Oscillations in energy metabolism

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 8, 2010, Pages 1353-1361

  Iotti, Stefano ^a,b   Borsari, Marco ^c   Bendahan, David ^d  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^d CNRS   (France)

Author keywords

Dissipative system; Energy metabolism; Magnetic resonance spectroscopy; Mathematical model; Metabolic dynamics; Metabolic instability; Mitochondrial oscillation

Indexed keywords

CREATINE PHOSPHATE; REACTIVE OXYGEN METABOLITE;

ANIMAL TISSUE; CELL PH; CHEMICAL REACTION; CONTROLLED STUDY; CYTOSOL; ENERGY METABOLISM; EXERCISE RECOVERY; HUMAN; HUMAN CELL; HUMAN TISSUE; MATHEMATICAL MODEL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OSCILLATION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE;

ANIMALS; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; PHOSPHOCREATINE;

ANIMALIA;

EID: 77953809512     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.02.019     Document Type: Review

References (92)

1. Nicolis G., Prigogine I. Self-Organization in Non-Equilibrium Systems: From Dissipative Structures to Order Thorough Fluctuations 1977, J. Wiley & Sons, New York.
2. Sel'kov E.E. Stabilization of energy charge, generation of oscillations and multiple steady states in energy metabolism as a result of purely stoichiometric regulation. Eur. J. Biochem. 1975, 59:151-157.
3. Liebermeister W. Response to temporal parameter fluctuations in biochemical networks. J. Theor. Biol. 2005, 234:423-438.
4. Cortassa S., Aon M.A., Winslow R.L., O'Rourke B. A mitochondrial oscillator dependent on reactive oxygen species. Biophys. J. 2004, 87:2060-2073.
5. Romashko D.N., Marban E., O'Rourke B. Subcellular metabolic transients and mitochondrial redox waves in heart cells. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:1618-1623.
6. Gooch V.D., Parker L. Adenine nucleotide control of heart mitochondrial oscillations. Biochim. Biophys. Acta 1971, 245:17-20.
7. Gooch V.D., Parker L. Oscillatory states of mitochondria. Studies on the oscillatory mechanism of liver and heart mitochondria. Arch. Biochem. Biophys. 1974, 163:759-768.
8. O'Rourke B., Ramza B.M., Marban E. Oscillations of membrane current and excitability driven by metabolic oscillations in heart cells. Science 1994, 265:962-966.
9. Mironov S.L., Richter D.W. Oscillations and hypoxic changes of mitochondrial variables in neurons of the brainstem respiratory centre of mice. J. Physiol. 2001, 533:227-236.
10. Vergun O., Votyakova T.V., Reynolds I.J. Spontaneous changes in mitochondrial membrane potential in single isolated brain mitochondria. Biophys. J. 2003, 85:3358-3366.
11. Vergun O., Reynolds I.J. Distinct characteristics of Ca(2+)-induced depolarization of isolated brain and liver mitochondria. Biochim. Biophys. Acta 2005, 1709:127-137.
12. Lloyd D., Eshantha L., Salgado J., Turner M.P., Murray D.B. Respiratory oscillations in yeast: clock-driven mitochondrial cycles of energization. FEBS Lett. 2002, 519:41-44.
13. Lloyd D., Salgado L.E., Turner M.P., Suller M.T., Murray D.B. Cycles of mitochondrial energization driven by the ultradian clock in a continuous culture of Saccharomyces cerevisiae. Microbiology 2002, 148:3715-3724.
14. Lloyd D., Murray D.B. The temporal architecture of eukaryotic growth. FEBS Lett. 2006, 580:2830-2835.
15. Lloyd D., Murray D.B. Ultradian metronome: timekeeper for orchestration of cellular coherence. Trends Biochem. Sci. 2005, 303:73-77.
16. Richter P.H., Ross J. Oscillations and efficiency in glycolysis. Biophys. Chem. 1980, 12:285-297.
17. Richter P.H., Ross J. Concentration oscillations and efficiency: glycolysis. Science 1981, 211:715-717.
18. Chance B., Yoshioka T. Sustained oscillations of ionic constituents of mitochondria. Arch. Biochem. Biophys. 1966, 117:451-465.
19. Gooch V.D., Parker L. Oscillatory systems in mitochondria. Biochim. Biophys. Acta 1974, 346:245-260.
