Combined in vivo and in silico investigations of activation of glycolysis in contracting skeletal muscle

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 2, 2013, Pages

  Schmitz, J P J ^a   Groenendaal, W ^a   Wessels, B ^a   Wiseman, R W ^b,c   Hilbers, P A J ^a   Nicolay, K ^a   Prompers, J J ^a   Jeneson, J A L ^a,d   van Riel, N V W ^a  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Michigan State University   (United States)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Calcium regulation; Computational modeling; Glycolysis; Skeletal muscle; Systems biology

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CREATINE PHOSPHATE;

ANIMAL EXPERIMENT; ARTICLE; BIOCHEMISTRY; COMPUTER MODEL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GLYCOLYSIS; IN VIVO STUDY; MALE; MUSCLE CONTRACTION; NONHUMAN; PH; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RAT; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE;

RATTUS;

EID: 84872389908     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00101.2012     Document Type: Article

References (56)

1. Akaike H. New look at statistical-model identification. IEEE Trans Automat Contr AC19: 716-723, 1974.
2. 2+ binding sites of calmodulin from bovine testis using 43Ca and 113Cd NMR. Eur J Biochem 126: 501-505, 1982.
3. Bakker BM, van EK, Jeneson JA, van Riel NA, Bruggeman FJ, Teusink B. Systems biology from micro-organisms to human metabolic diseases: the role of detailed kinetic models. Biochem Soc Trans 38: 1294-1301, 2010.
4. + movements within the sarcomere of fast-twitch mouse fibers stimulated by action potentials. J Gen Physiol 130: 283-302, 2007.
5. + and calmodulin. Int J Biochem 25: 297-305, 1993.
6. Blei ML, Conley KE, Kushmerick MJ. Separate measures of ATP utilization and recovery in human skeletal muscle. J Physiol 465: 203-222, 1993.
7. +. J Biol Chem 246: 1961-1967, 1971.
8. Chance B, Im J, Nioka S, Kushmerick M. Skeletal muscle energetics with PNMR: personal views and historic perspectives. NMR Biomed 19: 904-926, 2006.
9. Conley KE, Blei ML, Richards TL, Kushmerick MJ, Jubrias SA. Activation of glycolysis in human muscle in vivo. Am J Physiol Cell Physiol 273: C306-C315, 1997.
10. Connett RJ. Glycolytic regulation during an aerobic rest-to-work transition in dog gracilis muscle. J Appl Physiol 63: 2366-2374, 1987.
11. Costa LT, Da SD, Guimaraes CR, Zancan P, Sola-Penna M. Lactate favours the dissociation of skeletal muscle 6-phosphofructo-1-kinase tetramers down-regulating the enzyme and muscle glycolysis. Biochem J 408: 123-130, 2007.
12. Crowther GJ, Carey MF, Kemper WF, Conley KE. Control of glycolysis in contracting skeletal muscle. I. Turning it on. Am J Physiol Endocrinol Metab 282: E67-E73, 2002.
13. Crowther GJ, Gronka RK. Fiber recruitment affects oxidative recovery measurements of human muscle in vivo. Med Sci Sports Exerc 34: 1733-1737, 2002.
14. Crowther GJ, Kemper WF, Carey MF, Conley KE. Control of glycolysis in contracting skeletal muscle. II. Turning it off. Am J Physiol Endocrinol Metab 282: E74-E79, 2002.
15. Dawson MJ, Gadian DG, Wilkie DR. Studies of the biochemistry of contracting and relaxing muscle by the use of 31P n.m.r. in conjunction with other techniques. Philos Trans R Soc Lond B Biol Sci 289: 445-455, 1980.
16. De Feyter HM. Lipids & Mitochondria in Diabetic Muscle (PhD Thesis). Eindhoven, The Netherlands Univ of Technology, 2007.
