A computational model integrating electrophysiology, contraction, and mitochondrial bioenergetics in the ventricular myocyte

Biophysical Journal

Volumn 91, Issue 4, 2006, Pages 1564-1589

  Cortassa, Sonia ^a   Aon, Miguel A ^a   O'Rourke, Brian ^a   Jacques, Robert ^a   Tseng, Hsiang Jer ^a   Marbán, Eduardo ^a   Winslow, Raimond L ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; CALCIUM ION; CREATINE KINASE; MYOSIN ADENOSINE TRIPHOSPHATASE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SODIUM ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOENERGY; CITRIC ACID CYCLE; CONTROLLED STUDY; CYTOPLASM; ELECTROPHYSIOLOGY; ENZYME REGULATION; HEART MUSCLE CELL; HEART MUSCLE OXYGEN CONSUMPTION; HEART VENTRICLE; HEART WORK; ION TRANSPORT; MALE; MATHEMATICAL MODEL; METABOLIC REGULATION; MITOCHONDRION; MUSCLE CONTRACTION; MUSCLE EXCITATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; RAT; STEADY STATE;

EID: 33746809102     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.076174     Document Type: Article

References (71)

1. Balaban, R. S. 2002. Cardiac energy metabolism homeostasis: role of cytosolic calcium. J. Mol. Cell. Cardiol. 34:1259-1271.
2. Evans, L., and Y. Matsuoka. 1915. The effect of various mechanical conditions on the gaseous metabolism and efficiency of the mammalian heart. J. Physiol. (Lond.). 49:378-405.
3. Brown, G. C. 1992. Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem. J. 284:1-13.
4. Neely, J. R., H. Liebermeister, E. J. Battersby, and H. E. Morgan. 1967. Effect of pressure development on oxygen consumption by isolated rat heart. Am. J. Physiol. 212:804-814.
5. Williamson, J. R., C. Ford, J. Illingworth, and B. Safer. 1976. Coordination of citric acid cycle activity with electron transport flux. Circ. Res. 38:I39-I51.
6. Heineman, F. W., and R. S. Balaban. 1990. Control of mitochondrial respiration in the heart in vivo. Annu. Rev. Physiol. 52:523-542.
7. Saks, V. A., A. V. Kuznetsov, M. Vendelin, K. Guerrero, L. Kay, and E. K. Seppet. 2004. Functional coupling as a basic mechanism of feedback regulation of cardiac energy metabolism. Mol. Cell. Biochem. 256-257:185-199.
8. Chance, B., and G. R. Williams. 1955. A method for the localization of sites for oxidative phosphorylation. Nature. 176:250-254.
9. Saks, V. A., T. Kaambre, P. Sikk, M. Eimre, E. Orlova, K. Paju, A. Piirsoo, F. Appaix, L. Kay, V. Regitz-Zagrosek, E. Fleck, and E. Seppet. 2001. Intracellular energetic units in red muscle cells. Biochem. J. 356:643-657.
10. Kaasik, A., V. Veksler, E. Boehm, M. Novotova, A. Minajeva, and R. Ventura-Clapier. 2001. Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ. Res. 89:153-159.
11. Joubert, F., P. Mateo, B. Gillet, J. C. Beloeil, J. L. Mazet, and J. A. Hoerter. 2004. CK flux or direct ATP transfer: versatility of energy transfer pathways evidenced by NMR in the perfused heart. Mol. Cell. Biochem. 256-257:43-58.
12. 2, NADH, and light scattering. J. Biol. Chem. 276:2586-2599.
13. Bose, S., S. French, F. J. Evans, F. Joubert, and R. S. Balaban. 2003. Metabolic network control of oxidative phosphorylation: multiple roles of inorganic phosphate. J. Biol. Chem. 278:39155-39165.
14. 2+ dynamics: the roles of ryanodine receptor adaptation and sarcoplasmic reticulum load. Biophys. J. 74:1149-1168.
