Skeletal muscle function during exercise-fine-tuning of diverse subsystems by nitric oxide

International Journal of Molecular Sciences

Volumn 14, Issue 4, 2013, Pages 7109-7139

  Suhr, Frank ^a   Gehlert, Sebastian ^a   Grau, Marijke ^a   Bloch, Wilhelm ^a  

^a GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

Author keywords

cGMP; Exercise; Nitric oxide; Nitric oxide synthase; S nitrosylation; Signaling; Skeletal muscle

Indexed keywords

CATALASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE PEROXIDASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MYOGLOBIN; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

BIOSYNTHESIS; CELLULAR DISTRIBUTION; CYTOSKELETON; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; METABOLIC REGULATION; MUSCLE CONTRACTILITY; MUSCLE EXERCISE; MUSCLE FUNCTION; MUSCLE HYPERTROPHY; MUSCLE METABOLISM; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; ANIMAL; ENZYMOLOGY; EXERCISE; METABOLISM; PHYSIOLOGY;

ANIMALS; CYTOSKELETON; EXERCISE; HUMANS; MUSCLE, SKELETAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SIGNAL TRANSDUCTION;

EID: 84876012871     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14047109     Document Type: Review

References (195)

1. Stamler, J.S.; Meissner, G. Physiology of nitric oxide in skeletal muscle. Physiol. Rev. 2001, 81, 209-237.
2. Reid, M.B.; Haack, K.E.; Franchek, K.M.; Valberg, P.A.; Kobzik, L.;West, M.S. Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J. Appl. Physiol 1992, 73, 1797-1804.
3. Balon, T.W.; Nadler, J.L. Nitric oxide release is present from incubated skeletal muscle preparations. J. Appl. Physiol 1994, 77, 2519-2521.
4. Palomero, J.; Pye, D.; Kabayo, T.; Spiller, D.G.; Jackson, M.J. In situ detection and measurement of intracellular reactive oxygen species in single isolated mature skeletal muscle fibers by real time fluorescence microscopy. Antioxid. Redox. Signal. 2008, 10, 1463-1474.
5. Powers, S.K.; Jackson, M.J. Exercise-induced oxidative stress: Cellular mechanisms and impact on muscle force production. Physiol. Rev. 2008, 88, 1243-1276.
6. Pye, D.; Palomero, J.; Kabayo, T.; Jackson, M.J. Real-time measurement of nitric oxide in single mature mouse skeletal muscle fibres during contractions. J. Physiol. 2007, 581, 309-318.
7. Molavi, B.; Mehta, J.L. Oxidative stress in cardiovascular disease: Molecular basis of its deleterious effects, its detection, and therapeutic considerations. Curr. Opin. Cardiol. 2004, 19, 488-493.
8. Rao, G.N.; Berk, B.C. Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ. Res. 1992, 70, 593-599.
9. Droge, W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82, 47-95.
10. Jackson, M.J.; Papa, S.; Bolanos, J.; Bruckdorfer, R.; Carlsen, H.; Elliott, R.M.; Flier, J.; Griffiths, H.R.; Heales, S.; Holst, B.; et al. Antioxidants, reactive oxygen and nitrogen species, gene induction and mitochondrial function. Mol. Aspects Med. 2002, 23, 209-285.
11. Furchgott, R.F.; Zawadzki, J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980, 288, 373-376.
12. Palmer, R.M.; Ferrige, A.G.; Moncada, S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987, 327, 524-526.
13. Anderson, T.J.; Uehata, A.; Gerhard, M.D.; Meredith, I.T.; Knab, S.; Delagrange, D.; Lieberman, E.H.; Ganz, P.; Creager, M.A.; Yeung, A.C. Close relation of endothelial function in the human coronary and peripheral circulations. J. Am. Coll. Cardiol. 1995, 26, 1235-1241.
14. Oelze, M.; Mollnau, H.; Hoffmann, N.; Warnholtz, A.; Bodenschatz, M.; Smolenski, A.; Walter, U.; Skatchkov, M.; Meinertz, T.; Munzel, T. Vasodilator-stimulated phosphoprotein serine 239 phosphorylation as a sensitive monitor of defective nitric oxide/cGMP signaling and endothelial dysfunction. Circ. Res. 2000, 87, 999-1005.
15. Nathan, C.; Shiloh, M.U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 2000, 97, 8841-8848.
16. Pervin, S.; Singh, R.; Chaudhuri, G. Nitric oxide-induced cytostasis and cell cycle arrest of a human breast cancer cell line (MDA-MB-231): Potential role of cyclin D1. Proc. Natl. Acad. Sci. USA 2001, 98, 3583-3588.
17. Kolb, H.; Kolb-Bachofen, V. Nitric oxide in autoimmune disease: Cytotoxic or regulatory mediator? Immunol. Today 1998, 19, 556-561.
18. Stamler, J.; Mendelsohn, M.E.; Amarante, P.; Smick, D.; Andon, N.; Davies, P.F.; Cooke, J.P.; Loscalzo, J. N-acetylcysteine potentiates platelet inhibition by endothelium-derived relaxing factor. Circ. Res. 1989, 65, 789-795.
19. Radomski, M.W.; Palmer, R.M.; Moncada, S. The anti-aggregating properties of vascular endothelium: Interactions between prostacyclin and nitric oxide. Br. J. Pharmacol. 1987, 92, 639-646.
20. Anderson, J.E. A role for nitric oxide in muscle repair: Nitric oxide-mediated activation of muscle satellite cells. Mol. Biol. Cell 2000, 11, 1859-1874.
21. Hendgen-Cotta, U.; Grau, M.; Rassaf, T.; Gharini, P.; Kelm, M.; Kleinbongard, P. Reductive gas-phase chemiluminescence and flow injection analysis for measurement of the nitric oxide pool in biological matrices. Methods Enzymol. 2008, 441, 295-315.
22. Stamler, J.S.; Singel, D.J.; Loscalzo, J. Biochemistry of nitric oxide and its redox-activated forms. Science 1992, 258, 1898-1902.
