On the theoretical limits of detecting cyclic changes in cardiac high-energy phosphates and creatine kinase reaction kinetics using in vivo 31P MRS

NMR in Biomedicine

Volumn 28, Issue 6, 2015, Pages 694-705

  Weiss, Kilian ^a   Bottomley, Paul A ^a   Weiss, Robert G ^a  

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

Author keywords

31P MRS; ATP; Creatine kinase reaction; Creatine phosphate; Cyclic variations; High energy phosphates; Mathematical modelling

Indexed keywords

ADENOSINETRIPHOSPHATE; ENZYMES; HEART; MATHEMATICAL MODELS; PHOSPHATES; RATE CONSTANTS;

CREATINE KINASE; CYCLIC VARIATIONS; FORWARD RATE CONSTANTS; HIGH ENERGY PHOSPHATES; PSEUDO FIRST ORDER RATE CONSTANTS; REACTION VELOCITIES; SATURATION TRANSFER; ^31P MRS;

CHROMIUM COMPOUNDS;

ADENOSINE TRIPHOSPHATE; CREATINE KINASE; PHOSPHATE; PHOSPHORUS 31; PHOSPHORUS;

ARTICLE; CHEMICAL REACTION KINETICS; HEART; HEART CYCLE; HIGH ENERGY PHOSPHATE; HYDROLYSIS; IN VIVO STUDY; LIMIT OF DETECTION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; RATE CONSTANT; SIMULATION; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; CARDIAC MUSCLE; CHEMICAL MODEL; COMPUTER SIMULATION; ENZYME ACTIVATION; EVALUATION STUDY; HUMAN; KINETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY;

ADENOSINE TRIPHOSPHATE; BIOLOGICAL CLOCKS; COMPUTER SIMULATION; CREATINE KINASE; ENZYME ACTIVATION; HUMANS; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CARDIOVASCULAR; MODELS, CHEMICAL; MYOCARDIUM; PHOSPHORUS ISOTOPES; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 84929273341     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.3302     Document Type: Article

References (55)