20. Frenkel R. Control of reduced diphosphopyridine nucleotide oscillations in beef heart extracts. I. Effects of modifiers of phosphofructokinase activity. Arch. Biochem. Biophys. 1968, 125:151-156.
21. Ghosh A., Chance B. Oscillations of glycolytic intermediates in yeast cells. Biochem. Biophys. Res. Commun. 1964, 16:174-181.
22. Bernardi P., Pozzan M., Azzone G.F. Mitochondrial oscillation and activation of H+/cation exchange. J. Bioenerg. Biomembr. 1982, 14:387-403.
23. O'Rourke B. Pathophysiological and protective roles of mitochondrial ion channels. J. Physiol. 2000, 529:23-36.
24. Aon M.A., Cortassa S., Marban E., O'Rourke B. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 2003, 278:44735-44744.
25. Aon M.A., Cortassa S., O'Rourke B. The fundamental organization of cardiac mitochondria as a network of coupled oscillators. Biophys. J. 2006, 91:4317-4327.
26. Aon M.A., Cortassa S., Akar F.G., O'Rourke B. Mitochondrial criticality: a new concept at the turning point of life or death. Biochim. Biophys. Acta 2006, 1762:232-240.
27. Saleet Jafri M., Kotulska M. Modeling the mechanism of metabolic oscillations in ischemic cardiac myocytes. J. Theor. Biol. 2006, 242:801-817.
28. Iotti S., Gottardi G., Clementi V., Barbiroli B. The monoexponential pattern of phosphocreatine recovery after muscle exercise is a particular case of a more complex behaviour. Biochim. Biophys. Acta 2004, 1608:131-139.
29. Chance B., Im J., Nioka S., Kushmerick M. Skeletal muscle energetics with PNMR: personal views and historic perspectives. NMR Biomed. 2006, 19:904-926.
30. Wallimann T., Wyss M., Brdiczka D., Nicolay K., Eppenberger H.M. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem. J. 1992, 281:21-40.
31. 31P-NMR study. Proc. Natl. Acad. Sci. U.S.A. 1981, 78:6714-6718.
32. 31P-NMR. Magn. Reson. Med. 1984, 1:307-315.
33. Arnold D.L., Taylor D.J., Radda G.K. Investigation of human mitochondrial myopathies by phosphorus magnetic resonance spectroscopy. Ann. Neurol. 1985, 18:189-196.
34. Bendahan D., Confort-Gouny S., Kozak-Reiss G., Cozzone P.J. Heterogeneity of metabolic response to muscular exercise in humans. New criteria of invariance defined by in vivo phosphorus-31 NMR spectroscopy. FEBS Lett. 1990, 272:155-158.
35. 31P magnetic resonance spectroscopy in patients affected by migraine with aura. Neurology 1992, 42:1209-1214.
36. 31P MRS. The role of pH in the evaluation of phosphocreatine and inorganic phosphate recoveries from exercise. NMR Biomed. 1993, 6:248-253.
37. 31P magnetic resonance spectroscopy study of phosphocreatine recovery kinetics in skeletal muscle: the issue of intersubject variability. Biochim. Biophys. Acta 2000, 1457:18-26.
38. 31P-NMR in human muscle. Transient patterns with exercise. J. Appl. Physiol. 1985, 59:101-104.
39. Meyer R.A. A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am. J. Physiol. 1988, 254:C548-C553.
40. Marsh G.D., Paterson D.H., Potwarka J.J., Thompson R.T. Transient changes in muscle high-energy phosphate during moderate exercise. J. Appl. Physiol. 1993, 75:648-656.
41. Meyer R.A., Foley J.M. Testing models of respiratory control in skeletal muscle. Med. Sci. Sports Exerc. 1994, 26:52-57.
42. Nevill A.M., Jones D.A., McIntyre D., Bogdanis G.C., Nevill M.E. A model for phosphocreatine resynthesis. J. Appl. Physiol. 1997, 82:329-335.
43. Kushmerick M., Beard D.A. Strong inference for systems biology. PLoS Comput. Biol. 2009, 5:e1000459.
44. Chetverikova E.P. Oscillations in muscle creatine activity. Biological and Biochemical Oscillators 1973, 347-362. Academic Press, New York. B. Chance (Ed.).
45. Meyer R.A., Wiseman R.W., Jeneson J.A.L. Circuit models of muscle metabolism. J. Appl. Physiol. 1997, 83:2169-2171.
46. Harkema S.J., Meyer R.A. Effect of acidosis on control of respiration in skeletal muscle. Am. J. Physiol. 1997, 272:C491-C500.