23. Freeman, B. Free radical chemistry of nitric oxide. Looking at the dark side. Chest 1994, 105, 79S-84S.
24. Mellion, B.T.; Ignarro, L.J.; Ohlstein, E.H.; Pontecorvo, E.G.; Hyman, A.L.; Kadowitz, P.J. Evidence for the inhibitory role of guanosine 3',5'-monophosphate in ADP-induced human platelet aggregation in the presence of nitric oxide and related vasodilators. Blood 1981, 57, 946-955.
25. Lincoln, T.M. Cyclic GMP and mechanisms of vasodilation. Pharmacol. Ther. 1989, 41, 479-502.
26. Lincoln, T.M.; Dey, N.; Sellak, H. Invited review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: From the regulation of tone to gene expression. J. Appl. Physiol. 2001, 91, 1421-1430.
27. Hofmann, F.; Ammendola, A.; Schlossmann, J. Rising behind NO: cGMP-dependent protein kinases. J. Cell Sci. 2000, 113, 1671-1676.
28. Garthwaite, J.; Charles, S.L.; Chess-Williams, R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 1988, 336, 385-388.
29. Zhuo, M.; Hawkins, R.D. Long-term depression: A learning-related type of synaptic plasticity in the mammalian central nervous system. Rev. Neurosci. 1995, 6, 259-277.
30. Munzel, T.; Feil, R.; Mulsch, A.; Lohmann, S.M.; Hofmann, F.; Walter, U. Physiology and pathophysiology of vascular signaling controlled by guanosine 3',5'-cyclic monophosphate-dependent protein kinase [corrected]. Circulation 2003, 108, 2172-2183.
31. Bruckdorfer, R. The basics about nitric oxide. Mol. Aspects Med. 2005, 26, 3-31.
32. Thoonen, R.; Sips, P.Y.; Bloch, K.D.; Buys, E.S. Pathophysiology of hypertension in the absence of nitric oxide/cyclic GMP signaling. Curr. Hypertens. Rep. 2013, 15, 47-58.
33. Buono, R.; Vantaggiato, C.; Pisa, V.; Azzoni, E.; Bassi, M.T.; Brunelli, S.; Sciorati, C.; Clementi, E. Nitric oxide sustains long-term skeletal muscle regeneration by regulating fate of satellite cells via signaling pathways requiring Vangl2 and cyclic GMP. Stem Cells 2012, 30, 197-209.
34. Foster, M.W.; McMahon, T.J.; Stamler, J.S. S-nitrosylation in health and disease. Trends Mol. Med. 2003, 9, 160-168.
35. Martinez-Ruiz, A.; Lamas, S. S-nitrosylation: A potential new paradigm in signal transduction. Cardiovasc. Res. 2004, 62, 43-52.
36. Broillet, M.C. S-nitrosylation of proteins. Cell Mol. Life Sci. 1999, 55, 1036-1042.
37. Stamler, J.S.; Simon, D.I.; Osborne, J.A.; Mullins, M.E.; Jaraki, O.; Michel, T.; Singel, D.J.; Loscalzo, J. S-nitrosylation of proteins with nitric oxide: Synthesis and characterization of biologically active compounds. Proc. Natl. Acad. Sci. USA 1992, 89, 444-448.
38. Hess, D.T.; Matsumoto, A.; Kim, S.O.; Marshall, H.E.; Stamler, J.S. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 2005, 6, 150-166.
39. Lima, B.; Forrester, M.T.; Hess, D.T.; Stamler, J.S. S-nitrosylation in cardiovascular signaling. Circ. Res. 2010, 106, 633-646.
40. Palmer, R.M.; Rees, D.D.; Ashton, D.S.; Moncada, S. L-arginine is the physiological precursor for the formation of nitric oxide in endothelium-dependent relaxation. Biochem. Biophys. Res. Commun. 1988, 153, 1251-1256.
41. Filho, J.C.; Bergstrom, J.; Stehle, P.; Furst, P. Simultaneous measurements of free amino acid patterns of plasma, muscle and erythrocytes in healthy human subjects. Clin Nutr. 1997, 16, 299-305.
42. Stuehr, D.J.; Kwon, N.S.; Nathan, C.F.; Griffith, O.W.; Feldman, P.L.; Wiseman, J. N omega-hydroxy-L-arginine is an intermediate in the biosynthesis of nitric oxide from L-arginine. J. Biol. Chem. 1991, 266, 6259-6263.
43. Spiegelhalder, B.; Eisenbrand, G.; Preussmann, R. Influence of dietary nitrate on nitrite content of human saliva: Possible relevance to in vivo formation of N-nitroso compounds. Food Cosmet. Toxicol. 1976, 14, 545-548.
44. Tannenbaum, S.R.; Correa, P. Nitrate and gastric cancer risks. Nature 1985, 317, 675-676.
45. Zweier, J.L.; Samouilov, A.; Kuppusamy, P. Non-enzymatic nitric oxide synthesis in biological systems. Biochim. Biophys. Acta 1999, 1411, 250-262.
46. Cosby, K.; Partovi, K.S.; Crawford, J.H.; Patel, R.P.; Reiter, C.D.; Martyr, S.; Yang, B.K.; Waclawiw, M.A.; Zalos, G.; Xu, X.; et al. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat. Med. 2003, 9, 1498-1505.
47. Gladwin, M.T.; Shelhamer, J.H.; Schechter, A.N.; Pease-Fye, M.E.; Waclawiw, M.A.; Panza, J.A.; Ognibene, F.P.; Cannon, R.O., III. Role of circulating nitrite and S-nitrosohemoglobin in the regulation of regional blood flow in humans. Proc. Natl. Acad. Sci. USA 2000, 97, 11482-11487.
48. Isbell, T.S.; Gladwin, M.T.; Patel, R.P. Hemoglobin oxygen fractional saturation regulates nitrite-dependent vasodilation of aortic ring bioassays. Am. J. Physiol. Heart Circ. Physiol. 2007, 293, H2565-H2572.
49. Totzeck, M.; Hendgen-Cotta, U.B.; Luedike, P.; Berenbrink, M.; Klare, J.P.; Steinhoff, H.J.; Semmler, D.; Shiva, S.; Williams, D.; Kipar, A.; et al. Nitrite regulates hypoxic vasodilation via myoglobin-dependent nitric oxide generation. Circulation 2012, 126, 325-334.
