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

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 298, Issue 5, 2010, Pages

  Lee Young, Robert S ^a   Ayala, Julio E ^a   Hunley, Charles F ^a   James, Freyja D ^a   Bracy, Deanna P ^a   Kang, Li ^a   Wasserman, David H ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Blood flow; Mitochondria; Oxidative phosphorylation

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; GENOMIC DNA;

ANIMAL EXPERIMENT; ARTICLE; BODY COMPOSITION; CONTROLLED STUDY; ENZYME ACTIVITY; GASTROCNEMIUS MUSCLE; HYPOGLYCEMIA; IN VIVO STUDY; MOUSE; MUSCLE METABOLISM; MUSCLE MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BODY COMPOSITION; BODY WEIGHT; CALORIMETRY, INDIRECT; ENERGY METABOLISM; FEMALE; GLUCONEOGENESIS; GLYCOGEN; HYPOGLYCEMIA; INSULIN; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MITOCHONDRIA; MUSCLE, SKELETAL; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE PHOSPHORYLATION; PHOTOPERIOD; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL EXERTION; PREGNANCY; REGIONAL BLOOD FLOW; SIGNAL TRANSDUCTION;

EID: 77951727854     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00004.2010     Document Type: Article

References (51)

1. Ally A, Park G. Rapid determination of creatine, phosphocreatine, purine bases and nucleotides (ATP, ADP, AMP, GTP, GDP) in heart biopsies by gradient ion-pair reversed-phase liquid chromatography. J Chromatogr 575: 19-27, 1992.
2. Ayala JE, Bracy DP, Julien BM, Rottman JN, Fueger PT, Wasserman DH. Chronic treatment with sildenafil improves energy balance and insulin action in high fat-fed conscious mice. Diabetes 56: 1025-1033, 2007.
3. Ayala JE, Bracy DP, McGuinness OP, Wasserman DH. Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55: 390-397, 2006.
4. Balligand JL, Feron O, Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev 89: 481-534, 2009.
5. Bradley SJ, Kingwell BA, McConell GK. Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans. Diabetes 48: 1815-1821, 1999.
6. Bredt DS, Snyder SH. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 87: 682-685, 1990. (Pubitemid 20051434)
7. Chan TM, Exton JH. A rapid method for the determination of glycogen content and radioactivity in small quantities of tissue or isolated hepatocytes. Anal Biochem 71: 96-105, 1976.
8. Chen Z, Peng IC, Sun W, Su MI, Hsu PH, Fu Y, Zhu Y, DeFea K, Pan S, Tsai MD, Shyy JYJ. AMP-activated protein kinase functionally phosphorylates endothelial nitric oxide synthase Ser633. Circ Res 104: 496-505, 2009.
9. 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. (Pubitemid 29080812)
10. 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. (Pubitemid 37059489)
11. Cook S, Hugli O, Egli M, Menard B, Thalmann S, Sartori C, Perrin C, Nicod P, Thorens B, Vollenweider P, Scherrer U, Burcelin R. Partial gene deletion of endothelial nitric oxide synthase predisposes to exaggerated high-fat diet-induced insulin resistance and arterial hypertension. Diabetes 53: 2067-2072, 2004. (Pubitemid 38970756)
12. Csukly K, Ascah A, Matas J, Gardiner PF, Fontaine E, Burelle Y. Muscle denervation promotes opening of the permeability transition pore and increases the expression of cyclophilin D. J Physiol 574: 319-327, 2006. (Pubitemid 43905815)
13. Duplain H, Burcelin R, Sartori C, Cook S, Egli M, Lepori M, Vollenweider P, Pedrazzini T, Nicod P, Thorens B, Scherrer U. Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 104: 342-345, 2001. (Pubitemid 32666958)
