High-energy Phosphotransfer in the Failing Mouse Heart: Role of Adenylate Kinase and Glycolytic Enzymes

Overview

Journal Eur J Heart Fail

Publisher Wiley

Specialty Cardiology & Vascular Diseases

Date 2010 Oct 14

PMID 20940173

Citations 22

Authors

Dunja Aksentijevic

Craig A Lygate

Kimmo Makinen

Sevasti Zervou

Liam Sebag-Montefiore

Debra Medway

Hannah Barnes

Jurgen E Schneider

Stefan Neubauer

Affiliations

Soon will be listed here.

Abstract

Aims: To measure the activity of the key phosphotransfer enzymes creatine kinase (CK), adenylate kinase (AK), and glycolytic enzymes in two common mouse models of chronic heart failure.

Methods And Results: C57BL/6 mice were subjected to transverse aortic constriction (TAC), myocardial infarction induced by coronary artery ligation (CAL), or sham operation. Activities of phosphotransfer enzymes CK, AK, glyceraldehyde-3-phosphate dehydrogenase (GAPDH), 3-phosphoglycerate kinase (PGK), and pyruvate kinase were assessed spectrophotometrically. Mice were characterized by echocardiography or magnetic resonance imaging 5- to 8-week post-surgery and selected for the presence of congestive heart failure. All mice had severe left ventricular hypertrophy, impaired systolic function and pulmonary congestion compared with sham controls. A significant decrease in myocardial CK and maximal CK reaction velocity was observed in both experimental models of heart failure. However, the activity of AK and its isoforms remained unchanged, despite a reduction in its protein expression. In contrast, the activities of glycolytic phosphotransfer mediators GAPDH and PGK were 19 and 12% higher in TAC, and 31 and 23% higher in CAL models, respectively.

Conclusion: Chronic heart failure in the mouse is characterized by impaired CK function, unaltered AK, and increased activity of glycolytic phosphotransfer enzymes. This pattern of altered phosphotransfer activity was observed independent of the heart failure aetiology.

Citing Articles

Maintaining energy provision in the heart: the creatine kinase system in ischaemia-reperfusion injury and chronic heart failure.

Lygate C Clin Sci (Lond). 2024; 138(8):491-514.

PMID: 38639724 PMC: 11040329. DOI: 10.1042/CS20230616.

Role of AMP deaminase in diabetic cardiomyopathy.

Miura T, Kouzu H, Tanno M, Tatekoshi Y, Kuno A Mol Cell Biochem. 2024; 479(12):3195-3211.

PMID: 38386218 DOI: 10.1007/s11010-024-04951-z.

Rat and mouse cardiomyocytes show subtle differences in creatine kinase expression and compartmentalization.

Branovets J, Soodla K, Vendelin M, Birkedal R PLoS One. 2023; 18(11):e0294718.

PMID: 38011179 PMC: 10681188. DOI: 10.1371/journal.pone.0294718.

Subtle Role for Adenylate Kinase 1 in Maintaining Normal Basal Contractile Function and Metabolism in the Murine Heart.

Zervou S, McAndrew D, Whittington H, Lake H, Park K, Cha K Front Physiol. 2021; 12:623969.

PMID: 33867998 PMC: 8044416. DOI: 10.3389/fphys.2021.623969.

Proteomic and Structural Manifestations of Cardiomyopathy in Rat Models of Obesity and Weight Loss.

Liskiewicz A, Marczak L, Bogus K, Liskiewicz D, Przybyla M, Lewin-Kowalik J Front Endocrinol (Lausanne). 2021; 12:568197.

PMID: 33716957 PMC: 7945951. DOI: 10.3389/fendo.2021.568197.

References

McGregor E, Dunn M . Proteomics of heart disease. Hum Mol Genet. 2003; 12 Spec No 2:R135-44. DOI: 10.1093/hmg/ddg278. View

Dawson D, Lygate C, Saunders J, Schneider J, Ye X, Hulbert K . Quantitative 3-dimensional echocardiography for accurate and rapid cardiac phenotype characterization in mice. Circulation. 2004; 110(12):1632-7. DOI: 10.1161/01.CIR.0000142049.14227.AD. View

Lygate C, Fischer A, Sebag-Montefiore L, Wallis J, Ten Hove M, Neubauer S . The creatine kinase energy transport system in the failing mouse heart. J Mol Cell Cardiol. 2007; 42(6):1129-36. DOI: 10.1016/j.yjmcc.2007.03.899. View

Ten Hove M, Chan S, Lygate C, Monfared M, Boehm E, Hulbert K . Mechanisms of creatine depletion in chronically failing rat heart. J Mol Cell Cardiol. 2005; 38(2):309-13. DOI: 10.1016/j.yjmcc.2004.11.016. View