50. Shiva, S.; Huang, Z.; Grubina, R.; Sun, J.; Ringwood, L.A.; MacArthur, P.H.; Xu, X.; Murphy, E.; Darley-Usmar, V.M.; Gladwin, M.T. Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ. Res. 2007, 100, 654-661.
51. Rassaf, T.; Flogel, U.; Drexhage, C.; Hendgen-Cotta, U.; Kelm, M.; Schrader, J. Nitrite reductase function of deoxymyoglobin: oxygen sensor and regulator of cardiac energetics and function. Circ. Res. 2007, 100, 1749-1754.
52. Haynes, V.; Elfering, S.; Traaseth, N.; Giulivi, C. Mitochondrial nitric-oxide synthase: Enzyme expression, characterization, and regulation. J. Bioenerg. Biomembr. 2004, 36, 341-346.
53. Giulivi, C.; Poderoso, J.J.; Boveris, A. Production of nitric oxide by mitochondria. J. Biol. Chem. 1998, 273, 11038-11043.
54. Brenman, J.E.; Xia, H.; Chao, D.S.; Black, S.M.; Bredt, D.S. Regulation of neuronal nitric oxide synthase through alternative transcripts. Dev. Neurosci. 1997, 19, 224-231.
55. Silvagno, F.; Xia, H.; Bredt, D.S. Neuronal nitric-oxide synthase-mu, an alternatively spliced isoform expressed in differentiated skeletal muscle. J. Biol. Chem. 1996, 271, 11204-11208.
56. Amancharla, M.R.; Rodarte, J.R.; Boriek, A.M. Modeling the kinematics of the canine midcostal diaphragm. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280, R588-R597.
57. Ignarro, L.J. Heme-dependent activation of soluble guanylate cyclase by nitric oxide: Regulation of enzyme activity by porphyrins and metalloporphyrins. Semin. Hematol. 1989, 26, 63-76.
58. Kleinbongard, P.; Schulz, R.; Rassaf, T.; Lauer, T.; Dejam, A.; Jax, T.; Kumara, I.; Gharini, P.; Kabanova, S.; Ozuyaman, B.; et al. Red blood cells express a functional endothelial nitric oxide synthase. Blood 2006, 107, 2943-2951.
59. Cortese-Krott, M.M.; Rodriguez-Mateos, A.; Sansone, R.; Kuhnle, G.G.; Thasian-Sivarajah, S.; Krenz, T.; Horn, P.; Krisp, C.; Wolters, D.; Heiss, C.; et al. Human red blood cells at work: Identification and visualization of erythrocytic eNOS activity in health and disease. Blood 2012, 120, 4229-4237.
60. Suhr, F.; Brenig, J.; Muller, R.; Behrens, H.; Bloch, W.; Grau, M. Moderate exercise promotes human RBC-NOS activity, NO production and deformability through Akt kinase pathway. PLoS One 2012, 7, e45982.
61. Grau, M.; Pauly, S.; Ali, J.; Walpurgis, K.; Thevis, M.; Bloch, W.; Suhr, F. RBC-NOS-dependent S-nitrosylation of cytoskeletal proteins improves RBC dformability. PLoS One 2013, 8, e56759.
62. Cho, H.J.; Xie, Q.W.; Calaycay, J.; Mumford, R.A.; Swiderek, K.M.; Lee, T.D.; Nathan, C. Calmodulin is a subunit of nitric oxide synthase from macrophages. J. Exp. Med. 1992, 176, 599-604.
63. Nathan, C. Inducible nitric oxide synthase: What difference does it make? J. Clin. Invest. 1997, 100, 2417-2423.
64. Forstermann, U.; Closs, E.I.; Pollock, J.S.; Nakane, M.; Schwarz, P.; Gath, I.; Kleinert, H. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 1994, 23, 1121-1131.
65. Adams, V.; Yu, J.; Mobius-Winkler, S.; Linke, A.; Weigl, C.; Hilbrich, L.; Schuler, G.; Hambrecht, R. Increased inducible nitric oxide synthase in skeletal muscle biopsies from patients with chronic heart failure. Biochem. Mol. Med. 1997, 61, 152-160.
66. Ungureanu-Longrois, D.; Balligand, J.L.; Kelly, R.A.; Smith, T.W. Myocardial contractile dysfunction in the systemic inflammatory response syndrome: Role of a cytokine-inducible nitric oxide synthase in cardiac myocytes. J. Mol. Cell Cardiol. 1995, 27, 155-167.
67. Gielen, S.; Adams, V.; Linke, A.; Erbs, S.; Mobius-Winkler, S.; Schubert, A.; Schuler, G.; Hambrecht, R. Exercise training in chronic heart failure: Correlation between reduced local inflammation and improved oxidative capacity in the skeletal muscle. Eur. J. Cardiovasc. Prev. Rehabil. 2005, 12, 393-400.
68. Schulze, P.C.; Gielen, S.; Schuler, G.; Hambrecht, R. Chronic heart failure and skeletal muscle catabolism: Effects of exercise training. Int. J. Cardiol. 2002, 85, 141-149.
69. Akita, Y.; Otani, H.; Matsuhisa, S.; Kyoi, S.; Enoki, C.; Hattori, R.; Imamura, H.; Kamihata, H.; Kimura, Y.; Iwasaka, T. Exercise-induced activation of cardiac sympathetic nerve triggers cardioprotection via redox-sensitive activation of eNOS and upregulation of iNOS. Am. J. Physiol. Heart Circ. Physiol. 2007, 292, H2051-H2059.
70. Xu, W.; Charles, I.G.; Moncada, S.; Gorman, P.; Sheer, D.; Liu, L.; Emson, P. Mapping of the genes encoding human inducible and endothelial nitric oxide synthase (NOS2 and NOS3) to the pericentric region of chromosome 17 and to chromosome 7, respectively. Genomics 1994, 21, 419-422.
