High energy phosphate concentrations and AMPK phosphorylation in skeletal muscle from mice with inherited differences in hypoxic exercise tolerance

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 152, Issue 4, 2009, Pages 478-485

  Overton, Jeffrey D ^a   Adams, Glenn S ^a   McCall, R Dale ^a   Kinsey, Stephen T ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

AMPK; ATP; Energetics; Exercise; Hypoxia; Mouse; Muscle; Phosphocreatine

Indexed keywords

ANIMALIA; MUS;

EID: 60449112228     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2008.11.019     Document Type: Article

References (58)

1. Allen P.S., and Westerblad H. Roles of phosphate and calcium stores in muscle fatigue. J. Physiol. 536 (2001) 657-665
2. Allen P.S., Matheson G.O., Zhu G., Gheorgiu D., Dunlop R.S., Falconer T., Stanley C., and Hochachka P.W. Simultaneous 31P MRS of the soleus and gastrocnemius in Sherpas during graded calf muscle exercise. Am. J. Physiol. 273 (1997) R999-1007
3. Argov Z., Nagle D., Giger U., and Leigh Jr. J.S. Muscle bio-energetics in acute glycolytic block: in vivo phosphorus-nuclear magnetic resonance study of iodo-acetate injected rats. Eur. J. Appl. Physiol. Occup. Physiol. 58 (1989) 808-815
4. Arthur P.G., Hogan M.C., Bebou D.E., Wagner P.D., and Hochachka P.W. Modeling the effects of hypoxia on ATP turnover in exercising muscle. J. Appl. Physiol. 73 (1992) 737-742
5. Bernus G., Gonzalez de Suso J.M., Alonso J., Martin P.A., Prat J.A., and Arus C. 31P-MRS of quadriceps reveals quantitative differences between sprinters and long-distance runners. Med. Sci. Sports. Exerc. 25 (1993) 479-484
6. Brooks G.A., Butterfield G.E., Wolfe R.R., Groves B.M., Mazzeo R.S., Sutton J.R., Wolfel E.E., and Reeves J.T. Increased dependence on blood glucose after acclimatization to 4,300 m. J. Appl. Physiol. 70 (1991) 919-927
7. Brooks G.A., Wolfel E.E., Groves B.M., Bender P.R., Butterfield G.E., Cymerman A., Mazzeo R.S., Sutton J.R., Wolfe R.R., and Reeves J.T. Muscle accounts for glucose disposal but not blood lactate appearance during exercise after acclimatization to 4,300 m. J. Appl. Physiol. 72 (1992) 2435-2445
8. Dunnett M., Harris R.C., and Orme C.E. Reverse-phase ion-pairing high-performance liquid chromatography of phosphocreatine, creatine and creatinine in equine muscle. Scand. J. Clin. Lab. Invest. 51 (1991) 137-141
9. Fewell J.G., and Moerland T.S. Responses of mouse fast and slow skeletal muscle to streptozotocin diabetes: myosin isoenzymes and phosphorous metabolites. Mol. Cell. Biochem. 148 (1995) 147-154
10. Fujii N., Hayashi T., Hirshman M.F., Smith J.T., Habinowski S.A., Kaijser L., Mu J., Ljungqvist O., Birnbaum M.J., Witters L.A., et al. Exercise induces isoform-specific increase in 5′AMP-activated protein kinase activity in human skeletal muscle. Biochem. Biophys. Res. Commun. 273 (2000) 1150-1155
11. Green H., Roy B., Grant S., Burnett M., Tupling R., Otto C., Pipe A., and McKenzie D. Downregulation in muscle Na(+)-K(+)-ATPase following a 21-day expedition to 6,194 m. J. Appl. Physiol. 88 (2000) 634-640
12. Green H., Roy B., Grant S., Tupling R., Otto C., Pipe A., McKenzie D., and Ouyang J. Effects of a 21-day expedition to 6,194 m on human skeletal muscle SR Ca2+-ATPase. High Alt. Med. Biol. 1 (2000) 301-310
13. Green H.J., Sutton J.R., Cymerman A., Young P.M., and Houston C.S. Operation Everest II: adaptations in human skeletal muscle. J. Appl. Physiol. 66 (1989) 2454-2461
14. Green H.J., Sutton J.R., Wolfel E.E., Reeves J.T., Butterfield G.E., and Brooks G.A. Altitude acclimatization and energy metabolic adaptations in skeletal muscle during exercise. J. Appl. Physiol. 73 (1992) 2701-2708
15. Hardie D.G. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144 (2003) 5179-5183
16. Hardie D.G., Salt I.P., Hawley S.A., and Davies S.P. AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem. J. 338 (1999) 717-722
