Modeling the mechanism of metabolic oscillations in ischemic cardiac myocytes

Journal of Theoretical Biology

Volumn 242, Issue 4, 2006, Pages 801-817

  Saleet Jafri, M ^a,b   Kotulska, Malgorzata ^c  

^a GEORGE MASON UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^c WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

Computer model; Heart; Ischemia; Metabolic oscillations

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ANION CHANNEL; MAGNESIUM; NICOTINAMIDE ADENINE DINUCLEOTIDE; PHOSPHATE; PHOSPHATE TRANSPORTER; PROTON PUMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

BLOOD SYSTEM DISORDER; CARDIOVASCULAR DISEASE; METABOLISM; MITOCHONDRION; NUMERICAL MODEL; OSCILLATION;

ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; DISSOCIATION CONSTANT; ELECTRON TRANSPORT; ENERGY METABOLISM; HEART ARRHYTHMIA; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE POTENTIAL; HEART REPOLARIZATION; ION CURRENT; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; MICHAELIS CONSTANT; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; OSCILLATION; PH MEASUREMENT; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE;

BIOLOGICAL CLOCKS; COMPUTER SIMULATION; ENERGY METABOLISM; HUMANS; MITOCHONDRIA, HEART; MODELS, CARDIOVASCULAR; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC;

EID: 33748476241     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2006.05.007     Document Type: Article

References (65)

