In vivo alterations in cardiac metabolism and function in the spontaneously hypertensive rat heart

Cardiovascular Research

Volumn 95, Issue 1, 2012, Pages 69-76

  Dodd, Michael S ^a   Ball, Daniel R ^a   Schroeder, Marie A ^a   Le Page, Lydia M ^a   Atherton, Helen J ^a   Heather, Lisa C ^a   Seymour, Anne Marie ^b   Ashrafian, Houman ^a   Watkins, Hugh ^a   Clarke, Kieran ^a   Tyler, Damian J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF HULL   (United Kingdom)

Author keywords

Carbon 13 Magnetic resonance spectroscopy; Dynamic nuclear polarization; Metabolism; Pyruvate dehydrogenase; Spontaneously hypertensive rat

Indexed keywords

ACETYLCARNITINE; CITRIC ACID; GLUTAMIC ACID; PYRUVATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; DIASTOLE; ENZYME ACTIVITY; GLUCOSE OXIDATION; GLYCOLYSIS; HEART FUNCTION; HEART HYPERTROPHY; HEART MUSCLE METABOLISM; HEART RATE; HEART STROKE VOLUME; HYPERTENSION; IN VIVO STUDY; MALE; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; BICARBONATES; CARBON DIOXIDE; CARDIOMEGALY; CITRIC ACID CYCLE; HYDROGEN-ION CONCENTRATION; HYPERTENSION; MAGNETIC RESONANCE IMAGING, CINE; MALE; MYOCARDIUM; PYRUVATE DEHYDROGENASE COMPLEX; RATS; RATS, INBRED SHR; RATS, WISTAR;

EID: 84862901056     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs164     Document Type: Article

References (48)