17. Hochachka, P.W., and Matheson, G.O., submitted for publication. Regulating ATP turnover rates over broad dynamic work ranges in skeletal muscles. J. Appl. Physiol. 1992. 5,1697-703. Review.
18. Hochachka P.W., Bianconcini M.S., Parkhouse W.S., and Dobson G.P. On the role of actomyosin ATPases in regulation of ATP turnover rates during intense exercise. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 5764-5768
19. Hochachka, P.W., Buck, L.T., Doll, C.J., and Land, S.C., submitted for publication. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc. Natl. Acad. Sci. U. S. A. 93, 9493-8. Review.
20. Hochachka P.W., Clark C.M., Holden J.E., Stanley C., Ugurbil K., and Menon R.S. 31P magnetic resonance spectroscopy of the Sherpa heart: a phosphocreatine/adenosine triphosphate signature of metabolic defense against hypobaric hypoxia. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 1215-1220
21. Hochachka P.W., Rupert J.L., and Monge C. Adaptation and conservation of physiological systems in the evolution of human hypoxia tolerance. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 124 (1999) 1-17
22. Hoppeler H., and Vogt M. Muscle tissue adaptations to hypoxia. J. Exp. Biol. 204 (2001) 3133-3139
23. Hutber C.A., Hardie D.G., and Winder W.W. Electrical stimulation inactivates muscle acetyl-CoA carboxylase and increases AMP-activated protein kinase. Am. J. Physiol. 272 (1997) E262-266
24. Ingwall J.S., and Weiss R.G. Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ. Res. 95 (2004) 135-145
25. Jeneson J.A., Westerhoff H.V., and Kushmerick M.J. A metabolic control analysis of kinetic controls in ATP free energy metabolism in contracting skeletal muscle. Am. J. Physiol. Cell. Physiol. 279 (2000) C813-832
26. Kinsey S.T., and Moerland T.S. The use of NMR for examining intracellular pH in living systems (1999), Cambridge University Press
27. Kurth-Kraczek E.J., Hirshman M.F., Goodyear L.J., and Winder W.W. 5′ AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48 (1999) 1667-1671
28. Kushmerick M.J., Meyer R.A., and Brown T.R. Regulation of oxygen consumption in fast- and slow-twitch muscle. Am. J. Physiol. 263 (1992) C598-606
29. Kushmerick M.J., Moerland T.S., and Wiseman R.W. Mammalian skeletal muscle fibers distinguished by contents of phosphocreatine, ATP, and Pi. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 7521-7525
30. Lawson J.W., and Veech R.L. Effects of pH and free Mg2+ on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J. Biol. Chem. 254 (1979) 6528-6537
31. Lessard S.J., Chen Z.P., Watt M.J., Hashem M., Reid J.J., Febbraio M.A., Kemp B.E., and Hawley J.A. Chronic rosiglitazone treatment restores AMPKalpha2 activity in insulin-resistant rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 290 (2006) E251-257
32. Luedeke J.D., McCall R.D., Dillaman R.M., and Kinsey S.T. Properties of slow- and fast-twitch skeletal muscle from mice with an inherited capacity for hypoxic exercise. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 138 (2004) 373-382
33. Marconi C., Marzorati M., Sciuto D., Ferri A., and Cerretelli P. Economy of locomotion in high-altitude Tibetan migrants exposed to normoxia. J. Physiol. 569 (2005) 667-675
34. Matheson G.O., Allen P.S., Ellinger D.C., Hanstock C.C., Gheorghiu D., McKenzie D.C., Stanley C., Parkhouse W.S., and Hochachka P.W. Skeletal muscle metabolism and work capacity: a 31P-NMR study of Andean natives and lowlanders. J. Appl. Physiol. 70 (1991) 1963-1976
35. McCall R.D., and Frierson Jr. D. Inheritance of hypoxic exercise tolerance in mice. Behav. Genet. 27 (1997) 181-190
36. McClelland G.B., Hochachka P.W., and Weber J.M. Carbohydrate utilization during exercise after high-altitude acclimation: a new perspective. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 10288-10293
37. McLester Jr. J.R. Muscle contraction and fatigue. The role of adenosine 5′-diphosphate and inorganic phosphate. Sports Med. 23 (1997) 287-305
