Mapping hypoxia-induced bioenergetic rearrangement and metabolic signalling by 18O-assisted 31P NMR and 1 NMR spectroscopy

Molecular and Cellular Biochemistry

Volumn 256-257, Issue 1-2, 2004, Pages 281-289

  Pucar, Darko ^a   Dzeja, Petras P ^a   Bast, Peter ^a   Gumina, Richard J ^a   Drahl, Carmen ^a   Lim, Lynette ^a   Juranic, Nenad ^a   Macura, Slobodan ^a   Terzic, Andre ^a  

^a MAYO CLINIC   (United States)

Author keywords

Adenylate kinase; Creatine kinase; Energetics; Heart; Ischemia; Metabolism

Indexed keywords

ADENOSINE; ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; ALIPHATIC COMPOUND; AROMATIC COMPOUND; C REACTIVE PROTEIN; CREATINE KINASE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; GLYCEROPHOSPHATE; INOSINE PHOSPHATE; LACTATE DEHYDROGENASE; NUCLEOSIDE DERIVATIVE; OXYGEN 18; PHOSPHATASE; PHOSPHOTRANSFERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SCAVENGER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BIOENERGY; CONTROLLED STUDY; ENERGY CONSUMPTION; ENZYME MECHANISM; ENZYME SYNTHESIS; GLYCOLYSIS; HEART MUSCLE ISCHEMIA; HEART MUSCLE METABOLISM; HEART PROTECTION; MALE; METABOLIC PARAMETERS; METABOLIC REGULATION; NONHUMAN; PATHOPHYSIOLOGY; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PROTEIN ANALYSIS; PROTEIN TRANSPORT; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; REVIEW; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0842345394     PISSN: 03008177     EISSN: None     Source Type: Journal    
DOI: 10.1023/b:mcbi.0000009875.30308.7a     Document Type: Review

References (73)