15. Rice, J. J., M. S. Jafri, and R. L. Winslow. 2000. Modeling short-term interval-force relations in cardiac muscle. Am. J. Physiol. Heart Circ. Physiol. 278:H913-H931.
16. Cortassa, S., M. A. Aon, E. Marban, R. L. Winslow, and B. O'Rourke. 2003. An integrated model of cardiac mitochondrial energy metabolism and calcium dynamics. Biophys. J. 84:2734-2755.
17. 2+ during increased work in intact rat heart trabeculae. Biophys. J. 83:587-604.
18. Hoerter, J. A., R. Ventura-Clapier, and A. Kuznetsov. 1994. Compartmentation of creatine kinases during perinatal development of mammalian heart. Mol. Cell. Biochem. 133-134:277-286.
19. Saks, V. A., R. Ventura-Clapier, and M. K. Aliev. 1996. Metabolic control and metabolic capacity: two aspects of creatine kinase functioning in the cells. Biochim. Biophys. Acta. 1274:81-88.
20. Shannon, T. R., K. S. Ginsburg, and D. M. Bers. 2000. Reverse mode of the sarcoplasmic reticulum calcium pump and load-dependent cytosolic calcium decline in voltage-clamped cardiac ventricular myocytes. Biophys. J. 78:322-333.
21. +-dependent ATPase studied by ADP-inhibition patterns. J. Biochem. (Tokyo). 87:1721-1727.
22. Jeneson, J. A., H. V. Westerhoff, and M. J. Kushmerick. 2000. A metabolic control analysis of kinetic controls in ATP free energy metabolism in contracting skeletal muscle. Am. J. Physiol. Cell Physiol. 279:C813-C832.
23. Regnier, M., D. A. Martyn, and P. B. Chase. 1998. Calcium regulation of tension redevelopment kinetics with 2-deoxy-ATP or low [ATP] in rabbit skeletal muscle. Biophys. J. 74:2005-2015.
24. Karatzaferi, C., K. H. Myburgh, M. K. Chinn, K. Franks-Skiba, and R. Cooke. 2003. Effect of an ADP analog on isometric force and ATPase activity of active muscle fibers. Am. J. Physiol. Cell Physiol. 284:C816-C825.
25. Pate, E., and R. Cooke. 1989. A model of crossbridge action: the effects of ATP, ADP and Pi. J. Muscle Res. Cell Motil. 10:181-196.
26. Luo, C. H., and Y. Rudy. 1994. A dynamic model of the cardiac ventricular action potential. I. Simulations of ionic currents and concentration changes. Circ. Res. 74:1071-1096.
27. Nakao, M., and D. C. Gadsby. 1989. [Na] and [K] dependence of the Na/K pump current-voltage relationship in Guinea-pig ventricular myocytes. J. Gen. Physiol. 94:539-565.
28. Echarte, M. M., V. Levi, A. M. Villamil, R. C. Rossi, and J. P. Rossi. 2001. Quantitation of plasma membrane calcium pump phosphorylated intermediates by electrophoresis. Anal. Biochem. 289:267-273.
29. 2+-ATPase. J. Mol. Cell. Cardiol. 24:233-242.
30. Ebus, J. P., and G. J. Stienen. 1996. Origin of concurrent ATPase activities in skinned cardiac trabeculae from rat. J. Physiol. 492:675-687.
31. Cohen, S. D., and A. C. Hindmarsh. 1994. CVODE User Guide. In Lawrence Livermore National Laboratory report. Livermore, CA.
32. Brandes, R., and D. M. Bers. 1999. Analysis of the mechanisms of mitochondrial NADH regulation in cardiac trabeculae. Biophys. J. 77:1666-1682.
33. Mulieri, L. A., G. Hasenfuss, F. Ittleman, E. M. Blanchard, and N. R. Alpert. 1989. Protection of human left ventricular myocardium from cutting injury with 2,3-butanedione monoxime. Circ. Res. 65:1441-1449.
