Proteomic analyses of transgenic LQT1 and LQT2 rabbit hearts elucidate an increase in expression and activity of energy producing enzymes

Journal of Proteomics

Volumn 75, Issue 17, 2012, Pages 5254-5265

  Jindal, Hitesh K ^a   Merchant, Elisabeth ^a   Balschi, James A ^b   Zhangand, Yajie ^b   Koren, Gideon ^a  

^a BROWN UNIVERSITY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

2 D DIGE; Energetics; Long QT syndrome; Mass spectrometry; Metabolic remodeling; Proteomics

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALDEHYDE DEHYDROGENASE; ALPHA ACTININ 2; CREATINE KINASE; CYTOCHROME C OXIDASE; DESMOPLAKIN; DYNAMIN; ENOLASE; FATTY ACID; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCOGEN PHOSPHORYLASE; LACTATE DEHYDROGENASE; LAMIN A; LONG CHAIN ACYL COENZYME A DEHYDROGENASE; MALATE DEHYDROGENASE; PROTEIN DISULFIDE ISOMERASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE; UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; LONG QT SYNDROME; MALE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE ANALYSIS; RABBIT; TRANSGENIC ANIMAL; UPREGULATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ENERGY METABOLISM; ENZYME ACTIVATION; ENZYMES; ETHER-A-GO-GO POTASSIUM CHANNELS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEART; KCNQ1 POTASSIUM CHANNEL; LONG QT SYNDROME; MALE; MYOCARDIUM; PROTEOME; PROTEOMICS; RABBITS; ROMANO-WARD SYNDROME;

ORYCTOLAGUS CUNICULUS;

EID: 84865536323     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.06.034     Document Type: Article

References (63)