1. Teague WE, Jr, Dobson GP. Effect of temperature on the creatine kinase equilibrium. J. Biol. Chem. 1992; 267(20): 14 084-14 093.
2. Ingwall JS, Kramer MF, Fifer MA, Lorell BH, Shemin R, Grossman W, Allen PD. The creatine kinase system in normal and diseased human myocardium. N. Engl. J. Med. 1985; 313(17): 1050-1054.
3. Wallimann T. Bioenergetics: dissecting the role of creatine kinase. Curr. Biol. 1994; 4(1): 42-46.
4. Radda GK, Seeley PJ. Recent studies on cellular metabolism by nuclear magnetic resonance. Annu. Rev. Physiol. 1979; 41: 749-769.
5. Nunnally RL, Hollis DP. Adenosine triphosphate compartmentation in living hearts: a phosphorus nuclear magnetic resonance saturation transfer study. Biochemistry 1979; 18(16): 3642-3646.
6. Weiss RG, Gerstenblith G, Bottomley PA. ATP flux through creatine kinase in the normal, stressed, and failing human heart. Proc. Natl. Acad. Sci. U. S. A. 2005; 102(3): 808-813.
7. 31P-MRS. Circulation 1997; 96(9): 2969-2977.
8. Balaban RS, Kantor HL, Katz LA, Briggs RW. Relation between work and phosphate metabolite in the in vivo paced mammalian heart. Science 1986; 232(4754): 1121-1123.
9. Conway MA, Bristow JD, Blackledge MJ, Rajagopalan B, Radda GK. Cardiac metabolism during exercise measured by magnetic resonance spectroscopy. Lancet 1988; 2(8612): 692.
10. Hudsmith LE, Tyler DJ, Emmanuel Y, Petersen SE, Francis JM, Watkins H, Clarke K, Robson MD, Neubauer S. P-31 cardiac magnetic resonance spectroscopy during leg exercise at 3 Tesla. Int. J. Cardiovasc. Imaging 2009; 25(8): 819-826.
11. Monroe RG. Myocardial oxygen consumption during ventricular contraction and relaxation. Circ. Res. 1964; 14: 294-300.
12. Gibbs CL, Wendt IR, Kotsanas G, Young IR. The energy cost of relaxation in control and hypertrophic rabbit papillary muscles. Heart Vessels 1990; 5(4): 198-205.
13. Fossel ET, Morgan HE, Ingwall JS. Measurement of changes in high-energy phosphates in the cardiac cycle by using gated P-31 nuclear magnetic-resonance. Proc. Natl. Acad. Sci. USA 1980; 77(6): 3654-3658.
14. Tanaka K, Honda H, Akita N. A gating P-31 NMR method triggered by pulses for cardiac pacing. NMR Biomed. 1992; 5(6): 329-334.
15. Kusuoka H, Inoue M, Tsuneoka Y, Watari H, Hori M, Abe H. Augmented energy consumption during early systole as a mechanism of cyclical changes in high-energy phosphates in myocardium assessed by phosphorus nuclear magnetic resonance. Jpn. Circ. J. 1985; 49(10): 1099-1107.
16. Illing B, Horn M, Urban B, Stromer H, Schnackerz K, de Groot M, Haase A, Hu K, Ertl G, Neubauer S. Changes of myocardial high-energy phosphates with the cardiac cycle during acute or chronic myocardial stress. Magn. Reson. Med. 1998; 40(5): 727-732.
17. 31P nuclear magnetic resonance. Circ. J. 2002; 66(1): 80-86.
18. 31P-NMR spectroscopy in a whole animal. Biochem. Biophys. Res. Commun. 1986; 135(3): 808-815.
19. 31P NMR spectroscopy of rat organs, in situ, using chronically implanted radiofrequency coils. Proc. Natl. Acad. Sci. 1983; 80(24): 7491-7495.
20. Grist TM, Kneeland JB, Rilling WR, Jesmanowicz A, Froncisz W, Hyde JS. Gated cardiac MR imaging and P-31 MR spectroscopy in humans at 1.5T. Work in progress. Radiology 1989; 170(2): 357-361.
21. Balaban RS, Heineman FW. Control of mitochondrial respiration in the heart in vivo. Mol. Cell. Biochem. 1989; 89(2): 191-197.
22. Spindler M, Illing B, Horn M, de Groot M, Ertl G, Neubauer S. Temporal fluctuations of myocardial high-energy phosphate metabolites with the cardiac cycle. Basic Res. Cardiol. 2001; 96(6): 553-556.
23. Saks V, Dzeja P, Schlattner U, Vendelin M, Terzic A, Wallimann T. Cardiac system bioenergetics: metabolic basis of the Frank-Starling law. J. Physiol. 2006; 571(Pt 2): 253-273.
24. Smith CS, Bottomley PA, Schulman SP, Gerstenblith G, Weiss RG. Altered creatine kinase adenosine triphosphate kinetics in failing hypertrophied human myocardium. Circulation 2006; 114(11): 1151-1158.
25. Hirsch GA, Bottomley PA, Gerstenblith G, Weiss RG. Allopurinol acutely increases adenosine triphospate energy delivery in failing human hearts. J. Am. Coll. Cardiol. 2012; 59(9): 802-808.
26. Bottomley PA, Panjrath GS, Lai SH, Hirsch GA, Wu K, Najjar SS, Steinberg A, Gerstenblith G, Weiss RG. Metabolic rates of ATP transfer through creatine kinase (CK flux) predict clinical heart failure events and death. Sci. Transl. Med. 2013; 5(215): 215re3. DOI: 10.1126/scitranslmed.3007328.
27. Aliev MK, Saks VA. Compartmentalized energy transfer in cardiomyocytes: use of mathematical modeling for analysis of in vivo regulation of respiration. Biophys. J. 1997; 73(1): 428-445.
28. Wu F, Beard DA. Roles of the creatine kinase system and myoglobin in maintaining energetic state in the working heart. BMC Syst. Biol. 2009; 3: 22.