14. Etgen GJ Jr, Fryburg DA, Gibbs EM. Nitric oxide stimulates skeletal muscle glucose transport through a calcium/contraction- and phosphatidylinositol-3-kinase-independent pathway. Diabetes 46: 1915-1919, 1997.
15. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509, 1957.
16. Fujii N, Seifert MM, Kane EM, Peter LE, Ho RC, Winstead S, Hirshman MF, Goodyear LJ. Role of AMP-activated protein kinase in exercise capacity, whole body glucose homeostasis, and glucose transport in skeletal muscle. Insight from analysis of a transgenic mouse model. Diabetes Res Clin Pract 77 Suppl 1: S92-S98, 2007. (Pubitemid 47225133)
17. Hayashi T, Hirshman MF, Fujii N, Habinowski SA, Witters LA, Goodyear LJ. Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 49: 527-531, 2000. (Pubitemid 30183739)
18. Hickner RC, Kemeny G, Stallings HW, Manning SM, McIver KL. Relationship between body composition and skeletal muscle eNOS. Int J Obes (Lond) 30: 308-312, 2006. (Pubitemid 43237688)
19. Higaki Y, Hirshman 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. (Pubitemid 32127278)
20. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377: 239-242, 1995.
21. Kingwell BA, Formosa M, Muhlmann M, Bradley SJ, McConell GK. Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects. Diabetes 51: 2572-2580, 2002. (Pubitemid 34827409)
22. Kjaer M, Hanel B, Worm L, Perko G, Lewis SF, Sahlin K, Galbo H, Secher NH. Cardiovascular and neuroendocrine responses to exercise in hypoxia during impaired neural feedback from muscle. Am J Physiol Regul Integr Comp Physiol 277: R76-R85, 1999. (Pubitemid 29356780)
23. Kraegen EW, James DE, Jenkins AB, Chisholm DJ. Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am J Physiol Endocrinol Metab 248: E353-E362, 1985. (Pubitemid 15076599)
24. Lacza Z, Snipes JA, Zhang J, Horváth EM, Figueroa JP, Szabó C, Busija DW. Mitochondrial nitric oxide synthase is not eNOS, nNOS or iNOS. Free Radic Biol Med 35: 1217-1228, 2003. (Pubitemid 37357247)
25. Lau KS, Grange RW, Isotani E, Sarelius IH, Kamm KE, Huang PL, Stull JT. nNOS and eNOS modulate cGMP formation and vascular response in contracting fast-twitch skeletal muscle. Physiol Genomics 2: 21-27, 2000.
26. Le Gouill E, Jimenez M, Binnert C, Jayet PY, Thalmann S, Nicod P, Scherrer U, Vollenweider P. Endothelial nitric oxide synthase (eNOS) knockout mice have defective mitochondrial beta-oxidation. Diabetes 56: 2690-2696, 2007. (Pubitemid 350044910)
27. Lee-Young RS, Griffee SR, Lynes SE, Bracy DP, Ayala JE, McGuinness OP, Wasserman DH. Skeletal muscle AMP-activated protein kinase is essential for the metabolic response to exercise in vivo. J Biol Chem 284: 23925-23934, 2009.
28. Li H, Wallerath T, Forstermann U. Physiological mechanisms regulating the expression of endothelial-type NO synthase. Nitric Oxide 7: 132-147, 2002. (Pubitemid 35177005)
29. Lira VA, Soltow QA, Long JHD, Betters JL, Sellman JE, Criswell DS. Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle. Am J Physiol Endocrinol Metab 293: E1062-E1068, 2007.
30. Lowry OH, Passonneau JV. A Flexible System of Enzymatic Analysis. New York: Academic, 1972.
31. Maarbjerg SJ, Jorgensen SB, Rose AJ, Jeppesen J, Jensen TE, Treebak JT, Birk JB, Schjerling P, Wojtaszewski JF, Richter EA. Genetic impairment of α2-AMPK signaling does not reduce muscle glucose uptake during treadmill exercise in mice. Am J Physiol Endocrinol Metab 297: E924-E934, 2009.
32. Maxwell AJ, Schauble E, Bernstein D, Cooke JP. Limb blood flow during exercise is dependent on nitric oxide. Circulation 98: 369-374, 1998. (Pubitemid 28348060)
