Reductions in mitochondrial O2 consumption and preservation of high-energy phosphate levels after simulated ischemia in chronic hibernating myocardium

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 297, Issue 1, 2009, Pages

  Hu, Qingsong ^b   Suzuki, Gen ^b   Young, Rebeccah F ^b   Page, Brian J ^a,b   Fallavollita, James A ^a,b   Canty Jr , John M ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Energy metabolism; Mitochondrial respiration; Stunned myocardium

Indexed keywords

ADENINE NUCLEOTIDE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CREATINE; CREATINE PHOSPHATE; LACTIC ACID; PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENERGY METABOLISM; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE OXYGEN CONSUMPTION; HEART PROTECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; MITOCHONDRIAL RESPIRATION; MYOCARDIAL HIBERNATION; NONHUMAN; PRIORITY JOURNAL; SIMULATION; STUNNED HEART MUSCLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHRONIC DISEASE; CORONARY CIRCULATION; CORONARY OCCLUSION; CORONARY VESSELS; ELECTROPHYSIOLOGY; ENDOCARDIUM; ENERGY METABOLISM; FLUORESCENT DYES; LACTIC ACID; MITOCHONDRIA, HEART; MYOCARDIAL ISCHEMIA; MYOCARDIAL STUNNING; OXYGEN CONSUMPTION; PHOSPHATES; SWINE;

EID: 67650069937     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00992.2008     Document Type: Article

References (56)