47. Quistorff B., Johansen L., Sahlin K. Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. Biochem. J. 1993, 291:681-686.
48. McCully K.K., Fielding R.A., Evans W.J., Leigh J.S.J., Posner J.D. Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J. Appl. Physiol. 1993, 75:813-819.
49. 31P NMR spectroscopy and ergometer exercise test as evidence for muscle oxidative performance improvement with coenzyme Q in mitochondrial myopathies. Neurology 1992, 42(1992):1203-1208.
50. Paganini A.T., Foley J.M., Meyer R.A. Linear dependence of muscle phosphocreatine kinetics on oxidative capacity. Am. J. Physiol. 1997, 272:C501-C510.
51. Taylor D.J., Bore P.J., Styles P., Gadian D.G., Radda G.K. Bioenergetics of intact human muscle. A 31P nuclear magnetic resonance study. Mol. Biol. Med. 1983, 1:77-94.
52. Mahler M. First-order kinetics of muscle oxygen consumption, and an equivalent proportionality between QO2 and phosphorylcreatine level. Implications for the control of respiration. J. Gen. Physiol. 1985, 86:135-165.
53. Chance B., Leigh J.S., Clark B.J., Maris J., Kent J., Nioka S., Smith D. Control of oxidative metabolism and oxygen delivery in human skeletal muscle: a steady state analysis of the work/energy cost transfer function. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:8384-8388.
54. Kemp G.J. Interactions of mitochondrial ATP synthesis and the creatine kinase equilibrium in skeletal muscle. J. Theor. Biol. 1994, 170:239-246.
55. 31P NMR magnetization-transfer measurements of ATP turnover during steady-state isometric muscle contraction in the rat hind limb in vivo. Biochemistry 1989, 28:4887-4893.
56. Kemp G.J., Taylor D.J., Radda G.K. Control of phosphocreatine resynthesis during recovery from exercise in human skeletal muscle. NMR Biomed. 1993, 6:66-72.
57. Thompson C.H., Kemp G.J., Sanderson A.L., Radda G.K. Skeletal muscle mitochondrial function studied by kinetic analysis of postexercise phosphocreatine resynthesis. J. Appl. Physiol. 1995, 78:2131-2139.
58. Jeneson J.A.L., Wiseman R.W., Westerhoff H.V., Kushmerick M.J. The signal transduction function for oxidative phosphorylation is at least second order in ADP. J. Biol. Chem. 1996, 271:27995-27998.
59. Combs C.A., Aletras A.H., Balaban R.S. Effect of muscle action and metabolic strain on oxidative metabolic responses in human skeletal muscle. J. Appl. Physiol. 1999, 87:1768-1775.
60. Mahler M. Kinetics of oxygen consumption after a single isometric tetanus of frog sartorius muscle at 20 degrees C. J. Gen. Physiol. 1978, 71:559-580.
61. Kammermeier H. Meaning of energetic parameters. Basic Res. Cardiol. 1993, 88:380-384.
62. 31P-magnetic resonance spectroscopic studies. MAGMA 1997, 5:231-241.
63. Harkema S.J., Meyer R.A. Effect of acidosis on control of respiration in skeletal muscle. Am. J. Physiol. 1997, 272:C491-C500.
64. McMahon S., Jenkins D. Factors affecting the rate of phosphocreatine resynthesis following intense exercise. Sports Med. 2002, 32:761-784.
65. McCutcheon L.J., Byrd S.K., Hodgson D.R. Ultrastructural changes in skeletal muscle after fatiguing exercise. J. Appl. Physiol. 1992, 72:1111-1117.
66. Gollnick P.D., Ianuzzo C.D., Williams C., Hill T.R. Effect of prolonged, severe exercise on the ultrastructure of human skeletal muscle. Int. Z Angew Physiol. 1969, 27:257-265.
67. Dohm G.L., Barakat H., Stephenson T.P., Pennington S.N., Tapscott E.B. Changes in muscle mitochondrial lipid composition resulting from training and exhaustive exercise. Life Sci. 1975, 17:1075-1080.
68. Arnold D.L., Matthews P.M., Radda G.K. Metabolic recovery after exercise and the assessment of mitochondrial function in vivo in human skeletal muscle by means of P-31 NMR. Magn. Reson. Med. 1984, 1:307-315.
69. McCreary C.R., Chilibeck P.D., Marsh G.D., Paterson D.H., Cunningham D.A., Thompson R.T. Kinetics of pulmonary oxygen uptake and muscle phosphates during moderate-intensity calf exercise. J. Appl. Physiol. 1996, 81:1331-1338.