33. Merry TL, Steinberg GR, Lynch GS, McConell GK. Skeletal muscle glucose uptake during contraction is regulated by nitric oxide and ROS independently of AMPK. Am J Physiol Endocrinol Metab 298: E577-E585, 2010.
34. Momken I, Lechene P, Ventura-Clapier R, Veksler V. Voluntary physical activity alterations in endothelial nitric oxide synthase knockout mice. Am J Physiol Heart Circ Physiol 287: H914-H920, 2004. (Pubitemid 38955330)
35. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 329: 2002-2012, 1993.
36. Morgan CR, Lazarow A. Immunoassay of pancreatic and plasma insulin following alloxan injection of rats. Diabetes 14: 669-671, 1965.
37. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7: 1085-1094, 2001. (Pubitemid 32525754)
38. 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. (Pubitemid 39557743)
39. Ojaimi C, Li W, Kinugawa S, Post H, Csiszar A, Pacher P, Kaley G, Hintze TH. Transcriptional basis for exercise limitation in male eNOS-knockout mice with age: heart failure and the fetal phenotype. Am J Physiol Heart Circ Physiol 289: H1399-H1407, 2005. (Pubitemid 41368980)
40. Roberts CK, Barnard RJ, Jasman A, Balon TW. Acute exercise increases nitric oxide synthase activity in skeletal muscle. Am J Physiol Endocrinol Metab 277: E390-E394, 1999. (Pubitemid 29413846)
41. Roberts CK, Barnard RJ, Scheck SH, Balon TW. Exercise-stimulated glucose transport in skeletal muscle is nitric oxide dependent. Am J Physiol Endocrinol Metab 273: E220-E225, 1997. (Pubitemid 27342775)
42. Ross RM, Wadley GD, Clark MG, Rattigan S, McConell GK. Local nitric oxide synthase inhibition reduces skeletal muscle glucose uptake but not capillary blood flow during in situ muscle contraction in rats. Diabetes 56: 2885-2892, 2007. (Pubitemid 350223622)
43. Rottman JN, Bracy D, Malabanan C, Yue Z, Clanton J, Wasserman DH. Contrasting effects of exercise and NOS inhibition on tissue-specific fatty acid and glucose uptake in mice. Am J Physiol Endocrinol Metab 283: E116-E123, 2002. (Pubitemid 34686676)
44. Shearer J, Coenen KR, Pencek RR, Swift LL, Wasserman DH, Rottman JN. Long-chain fatty acid uptake in vivo: Comparison of [(125)I]-BMIPP and [(3)H]-bromopalmitate. Lipids 43: 703-711, 2008.
45. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 93: 13176-13181, 1996. (Pubitemid 26382789)
46. Stephens TJ, Canny BJ, Snow RJ, McConell GK. 5′-aminoimidazole-4- carboxyamide-ribonucleoside-activated glucose transport is not prevented by nitric oxide synthase inhibition in rat isolated skeletal muscle. Clin Exp Pharmacol Physiol 31: 419-423, 2004. (Pubitemid 39044120)
47. Valerio A, Cardile A, Cozzi V, Bracale R, Tedesco L, Pisconti A, Palomba L, Cantoni O, Clementi E, Moncada S, Carruba MO, Nisoli E. TNF-α downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116: 2791-2798, 2006. (Pubitemid 44511642)
48. Wadley GD, Choate J, McConell GK. NOS isoform-specific regulation of basal but not exercise-induced mitochondrial biogenesis in mouse skeletal muscle. J Physiol 585: 253-262, 2007. (Pubitemid 350131117)
49. Wadley GD, Choate J, McConell. Reply from G. D. Wadley, G. K. Choate, and J. McConell. J Physiol 586: 915-916, 2008.
50. Zhang J, Xie Z, Dong Y, Wang S, Liu C, Zou MH. Identification of nitric oxide as an endogenous activator of the AMP-activated protein kinase in vascular endothelial cells. J Biol Chem 283: 27452-27461, 2008.
51. Zinker BA, Wilson RD, Wasserman DH. Interaction of decreased arterial PO2 and exercise on carbohydrate metabolism in the dog. Am J Physiol Endocrinol Metab 269: E409-E417, 1995.