1. Ausma J, Thone F, Dispersyn GD, Flameng W, Vanoverschelde JL, Ramaekers FC, Borgers M. Dedifferentiated cardiomyocytes from chronic hibernating myocardium are ischemia-tolerant. Mol Cell Biochem 186: 159-168, 1998.
2. Banas MD, Baldwa S, Suzuki G, Canty JM, Fallavollita JA. Determinants of contractile reserve in viable, chronically dysfunctional myocardium. Am J Physiol Heart Circ Physiol 292: H2791-H2797, 2007.
3. Bolli R. Mechanism of myocardial stunning. Circulation 82: 723-738, 1990.
4. Canty JM, Fallavollita JA. Hibernating myocardium. J Nucl Cardiol 12: 104-119, 2005.
5. Canty JM Jr. Coronary blood flow and myocardial ischemia. In: Braunwald's Heart Disease, edited by Libby P, Bonow RO, Mann DL, and Zipes DP. Philadelphia: Elsevier, 2007, p. 1167-1194.
6. Canty JM Jr, Suzuki G, Banas MD, Verheyen F, Borgers M, Fallavollita JA. Hibernating myocardium: chronically adapted to ischemia but vulnerable to sudden death. Circ Res 94: 1142-1149, 2004.
7. Depre C, Vatner SF. Cardioprotection in stunned and hibernating myocardium. Heart Fail Rev 12: 307-317, 2007.
8. + channel protects the ischemic heart. Am J Physiol Heart Circ Physiol 283: H284-H295, 2002.
9. Duan X, Young RF, Straubinger RM, Page BJ, Cao J, Wang H, Yu Y, Canty JM Jr, Qu J. A straightforward and highly efficient precipitation/on-pellet digestion procedure coupled to a long gradient nano-LC separation and Oprbitrap mass spectrometry for label-free expression profiling of the swine heart mitochondrial proteome. J Proteome Res. In press.
10. Elsasser A, Muller KD, Skwara W, Bode C, Kubler W, Vogt AM. Severe energy deprivation of human hibernating myocardium as possible common pathomechanism of contractile dysfunction, structural degeneration and cell death. J Am Coll Cardiol 39: 1189-1198, 2002.
11. Fallavollita JA, Malm BJ, Canty JM Jr. Hibernating myocardium retains metabolic and contractile reserve despite regional reductions in flow, function, and oxygen consumption at rest. Circ Res 92: 48-55, 2003.
12. 18F-2- deoxyglucose deposition and regional flow in pigs with chronically dysfunctional myocardium: evidence for transmural variations in chronic hibernating myocardium. Circulation 95: 1900-1909, 1997.
13. Gho BCG, Schoemaker RG, van den Doel MA, Duncker DJ, Verdouw PD. Myocardial protection by brief ischemia in noncardiac tissue. Circulation 94: 2193-2200, 1996.
14. Harrison BS, Eberli D, Lee SJ, Atala A, Yoo JJ. Oxygen producing biomaterials for tissue regeneration. Biomaterials 28: 4628-4634, 2007.
15. Hausenloy DJ, Mwamure PK, Venugopal V, Harris J, Barnard M, Grundy E, Ashley E, Vichare S, Di Salvo C, Kolvekar S, Hayward M, Keogh B, MacAllister RJ, Yellon DM. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet 370: 575-579, 2007.
16. Heusch G. Obesity - a risk factor or a RISK factor for myocardial infarction? Br J Pharmacol 149: 1-3, 2006.
17. Heusch G, Post H, Michel MC, Kelm M, Schulz R. Endogenous nitric oxide and myocardial adaptation to ischemia. Circ Res 87: 146-152, 2000.
18. Heusch G, Schulz R, Rahimtoola SH. Myocardial hibernation: a delicate balance. Am J Physiol Heart Circ Physiol 288: H984-H999, 2005.
19. Hoppel C, DiMarco JP, Tandler B. Riboflavin and rat hepatic cell structure and function. Mitochondrial oxidative metabolism in deficiency states. J Biol Chem 254: 4164-4170, 1979.
20. Hu Q, Wang X, Lee J, Mansoor A, Liu J, Zeng L, Swingen C, Zhang G, Feygin J, Ochiai K, Bransford TL, From AH, Bache RJ, Zhang J. Profound bioenergetic abnormalities in peri-infarct myocardial regions. Am J Physiol Heart Circ Physiol 291: H648-H657, 2006.
21. Ingwall JS, Weiss RG. Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ Res 95: 135-145, 2004.
22. Jennings RB, Murry CE, Reimer KA. Energy metabolism in preconditioned and control myocardium: effect of total ischemia. J Mol Cell Cardiol 23: 1449-1458, 1991.
23. Jennings RB, Reimer KA, Hill ML, Mayer SE. Total ischemia in dog hearts, in vitro. 1. Comparison of high energy phosphate production, utilization, and depletion, and of adenine nucleotide catabolism in total ischemia in vitro vs. severe ischemia in vivo. Circ Res 49: 892-900, 1981.
24. Jennings RB, Reimer KA, Steenbergen C. Effect of inhibition of the mitochondrial ATPase on net myocardial ATP in total ischemia. J Mol Cell Cardiol 23: 1383-1395, 1991.
25. Kalra DK, Zhu X, Ramchandani MK, Lawrie G, Reardon MJ, Lee-Jackson D, Winters WL, Sivasubramanian N, Mann DL, Zoghbi WA. Increased myocardial gene expression of tumor necrosis factor-α and nitric oxide synthase-2: a potential mechanism for depressed myocardial function in hibernating myocardium in humans. Circulation 105: 1537-1540, 2002.
26. Kowallik P, Schulz R, Guth BD, Schade A, Paffhausen W, Gross R, Heusch G. Measurement of regional myocardial blood flow with multiple colored microspheres. Circ Res 83: 974-982, 1991.
27. eq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J Biol Chem 254: 6528-6537, 1979.
28. 31P magnetic resonance spectroscopy of mouse heart at 4.7 Tesla. J Magn Reson Imaging 24: 1269-1276, 2006.
29. Martin C, Schulz R, Rose J, Heusch G. Inorganic phosphate content and free energy change of ATP hydrolysis in regional short-term hibernating myocardium. Cardiovasc Res 39: 318-326, 1998.
30. McFalls EO, Baldwin D, Palmer B, Marx D, Jaimes D, Ward HB. Regional glucose uptake within hypoperfused swine myocardium as measured by positron emission tomography. Am J Physiol Heart Circ Physiol 272: H343-H349, 1997.