71. Alderton, W.K.; Cooper, C.E.; Knowles, R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 2001, 357, 593-615.
72. Bredt, D.S.; Snyder, S.H. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA 1990, 87, 682-685.
73. Yui, Y.; Hattori, R.; Kosuga, K.; Eizawa, H.; Hiki, K.; Kawai, C. Purification of nitric oxide synthase from rat macrophages. J. Biol. Chem. 1991, 266, 12544-12547.
74. Pollock, J.S.; Forstermann, U.; Mitchell, J.A.; Warner, T.D.; Schmidt, H.H.; Nakane, M.; Murad, F. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc. Natl. Acad. Sci. USA 1991, 88, 10480-10484.
75. Asano, K.; Chee, C.B.; Gaston, B.; Lilly, C.M.; Gerard, C.; Drazen, J.M.; Stamler, J.S. Constitutive and inducible nitric oxide synthase gene expression, regulation, and activity in human lung epithelial cells. Proc. Natl. Acad. Sci. USA 1994, 91, 10089-10093.
76. Nathan, C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 1992, 6, 3051-3064.
77. Snyder, L.M.; Fortier, N.L.; Trainor, J.; Jacobs, J.; Leb, L.; Lubin, B.; Chiu, D.; Shohet, S.; Mohandas, N. Effect of hydrogen peroxide exposure on normal human erythrocyte deformability, morphology, surface characteristics, and spectrin-hemoglobin cross-linking. J. Clin. Invest. 1985, 76, 1971-1977.
78. Shaul, P.W. Regulation of endothelial nitric oxide synthase: Location, location, location. Annu. Rev. Physiol. 2002, 64, 749-774.
79. Chang, W.J.; Iannaccone, S.T.; Lau, K.S.; Masters, B.S.; McCabe, T.J.; McMillan, K.; Padre, R.C.; Spencer, M.J.; Tidball, J.G.; Stull, J.T. Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc. Natl. Acad. Sci. USA 1996, 93, 9142-9147.
80. Frandsen, U.; Lopez-Figueroa, M.; Hellsten, Y. Localization of nitric oxide synthase in human skeletal muscle. Biochem. Biophys. Res. Commun. 1996, 227, 88-93.
81. Ho, K.M.; McMurray, G.; Brading, A.F.; Noble, J.G.; Ny, L.; Andersson, K.E. Nitric oxide synthase in the heterogeneous population of intramural striated muscle fibres of the human membranous urethral sphincter. J. Urol. 1998, 159, 1091-1096.
82. Nakane, M.; Schmidt, H.H.; Pollock, J.S.; Forstermann, U.; Murad, F. Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle. FEBS Lett. 1993, 316, 175-180.
83. Blottner, D.; Luck, G. Nitric oxide synthase (NOS) in mouse skeletal muscle development and differentiated myoblasts. Cell Tissue Res. 1998, 292, 293-302.
84. Christova, T.; Grozdanovic, Z.; Gossrau, R. Nitric oxide synthase (NOS) I during postnatal development in rat and mouse skeletal muscle. Acta Histochem. 1997, 99, 311-324.
85. Guo, Y.; Greenwood, M.T.; Petrof, B.J.; Hussain, S.N. Expression and regulation of protein inhibitor of neuronal nitric oxide synthase in ventilatory muscles. Am. J. Respir. Cell Mol. Biol. 1999, 20, 319-326.
86. Kobzik, L.; Reid, M.B.; Bredt, D.S.; Stamler, J.S. Nitric oxide in skeletal muscle. Nature 1994, 372, 546-548.
87. Gath, I.; Closs, E.I.; Godtel-Armbrust, U.; Schmitt, S.; Nakane, M.; Wessler, I.; Forstermann, U. Inducible NO synthase II and neuronal NO synthase I are constitutively expressed in different structures of guinea pig skeletal muscle: Implications for contractile function. FASEB J. 1996, 10, 1614-1620.
88. El, D.Q.; Guo, Y.; Comtois, A.; Zhu, E.; Greenwood, M.T.; Bredt, D.S.; Hussain, S.N. Ontogenesis of nitric oxide synthases in the ventilatory muscles. Am. J. Respir. Cell Mol. Biol. 1998, 18, 844-852.
89. Kapur, S.; Bedard, S.; Marcotte, B.; Cote, C.H.; Marette, A. Expression of nitric oxide synthase in skeletal muscle: A novel role for nitric oxide as a modulator of insulin action. Diabetes 1997, 46, 1691-1700.
90. Gossrau, R. Caveolin-3 and nitric oxide synthase I in healthy and diseased skeletal muscle. Acta Histochem. 1998, 100, 99-112.
91. Kusner, L.L.; Kaminski, H.J. Nitric oxide synthase is concentrated at the skeletal muscle endplate. Brain Res. 1996, 730, 238-242.
92. Grozdanovic, Z.; Gosztonyi, G.; Gossrau, R. Nitric oxide synthase I (NOS-I) is deficient in the sarcolemma of striated muscle fibers in patients with Duchenne muscular dystrophy, suggesting an association with dystrophin. Acta Histochem. 1996, 98, 61-69.
93. Wakayama, Y.; Inoue, M.; Murahashi, M.; Shibuya, S.; Jimi, T.; Kojima, H.; Oniki, H. Ultrastructural localization of alpha 1-syntrophin and neuronal nitric oxide synthase in normal skeletal myofiber, and their relation to each other and to dystrophin. Acta Neuropathol. 1997, 94, 455-464.
94. Williams, G.; Brown, T.; Becker, L.; Prager, M.; Giroir, B.P. Cytokine-induced expression of nitric oxide synthase in C2C12 skeletal muscle myocytes. Am. J. Physiol 1994, 267, R1020-R1025.
95. Kobzik, L.; Stringer, B.; Balligand, J.L.; Reid, M.B.; Stamler, J.S. Endothelial type nitric oxide synthase in skeletal muscle fibers: mitochondrial relationships. Biochem. Biophys. Res. Commun. 1995, 211, 375-381.
96. Bates, T.E.; Loesch, A.; Burnstock, G.; Clark, J.B. Mitochondrial nitric oxide synthase: A ubiquitous regulator of oxidative phosphorylation? Biochem. Biophys. Res. Commun. 1996, 218, 40-44.