17. De Feyter HM, Lenaers E, Houten SM, Schrauwen P, Hesselink MK, Wanders RJ, Nicolay K, Prompers JJ. Increased intramyocellular lipid content but normal skeletal muscle mitochondrial oxidative capacity throughout the pathogenesis of type 2 diabetes. FASEB J 22: 3947-3955, 2008.
18. Eagle GR, Scopes RK. Control of substrate cycling at fructose phosphates in a reconstituted muscle glycolytic system. Arch Biochem Biophys 208: 593-601, 1981.
19. Forbes SC, Paganini AT, Slade JM, Towse TF, Meyer RA. Phosphocreatine recovery kinetics following low- and high-intensity exercise in human triceps surae and rat posterior hindlimb muscles. Am J Physiol Regul Integr Comp Physiol 296: R161-R170, 2009.
20. Fothergill-Gilmore LA, Michels PA. Evolution of glycolysis. Prog Biophys Mol Biol 59: 105-235, 1993.
21. +/calmodulin-dependent protein kinase II produce opposing effects on the affinity of calmodulin for calcium. J Biol Chem 279: 39374-39382, 2004.
22. Gevers W, Dowdle E. The effect of pH on glycolysis in vitro. Clin Sci 25: 343-349, 1963.
23. Glass-Marmor L, Beitner R. Detachment of glycolytic enzymes from cytoskeleton of melanoma cells induced by calmodulin antagonists. Eur J Pharmacol 328: 241-248, 1997.
24. 2+-induced changes in energy metabolism and viability of melanoma cells. Br J Cancer 81: 219-224, 1999.
25. Groenendaal W. Spatiotemporal Skeletal Muscle Dynamics; Experimental Observations and Numerical Analyses (PhD Thesis). Eindhoven, The Netherlands: Univ of Technology, 2011.
26. Groenendaal W, Jeneson JA, Verhoog PJ, van Riel NA, Ten Eikelder HM, Nicolay K, Hilbers PA. Computational modelling identifies the impact of subtle anatomical variations between amphibian and mammalian skeletal muscle on spatiotemporal calcium dynamics. IET Syst Biol 2: 411-422, 2008.
27. Houtman CJ, Heerschap A, Zwarts MJ, Stegeman DF. PH heterogeneity in tibial anterior muscle during isometric activity studied by (31)PNMR spectroscopy. J Appl Physiol 91: 191-200, 2001.
28. Houtman CJ, Heerschap A, Zwarts MJ, Stegeman DF. An additional phase in PCr use during sustained isometric exercise at 30% MVC in the tibialis anterior muscle. NMR Biomed 15: 270-277, 2002.
29. + binding sites of calmodulin. J Biol Chem 271: 761-767, 1996.
30. Koren-Schwartzer N, Chen-Zion M, Ben-Porat H, Beitner R. Serotonin- induced decrease in brain ATP, stimulation of brain anaerobic glycolysis and elevation of plasma hemoglobin; the protective action of calmodulin antagonists. Gen Pharmacol 25: 1257-1262, 1994.
31. Krause U, Wegener G. Control of glycolysis in vertebrate skeletal muscle during exercise. Am J Physiol Regul Integr Comp Physiol 270: R821-R829, 1996.
32. Landowne D, Ritchie JM. On the control of glycogenolysis in mammalian nervous tissue by calcium. J Physiol 212: 503-517, 1971.
33. Lilling G, Beitner R. Altered allosteric properties of cytoskeleton-bound phosphofructokinase in muscle from mice with X chromosome-linked muscular dystrophy (mdx). Biochem Med Metab Biol 45: 319-325, 1991.
34. Maltin CA, Delday MI, Baillie AG, Grubb DA, Garlick PJ. Fiber-type composition of nine rat muscles. I. Changes during the first year of life. Am J Physiol Endocrinol Metab 257: E823-E827, 1989.
35. Marinho-Carvalho MM, Costa-Mattos PV, Spitz GA, Zancan P, Sola-Penna M. Calmodulin upregulates skeletal muscle 6-phosphofructo- 1-kinase reversing the inhibitory effects of allosteric modulators. Biochim Biophys Acta 1794: 1175-1180, 2009.