70. 31P-MRS. MAGMA 1997, 5:372-378.
71. Argov Z., De Stefano N., Arnold D.L. ADP recovery after a brief ischemic exercise in normal and diseased human muscle: a 31P MRS study. NMR Biomed. 1996, 9:165-172.
72. Walter G., Vandenborne K., McCully K.K., Leigh J.S. Noninvasive measurement of phosphocreatine recovery kinetics in single human muscles. Am. J. Physiol. 1997, 272:C525-C534.
73. Takahashi H., Inaki M., Fujimoto K., Katsuta S., Anno I., Niitsu M., Itai Y. Control of the rate of phosphocreatine resynthesis after exercise in trained and untrained human quadriceps muscles. Eur. J. Appl. Physiol. Occup. Physiol. 1995, 71:396-404.
74. McCully K.K., Iotti S., Kendrick K., Wang Z., Posner J.D., Jr J.S., Leigh B.Chance Simultaneous in vivo measurements of oxygen saturation and PCr kinetics following exercise in normal humans. J. Appl. Physiol. 1994, 77:5-10.
75. van den Broek N.M., De Feyter H.M., de Graaf L., Nicolay K., Prompers J.J. Intersubject differences in the effect of acidosis on phosphocreatine recovery kinetics in muscle after exercise are due to differences in proton efflux rates. Am. J. Physiol. Cell Physiol. 2007, 293:C228-C237.
76. Rate control of Biological Processes 1973, Cambridge Univ. Press, London. D.D. Davies (Ed.).
77. Westerhoff H.V., Van Dam K. Thermodynamics and Control of Biological Free-Energy Transduction 1987, Elsevier, Amsterdam.
78. Barbiroli B., Montagna P., Cortelli P., Iotti S., Lodi R., Barboni P., Monari L., Lugaresi E., Frassineti C., Zaniol P. Detective brain and muscle energy metabolism shown by in vivo 31P magnetic resonance spectroscopy in non-affected carriers of 11778 mtDNA mutation. Neurology 1995, 45:1364-1369.
79. Barbiroli B., Iotti S., Lodi R. In vivo assessment of human skeletal muscle mitochondria respiration in health and disease. Mol. Cell. Biochem. 1997, 74:11-15.
80. McCann D.J., Mole P.A., Caton J.R. Phosphocreatine kinetics in humans during exercise and recovering. Med. Sci. Sports Exerc. 1995, 27:378-387.
81. Iotti S., Frassineti C., Sabatini A., Vacca A., Barbiroli B. Quantitative mathematical expressions for accurate in vivo assessment of cytosolic [ADP] and ΔG of ATP hydrolysis in the human brain and skeletal muscle. Biochim. Biophys. Acta 2005, 1708:164-177.
82. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 1961, 191:144-148.
83. Mitchell P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol. Rev. 1966, 41:445-502.
84. +-potential as a convertible energy source for the living cell. FEBS Lett. 1977, 74:1-9.
85. Rees D.C., Howard J.B. Structural bioenergetics and energy transduction mechanisms. J. Mol. Biol. 1999, 293:343-350.
86. Walker D.A., Sivak M.N., Prinsley R.T., Cheesbrough J.K. Simultaneous measurement of oscillations in oxygen evolution and chlorophyll a fluorescence in leaf pieces. Plant Physiol. 1983, 73:542-549.
87. Kocks P., Ross J. Kinetic model for (damped) oscillations of transthylakoid pH in plants. J. Phys. Chem. 1995, 99:16490-16497.
88. Sadykov Y.H., Holmuhamedov E.L., Evtodienko Y.V. Effect of pH and proton buffer on oscillations of ion fluxes in rat erythrocytes. Eur. J. Biochem. 1984, 143:369-371.
89. Cook P.F., Kenyon G.L., Cleland W.W. Use of pH studies to elucidate the catalytic mechanism of rabbit muscle creatine kinase. Biochemistry 1981, 20:1204-1210.
90. McLeish M.J., Kenyon G.L. Relating structure to mechanism in creatine kinase. Crit. Rev. Biochem. Mol. Biol. 2005, 40:1-20.
91. Harris R.C., Edwards R.H.T., Hultman E., Nordesjo L.O., Nylind B., Sahlin K. The time course of phosphorylcreatine resynthesis during recovery of the quadriceps muscle in man. Pfluegers Arch. 1976, 367:137-142.
92. Katchalsky A., Curran P.F. Nonequilibrium Thermodynamics in Biophysics 1965, Harvard University Press, Cambridge, Massachusetts.