31. McFalls EO, Hou M, Bache RJ, Best A, Marx D, Sikora J, Ward HB. Activation of p38 MAPK and increased glucose transport in chronic hibernating swine myocardium. Am J Physiol Heart Circ Physiol 287: H1328-H1334, 2004.
32. McFalls EO, Kelly RF, Hu Q, Mansoor A, Lee J, Kuskowski M, Sikora J, Ward HB, Zhang J. The energetic state within hibernating myocardium is normal during dobutamine despite inhibition of ATP-dependent potassium channel opening with glibenclamide. Am J Physiol Heart Circ Physiol 293: H2945-H2951, 2007.
33. McFalls EO, Sluiter W, Schoonderwoerd K, Manintveld OC, Lamers JM, Bezstarosti K, van Beusekom HM, Sikora J, Ward HB, Merkus D, Duncker DJ. Mitochondrial adaptations within chronically ischemic swine myocardium. J Mol Cell Cardiol 41: 980-988, 2006.
34. Milei J, Fraga CG, Grana DR, Ferreira R, Ambrosio G. Ultrastructural evidence of increased tolerance of hibernating myocardium to cardioplegic ischemia-reperfusion injury. J Am Coll Cardiol 43: 2329-2336, 2004.
35. Miller EJ, Li J, Leng L, McDonald C, Atsumi T, Bucala R, Young LH. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature 451: 578-582, 2008.
36. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Muller C, Carling D, Kahn BB. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415: 339-343, 2002.
37. Murry CE, Richard VJ, Reimer KA, Jennings RB. Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ Res 66: 913-931, 1990.
38. Ovize M, Kloner RA, Przyklenk K. Stretch preconditions canine myocardium. Am J Physiol Heart Circ Physiol 266: H137-H146, 1994.
39. Page B, Young R, Iyer V, Suzuki G, Lis M, Korotchkina K, Patel M, Blumenthal K, Fallavollita J, Canty JM Jr. Persistent regional down-regulation in mitochondrial enzymes and upregulation of stress proteins in swine with chronic hibernating myocardium. Circ Res 102: 103-112, 2008.
40. Palmer JW, Tandler B, Hoppel CL. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 252: 8731-8739, 1977.
41. Pantely GA, Malone SA, Rhen WS, Anselone CG, Arai A, Bristow J, Bristow JD. Regeneration of myocardial phosphocreatine in pigs despite continued moderate ischemia. Circ Res 67: 1481-1493, 1990.
42. Russell RR 3rd, Li J, Coven DL, Pypaert M, Zechner C, Palmeri M, Giordano FJ, Mu J, Birnbaum MJ, Young LH. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest 114: 495-503, 2004.
43. Schiller NB, Shah PM, Crawford M, DeMaria A, Devereux R, Feigenbaum H, Gutgesell H, Reichek N, Sahn D, Schnittger I. Recommendations for quantitation of the left ventricle by two-dimensional echocardiography. American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. J Am Soc Echocardiogr 2: 358-367, 1989.
44. Schott P, Asif AR, Graf C, Toischer K, Hasenfuss G, Kogler H. Myocardial adaptation of energy metabolism to elevated preload depends on calcineurin activity: a proteomic approach. Basic Res Cardiol 103: 232-243, 2008.
45. Schulz R, Guth BD, Pieper K, Martin C, Heusch G. Recruitment of an inotropic reserve in moderately ischemic myocardium at the expense of metabolic recovery: a model of short-term hibernation. Circ Res 70: 1282-1295, 1992.
46. Schulz R, Rose J, Martin C, Brodde OE, Heusch G. Development of short-term myocardial hibernation: its limitation by the severity of ischemia and inotropic stimulation. Circulation 88: 684-695, 1993.
47. ATP channels. Am J Physiol Heart Circ Physiol 268: H2294-H2301, 1995.
48. Sellevold OFM, Jynge P, Aarstad K. High performance liquid chromatography: a rapid isocratic method for determination of creatine compounds and adenine nucleotides in myocardial tissue. J Mol Cell Cardiol 18: 517-527, 1986.
49. Shibata R, Sato K, Pimentel DR, Takemura Y, Kihara S, Ohashi K, Funahashi T, Ouchi N, Walsh K. Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2-dependent mechanisms. Nat Med 11: 1096-1103, 2005.
50. Smith CCT, Mocanu MM, Davidson SM, Wynne AM, Simpkin JC, Yellon DM. Leptin, the obesity-associated hormone, exhibits direct cardioprotective effects. Br J Pharmacol 149: 5-13, 2006.
51. Suto N, Mikuniya A, Okubo T, Hanada H, Shinozaki N, Okumura K. Nitric oxide modulates cardiac contractility and oxygen consumption without changing contractile efficiency. Am J Physiol Heart Circ Physiol 275: H41-H49, 1998.
52. Suzuki G, Lee TC, Fallavollita JA, Canty JM Jr. Adenoviral gene transfer of FGF-5 to hibernating myocardium improves function and stimulates myocytes to hypertrophy and reenter the cell cycle. Circ Res 96: 767-775, 2005.
53. Thijssen VL, Borgers M, Lenders MH, Ramaekers FC, Suzuki G, Palka B, Fallavollita JA, Thomas SA, Canty JM Jr. Temporal and spatial variations in structural protein expression during the progression from stunned to hibernating myocardium. Circulation 110: 3313-3321, 2004.
54. Thomas SA, Fallavollita JA, Borgers M, Canty JM Jr. Dissociation of regional adaptations to ischemia and global myolysis in an accelerated swine model of chronic hibernating myocardium. Circ Res 91: 970-977, 2002.
55. Vander Heide RS, Reimer KA, Jennings RB. Adenosine slows ischaemic metabolism in canine myocardium in vitro: relationship to ischaemic preconditioning. Cardiovasc Res 27: 669-673, 1993.
56. Wiggers H, Noreng M, Paulsen PK, Bottcher M, Egeblad H, Nielsen TT, Botker HE. Energy stores and metabolites in chronic reversibly and irreversibly dysfunctional myocardium in humans. J Am Coll Cardiol 37: 100-108, 2001.