1. Jennings RB, Reimer KA: The cell biology of acute myocardial ischemia. Annu Rev Med 42: 225-246, 1991
2. Saks VA, Tiivel T, Kay L, Novel-Chate V, Daneshrad Z, Rossi A, Fontaine E, Keriel C, Leverve X, Ventura-Clapier R, Anflous K, Samuel JL, Rappaport L: On the regulation of cellular energetics in health and disease. Mol Cell Biochem 160-161: 195-208, 1996
3. Opie LH: Biochemical changes associated with reversible myocardial ischemia. In: G.R. Heyndricks, S.F. Vatner, W. Wijns (eds). Clinical Pathophysiology of Myocardial Ischemia. Lippincot-Raven, New York, 1997, pp 1-19
4. Taegtmeyer H, King LM, Jones BE: Energy substrate metabolism, myocardial ischemia, and targets for pharmacotherapy. Am J Cardiol 82: 54K-60K, 1998
5. Piper HM: Energy deficiency, calcium overload or oxidative stress: Possible causes of irreversible ischemic myocardial injury. Klin Wochenschr 67: 465-476, 1989
6. Di Lisa F: Mitochondrial contribution in the progression of cardiac ischemic injury. IUBMB Life 52: 255-261, 2001
7. Murry CE, Jennings RB, Reimer KA: Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124-1136, 1986
8. Dzeja PP, Terzic A: Phosphotransfer networks and cellular energetics. J Exp Biol 206: 2039-2047, 2003
9. Opie LH, Sack MN: Metabolic plasticity and the promotion of cardiac protection in ischemia and ischemic preconditioning. J Mol Cell Cardiol 34: 1077-1089, 2002
10. Taegtmeyer H: Genetics of energetics: Transcriptional responses in cardiac metabolism. Ann Biomed Eng 28: 871-876, 2000
11. 31P NMR. J Biol Chem 276: 44812-44819, 2001
12. Barger PM, Kelly DP: PPAR signaling in the control of cardiac energy metabolism. Trends Cardiovasc Med 10: 238-245, 2000
13. Fryer RM, Auchampach JA, Gross GJ: Therapeutic receptor targets of ischemic preconditioning. Cardiovasc Res 55: 520-525, 2002
14. Bessman SP, Carpenter CL: The creatine-creatine phosphate energy shuttle. Annu Rev Biochem 54: 831-862, 1985
15. 31P NMR magnetization transfer study. J Biol Chem 260: 3512-3517, 1985
16. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM: 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 281: 21-40, 1992
17. Saks VA, Khuchua ZA, Vasilyeva EV, Belikova OY, Kuznetsov AV: Metabolic compartmentation and substrate channelling in muscle cells. Role of coupled creatine kinases in in vivo regulation of cellular respiration - a synthesis. Mol Cell Biochem 133-134: 155-192, 1994
18. Dzeja PP, Zeleznikar RJ, Goldberg ND: Adenylate kinase: kinetic behavior in intact cells indicates it is integral to multiple cellular processes. Mol Cell Biochem 184: 169-182, 1998
19. Dzeja PP, Vitkevicius KT, Redfield MM, Burnett JC, Terzic A: Adenylate kinase-catalyzed phosphotransfer in the myocardium: Increased contribution in heart failure. Circ Res 84: 1137-1143, 1999
20. Ventura-Clapier R, Kuznetsov A, Veksler V, Boehm E, Anflous K: Functional coupling of creatine kinases in muscles: Species and tissue specificity. Mol Cell Biochem 184: 231-247, 1998
21. Dzeja PP, Redfield MM, Burnett JC, Terzic A: Failing energetics in failing hearts. Curr Cardiol Rep 2: 212-217, 2000
22. Pucar D, Janssen E, Dzeja PP, Juranic N, Macura S, Wieringa B, Terzic A: Compromised energetics in the adenylate kinase AK1 gene knockout heart under metabolic stress. J Biol Chem 275: 41424-41429, 2000
23. Janssen E, Dzeja PP, Oerlemans F, Simonetti AW, Heerschap A, de Haan A, Rush PS, Terjung RR, Wieringa B, Terzic A: Adenylate kinase 1 gene deletion disrupts muscle energetic economy despite metabolic rearrangement. EMBO J 19: 6371-6381, 2000
24. Gudbjarnason S, Mathes P, Ravens KG: Functional compartmentation of ATP and creatine phosphate in heart muscle. J Mol Cell Cardiol 1: 325-339, 1970
25. Rovetto MJ, Whitmer JT, Neely JR: Comparison of the effects of anoxia and whole heart ischemia on carbohydrate utilization in isolated working rat hearts. Circ Res 32: 699-711, 1973
