide synthase in human skeletal muscle. J Appl Physiol 89 (2000) 1033-1038
17. McConnell G.K., Bradley S.J., Stephens T.J., Canny B.J., Kingwell B.A., and Lee-Young R.S. Skeletal muscle nNOSmu protein content is increased by exercise training in humans. Am J Physiol Regul Integr Comp Physiol 293 (2007) 821-828
18. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care 26 Suppl 1 (2003) S5-S20
19. Colman P.G., Thomas D.W., Zimmet P.Z., Welborn T.A., Garcia-Webb P., and Moore M.P. New classification and criteria for diagnosis of diabetes mellitus. Position statement from the Australian Diabetes Society, New Zealand Society for the Study of Diabetes, Royal College of Pathologists of Australasia and Australasian Association of Clinical Biochemists. Med J Aust 170 (1999) 375-378
20. Matthews D.R., Hosker J.P., Rudenski A.S., Naylor B.A., Treacher D.F., and Turner R.C. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28 (1985) 412-419
21. Haffner S.M., Miettinen H., and Stern M.P. The homeostasis model in the San Antonio Heart Study. Diabetes Care 20 (1997) 1087-1092
22. Bonora E., Targher G., Alberiche M., Bonadonna R.C., Saggiani F., Zenere M.B., et al. Homeostasis model assessment closely mirrors the glucose clamp technique in the assessment of insulin sensitivity: studies in subjects with various degrees of glucose tolerance and insulin sensitivity. Diabetes Care 23 (2000) 57-63
23. Matsuda M., and De Fronzo R.A. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 22 (1999) 1462-1470
24. Phillips D.I., Clark P.M., Hales C.N., and Osmond C. Understanding oral glucose tolerance: comparison of glucose or insulin measurements during the oral glucose tolerance test with specific measurements of insulin resistance and insulin secretion. Diabet Med 11 (1994) 286-292
25. Radziuk J. Insulin sensitivity and its measurement: structural commonalities among the methods. J Clin Endocrinol Metab 85 (2000) 4426-4433
26. Levine R., and Haft D.E. Carbohydrate homeostasis. N Engl J Med 283 (1970) 237-246
27. Myllynen P., Koivisto V.A., and Nikkila E.A. Glucose intolerance and insulin resistance accompany immobilization. Acta Med Scand 222 (1987) 75-81
28. Seltzer H.S., Allen E.W., Herron Jr. A.L., and Brennan M.T. Insulin secretion in response to glycemic stimulus: relation of delayed initial release to carbohydrate intolerance in mild diabetes mellitus. J Clin Invest 46 (1967) 323-335
29. ACSM: American College of Sports Medicine. ACSM's guidelines for exercise testing and prescription (1995), Williams and Wilkins, Baltimore
30. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35 (1975) 609-616
31. Bredt D.S., Hwang P.M., Glatt C.E., Lowenstein C., Reed R.R., and Snyder S.H. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351 (1991) 714-718
32. McConell G.K., and Kingwell B.A. Does nitric oxide regulate skeletal muscle glucose uptake during exercise?. Exerc Sport Sci Rev 34 (2006) 36-41
33. Chen Z.P., McConell G.K., Michell B.J., Snow R.J., Canny B.J., and Kemp B.E. AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation. Am J Physiol Endocrinol Metab 279 (2000) E1202-E1206
34. Chen Z.-P., Stephens T.J., Murthy S., Canny B.J., Hargreaves M., Witters L.A., et al. Effect of exercise intensity on skeletal muscle AMPK signaling in humans. Diabetes 52 (2003) 2205-2212
35. Stephens T.J., Chen Z.P., Canny B.J., Michell B.J., Kemp B.E., and McConell G.K. Progressive increase in human skeletal muscle AMPK[alpha]2 activity and ACC phosphorylation during exercise. Am J Physiol Endocrinol Metab 282 (2002) E688-E694
36. Kingwell B.A. Nitric oxide as a metabolic regulator during exercise: effects of training in health and disease. Clin Exp Pharmacol Physiol 27 (2000) 239-250
37. Silvagno F., Xia H., and Bredt D.S. Neuronal nitric-oxide synthase-mu, an alternatively spliced isoform expressed in differentiated skeletal muscle. J Biol Chem 271 (1996) 11204-11208
38. Gath I., Godtel-Armbrust U., and Forstermann U. Expressional downregulation of neuronal-type NO synthase I in guinea pig skeletal muscle in response to bacterial lipopolysaccharide. FEBS Lett 410 (1997) 319-323
39. Bedard S., Marcotte B., and Marette A. Cytokines modulate glucose transport in skeletal muscle by inducing the expression of inducible nitric oxide synthase. Biochem J 325 (1997) 487-493
40. Perreault M., and Marette A. Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat Med 7 (2001) 1138-1143
41. Kobzik L., Reid M.B., Bredt D.S., and Stamler J.S. Nitric oxide in skeletal muscle. [see comments]. Nature 372 (1994) 546-548