1. Albe K.R., Butler M.H., and Wright B.E. Cellular concentrations of enzymes and their substrates. J. Theor. Biol. 143 2 (1990) 163-195
2. Aon M.A., Cortassa S., Marban E., and O'Rourke B. Sychronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 278 45 (2003) 44735-44744
3. Armiger L., Headrick J., Jordan L., and Willis R. Bound inorganic phosphate and early contractile failure in global ischemia. Basic Res. Cardiol. 90 (1995) 482-488
4. Barbour R.L., and Chan S.H.P. Characterization of the kinetics and mechanism of the mitochondrial ADP-ATP carrier. J. Biol. Chem. 256 4 (1981) 1940-1948
5. Beavis A. Properties of the inner membrane anion channel in intact mitochondria. J. Bioenerg. Biomembr. 24 1 (1992) 77-90
6. Beavis A., and Powers M. On the regulation of the mitochondrial inner membrane anion channel by magnesium and protons. J. Biol. Chem. 264 29 (1989) 17148-17155
7. Berkich D.A., Salama G., and LaNoue K.F. Mitochondrial membrane potentials in ischemic hearts. Arch. Biochem. Biophys. 420 (2003) 279-286
8. Berkich, D.A., Williams, G.D., Masiakos, P.T., Smith, M.B., D., B.P., LaNoue, K.F., 1991. Rates of various reactions catalyzed by ATP synthase as related to the mechanisms of ATP synthesis. J. Biol. Chem. 266, 123-129.
9. +/cation exchange. J. Bioenerg. Biomembr. 14 5/6 (1982) 387-403
10. Bers D. Excitation-Contraction Coupling and Cardiac Contractile Force. Developments in Cardiovascular Medicine. Second ed (2001), Kluwer Academic Publishers, Dordrecht p. 237
11. Brady N.R., Elmore S.P., van Beek J.J.H.G.M., Krab K., and Courtoy P.J. Coordinated behavior of mitochondria in both space and time: a reactive oxygen species-activated wave of mitochondrial depolarization. Biophys. J. 87 (2004) 2022-2034
12. Bromberg J.P. Physical Chemistry. Second ed (1984), Allyn and Bacon, Inc., United States pp. 341-347
13. Chance B., and Yoshioka T. Sustained oscillations of ionic constituents of mitochondria. Arch. Biochem. Biophys. 117 2 (1966) 451-465
14. Chen Q., Vasquez E.J., Moghaddas S., Hoppel C.L., and Lesnefsky E.J. Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 278 (2003) 36027-36031
15. Corkey B., Duszynski J., Rich T., Matschinsky B., and Williamson J. Regulation of free and bound magnesium in rat hepatocytes and isolated mitochondria. J. Biol. Chem. 261 6 (1986) 2567-2574
16. Cortassa S., Aon M.A., Marban E., Winslow R.L., and O'Rourke B. An integrated model of cardiac mitochondrial energy metabolism and calcium dynamics. Biophys J 84 (2003) 2734-2755
17. Cortassa S., Aon M.A., Winslow R.L., and O'Rourke B. A Mitochondrial Oscillator Dependent on Reactive Oxygen Species. Biophys. J. 87 (2004) 2060-2073
18. DeRobertis E., and DeRobertis Jr. E. Cell and Molecular Biology. eighth ed (1987), Lea and Febiger, Philadelphia
19. DiLisa F., Blank P., Gambassi G., Silverman H., Stern M., and Hansford R. Mitochondrial membrane potential in single living adult rat cardiac myocytes exposed to anoxia or metabolic inhibition. J. Physiol. 486 (1995) 1-13
20. Donoso P., Mill J.G., O'Neill S.C., and Eisner D.A. Fluorescent measurements of cytoplasmic and mitochondrial sodium concentrations in rat ventricular myocytes. J. Physiol. 448 (1992) 493-509
21. Eng J., Lynch R.M., and Balaban R.S. Nicotinamide adenine dinucleotide fluorescence spectroscopy and imaging of isolated cardiac myocytes. Biophys. J. 55 (1989) 621-630
22. 0-ATPase synthases: glimpses of interacting parts in a dynamic molecular machine. J. Exp. Biol. 200 (1997) 217-224
23. Frenkel R. Control of reduced diphosphopyridine nucleotide oscillations in beef heart extracts. II. Oscillations of glycolytic intermediates and adenine nucleotides. Arch. Biochem. Biophys 125 1 (1968) 157-165
24. 2+ exchange in ferret heart mitochondria. Biochem. Biophys. Res. Comm. 166 3 (1990) 1352-1357
25. Ghosh A., and Chance B. Oscillations of glycolytic intermediates in yeast cells. Biochem. Biophys. Res. Comm. 16 2 (1964) 174-181
26. Gooch V., and Packer L. Adenine nucleotide control of heart mitochondrial oscillations. Biochim. Biophys. Acta 245 1 (1971) 17-20
27. Gooch V., and Packer L. Oscillatory states of mitochondria. Studies on the oscillatory mechanism of liver and heart mitochondria. Arch. Biochem. Biophys. 163 2 (1974) 759-768
28. Goto S., Chuman H., Majima E., and Terada H. How does the mitochondrial ADP/ATP carrier distinguish transportable ATP and ADP from untransportable AMP and GTP? Dynamics modeling of the recognition/translocation process in the major substrate binding region. Biochim Biophys. Acta. 1589 2 (2002) 203-218
29. Gursahani H.I., and Schaefer S. Acidification reduces mitochondrial calcium uptake in rat cardiac mitochondria. Am. J. Physiol. Heart Circ. Physiol. 287 (2004) H2659-H2665
30. Hagedorn P.H., Flyvbjerg H., and Moller I.M. Modeling NADH turnover in plant mitochondria. Physio Plantarum 120 (2004) 370-385
31. Hochachka P. The metabolic implications of intracellular circulation. Proc. Natl. Acad. Sci. USA 96 22 (1999) 12233-12239
32. 2+ in heart mitochondria. Biochim. Biophys. Acta 1320 3 (1997) 310-320
33. Kaim G., and Dimroth P. ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J 18 15 (1999) 4118-4127