97. Grozdanovic, Z.; Nakos, G.; Dahrmann, G.; Mayer, B.; Gossrau, R. Species-independent expression of nitric oxide synthase in the sarcolemma region of visceral and somatic striated muscle fibers. Cell Tissue Res. 1995, 281, 493-499.
98. Heinzel, B.; John, M.; Klatt, P.; Bohme, E.; Mayer, B. Ca2+/calmodulin-dependent formation of hydrogen peroxide by brain nitric oxide synthase. Biochem. J. 1992, 281, 627-630.
99. Laursen, J.B.; Somers, M.; Kurz, S.; McCann, L.; Warnholtz, A.; Freeman, B.A.; Tarpey, M.; Fukai, T.; Harrison, D.G. Endothelial regulation of vasomotion in apoE-deficient mice: Implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation 2001, 103, 1282-1288.
100. Cai, H.; Harrison, D.G. Endothelial dysfunction in cardiovascular diseases: The role of oxidant stress. Circ. Res. 2000, 87, 840-844.
101. Xia, Y.; Tsai, A.L.; Berka, V.; Zweier, J.L. Superoxide generation from endothelial nitric-oxide synthase. A Ca2+/calmodulin-dependent and tetrahydrobiopterin regulatory process. J. Biol. Chem. 1998, 273, 25804-25808.
102. Vasquez-Vivar, J.; Kalyanaraman, B.; Martasek, P.; Hogg, N.; Masters, B.S.; Karoui, H.; Tordo, P.; Pritchard, K.A., Jr. Superoxide generation by endothelial nitric oxide synthase: The influence of cofactors. Proc. Natl. Acad. Sci. USA 1998, 95, 9220-9225.
103. Wink, D.A.; Cook, J.A.; Pacelli, R.; Liebmann, J.; Krishna, M.C.; Mitchell, J.B. Nitric oxide (NO) protects against cellular damage by reactive oxygen species. Toxicol. Lett. 1995, 82-83, 221-226.
104. Brenman, J.E.; Chao, D.S.; Gee, S.H.; McGee, A.W.; Craven, S.E.; Santillano, D.R.; Wu, Z.; Huang, F.; Xia, H.; Peters, M.F.; et al. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 1996, 84, 757-767.
105. Rando, T.A. Role of nitric oxide in the pathogenesis of muscular dystrophies: A "two hit" hypothesis of the cause of muscle necrosis. Microsc. Res. Tech. 2001, 55, 223-235.
106. Carmignac, V.; Durbeej, M. Cell-matrix interactions in muscle disease. J. Pathol. 2012, 226, 200-218.
107. Van Deutekom, J.C.; van Ommen, G.J. Advances in Duchenne muscular dystrophy gene therapy. Nat. Rev. Genet. 2003, 4, 774-783.
108. Brenman, J.E.; Chao, D.S.; Xia, H.; Aldape, K.; Bredt, D.S. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 1995, 82, 743-752.
109. Lai, Y.; Thomas, G.D.; Yue, Y.; Yang, H.T.; Li, D.; Long, C.; Judge, L.; Bostick, B.; Chamberlain, J.S.; Terjung, R.L.; et al. Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J. Clin. Invest. 2009, 119, 624-635.
110. Lai, Y.; Zhao, J.; Yue, Y.; Duan, D. α2 and α3 helices of dystrophin R16 and R17 frame a microdomain in the α1 helix of dystrophin R17 for neuronal NOS binding. Proc. Natl. Acad. Sci. USA 2013, 110, 525-530.
111. Wehling-Henricks, M.; Tidball, J.G. Neuronal nitric oxide synthase-rescue of dystrophin/utrophin double knockout mice does not require nNOS localization to the cell membrane. PLoS One 2011, 6, e25071.
112. Keesey, J.C. Clinical evaluation and management of myasthenia gravis. Muscle Nerve 2004, 29, 484-505.
113. Meinen, S.; Lin, S.; Ruegg, M.A.; Punga, A.R. Fatigue and muscle atrophy in a mouse model of myasthenia gravis is paralleled by loss of sarcolemmal nNOS. PLoS One 2012, 7, e44148.
114. Berchtold, M.W.; Brinkmeier, H.; Muntener, M. Calcium ion in skeletal muscle: Its crucial role for muscle function, plasticity, and disease. Physiol. Rev. 2000, 80, 1215-1265.
115. Grozdanovic, Z.; Baumgarten, H.G. Nitric oxide synthase in skeletal muscle fibers: A signaling component of the dystrophin-glycoprotein complex. Histol. Histopathol. 1999, 14, 243-256.
116. Beltman, J.G.; de Haan, A.; Haan, H.; Gerrits, H.L.; van Mechelen, W.; Sargeant, A.J. Metabolically assessed muscle fibre recruitment in brief isometric contractions at different intensities. Eur. J. Appl. Physiol 2004, 92, 485-492.
117. Reid, M.B. Role of nitric oxide in skeletal muscle: Synthesis, distribution and functional importance. Acta Physiol. Scand. 1998, 162, 401-409.
118. Betzenhauser, M.J.; Marks, A.R. Ryanodine receptor channelopathies. Pflugers Arch. 2010, 460, 467-480.
119. Andersson, D.C.; Betzenhauser, M.J.; Reiken, S.; Meli, A.C.; Umanskaya, A.; Xie, W.; Shiomi, T.; Zalk, R.; LaCampagne, A.; Marks, A.R. Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab 2011, 14, 196-207.
120. Bellinger, A.M.; Reiken, S.; Dura, M.; Murphy, P.W.; Deng, S.X.; Landry, D.W.; Nieman, D.; Lehnart, S.E.; Samaru, M.; LaCampagne, A.; et al. Remodeling of ryanodine receptor complex causes "leaky" channels: A molecular mechanism for decreased exercise capacity. Proc. Natl. Acad. Sci. USA 2008, 105, 2198-2202.
121. Gehlert, S.; Bungartz, G.; Willkomm, L.; Korkmaz, Y.; Pfannkuche, K.; Schiffer, T.; Bloch, W.; Suhr, F. Intense resistance exercise induces early and transient increases in ryanodine receptor 1 phosphorylation in human skeletal muscle. PLoS One 2012, 7, e49326.