38. Meyer R.A., Brown T.R., and Kushmerick M.J. Phosphorus nuclear magnetic resonance of fast- and slow-twitch muscle. Am. J. Physiol. 248 (1985) C279-287
39. Mitani A., Takeyasu S., Yanase H., Nakamura Y., and Kataoka K. Changes in intracellular Ca2+ and energy levels during in vitro ischemia in the gerbil hippocampal slice. J. Neurochem. 62 (1994) 626-634
40. Mu J., Brozinick Jr. J.T., Valladares O., Bucan M., and Birnbaum M.J. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol. Cell. 7 (2001) 1085-1094
41. Ou L.C., and Leiter J.C. Effects of exposure to a simulated altitude of 5500 m on energy metabolic pathways in rats. Respir. Physiol. Neurobiol. 141 (2004) 59-71
42. Roberts A.C., Butterfield G.E., Cymerman A., Reeves J.T., Wolfel E.E., and Brooks G.A. Acclimatization to 4,300-m altitude decreases reliance on fat as a substrate. J. Appl. Physiol. 81 (1996) 1762-1771
43. Roberts A.C., Reeves J.T., Butterfield G.E., Mazzeo R.S., Sutton J.R., Wolfel E.E., and Brooks G.A. Altitude and beta-blockade augment glucose utilization during submaximal exercise. J. Appl. Physiol. 80 (1996) 605-615
44. Saggerson D., Ghadiminejad I., and Awan M. Regulation of mitochondrial carnitine palmitoyl transferases from liver and extrahepatic tissues. Adv. Enzyme Regul. 32 (1992) 285-306
45. Sakamoto K., Göransson O., Hardie D.G., and Alessi D.R. Activity of LKB1 and AMPK-related kinases in skeletal muscle: effects of contraction, phenformin, and AICAR. Am. J. Physiol. Endocrinol. Metab. 287 (2004) E310-317
46. Schunk K., Losch O., Kreitner K.F., Kersjes W., Schadmand-Fischer S., and Thelen M. Contributions of dynamic phosphorus-31 magnetic resonance spectroscopy to the analysis of muscle fiber distribution. Invest. Radiol. 34 (1999) 348-356
47. Ten Hove M., and Neubauer S. MR spectroscopy in heart failure-clinical and experimental findings. Heart Fail. Rev. 12 (2007) 48-57
48. Terjung R.L., Dudley G.A., and Meyer R.A. Metabolic and circulatory limitations to muscular performance at the organ level. J. Exp. Biol. 115 (1985) 307-318
49. Thomson D.M., Porter B.B., Tall J.H., Kim H.J., Barrow J.R., and Winder W.W. Skeletal muscle and heart LKB1 deficiency causes decreased voluntary running and reduced muscle mitochondrial marker enzyme expression in mice. Am. J. Physiol. Endocrinol. Metab. 292 1 (2007) E196-202
50. Vavvas D., Apazidis A., Saha A.K., Gamble J., Patel A., Kemp B.E., Witters L.A., and Ruderman N.B. Contraction-induced changes in acetyl-CoA carboxylase and 5′-AMP-activated kinase in skeletal muscle. J. Biol. Chem. 272 (1997) 13255-13261
51. Wadley G.D., Lee-Young R.S., Canny B.J., Wasuntarawat C., Chen Z.P., Hargreaves M., Kemp B.E., and McConell G.K. Effect of exercise intensity and hypoxia on skeletal muscle AMPK signaling and substrate metabolism in humans. Am. J. Physiol. Endocrinol. Metab. 290 (2006) E694-702
52. Westerblad H., and Allen D.G. The effects of intracellular injections of phosphate on intracellular calcium and force in single fibres of mouse skeletal muscle. Pflugers Arch. 431 (1996) 964-970
53. Westerblad H., Allen D.G., Bruton J.D., Andrade F.H., and Lannergren J. Mechanisms underlying the reduction of isometric force in skeletal muscle fatigue. Acta Physiol. Scand. 162 (1998) 253-260
54. Westerblad H., Lee J.A., Lannergren J., and Allen D.G. Cellular mechanisms of fatigue in skeletal muscle. Am. J. Physiol. 261 (1991) C195-209
55. 2 and leg blood flow during submaximal exercise. J. Appl. Physiol. 87(2) (1999) 643-651
56. Winder W.W., and Hardie D.G. Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am. J. Physiol. 270 (1996) E299-304
57. Winder W.W., and Hardie D.G. AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am. J. Physiol. 277 (1999) E1-10
58. Wojtaszewski J.F., MacDonald C., Nielsen J.N., Hellsten Y., Hardie D.G., Kemp B.E., Kiens B., and Richter E.A. Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 284 (2003) E813-822