26. 31P NMR. J Biol Chem 263: 10600-10607, 1988
27. 23Na-nuclear magnetic resonance study of the isolated rat heart. Circulation 86: 302-310, 1992
28. Van Wylen DG: Effect of ischemic preconditioning on interstitial purine metabolite and lactate accumulation during myocardial ischemia. Circulation 89: 2283-2289, 1994
29. Ventura-Clapier R, Veksler V, Hoerter JA: Myofibrillar creatine kinase and cardiac contraction. Mol Cell Biochem 133-134: 125-144, 1994
30. Hamman BL, Bittl JA, Jacobus WE, Allen PD, Spencer RS, Tian R, Ingwall JS: Inhibition of the creatine kinase reaction decreases the contractile reserve of isolated rat hearts. Am J Physiol 269: H1030-H1036, 1995
31. Zhang J, Ugurbil K, From AH, Bache RJ: Use of magnetic resonance spectroscopy for in vivo evaluation of high-energy phosphate metabolism in normal and abnormal myocardium. J Cardiovasc Magn Reson 2: 23-32, 2000
32. Pucar D, Bast P, Gumina RJ, Lim L, Drahl C, Juranic N, Macura S, Janssen E, Wieringa B, Terzic A, Dzeja PP: Adenylate kinase AK1 knockout heart: Energetics and functional performance under ischemia-reperfusion. Am J Physiol 283: H776-H782, 2002
33. 31P NMR. MAGMA 14: 180-181, 2002
34. 31P NMR: A novel approach to monitor the dynamics of energy metabolism in intact heart muscle. MAGMA 14: 178-180, 2002
35. 31P nuclear magnetic resonance applied to a study of enzyme-catalyzed phosphate - phosphate exchange and phosphate (oxygen) - water exchange reactions. Proc Natl Acad Sci USA 75: 200-203, 1978
36. 18O]ATP species formation. Proc Natl Acad Sci USA 76: 3646-3650, 1979
37. 18O from water. Biophys J 55: 79-99, 1989
38. 18O labeling of metabolite phosphoryls. J Biol Chem 266: 15110-15119, 1991
39. Dzeja PP, Zeleznikar RJ, Goldberg ND: Suppression of creatine kinase-catalyzed phosphotransfer results in increased phosphoryl transfer by adenylate kinase in intact skeletal muscle. J Biol Chem 271: 12847-12851, 1996
40. Zeleznikar RJ, Dzeja PP, Goldberg ND: Adenylate kinase-catalyzed phosphoryl transfer couples ATP utilization with its generation by glycolysis in intact muscle. J Biol Chem 270: 7311-7319, 1995
41. Laclau MN, Boudina S, Thambo JB, Tariosse L, Gouverneur G Bonoron-Adele S, Saks VA, Garlid KD, Dos Santos P: Cardioprotection by ischemic preconditioning preserves mitochondrial function and functional coupling between adenine nucleotide translocase and creatine kinase. J Mol Cell Cardiol 33:947-956, 2001
42. + channels by antagonizing ATP-dependent gating. Neuron 12: 885-893, 1994
43. 2+ loading: Insight into cardioprotection during cardioplegia. Ann Thorac Surg 65: 586-591, 1998
44. Hohl CM: AMP deaminase in piglet cardiac myocytes: effect on nucleotide metabolism during ischemia. Am J Physiol 276: H1502-H1510, 1999
45. Virag L, Szabo C: Purines inhibit poly(ADP-ribose) polymerase activation and modulate oxidant-induced cell death. FASEB J 15: 99-107, 2001
46. Camara-Artigas A, Parody-Morreale A, Baron C: Analogous activation of bovine liver glycogen phosphorylase by AMP and IMP. Int J Biochem Cell Biol 29: 849-856, 1997
47. Rovetto MJ, Lamberton WF, Neely JR: Mechanisms of glycolytic inhibition in ischemic rat hearts. Circ Res 37: 742-751, 1975
48. Doenst T, Han Q, Goodwin GW, Guthrie PH, Taegtmeyer H: Insulin does not change the intracellular distribution of hexokinase in rat heart. Am J Physiol 275: E558-E567, 1998
49. Kubo S, Noda LH: Adenylate kinase of porcine heart. Eur J Biochem 48: 325-331, 1974
50. + channels by adenylate kinase activity. J Biol Chem 271: 31903-31908, 1996
51. + channels. FASEB J 12: 523-529, 1998
52. Carrasco AJ, Dzeja PP, Alekseev AE, Pucar D, Zingman LV, Abraham MR, Hodgson D, Bienengraeber M, Puceat M, Janssen E, Wieringa B, Terzic A: Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP-sensitive potassium channels. Proc Natl Acad Sci USA 98: 7623-7628, 2001