122. Bellinger, A.M.; Mongillo, M.; Marks, A.R. Stressed out: The skeletal muscle ryanodine receptor as a target of stress. J. Clin. Invest. 2008, 118, 445-453.
123. Bellinger, A.M.; Reiken, S.; Carlson, C.; Mongillo, M.; Liu, X.; Rothman, L.; Matecki, S.; LaCampagne, A.; Marks, A.R. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat. Med. 2009, 15, 325-330.
124. Sun, J.; Xin, C.; Eu, J.P.; Stamler, J.S.; Meissner, G. Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc. Natl. Acad. Sci. USA 2001, 98, 11158-11162.
125. Suhr, F.; Gehlert, S.; Braun, K.; Bungartz, G.; Kern, P.; Willkomm, L.; Pfannkuche, K.; Krüger, M.; Bloch, W. Institute of Cardiovascular Research and Sport Medicine, German Sport University Cologne, Cologne, Germany. Unpublished work, 2013.
126. Shen, W.; Hintze, T.H.; Wolin, M.S. Nitric oxide. An important signaling mechanism between vascular endothelium and parenchymal cells in the regulation of oxygen consumption. Circulation 1995, 92, 3505-3512.
127. Morrison, R.J.; Miller, C.C., III; Reid, M.B. Nitric oxide effects on shortening velocity and power production in the rat diaphragm. J. Appl. Physiol. 1996, 80, 1065-1069.
128. Perkins, W.J.; Han, Y.S.; Sieck, G.C. Skeletal muscle force and actomyosin ATPase activity reduced by nitric oxide donor. J. Appl. Physiol. 1997, 83, 1326-1332.
129. Marechal, G.; Beckers-Bleukx, G. Effect of nitric oxide on the maximal velocity of shortening of a mouse skeletal muscle. Pflugers Arch. 1998, 436, 906-913.
130. Morrison, R.J.; Miller, C.C., III; Reid, M.B. Nitric oxide effects on force-velocity characteristics of the rat diaphragm. Comp. Biochem. Physiol. A 1998, 119, 203-209.
131. Evangelista, A.M.; Rao, V.S.; Filo, A.R.; Marozkina, N.V.; Doctor, A.; Jones, D.R.; Gaston, B.; Guilford, W.H. Direct regulation of striated muscle myosins by nitric oxide and endogenous nitrosothiols. PLoS One 2010, 5, e11209.
132. Halliwell, B.; Cross, C.E. Oxygen-derived species: Their relation to human disease and environmental stress. Environ. Health Perspect. 1994, 102, 5-12.
133. Vollaard, N.B.; Shearman, J.P.; Cooper, C.E. Exercise-induced oxidative stress: Myths, realities and physiological relevance. Sports Med. 2005, 35, 1045-1062.
134. Boveris, A.; Chance, B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 1973, 134, 707-716.
135. Xia, R.; Webb, J.A.; Gnall, L.L.; Cutler, K.; Abramson, J.J. Skeletal muscle sarcoplasmic reticulum contains a NADH-dependent oxidase that generates superoxide. Am. J. Physiol Cell Physiol. 2003, 285, C215-C221.
136. Espinosa, A.; Leiva, A.; Pena, M.; Muller, M.; Debandi, A.; Hidalgo, C.; Carrasco, M.A.; Jaimovich, E. Myotube depolarization generates reactive oxygen species through NAD(P)H oxidase; ROS-elicited Ca2+ stimulates ERK, CREB, early genes. J. Cell Physiol. 2006, 209, 379-388.
137. Hidalgo, C.; Sanchez, G.; Barrientos, G.; Aracena-Parks, P. A transverse tubule NADPH oxidase activity stimulates calcium release from isolated triads via ryanodine receptor type 1 S-glutathionylation. J. Biol. Chem. 2006, 281, 26473-26482.
138. Sen, C.K.; Packer, L. Antioxidant and redox regulation of gene transcription. FASEB J. 1996, 10, 709-720.
139. Reid, M.B. Invited review: Redox modulation of skeletal muscle contraction: What we know and what we don't. J. Appl. Physiol. 2001, 90, 724-731.
140. Supinski, G.S.; Callahan, L.A. Free radical-mediated skeletal muscle dysfunction in inflammatory conditions. J. Appl. Physiol 2007, 102, 2056-2063.
141. Reid, M.B.; Khawli, F.A.; Moody, M.R. Reactive oxygen in skeletal muscle. III. Contractility of unfatigued muscle. J. Appl. Physiol. 1993, 75, 1081-1087.
142. Ji, L.L.; Stratman, F.W.; Lardy, H.A. Antioxidant enzyme systems in rat liver and skeletal muscle. Influences of selenium deficiency, chronic training, and acute exercise. Arch. Biochem. Biophys. 1988, 263, 150-160.
143. Powers, S.K.; Criswell, D.; Lawler, J.; Ji, L.L.; Martin, D.; Herb, R.A.; Dudley, G. Influence of exercise and fiber type on antioxidant enzyme activity in rat skeletal muscle. Am. J. Physiol. 1994, 266, R375-R380.
144. Criswell, D.; Powers, S.; Dodd, S.; Lawler, J.; Edwards, W.; Renshler, K.; Grinton, S. High intensity training-induced changes in skeletal muscle antioxidant enzyme activity. Med. Sci. Sports Exerc. 1993, 25, 1135-1140.
145. Lawler, J.M.; Kwak, H.B.; Song, W.; Parker, J.L. Exercise training reverses downregulation of HSP70 and antioxidant enzymes in porcine skeletal muscle after chronic coronary artery occlusion. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291, R1756-R1763.
146. Bjornstedt, M.; Xue, J.; Huang, W.; Akesson, B.; Holmgren, A. The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J. Biol. Chem. 1994, 269, 29382-29384.
147. Bjornstedt, M.; Kumar, S.; Bjorkhem, L.; Spyrou, G.; Holmgren, A. Selenium and the thioredoxin and glutaredoxin systems. Biomed. Environ. Sci. 1997, 10, 271-279.
148. Lawler, J.M.; Powers, S.K.; Van, D.H.; Visser, T.; Kordus, M.J.; Ji, L.L. Metabolic and antioxidant enzyme activities in the diaphragm: Effects of acute exercise. Respir. Physiol 1994, 96, 139-149.