1. Moss A.J., Long Q.T. Syndrome. JAMA 2003, 289:2041-2044.
2. Priori S.G., Bloise R., Crotti L. The long QT syndrome. Europace 2001, 3:16-27.
3. Roden D.M. Clinical practice. Long-QT syndrome. N Engl J Med 2008, 358:169-176.
4. Brunner M., Peng X., Liu G.X., Ren X.Q., Ziv O., Choi B.R., et al. Mechanisms of cardiac arrhythmias and sudden death in transgenic rabbits with long QT syndrome. J Clin Invest 2008, 118:2246-2259.
5. Tomaselli G.F., Beuckelmann D.J., Calkins H.G., Berger R.D., Kessler P.D., Lawrence J.H., et al. Sudden cardiac death in heart failure. The role of abnormal repolarization. Circulation 1994, 90:2534-2539.
6. Lu J.T., Kass R.S. Recent progress in congenital long QT syndrome. Curr Opin Cardiol 2010, 25:216-221.
7. Curran M.E., Splawski I., Timothy K.W., Vincent G.M., Green E.D., Keating M.T. A molecular basis for cardiac arrhythmia: HERG mutations cause long QT syndrome. Cell 1995, 80:795-803.
8. Sanguinetti M.C., Curran M.E., Spector P.S., Keating M.T. Spectrum of HERG K+-channel dysfunction in an inherited cardiac arrhythmia. Proc Natl Acad Sci U S A 1996, 93:2208-2212.
9. Sanguinetti M.C., Curran M.E., Zou A., Shen J., Spector P.S., Atkinson D.L., et al. Coassembly of K(V)LQT1 and minK (IsK) proteins to form cardiac I(Ks) potassium channel. Nature 1996, 384:80-83.
10. Sanguinetti M.C., Jiang C., Curran M.E., Keating M.T. A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell 1995, 81:299-307.
11. Rosati B., McKinnon D. Regulation of ion channel expression. Circ Res 2004, 94:874-883.
12. Nattel S., Maguy A., Le Bouter S., Yeh Y.H. Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev 2007, 87:425-456.
13. Grant J.E., Bradshaw A.D., Schwacke J.H., Baicu C.F., Zile M.R., Schey K.L. Quantification of protein expression changes in the aging left ventricle of Rattus norvegicus. J Proteome Res 2009, 8:4252-4263.
14. Didangelos A., Simper D., Monaco C., Mayr M. Proteomics of acute coronary syndromes. Curr Atheroscler Rep 2009, 11:188-195.
15. White M.Y., Cordwell S.J., McCarron H.C., Prasan A.M., Craft G., Hambly B.D., et al. Proteomics of ischemia/reperfusion injury in rabbit myocardium reveals alterations to proteins of essential functional systems. Proteomics 2005, 5:1395-1410.
16. Sakai J., Ishikawa H., Kojima S., Satoh H., Yamamoto S., Kanaoka M. Proteomic analysis of rat heart in ischemia and ischemia-reperfusion using fluorescence two-dimensional difference gel electrophoresis. Proteomics 2003, 3:1318-1324.
17. Cieniewski-Bernard C., Mulder P., Henry J.P., Drobecq H., Dubois E., Pottiez G., et al. Proteomic analysis of left ventricular remodeling in an experimental model of heart failure. J Proteome Res 2008, 7:5004-5016.
18. Jacquet S., Yin X.K., Sicard P., Clark J., Kanaganayagam G.S., Mayr M., et al. Identification of cardiac myosin-binding protein c as a candidate biomarker of myocardial infarction by proteomics analysis. Mol Cell Proteomics 2009, 8:2687-2699.
19. Heinke M.Y., Wheeler C.H., Chang D., Einstein R., Drake-Holland A., Dunn M.J., et al. Protein changes observed in pacing-induced heart failure using two-dimensional electrophoresis. Electrophoresis 1998, 19:2021-2030.
20. De Souza A.I., Cardin S., Wait R., Patel N., Shiroshita-Takeshita A., Camm A.J., et al. Insights into molecular mechanisms of atrial profibrillatory remodelling in congestive heart failure using a proteomics approach. Heart 2008, 94:A52-A53.
21. Heinke M.Y., Wheeler C.H., Yan J.X., Amin V., Chang D., Einstein R., et al. Changes in myocardial protein expression in pacing-induced canine heart failure. Electrophoresis 1999, 20:2086-2093.
22. Stanley B.A., Graham D.R., James J., Mitsak M., Tarwater P.M., Robbins J., et al. Altered myofilament stoichiometry in response to heart failure in a cardioprotective alpha-myosin heavy chain transgenic rabbit model. Proteomics Clin Appl 2011, 5:147-158.
23. Weekes J., Wheeler C.H., Yan J.X., Weil J., Eschenhagen T., Scholtysik G., et al. Bovine dilated cardiomyopathy: proteomic analysis of an animal model of human dilated cardiomyopathy. Electrophoresis 1999, 20:898-906.
24. Unlu M., Morgan M.E., Minden J.S. Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 1997, 18:2071-2077.
25. Tannu N.S., Hemby S.E. Two-dimensional fluorescence difference gel electrophoresis for comparative proteomics profiling. Nat Protoc 2006, 1:1732-1742.
26. Zhou G., Li H., DeCamp D., Chen S., Shu H., Gong Y., et al. 2D differential in-gel electrophoresis for the identification of esophageal scans cell cancer-specific protein markers. Mol Cell Proteomics 2002, 1:117-124.
27. Guerreiro N., Staufenbiel M., Gomez-Mancilla B. Proteomic 2-D DIGE profiling of APP23 transgenic mice brain from pre-plaque and plaque phenotypes. J Alzheimers Dis 2008, 13:17-30.
28. Lewis T.S., Hunt J.B., Aveline L.D., Jonscher K.R., Louie D.F., Yeh J.M., et al. Identification of novel MAP kinase pathway signaling targets by functional proteomics and mass spectrometry. Mol Cell 2000, 6:1343-1354.
29. Gharbi S., Gaffney P., Yang A., Zvelebil M.J., Cramer R., Waterfield M.D., et al. Evaluation of two-dimensional differential gel electrophoresis for proteomic expression analysis of a model breast cancer cell system. Mol Cell Proteomics 2002, 1:91-98.