53. Zingman LV, Hodgson DM, Bast PH, Kane GC, Perez-Terzic C, Gumina RJ, Pucar D, Bienengraeber M, Dzeja PP, Miki T, Seino S, Alekseev AE, Terzic A: Kir6.2 is required for adaptation to stress. Proc Natl Acad Sci USA 99: 13278-13283, 2002
54. ATP channels in cardioprotection against ischemia/reperfusion injury in mice. J Clin Invest 109: 509-516, 2002
55. Gumina RJ, Pucar D, Bast P, Hodgson DM, Kurtz CE, Dzeja PP, Miki T, Seino S, Terzic A: Knockout of Kir6.2 negates ischemic preconditioning-induced protection of myocardial energetics. Am J Physiol 284: H2106-H2113, 2003
56. Hardie DG: Roles of the AMP-activated/SNF1 protein kinase family in the response to cellular stress. Biochem Soc Symp 64: 13-27, 1999
57. Blair E, Redwood C, Ashrafian H, Oliveira M, Broxholme J, Kerr B, Salmon A, Ostman-Smith I, Watkins H: Mutations in the gamma(2) subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: Evidence for the central role of energy compromise in disease pathogenesis. Hum Mol Genet 10: 1215-1220, 2001
58. Ottaway JH, Mowbray J: The role of compartmentation in the control of glycolysis. Curr Top Cell Reg 12: 107-208, 1977
59. Jeffrey FM, Storey CJ, Malloy CR: Predicting functional recovery from ischemia in the rat myocardium. Basic Res Cardiol 87: 548-558, 1992
60. Auffermann W, Wagner S, Wu S, Buser P, Parmley WW, Wikman-Coffelt J: Calcium inhibition of glycolysis contributes to ischaemic injury. Cardiovasc Res 24: 510-520, 1990
61. Van Dobbenburgh JO, Lahpor JR, Woolley SR, de Jonge N, Klopping C, Van Echteld CJ: Functional recovery after human heart transplantation is related to the metabolic condition of the hypothermic donor heart. Circulation 94: 2831-2836, 1996
62. Schaefer S, Carr LJ, Prussel E, Ramasamy R: Effects of glycogen depletion on ischemic injury in isolated rat hearts: Insights into preconditioning. Am J Physiol 268: H935-H944, 1995
63. 31P-NMR and surface fluorometry study. Basic Res Cardiol 85: 342-357, 1990
64. Zeleznikar RJ, Heyman RA, Graeff RM, Walseth TF, Dawis SM, Butz EA, Goldberg ND: Evidence for compartmentalized adenylate kinase catalysis serving a high energy phosphoryl transfer function in rat skeletal muscle. J Biol Chem 265: 300-311, 1990
65. 31P-NMR magnetization transfer study of the isolated ferret heart. Circ Res 63: 1-15, 1988
66. Joubert F, Gillet B, Mazet JL, Mateo P, Beloeil J, Hoerter JA: Evidence for myocardial ATP compartmentation from NMR inversion transfer analysis of creatine kinase fluxes. Biophys J 79: 1-13, 2000
67. Hugel S, Horn M, de Groot M, Remkes H, Dienesch C, Hu K, Ertl G, Neubauer S: Effects of ACE inhibition and beta-receptor blockade on energy metabolism in rats postmyocardial infarction. Am J Physiol 277: H2167-H2175, 1999
68. van Zijl PC, Moonen CT: In situ changes in purine nucleotide and N-acetyl concentrations upon inducing global ischemia in cat brain. Magn Reson Med 29: 381-385, 1993
69. Middleton DA, Hockings PD, Glen S, Reid DG, Rose SE, Crozier S, Roffman W, Rothaul AL, Hunter AJ, Doddrell DM: Image directed proton spectroscopy of gerbil brain at 7 tesla. NMR Biomed 8: 118-126, 1995
70. Decanniere C, Eleff S, Davis D, van Zijl PC: Correlation of rapid changes in the average water diffusion constant and the concentrations of lactate and ATP breakdown products during global ischemia in cat brain. Magn Reson Med 34: 343-352, 1995
71. Stromski ME, Cooper K, Thulin G, Gaudio KM, Siegel NJ, Shulman RG: Chemical and functional correlates of postischemic renal ATP levels. Proc Natl Acad Sci USA 83: 6142-6145, 1986
72. 31P HMQC experiments, with selective pulses, for the assignment of less abundant metabolites. NMR Biomed 8: 190-196, 1995
73. Kalic M, Busselmann G, Lauterwein J, Kamp G: Phosphorous metabolites in boar spermatozoa. Identification of AMP by multinuclear magnetic resonance. Biochim Biophys Acta 1320: 208-216, 1997