149. Karanth, J.; Kumar, R.; Jeevaratnam, K. Response of antioxidant system in rats to dietary fat and physical activity. Indian J. Physiol. Pharmacol. 2004, 48, 446-452.
150. Lambertucci, R.H.; Levada-Pires, A.C.; Rossoni, L.V.; Curi, R.; Pithon-Curi, T.C. Effects of aerobic exercise training on antioxidant enzyme activities and mRNA levels in soleus muscle from young and aged rats. Mech. Ageing Dev. 2007, 128, 267-275.
151. Leeuwenburgh, C.; Fiebig, R.; Chandwaney, R.; Ji, L.L. Aging and exercise training in skeletal muscle: Responses of glutathione and antioxidant enzyme systems. Am. J. Physiol. 1994, 267, R439-R445.
152. Vincent, H.K.; Powers, S.K.; Stewart, D.J.; Demirel, H.A.; Shanely, R.A.; Naito, H. Short-term exercise training improves diaphragm antioxidant capacity and endurance. Eur. J. Appl. Physiol. 2000, 81, 67-74.
153. Tibballs, J. The role of nitric oxide (formerly endothelium-derived relaxing factor-EDRF) in vasodilatation and vasodilator therapy. Anaesth. Intensive Care 1993, 21, 759-773.
154. Hirai, D.M.; Copp, S.W.; Ferguson, S.K.; Holdsworth, C.T.; McCullough, D.J.; Behnke, B.J.; Musch, T.I.; Poole, D.C. Exercise training and muscle microvascular oxygenation: Functional role of nitric oxide. J. Appl. Physiol. 2012, 113, 557-565.
155. Ferguson, S.K.; Hirai, D.M.; Copp, S.W.; Holdsworth, C.T.; Allen, J.D.; Jones, A.M.; Musch, T.I.; Poole, D.C. Impact of dietary nitrate supplementation via beetroot juice on exercising muscle vascular control in rats. J. Physiol. 2013, 591, 547-557.
156. Wolosker, H.; Panizzutti, R.; Engelender, S. Inhibition of creatine kinase by S-nitrosoglutathione. FEBS Lett. 1996, 392, 274-276.
157. Gross, W.L.; Bak, M.I.; Ingwall, J.S.; Arstall, M.A.; Smith, T.W.; Balligand, J.L.; Kelly, R.A. Nitric oxide inhibits creatine kinase and regulates rat heart contractile reserve. Proc. Natl. Acad. Sci. USA 1996, 93, 5604-5609.
158. Wilson, C.M.; Cushman, S.W. Insulin stimulation of glucose transport activity in rat skeletal muscle: Increase in cell surface GLUT4 as assessed by photolabelling. Biochem. J. 1994, 299, 755-759.
159. Youn, J.H.; Gulve, E.A.; Holloszy, J.O. Calcium stimulates glucose transport in skeletal muscle by a pathway independent of contraction. Am. J. Physiol. 1991, 260, C555-C561.
160. Lund, S.; Holman, G.D.; Schmitz, O.; Pedersen, O. Contraction stimulates translocation of glucose transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin. Proc. Natl. Acad. Sci. USA 1995, 92, 5817-5821.
161. Roy, D.; Marette, A. Exercise induces the translocation of GLUT4 to transverse tubules from an intracellular pool in rat skeletal muscle. Biochem. Biophys. Res. Commun. 1996, 223, 147-152.
162. Lemieux, K.; Konrad, D.; Klip, A.; Marette, A. The AMP-activated protein kinase activator AICAR does not induce GLUT4 translocation to transverse tubules but stimulates glucose uptake and p38 mitogen-activated protein kinases alpha and beta in skeletal muscle. FASEB J. 2003, 17, 1658-1665.
163. Etgen, G.J., Jr.; Fryburg, D.A.; Gibbs, E.M. Nitric oxide stimulates skeletal muscle glucose transport through a calcium/contraction-and phosphatidylinositol-3-kinase-independent pathway. Diabetes 1997, 46, 1915-1919.
164. Mohr, S.; Stamler, J.S.; Brune, B. Posttranslational modification of glyceraldehyde-3-phosphate dehydrogenase by S-nitrosylation and subsequent NADH attachment. J. Biol. Chem. 1996, 271, 4209-4214.
165. Brown, G.C. Nitric oxide regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett. 1995, 369, 136-139.
166. Palacios-Callender, M.; Hollis, V.; Frakich, N.; Mateo, J.; Moncada, S. Cytochrome c oxidase maintains mitochondrial respiration during partial inhibition by nitric oxide. J. Cell Sci. 2007, 120, 160-165.
167. Glass, D.J. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat. Cell Biol. 2003, 5, 87-90.
168. Sellman, J.E.; DeRuisseau, K.C.; Betters, J.L.; Lira, V.A.; Soltow, Q.A.; Selsby, J.T.; Criswell, D.S. In vivo inhibition of nitric oxide synthase impairs upregulation of contractile protein mRNA in overloaded plantaris muscle. J. Appl. Physiol. 2006, 100, 258-265.
169. Leiter, J.R.; Upadhaya, R.; Anderson, J.E. Nitric oxide and voluntary exercise together promote quadriceps hypertrophy and increase vascular density in female 18-mo-old mice. Am. J. Physiol. Cell Physiol. 2012, 302, C1306-C1315.
170. Ito, N.; Ruegg, U.T.; Kudo, A.; Miyagoe-Suzuki, Y.; Takeda, S. Activation of calcium signaling through Trpv1 by nNOS and peroxynitrite as a key trigger of skeletal muscle hypertrophy. Nat. Med. 2013, 19, 101-106.
171. Samengo, G.; Avik, A.; Fedor, B.; Whittaker, D.; Myung, K.H.; Wehling-Henricks, M.; Tidball, J.G. Age-related loss of nitric oxide synthase in skeletal muscle causes reductions in calpain S-nitrosylation that increase myofibril degradation and sarcopenia. Aging Cell 2012, 11, 1036-1045.