34. Janssen, P. M., L. B. Stull, and E. Marban. 2002. Myofilament properties comprise the rate-limiting step for cardiac relaxation at body temperature in the rat. Am. J. Physiol. Heart Circ. Physiol. 282:H499-H507.
35. Szigligeti, P., C. Pankucsi, T. Banyasz, A. Varro, and P. P. Nanasi. 1996. Action potential duration and force-frequency relationship in isolated rabbit, Guinea-pig and rat cardiac muscle. J. Comp. Physiol. [B]. 166:150-155.
36. 2+-content in isolated rat and rabbit myocardium. J. Mol. Cell. Cardiol. 32:2249-2258.
37. Neely, J. R., M. Whitmer, and S. Mochizuki. 1976. Effects of mechanical activity and hormones on myocardial glucose and fatty acid utilization. Circ. Res. 38:I22-I30.
38. Elliott, A. C., G. L. Smith, and D. G. Allen. 1994. The metabolic consequences of an increase in the frequency of stimulation in isolated ferret hearts. J. Physiol. 474:147-159.
39. Jacobus, W. E. 1985. Respiratory control and the integration of heart high-energy phosphate metabolism by mitochondrial creatine kinase. Annu. Rev. Physiol. 47:707-725.
40. Chen, C., Y. Ko, M. Delannoy, S. J. Ludtke, W. Chiu, and P. L. Pedersen. 2004. Mitochondrial ATP synthasome: three-dimensional structure by electron microscopy of the ATP synthase in complex formation with carriers for Pi and ADP/ATP. J. Biol. Chem. 279:31761-31768.
41. Bers, D. M. 2001. Excitation-Contraction Coupling and Cardiac Contractile Force. Kluwer Academic Publishers, Dordrecht, The Netherlands; Boston, MA.
42. Eijgelshoven, M. H., J. H. van Beek, I. Mottet, M. G. Nederhoff, C. J. van Echteld, and N. Westerhof. 1994. Cardiac high-energy phosphates adapt faster than oxygen consumption to changes in heart rate. Circ. Res. 75:751-759.
43. Harrison, G. J., M. H. van Wijhe, B. de Groot, F. J. Dijk, L. A. Gustafson, and J. H. van Beek. 2003. Glycolytic buffering affects cardiac bioenergetic signaling and contractile reserve similar to creatine kinase. Am. J. Physiol. Heart Circ. Physiol. 285:H883-H890.
44. 2+ increases the mitochondrial NADH concentration during elevated work in intact cardiac muscle. Circ. Res. 80:82-87.
45. Kadenbach, B. 2003. Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim. Biophys. Acta. 1604:77-94.
46. 31P NMR magnetization transfer study. J. Biol. Chem. 260:3512-3517.
47. Johnson, E. A. 1979. Force-interval relationship in cardiac muscle. In Handbook of Physiology. The Cardiovascular System. The Heart. American Physiological Society, Bethesda, MD. 475-492.
48. Wier, W. G., and D. T. Yue. 1986. Intracellular calcium transients underlying the short-term force-interval relationship in ferret ventricular myocardium. J. Physiol. 376:507-530.
49. Huser, J., L. A. Blatter, and S. S. Sheu. 2000. Mitochondrial calcium in heart cells: beat-to-beat oscillations or slow integration of cytosolic transients? J. Bioenerg. Biomembr. 32:27-33.
50. 2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ. Res. In press.
51. Pozzan, T., and R. Rizzuto. 2000. The renaissance of mitochondrial calcium transport. Eur. J. Biochem. 267:5269-5273.
52. Magnus, G., and J. Keizer. 1998. Model of β-cell mitochondrial calcium handling and electrical activity. I. Cytoplasmic variables. Am. J. Physiol. 274:C1158-C1173.