1. WHO. Global Health Observatory Data Repository [Internet]. Available from: http://apps.who.int/ghodata/(17 February 2012).
2. Opie LH. Heart Physiology: From Cell to Circulation. 4th ed. Philadelphia: Lippincott Williams & Wilkins; 2004.
3. Visscher MB, Mulder AG. The carbohydrate metabolism of the heart. Am J Physiol 1930;94:630-640.
4. Bing RJ, Siegel A, Ungar I, Gilbert M. Metabolism of the human heart II. Studies on fat, ketone and amino acid metabolism. Am J Med 1954;16:504-515.
5. Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1963;1785:785-789.
6. Neubauer S. The failing heart-an engine out of fuel. New Engl J Med 2007;356: 1140-1151.
7. Ashrafian H, Redwood C, Blair E, Watkins H. Hypertrophic cardiomyopathy: a paradigm for myocardial energy depletion. Trends Genet 2003;19:263-268.
8. Iemitsu M, Shimojo N, Maeda S, Irukayama-Tomobe Y, Sakai S, Ohkubo T et al. The benefit of medium-chain triglyceride therapy on the cardiac function of SHRs is associated with a reversal of metabolic and signaling alterations. Am J Physiol Heart Circ Physiol 2008;295:H136-H144.
9. Shimamoto N, Goto N, Tanabe M, Imamoto T, Fujiwara S, Hirata M. Myocardial energy metabolism in the hypertrophied hearts of spontaneously hypertensive rats. Basic Res Cardiol 1982;77:359-371.
10. McGuire PG, Twietmeyer TA. Aortic endothelial junctions in developing hypertension. Hypertension 1985;7:483-490.
11. Aitman TJ, Glazier AM, Wallace CA, Cooper LD, Norsworthy PJ, Wahid FN et al. Identification of Cd36 (Fat) as an insulin-resistance gene causing defective fatty acid and glucose metabolism in hypertensive rats. Nat Genet 1999;21:76-83.
12. Hajri T, Han XX, Bonen A, Abumrad NA. Defective fatty acid uptake modulates insulin responsiveness and metabolic responses to diet in CD36-null mice. J Clin Invest 2002;109:1381-1389.
13. Labarthe F, Khairallah M, Bouchard B, Stanley WC, Des Rosiers C. Fatty acid oxidation and its impact on response of spontaneously hypertensive rat hearts to an adrenergic stress: benefits of a medium-chain fatty acid. Am J Physiol Heart Circ Physiol 2005; 288:1425-1436.
14. Hajri T, Ibrahimi A, Coburn CT, Knapp FF, Kurtz T, Pravenec M et al. Defective fatty acid uptake in the spontaneously hypertensive rat is a primary determinant of altered glucose metabolism, hyperinsulinemia, and myocardial hypertrophy. J Biol Chem 2001; 276:23661-23666.
15. Rimbaud S, Sanchez H, Garnier A, Fortin D, Bigard X, Veksler V et al. Stimulus specific changes of energy metabolismin hypertrophied heart. JMol Cell Cardiol 2009;46:952-959.
16. Atherton HJ, Schroeder MA, Dodd MS, Heather LC, Carter EE, Cochlin LE et al. Validation of the in vivo assessment of pyruvate dehydrogenase activity using hyperpolarised (13)C MRS. NMR Biomed 2011;24:201-208.
17. Schroeder MA, Cochlin LE, Heather LC, Clarke K, Radda GK, Tyler DJ. In vivo assessment of pyruvate dehydrogenase flux in the heart using hyperpolarized carbon-13 magnetic resonance. P Natl Acad Sci USA 2008;105:12051-12056.
18. Seymour AM, Chatham JC. The effects of hypertrophy and diabetes on cardiac pyruvate dehydrogenase activity. J Mol Cell Cardiol 1997;29:2771-2778.
19. Wu P, Sato J, Zhao Y, Jaskiewicz J, Popov KM, Harris RA. Starvation and diabetes increase the amount of pyruvate dehydrogenase kinase isoenzyme 4 in rat heart. Biochem J 1998;329:197-201.
20. Paternostro G, Clarke K, Heath J, Seymour AM, Radda GK. Decreased GLUT-4 mRNA content and insulin-sensitive deoxyglucose uptake show insulin resistance in the hypertensive rat heart. Cardiovasc Res 1995;30:205-211.
21. Ardenkjaer-Larsen JH, Fridlund B, Gram A, Hansson G, Hansson L, Lerche MH et al. Increase in signal-to-noise ratio of .10 000 times in liquid-state NMR. P Natl Acad Sci USA 2003;100:10158-10163.
22. Golman K, Ardenkjaer-Larsen JH, Petersson JS, Mansson S, Leunbach I. Molecular imaging with endogenous substances. P Natl Acad Sci USA 2003;100:10435-10439.
23. Golman K, Olsson LE, Axelsson O, Mansson S, Karlsson M, Petersson JS. Molecular imaging using hyperpolarized 13C. Br J Radiol 2003;76:S118-S127.
24. Schroeder MA, Atherton HJ, Dodd MS, Lee P, Cochlin LE, Radda GK et al. The cycling of acetyl-CoA through acetylcarnitine buffers cardiac substrate supply: a hyperpolarised 13C magnetic resonance study. Circ Cardiovasc Imaging 2012;5:201-209.
25. Schroeder MA, Atherton HJ, Ball DR, Cole MA, Heather LC, Griffin JL et al. Real-time assessment of Krebs cycle metabolism using hyperpolarized 13C magnetic resonance spectroscopy. FASEB J 2009;23:2529-2538.
