Similar mitochondrial activation kinetics in wild-type and creatine kinase-deficient fast-twitch muscle indicate significant Pi control of respiration

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 6, 2011, Pages 1316-1325

  Jeneson, Jeroen A L ^a,b   Veld, Frank Ter ^b   Schmitz, Joep P J ^a   Meyer, Ronald A ^c   Hilbers, Peter A J ^a   Nicolay, Klaas ^a  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Computational modeling; Metabolic control; Mitochondria; Skeletal muscle

Indexed keywords

ADENOSINE TRIPHOSPHATE; MITOCHONDRIAL CREATINE KINASE;

ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CELL KINETICS; CELL METABOLISM; ELECTROSTIMULATION; FAST MUSCLE; FEEDBACK SYSTEM; IN VITRO STUDY; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE FIBRIL; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN DIFFUSION; PHENOTYPE; PRIORITY JOURNAL;

EID: 79958774888     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00204.2010     Document Type: Article

References (31)

1. Balaban RS. Domestication of the cardiac mitochondrion for energy conversion. J Mol Cell Cardiol 46: 832-841, 2009.
2. Blei ML, Conley KE, Kushmerick MJ. Separate measures of ATP utilization and recovery in human skeletal muscle. J Physiol 465: 203-222, 1993.
3. Bose S, French S, Evans FJ, Joubert F, Balaban RS. Metabolic network control of oxidative phosphorylation: multiple roles of inorganic phosphate. J Biol Chem 278: 39155-39165, 2003.
4. Brand MD. The efficiency and plasticity of mitochondrial energy trans-duction. Biochem Soc Trans 33: 897-904, 2005.
5. Chance B, Im J, Nioka S, Kushmerick MJ. Skeletal muscle energetics with PNMR: personal views and historic perspectives. NMR Biomed 19: 904-926, 2006.
6. Dahlstedt AJ, Katz A, Westerblad H. Role of myoplasmic phosphate in contractile function of skeletal muscle: studies on creatine kinase-deficient mice. J Physiol 533: 379-388, 2001.
7. Grote J, Thews G. [Requirements for the oxygen supply of heart muscle tissue.]. Pflügers Arch 276: 142-165, 1962.
8. Haller T, Ortner M, Gnaiger E. A respirometer for investigating oxi-dative cell metabolism: toward optimization of respiratory studies. Anal Biochem 218: 338-342, 1994.
9. Hancock CR, Brault JJ, Wiseman RW, Terjung RL, Meyer RA. 31P-NMR observations of free ADP during fatiguing, repetitive contractions of murine skeletal muscle lacking AK-1. Am J Physiol Cell Physiol 288: C1298-C1304, 2005.
10. Hunter P, Nielsen P. A strategy for integrative computational physiology. Physiology 20, 316-325, 2005.
11. Jeneson JA, de Snoo MW, Verlinden NA, Joosten BJ, Doornenbal A, Schot A, Everts ME. Treadmill but not wheel running improves fatigue resistance of isolated extensor digitorum longus muscle in mice. Acta Physiol (Oxf) 190: 151-161, 2007.
12. Jeneson JA, Schmitz JP, van den Broek NA, van Riel NA, Hilbers PA, Nicolay K, Prompers JJ. Magnitude and control of mitochondrial ADP sensitivity. Am J Physiol Endocrinol Metab 297: E774-E784, 2009.
13. Jeneson JA, Westerhoff HV, Kushmerick MJ. A metabolic control analysis of kinetic controls in ATP free energy metabolism in contracting skeletal muscle. Am J Physiol Cell Physiol 279: C813-C832, 2000.
14. Jeneson JA, Wiseman RW, Westerhoff HV, Kushmerick MJ. The signal transduction function for oxidative phosphorylation is at least second order in ADP. J Biol Chem 271: 27995-27998, 1996.
15. Kushmerick MJ. Energy balance in muscle activity: simulations of ATPase coupled to oxidative phosphorylation and to creatine kinase. Comp Biochem Physiol B Biochem Mol Biol 120: 109-123, 1998.
16. Kushmerick MJ, Meyer RA, Brown TR. Regulation of oxygen consumption in fast- and slow-twitch muscle. Am J Physiol Cell Physiol 263: C598-C606, 1992.
17. Kushmerick MJ, Moerland TS, Wiseman RW. Mammalian skeletal muscle fibers distinguished by contents of phosphocreatine, ATP, and Pi. Proc Natl Acad Sci USA 89: 7521-7525, 1993.
18. Mast F, Elzinga G. Time course of aerobic recovery after contraction of rabbit papillary muscle. Am J Physiol Heart Circ Physiol 253: H325-H332, 1987.
19. Meyer RA. Linear dependence of muscle phosphocreatine kinetics on total creatine content. Am J Physiol Cell Physiol 257: C1149-C1157, 1989.
20. Meyer RA, Sweeney HL, Kushmerick MJ. A simple analysis of the "phosphocreatine shuttle". Am J Physiol Cell Physiol 246: C365-C377, 1984.
21. Moerland TS, Kushmerick MJ. Contractile economy and aerobic recovery metabolism in skeletal muscle adapted to creatine depletion. Am J Physiol Cell Physiol 267: C127-C137, 1994.
22. Roman BB, Meyer RA, Wiseman RW. Phosphocreatine kinetics at the onset of contractions in skeletal muscle of MM creatine kinase knockout mice. Am J Physiol Cell Physiol 283: C1776-C1783, 2002.
23. 2+ responses in muscles with combined mitochondrial and cytosolic creatine kinase deficiencies. Cell 89: 93-103, 1997.
24. Steeghs K, Oerlemans FF, de Haan A, Heerschap A, Verdoodt L, de Bie M, Ruitenbeek W, Benders A, Jost C, van Deursen J, Tulsson P, Terjung R, Jap P, Jacob W, Pette D, Wieringa B. Cytoarchitectural and metabolic adaptations in muscles with mitochondrial and cytosolic crea-tine kinase deficiencies. Mol Cell Biochem 184: 183-194, 1998.
25. Sweeney HL. The importance of the creatine kinase reaction: the concept of metabolic capacitance. Med Sci Sports Exerc 26: 30-36, 1994.
26. Ter Veld F, Nicolay K, Jeneson JA. Increased resistance to fatigue in creatine kinase deficient muscle is not due to improved contractile economy. Pflügers Arch 452: 342-348, 2006.
27. Van den Broek NM, de Feyter HM, de Graaf L, Nicolay K, Prompers JJ. Intersubject differences in the effect of acidosis on phosphocreatine recovery kinetics in muscle after exercise are due to differences in proton efflux rate. Am J Physiol Cell Physiol 293: C228-C237, 2007.
28. Van Stiphout RG, van Riel NA, Verhoog PJ, Hilbers PA, Nicolay K, Jeneson JA. Computational model of excitable cell indicates ATP free energy dynamics in response to calcium oscillations are undampened by cytosolic ATP buffers. IEE Proc Syst Biol 153: 405-408, 2006.
29. Wiseman RW, Beck TW, Chase PB. Effect of intracellular pH on force development depends on temperature in intact skeletal muscle from mouse. Am J Physiol Cell Physiol 271: C878-C886, 1996.
30. Wu F, Jeneson JA, Beard DA. Oxidative ATP synthesis in skeletal muscle is controlled by substrate feedback. Am J Physiol Cell Physiol 292: C115-C124, 2007.
31. Wu F, Zhang J, Beard DA. Experimentally observed phenomena on cardiac energetics in heart failure emerge from simulations of cardiac metabolism. Proc Natl Acad Sci USA 106: 7143-7148, 2009.