36. Marinho-Carvalho MM, Zancan P, Sola-Penna M. Modulation of 6-phosphofructo-1-kinase oligomeric equilibrium by calmodulin: formation of active dimers. Mol Genet Metab 87: 253-261, 2006.
37. Moreno-Sanchez R, Marin-Hernandez A, Gallardo-Perez JC, Quezada H, Encalada R, Rodriguez-Enriquez S, Saavedra E. Phosphofructokinase type 1 kinetics, isoform expression, and gene polymorphisms in cancer cells. J Cell Biochem 113: 1692-1703, 2012.
38. Pelicano H, Martin DS, Xu RH, Huang P. Glycolysis inhibition for anticancer treatment. Oncogene 25: 4633-4646, 2006.
39. Penso J, Beitner R. Detachment of glycolytic enzymes from cytoskeleton of Lewis lung carcinoma and colon adenocarcinoma cells induced by clotrimazole and its correlation to cell viability and morphology. Mol Genet Metab 1853-1858, 199576: 181-188, 2002.
40. Peters SJ, Spriet LL. Skeletal muscle phosphofructokinase activity examined under physiological conditions in vitro. J Appl Physiol 78:.
41. Prompers JJ, Jeneson JA, Drost MR, Oomens CC, Strijkers GJ, Nicolay K. Dynamic MRS and MRI of skeletal muscle function and biomechanics. NMR Biomed 19: 927-953, 2006.
42. Quistorff B, Johansen L, Sahlin K. Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. Biochem J 291. 681-686, 1993.
43. Romano AH, Conway T. Evolution of carbohydrate metabolic pathways. Res Microbiol 147: 448-455, 1996.
44. Rovira J, Irimia JM, Guerrero M, Cadefau JA, Cusso R. Upregulation of heart PFK-2/FBPase-2 isozyme in skeletal muscle after persistent contraction. Pflügers Arch 463: 603-613, 2012.
45. Saucerman JJ, Bers DM. Calmodulin mediates differential sensitivity of CaMKII and calcineurin to local Ca2+ in cardiac myocytes. Biophys J 95: 4597-4612, 2008.
46. Schmitz JP, van Riel NA, Nicolay K, Hilbers PA, Jeneson JA. Silencing of glycolysis in muscle: experimental observation and numerical analysis. Exp Physiol 95: 380-397, 2010.
47. Schuster S, Fell DA, Dandekar T. A general definition of metabolic pathways useful for systematic organization and analysis of complex metabolic networks. Nat Biotechnol 18: 326-332, 2000.
48. +) ionophore A23187 and calmodulin antagonists on regulatory mechanisms of glycolysis and cell viability of NIH-3T3 fibroblasts. Mol Genet Metab 67: 334-342, 1999.
49. Taylor DJ, Styles P, Matthews PM, Arnold DA, Gadian DG, Bore P, Radda GK. Energetics of human muscle: exercise-induced ATP depletion. Magn Reson Med 3: 44-54, 1986.
50. Tobin RB, Mackerer CR, Mehlman MA. pH effects on oxidative phosphorylation of rat liver mitochondria. Am J Physiol 223: 83-88, 1972.
51. Trivedi B, Danforth WH. Effect of pH on the kinetics of frog muscle phosphofructokinase. J Biol Chem 241: 4110-4112, 1966.
52. Vanhamme L, van den BA, Van HS. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129: 35-43, 1997.
53. Veech RL, Lawson JW, Cornell NW, Krebs HA. Cytosolic phosphorylation potential. J Biol Chem 254: 6538-6547, 1979.
54. Vinnakota KC, Rusk J, Palmer L, Shankland E, Kushmerick MJ. Common phenotype of resting mouse extensor digitorum longus and soleus muscles: equal ATPase and glycolytic flux during transient anoxia. J Physiol 588: 1961-1983, 2010.
55. Walter G, Vandenborne K, Elliott M, Leigh JS. In vivo ATP synthesis rates in single human muscles during high intensity exercise. J Physiol 519: 901-910, 1999.
56. Waser MR, Garfinkel L, Kohn MC, Garfinkel D. Computer modeling of muscle phosphofructokinase kinetics. J Theor Biol 103: 295-312, 1983.