34. Kinnally K., Antonenko Y., Snyder S., McEnery M., and Tedeschi H. Mitochondrial benzodiazepine receptor linked to inner membrane ion channels by nanomolar actions of ligands. Proc. Natl. Acad. Sci. USA 90 4 (1993) 1374-1378
35. Kinnally K., Antonenko Y., and Zorov D. Modulation of Inner Mitochondrial Membrane Channel Activity. J. Bioenerg Biomembr. 24 1 (1992) 99-110
36. Kirichok Y., Krapivinsky G., and Clapham D.E. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427 (2004) 360-364
37. Knox B.E., and Tsong T.Y. Voltage-driven ATP synthesis by beef heart mitochondrial F1F0-ATPase. J. Biol. Chem. 259 (1984) 4757-4763
38. Korzeniewski B., and Zoladz J.A. A model of oxidative phosphorylation in mammalian skeletal muscle. Biophys. Chem. 92 (2001) 17-34
39. Livingston B., Altschuld R., and Hohl C. Metabolic compartmentalization in neonatal swine myocytes. Pediatr. Res. 40 1 (1996) 59-65
40. Lloyd D., Eshantha L., Salgado J., Turner M., and Murray D. Respiratory oscillations in yeast: clock-driven mitochondrial cycles of energization. FEBS Lett 519 1-3 (2002) 41-44
41. 2+ handling. Am. J. Physiol. 273 2, Part 1 (1997) C717-C733
42. Magnus G., and Keizer J. Model of beta-cell mitochondrial calcium handling and electrical activity. I. Cytoplasmic variables. Am. J. Physiol. 274 4, Part 1 (1998) C1158-C1173
43. Mironov S., and Richter D. Oscillations and hypoxic changes of mitochondrial variables in neurons of the brainstem respiratory centre of mice. J. Physiol. 533 Part 1 (2001) 227-236
44. Murphy M., and Brand M. Membrane-potential-dependent changes in the stoichiometry of charge translocation by the mitochondrial electron transport chain. Eur. J. Biochem. 173 3 (1988) 637-644
45. Murphy M., and Brand M. The stoichiometry of charge translocation by cytochrome oxidase and the cytochrome bc1 complex of mitochondria at high membrane potential. Eur. J. Biochem. 173 3 (1988) 645-651
46. Murphy R., Diwan J., King M., and Kinnally K. Two high conductance channels of the mitochondrial inner membrane are independent of the human mitochondrial genome. FEBS Lett. 425 2 (1998) 259-262
47. Nyguen M.-H.T., and Jafri M.S. Mitochondrial calcium signalling and energy metabolism. Ann. N. Y. Acad. Sci. 1047 (2005) 127-137
48. O'Rourke B. Pathophysiological and protective roles of mitochondrial ion channels. J. Physiol. 529 1 (2000) 23-36
49. O'Rourke B., Ramza B., and Marban E. Oscillations of membrane current and excitability driven by metabolic oscillations in heart cells. Science 265 5174 (1994) 962-966
50. Petronilli V., Miotto G., Canton M., Colonna R., Bernardi P., and DiLisa F. Imaging the mitochondrial permeability transition pore in intact cells. Biofactors 8 (1998) 263-272
51. Pfaff E., and Klingenberg M. Adenine nucleotide translocation of mitochondria. I. Specificity and control. Eur. J. Biochem. 6 (1968) 66-79
52. Romashko D., Marban E., and O'Rourke B. Subcellular metabolic transients and mitochondrial redox waves in heart cells. Proc Natl Acad Sci USA 95 4 (1998) 1618-1623
53. Sato K., Kashiwaya Y., Keon C.A., Tsuchiya N., King M.T., Radda G.K., Chance B., Clarke K., and Veech R.L. Insulin, ketone bodies, and mitochondrial energy transduction. FASEB J 9 (1995) 651-658
54. Scalettar B., Abney J., and Hackenbrock C. Dynamics, structure, and function are coupled in the mitochondrial matrix. Proc Natl Acad Sci USA 88 18 (1991) 8057-8061
55. Skárka L., and Ostádal B. Mitochondrial membrane potential in cardiac myocytes. Physiol. Rres. 51 (2002) 425-434
56. - antiports catalyzed by reconstituted phosphate carrier from beef heart mitochondria. J. Biol. Chem. 269 15 (1994) 11240-11246
57. St-Pierre J., Buckingham J.A., Roebuck S.J., and Brand M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277 (2002) 44784-44790
58. Taegtmeyer H., King L., and Jones B. Energy substrate metabolism, myocardial ischemia, and targets for pharmacotherapy. Am. J. Cardiol. 82 5A (1998) 54K-60K
59. 2+-indicating fluorophores. Biophys J. 79 (2000) 39-50
60. Velden J.V.D., Klein L., Zaremba R., Boontje N., Huybregts J., Stooker W., Eigsman L., Jong J.D., Visser C., Visser F., and Stienen G. Effects of calcium, inorganic phosphate, and pH on Isometric force n single skinned cardiomyocytes from donor and failing human hearts. Circulation 104 10 (2001) 1140-1146
61. Vergun O., Votyakova T.V., and Reynolds I.J. Spontaneous changes in mitochondrial membrane potential in single isolated brain mitochondria. Biophys. J. 85 (2003) 3358-3366
62. 2+-induced depolarization in brain and liver mitochondria. Biophys. J. 86 1 (2004) 506A
63. 2+ oscillations. Biophys. J. 67 (1994) 447-456
64. Westerhoff H.V., van Echteld C.J.A., and Jeneson J.A.L. On the expected relationship between Gibbs eneergy of ATP hydrolysis and muscle performance. Biophys. Chem. 54 (1995) 137-142
65. Wingrove D.E., and Gunter T.E. Kinetics of mitochondrial calcium transport. II. A kinetic description of the sodium-dependent calcium efflux mechanism of liver mitochondria and inhibition by ruthenium red and by tetraphenylphosphonium. J. Biol. Chem. 261 (1986) 15166-15171