53. Matsuoka, S., N. Sarai, H. Jo, and A. Noma. 2004. Simulation of ATP metabolism in cardiac excitation-contraction coupling. Prog. Biophys. Mol. Biol. 85:279-299.
54. Korzeniewski, B., and J. P. Mazat. 1996. Theoretical studies on the control of oxidative phosphorylation in muscle mitochondria: application to mitochondrial deficiencies. Biochem. J. 319:143-148.
55. Vendelin, M., O. Kongas, and V. Saks. 2000. Regulation of mitochondrial respiration in heart cells analyzed by reaction-diffusion model of energy transfer. Am. J. Physiol. Cell Physiol. 278:C747-C764.
56. Vendelin, M., M. Lemba, and V. A. Saks. 2004. Analysis of functional coupling: mitochondrial creatine kinase and adenine nucleotide translocase. Biophys. J. 87:696-713.
57. Page, E. 1978. Quantitative ultrastructural analysis in cardiac membrane physiology. Am. J. Physiol. 235:C147-C158.
58. 2+ electrochemical gradients in cardiac muscle and their relationship to force development. J. Gen. Physiol. 80:325-351.
59. Sheu, S. S. 1989. Cytosolic sodium concentration regulates contractility of cardiac muscle. Basic Res. Cardiol. 84(Suppl 1):35-45.
60. 2+-dependent ATPase and myosin ATPase. Mol. Cell. Biochem. 77:143-152.
61. Winslow, R. L., J. Rice, S. Jafri, E. Marban, and B. O'Rourke. 1999. Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure, II: model studies. Circ. Res. 84:571-586.
62. Ruf, T., S. Hebisch, R. Gross, N. Alpert, H. Just, and C. Holubarsch. 1996. Modulation of myocardial economy and efficiency in mammalian failing and non-failing myocardium by calcium channel activation and β-adrenergic stimulation. Cardiovasc. Res. 32:1047-1055.
63. Selivanov, V. A., A. E. Alekseev, D. M. Hodgson, P. P. Dzeja, and A. Terzic. 2004. Nucleotide-gated KATP channels integrated with creatine and adenylate kinases: amplification, tuning and sensing of energetic signals in the compartmentalized cellular environment. Mol. Cell. Biochem. 256-257:243-256.
64. Joubert, F., B. Gillet, J. L. Mazet, P. Mateo, J. Beloeil, and J. A. Hoerter. 2000. Evidence for myocardial ATP compartmentation from NMR inversion transfer analysis of creatine kinase fluxes. Biophys. J. 79:1-13.
65. Ingwall, J. S., and R. G. Weiss. 2004. Is the failing heart energy-starved? On using chemical energy to support cardiac function. Circ. Res. 95:135-145.
66. Saupe, K. W., M. Spindler, J. C. Hopkins, W. Shen, and J. S. Ingwall. 2000. Kinetic, thermodynamic, and developmental consequences of deleting creatine kinase isoenzymes from the heart. Reaction kinetics of the creatine kinase isoenzymes in the intact heart. J. Biol. Chem. 275:19742-19746.
67. Clark, J. F., A. V. Kuznetsov, and G. K. Radda. 1997. ADP-regenerating enzyme systems in mitochondria of guinea pig myometrium and heart. Am. J. Physiol. 272:C399-C404.
68. + ratios. Biochem. J. 252:181-189.
69. Randle, P. J., and P. K. Tubbs. 1979. Carbohydrate and fatty acid metabolism. In Handbook of Physiology. R. M. Berne, N. Sperelakis, and R. Geiger, editors. American Physiological Society, Bethesda, MD. 805-844.
70. Gunter, K. K., and T. E. Gunter. 1994. Transport of calcium by mitochondria. J. Bioenerg. Biomembr. 26:471-485.
71. Gunter, T. E., and D. R. Pfeiffer. 1990. Mechanisms by which mitochondria transport calcium. Am. J. Physiol. 258:C755-C786.