Dzeja P, Terzic A . Adenylate kinase and AMP signaling networks: metabolic monitoring, signal communication and body energy sensing. Int J Mol Sci. 2009; 10(4):1729-1772. PMC: 2680645. DOI: 10.3390/ijms10041729. View

Neubauer S, Horn M, Cramer M, Harre K, Newell J, Peters W . Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation. 1997; 96(7):2190-6. DOI: 10.1161/01.cir.96.7.2190. View

Kress L, BONO Jr V, NODA L . The sulfhydryl groups of rabbit muscle adenosine triphosphate-adenosine monophosphate phosphotransferase. Activity of enzyme treated with mercurials. J Biol Chem. 1966; 241(10):2293-300. View

Ten Hove M, Lygate C, Fischer A, Schneider J, Sang A, Hulbert K . Reduced inotropic reserve and increased susceptibility to cardiac ischemia/reperfusion injury in phosphocreatine-deficient guanidinoacetate-N-methyltransferase-knockout mice. Circulation. 2005; 111(19):2477-85. DOI: 10.1161/01.CIR.0000165147.99592.01. View

Dzeja P, Pucar D, Redfield M, Burnett J, Terzic A . Reduced activity of enzymes coupling ATP-generating with ATP-consuming processes in the failing myocardium. Mol Cell Biochem. 2000; 201(1-2):33-40. DOI: 10.1023/a:1007016703229. View

10.

Dzeja P, Zeleznikar R, Goldberg N . Suppression of creatine kinase-catalyzed phosphotransfer results in increased phosphoryl transfer by adenylate kinase in intact skeletal muscle. J Biol Chem. 1996; 271(22):12847-51. DOI: 10.1074/jbc.271.22.12847. View

11.

Frederich M, Balschi J . The relationship between AMP-activated protein kinase activity and AMP concentration in the isolated perfused rat heart. J Biol Chem. 2001; 277(3):1928-32. DOI: 10.1074/jbc.M107128200. View

12.

Schneider J, Cassidy P, Lygate C, Tyler D, Wiesmann F, Grieve S . Fast, high-resolution in vivo cine magnetic resonance imaging in normal and failing mouse hearts on a vertical 11.7 T system. J Magn Reson Imaging. 2003; 18(6):691-701. DOI: 10.1002/jmri.10411. View

13.

Pucar D, Bast P, Gumina R, Lim L, Drahl C, Juranic N . Adenylate kinase AK1 knockout heart: energetics and functional performance under ischemia-reperfusion. Am J Physiol Heart Circ Physiol. 2002; 283(2):H776-82. DOI: 10.1152/ajpheart.00116.2002. View

14.

Dzeja P, Vitkevicius K, Redfield M, Burnett J, Terzic A . Adenylate kinase-catalyzed phosphotransfer in the myocardium : increased contribution in heart failure. Circ Res. 1999; 84(10):1137-43. DOI: 10.1161/01.res.84.10.1137. View

15.

Lygate C, Schneider J, Hulbert K, Ten Hove M, Sebag-Montefiore L, Cassidy P . Serial high resolution 3D-MRI after aortic banding in mice: band internalization is a source of variability in the hypertrophic response. Basic Res Cardiol. 2005; 101(1):8-16. DOI: 10.1007/s00395-005-0546-3. View

16.

de Groof A, Oerlemans F, Jost C, Wieringa B . Changes in glycolytic network and mitochondrial design in creatine kinase-deficient muscles. Muscle Nerve. 2001; 24(9):1188-96. DOI: 10.1002/mus.1131. View

17.

Neubauer S, Frank M, Hu K, Remkes H, Laser A, Horn M . Changes of creatine kinase gene expression in rat heart post-myocardial infarction. J Mol Cell Cardiol. 1998; 30(4):803-10. DOI: 10.1006/jmcc.1998.0645. View

18.

Dzeja P, Terzic A . Phosphotransfer networks and cellular energetics. J Exp Biol. 2003; 206(Pt 12):2039-47. DOI: 10.1242/jeb.00426. View

19.

Saupe K, Spindler M, Tian R, Ingwall J . Impaired cardiac energetics in mice lacking muscle-specific isoenzymes of creatine kinase. Circ Res. 1998; 82(8):898-907. DOI: 10.1161/01.res.82.8.898. View

20.

Janssen E, Terzic A, Wieringa B, Dzeja P . Impaired intracellular energetic communication in muscles from creatine kinase and adenylate kinase (M-CK/AK1) double knock-out mice. J Biol Chem. 2003; 278(33):30441-9. DOI: 10.1074/jbc.M303150200. View