29. 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. 1998; 120(1): 109-123.
30. van Beek JH. Adenine nucleotide-creatine-phosphate module in myocardial metabolic system explains fast phase of dynamic regulation of oxidative phosphorylation. Am. J. Physiol. Cell Physiol. 2007; 293(3): C815-C829.
31. Hettling H, van Beek JH. Analyzing the functional properties of the creatine kinase system with multiscale 'sloppy' modeling. PLoS Comput. Biol. 2011; 7(8): e1002130.
32. 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. U. S. A. 2009; 106(17): 7143-7148.
33. Bottomley PA, Ouwerkerk R, Lee RF, Weiss RG. Four-angle saturation transfer (FAST) method for measuring creatine kinase reaction rates in vivo. Magn. Reson. Med. 2002; 47(5): 850-863.
34. 31P spectroscopy for measuring human creatine kinase reaction kinetics. Magn. Reson. Med. 2010; 63(6): 1493-1501.
35. Kupriyanov VV, Steinschneider AY, Ruuge EK, Kapelko VI, Zueva MY, Lakomkin VL, Smirnov VN, Saks VA. Regulation of energy flux through the creatine-kinase reaction in vitro and in perfused rat-heart - P-31-NMR studies. Biochim. Biophys. Acta 1984; 805(4): 319-331.
36. Vinnakota KC, Bassingthwaighte JB. Myocardial density and composition: a basis for calculating intracellular metabolite concentrations. Am. J. Physiol. Heart Circ. Physiol. 2004; 286(5): H1742-H1749.
37. Morrison JF, Cleland WW. Isotope exchange studies of the mechanism of the reaction catalyzed by adenosine triphosphate:creatine phosphotransferase. J. Biol. Chem. 1966; 241(3): 673-683.
38. 2+ ions. Eur. J. Biochem. 1975; 57(1): 273-290.
39. 31P NMR surface coil studies in brain, heart, and skeletal muscle of the living rat. Biochemistry 1987; 26(19): 6083-6090.
40. Nascimben L, Ingwall JS, Pauletto P, Friedrich J, Gwathmey JK, Saks V, Pessina AC, Allen PD. Creatine kinase system in failing and nonfailing human myocardium. Circulation 1996; 94(8): 1894-1901.
41. Gibbs C. The cytoplasmic phosphorylation potential. Its possible role in the control of myocardial respiration and cardiac contractility. J. Mol. Cell. Cardiol. 1985; 17(8): 727-731.
42. 31P spectroscopy at 3 Tesla using adiabatic pulses. Magn. Reson. Med. 2009; 61(4): 785-795.
43. Schlattner U, Tokarska-Schlattner M, Wallimann T. Mitochondrial creatine kinase in human health and disease. Biochim. Biophys. Acta 2006; 1762(2): 164-180.
44. Ingwall JS, Weiss RG. Is the failing heart energy starved? Circ. Res. 2004; 95(2): 135-145.
45. Duwel CM, Westerhof N. Feline left ventricular oxygen consumption is not affected by volume expansion, ejection or redevelopment of pressure during relaxation. Pflugers Arch. 1988; 412(4): 409-416.
46. Yasumura Y, Nozawa T, Futaki S, Tanaka N, Suga H. Time-invariant oxygen cost of mechanical energy in dog left ventricle: consistency and inconsistency of time-varying elastance model with myocardial energetics. Circ. Res. 1989; 64(4): 764-778.
47. Beer M, Seyfarth T, Sandstede J, Landschutz W, Lipke C, Kostler H, von Kienlin M, Harre K, Hahn D, Neubauer S. Absolute concentrations of high-energy phosphate metabolites in normal, hypertrophied, and failing human myocardium measured noninvasively with P-31-SLOOP magnetic resonance spectroscopy. J. Am. Coll. Cardiol. 2002; 40(7): 1267-1274.
48. Xiong Q, Ye L, Zhang P, Lepley M, Tian J, Li J, Zhang L, Swingen C, Vaughan JT, Kaufman DS, Zhang J. Functional consequences of human induced pluripotent stem cell therapy: myocardial ATP turnover rate in the in vivo swine heart with postinfarction remodeling. Circulation 2013; 127(9): 997-1008.
49. Rodgers CT, Clarke WT, Snyder C, Vaughan JT, Neubauer S, Robson MD. Human cardiac P magnetic resonance spectroscopy at 7 tesla. Magn. Reson. Med. 2014; 72(2): 304-315.
50. Rodgers CT, Robson MD. Receive array magnetic resonance spectroscopy: whitened singular value decomposition (WSVD) gives optimal Bayesian solution. Magn. Reson. Med. 2010; 63(4): 881-891.
51. Martini N, Santarelli MF, Giovannetti G, Milanesi M, De Marchi D, Positano V, Landini L. Noise correlations and SNR in phased-array MRS. NMR Biomed. 2010; 23(1): 66-73.
52. Weiss K, Martini N, Boesiger P, Kozerke S. Cardiac proton spectroscopy using large coil arrays. NMR Biomed. 2013; 26(3): 276-284.
53. Atalar E, Bottomley PA, Ocali O, Correia LC, Kelemen MD, Lima JA, Zerhouni EA. High resolution intravascular MRI and MRS by using a catheter receiver coil. Magn. Reson. Med. 1996; 36(4): 596-605.
54. Veech RL, Lawson JW, Cornell NW, Krebs HA. Cytosolic phosphorylation potential. J. Biol. Chem. 1979; 254(14): 6538-6547.
55. Ganz W, Tamura K, Marcus HS, Donoso R, Yoshida S, Swan HJ. Measurement of coronary sinus blood flow by continuous thermodilution in man. Circulation 1971; 44(2): 181-195.