172. Gundersen, K.; Bruusgaard, J.C. Nuclear domains during muscle atrophy: Nuclei lost or paradigm lost? J. Physiol. 2008, 586, 2675-2681.
173. Qaisar, R.; Renaud, G.; Morine, K.; Barton, E.R.; Sweeney, H.L.; Larsson, L. Is functional hypertrophy and specific force coupled with the addition of myonuclei at the single muscle fiber level? FASEB J. 2012, 26, 1077-1085.
174. Walker, D.K.; Fry, C.S.; Drummond, M.J.; Dickinson, J.M.; Timmerman, K.L.; Gundermann, D.M.; Jennings, K.; Volpi, E.; Rasmussen, B.B. PAX7+ satellite cells in young and older adults following resistance exercise. Muscle Nerve 2012, 46, 51-59.
175. Mackey, A.L.; Esmarck, B.; Kadi, F.; Koskinen, S.O.; Kongsgaard, M.; Sylvestersen, A.; Hansen, J.J.; Larsen, G.; Kjaer, M. Enhanced satellite cell proliferation with resistance training in elderly men and women. Scand. J. Med. Sci. Sports 2007, 17, 34-42.
176. Martins, K.J.; St-Louis, M.; Murdoch, G.K.; MacLean, I.M.; McDonald, P.; Dixon, W.T.; Putman, C.T.; Michel, R.N. Nitric oxide synthase inhibition prevents activity-induced calcineurin-NFATc1 signalling and fast-to-slow skeletal muscle fibre type conversions. J. Physiol. 2012, 590, 1427-1442.
177. Zammit, P.S.; Partridge, T.A.; Yablonka-Reuveni, Z. The skeletal muscle satellite cell: The stem cell that came in from the cold. J. Histochem. Cytochem. 2006, 54, 1177-1191.
178. Friday, B.B.; Pavlath, G.K. A calcineurin-and NFAT-dependent pathway regulates Myf5 gene expression in skeletal muscle reserve cells. J. Cell Sci. 2001, 114, 303-310.
179. Tengan, C.H.; Rodrigues, G.S.; Godinho, R.O. Nitric oxide in skeletal muscle: Role on mitochondrial biogenesis and function. Int. J. Mol. Sci. 2012, 13, 17160-17184.
180. Cerqueira, F.M.; Laurindo, F.R.; Kowaltowski, A.J. Mild mitochondrial uncoupling and calorie restriction increase fasting eNOS, akt and mitochondrial biogenesis. PLoS One 2011, 6, e18433.
181. Hood, D.A. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl. Physiol. Nutr. Metab 2009, 34, 465-472.
182. Hood, D.A. Invited review: Contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol. 2001, 90, 1137-1157.
183. Gomes, E.C.; Silva, A.N.; de Oliveira, M.R. Oxidants, antioxidants, and the beneficial roles of exercise-induced production of reactive species. Oxid. Med. Cell Longev. 2012, 2012, 756132.
184. Jorgensen, S.B.; Richter, E.A.; Wojtaszewski, J.F. Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J. Physiol. 2006, 574, 17-31.
185. Kulisz, A.; Chen, N.; Chandel, N.S.; Shao, Z.; Schumacker, P.T. Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes. Am. J. Physiol. Lung Cell Mol. Physiol. 2002, 282, L1324-L1329.
186. Liu, C.; Lin, J.D. PGC-1 coactivators in the control of energy metabolism. Acta Biochim. Biophys. Sin. (Shanghai) 2011, 43, 248-257.
187. Sriwijitkamol, A.; Coletta, D.K.; Wajcberg, E.; Balbontin, G.B.; Reyna, S.M.; Barrientes, J.; Eagan, P.A.; Jenkinson, C.P.; Cersosimo, E.; DeFronzo, R.A.; et al. Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: A time-course and dose-response study. Diabetes 2007, 56, 836-848.
188. McConell, G.K.; Ng, G.P.; Phillips, M.; Ruan, Z.; Macaulay, S.L.; Wadley, G.D. Central role of nitric oxide synthase in AICAR and caffeine-induced mitochondrial biogenesis in L6 myocytes. J. Appl. Physiol. 2010, 108, 589-595.
189. Wadley, G.D.; Choate, J.; McConell, G.K. NOS isoform-specific regulation of basal but not exercise-induced mitochondrial biogenesis in mouse skeletal muscle. J. Physiol. 2007, 585, 253-262.
190. Clementi, E.; Nisoli, E. Nitric oxide and mitochondrial biogenesis: A key to long-term regulation of cellular metabolism. Comp. Biochem. Physiol. A 2005, 142, 102-110.
191. Mortensen, O.H.; Frandsen, L.; Schjerling, P.; Nishimura, E.; Grunnet, N. PGC-1alpha and PGC-1beta have both similar and distinct effects on myofiber switching toward an oxidative phenotype. Am. J. Physiol. Endocrinol. Metab 2006, 291, E807-E816.
192. Gehlert, S.; Weber, S.; Weidmann, B.; Gutsche, K.; Platen, P.; Graf, C.; Kappes-Horn, K.; Bloch, W. Cycling exercise-induced myofiber transitions in skeletal muscle depend on basal fiber type distribution. Eur. J. Appl. Physiol. 2011, 112, 2393-2402.
193. Murgia, M.; Serrano, A.L.; Calabria, E.; Pallafacchina, G.; Lomo, T.; Schiaffino, S. Ras is involved in nerve-activity-dependent regulation of muscle genes. Nat. Cell Biol. 2000, 2, 142-147.
194. Calabria, E.; Ciciliot, S.; Moretti, I.; Garcia, M.; Picard, A.; Dyar, K.A.; Pallafacchina, G.; Tothova, J.; Schiaffino, S.; Murgia, M. NFAT isoforms control activity-dependent muscle fiber type specification. Proc. Natl. Acad. Sci. USA 2009, 106, 13335-13340.
195. Drenning, J.A.; Lira, V.A.; Simmons, C.G.; Soltow, Q.A.; Sellman, J.E.; Criswell, D.S. Nitric oxide facilitates NFAT-dependent transcription in mouse myotubes. Am. J. Physiol. Cell Physiol. 2008, 294, C1088-C1095.