26. Cassidy PJ, Schneider JE, Grieve SM, Lygate CA, Tyler DJ, Neubauer S et al. An animal handling system for small animals in vivo MR. ISMRM (Abstract). 2005. p488.
27. Tyler D, Lygate C, Schneider J, Cassidy P, Neubauer S, Clarke K. CINE-MR imaging of the normal and infarcted rat heart using an 11.7 T vertical bore MR system. J Cardiovasc Magn Res 2006;8:327-333.
28. Stuckey D, Carr C, Tyler D, Aasum E, Clarke K. Novel MRI method to detect altered left ventricular ejection and filling patterns in rodent models of disease. Magn Reson Med 2008;60:582-587.
29. Naressi A, Couturier C, Castang I, de Beer R, Graveron-Demilly D. Java-based graphical user interface for MRUI, a software package for quantitation of in vivo/medical magnetic resonance spectroscopy signals. Comput Biol Med 2001;31: 269-286.
30. Zierhut ML, Yen Y-FF, Chen AP, Bok R, Albers MJ, Zhang V et al. Kinetic modeling of hyperpolarized 13C1-pyruvate metabolism in normal rats and TRAMP mice. J Magn Reson 2010;202:85-92.
31. Atherton HJ, Dodd MS, Heather LC, Schroeder MA, Griffin JL, Radda GK et al. Role of pyruvate dehydrogenase inhibition in the development of hypertrophy in the hyperthyroid rat heart: a combined magnetic resonance imaging and hyperpolarized magnetic resonance spectroscopy study. Circulation 2011;123:2552-2561.
32. Schroeder MA, Swietach P, Atherton HJ, Gallagher FA, Lee P, Radda GK et al. Measuring intracellular pH in the heart using hyperpolarized carbon dioxide and bicarbonate: a 13C and 31P magnetic resonance spectroscopy study. Cardiovasc Res 2010;86: 82-91.
33. Heather LC, Cole MA, Lygate CA, Evans RD, Stuckey DJ, Murray AJ et al. Fatty acid transporter levels and palmitate oxidation rate correlate with ejection fraction in the infarcted rat heart. Cardiovascr Res 2006;72:430-437.
34. Cross HR, Clarke K, Opie LH, Radda GK, Heart I, Town C. Young investigator finalist from 1994 ISHR European section meeting is lactate-induced myocardial ischaemic injury mediated by decreased pH or increased intracellular lactate? J Mol Cell Cardiol 1995;27:1369-1381.
35. Murray AJ, Lygate CA, Cole MA, Carr CA, Radda GK, Neubauer S et al. Insulin resistance, abnormal energy metabolism and increased ischemic damage in the chronically infarcted rat heart. Cardiovasc Res 2006;71:149-157.
36. Cuneo ME, Grassi de Gende AO. Cardiac sarcoplasmic reticulum characteristics in hypertrophic hearts from spontaneously hypertensive rats. Basic Res Cardiol 1988; 83:286-295.
37. Meerson FZ. Compensatory hyperfunction of the heart and cardiac insufficiency. Circ Res 1962;X:250-258.
38. Felig P, Pozefsky T, Marliss E, Cahill GF. Alanine: key role in gluconeogenesis. Science 1970;167:1003-1004.
39. Conlay LA, Maher TJ, Wurtman RJ. Alanine increases blood pressure during hypotension. Pharmacol Toxicol 1990;66:415-416.
40. Holmes E, Loo RL, Stamler J, Bictash M, Yap IKS, Chan Q et al. Human metabolic phenotype diversity and its association with diet and blood pressure. Nature 2008; 453:396-400.
41. Lauzier B, Merlen C, Vaillant F, McDuff J, Bouchard B, Beguin PC et al. Posttranslational modifications, a key process in CD36 function: lessons from the spontaneously hypertensive rat heart. J Mol Cell Cardiol 2011;51:99-108.
42. Bowker-Kinley MM, Davis WI, Wu P, Harris RA, Popov KM. Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem J 1998;329:191-196.
43. Huang B, Wu P, Bowker-Kinley MM, Harris RA. Regulation of pyruvate dehydrogenase kinase expression by peroxisome proliferator-activated receptor-alpha ligands, glucocorticoids, and insulin. Diabetes 2002;51:276-283.
44. Kim J-W, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006;3:177-185.
45. Denton RMM, Randle PJ, Martin BR. Stimulation by calcium ions of pyruvate dehydrogenase phosphate phosphatase. Biochem J 1972;128:161-163.
46. Christe M, Rodgers RL. Altered glucose and fatty acid oxidation in hearts of the spontaneously hypertensive rat. J Mol Cell Cardiol 1994;26:1371-1375.
47. Schroeder MA, Clarke K, Neubauer S, Tyler DJ. Hyperpolarized magnetic resonance: a novel technique for the in vivo assessment of cardiovascular disease. Circulation 2011;124:1580-1594.
48. Schroeder MA, Atherton HJ, Cochlin LE, Clarke K, Radda GK, Tyler DJ. The effect of hyperpolarized tracer concentration on myocardial uptake and metabolism. Magn Reson Med 2009;61:1007-1014.