30. Mayr M., Yusuf S., Weir G., Chung Y.L., Mayr U., Yin X., et al. Combined metabolomic and proteomic analysis of human atrial fibrillation. J Am Coll Cardiol 2008, 51:585-594.
31. Kourliouros A., Yin X.K., Didangelos A., Hosseini M.T., Valencia O., Mayr M., et al. Substrate modifications precede the development of atrial fibrillation after cardiac surgery: a proteomic study. Ann Thorac Surg 2011, 92:104-110.
32. Warren C.M., Arteaga G.M., Rajan S., Ahmed R.P.H., Wieczorek D.F., Solaro R.J. Use of 2-D DIGE analysis reveals altered phosphorylation in a tropomyosin mutant (Glu54Lys) linked to dilated cardiomyopathy. Proteomics 2008, 8:100-105.
33. De Souza A.I., Cardin S., Wait R., Chung Y.L., Vijayakumar M., Maguy A., et al. Proteomic and metabolomic analysis of atrial profibrillatory remodelling in congestive heart failure. J Mol Cell Cardiol 2010, 49:851-863.
34. Odening K.E., Hyder O., Chaves L., Schofield L., Brunner M., Kirk M., et al. Pharmacogenomics of anesthetic drugs in transgenic LQT1 and LQT2 rabbits reveal genotype-specific differential effects on cardiac repolarization. Am J Physiol Heart Circ Physiol 2008, 295:H2264-H2272.
35. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
36. Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006, 1:2856-2860.
37. Elias J.E., Gygi S.P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 2007, 4:207-214.
38. Jindal H.K., Folco E.J., Liu G.X., Koren G. Posttranslational modification of voltage-dependent potassium channel Kv1.5: COOH-terminal palmitoylation modulates its biological properties. Am J Physiol Heart Circ Physiol 2008, 294:H2012-H2021.
39. Ortmeyer H.K., Bodkin N.L., Hansen B.C. Insulin regulates liver glycogen synthase and glycogen phosphorylase activity reciprocally in rhesus monkeys. Am J Physiol 1997, 272:E133-E138.
40. Gilboe D.P., Larson K.L., Nuttall F.Q. Radioactive method for the assay of glycogen phosphorylases. Anal Biochem 1972, 47:20-27.
41. Gibbs M., Earl J.M., Ritchie J.L. Metabolism of ribose-1-C14 by cell-free extracts of yeast. J Biol Chem 1955, 217:161-168.
42. Ingwall J.S. On substrate selection for ATP synthesis in the failing human myocardium. Am J Physiol Heart Circ Physiol 2007, 293:H3225-H3226.
43. Ingwall J.S. Energy metabolism in heart failure and remodelling. Cardiovasc Res 2009, 81:412-419.
44. Ingwall J.S., Weiss R.G. Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ Res 2004, 95:135-145.
45. Allard M.F., Schonekess B.O., Henning S.L., English D.R., Lopaschuk G.D. Contribution of oxidative metabolism and glycolysis to ATP production in hypertrophied hearts. Am J Physiol 1994, 267:H742-H750.
46. Apstein C.S. Glucose-insulin-potassium for acute myocardial infarction: remarkable results from a new prospective, randomized trial. Circulation 1998, 98:2223-2226.
47. Liao R., Jain M., Cui L., D'Agostino J., Aiello F., Luptak I., et al. Cardiac-specific overexpression of GLUT1 prevents the development of heart failure attributable to pressure overload in mice. Circulation 2002, 106:2125-2131.
48. Osorio J.C., Stanley W.C., Linke A., Castellari M., Diep Q.N., Panchal A.R., et al. Impaired myocardial fatty acid oxidation and reduced protein expression of retinoid X receptor-alpha in pacing-induced heart failure. Circulation 2002, 106:606-612.
49. Barth A.S., Merk S., Arnoldi E., Zwermann L., Kloos P., Gebauer M., et al. Reprogramming of the human atrial transcriptome in permanent atrial fibrillation: expression of a ventricular-like genomic signature. Circ Res 2005, 96:1022-1029.
50. McDonald T.F., MacLeod D.P. Metabolism and the electrical activity of anoxic ventricular muscle. J Physiol 1973, 229:559-582.
51. Taniguchi J., Noma A., Irisawa H. Modification of the cardiac action potential by intracellular injection of adenosine triphosphate and related substances in guinea pig single ventricular cells. Circ Res 1983, 53:131-139.
52. Barth A.S., Tomaselli G.F. Cardiac metabolism and arrhythmias. Circ Arrhythm Electrophysiol 2009, 2:327-335.
53. Beuckelmann D.J., Nabauer M., Erdmann E. Intracellular calcium handling in isolated ventricular myocytes from patients with terminal heart failure. Circulation 1992, 85:1046-1055.
54. Gwathmey J.K., Copelas L., MacKinnon R., Schoen F.J., Feldman M.D., Grossman W., et al. Abnormal intracellular calcium handling in myocardium from patients with end-stage heart failure. Circ Res 1987, 61:70-76.
55. London B., Baker L.C., Lee J.S., Shusterman V., Choi B.R., Kubota T., et al. Calcium-dependent arrhythmias in transgenic mice with heart failure. Am J Physiol Heart Circ Physiol 2003, 284:H431-H441.
56. Balaban R.S. Cardiac energy metabolism homeostasis: role of cytosolic calcium. J Mol Cell Cardiol 2002, 34:1259-1271.
57. Denton R.M., Randle P.J., Bridges B.J., Cooper R.H., Kerbey A.L., Pask H.T., et al. Regulation of mammalian pyruvate dehydrogenase. Mol Cell Biochem 1975, 9:27-53.
58. Hansford R.G. Physiological role of mitochondrial Ca2+ transport. J Bioenerg Biomembr 1994, 26:495-508.
59. Randle P.J., Denton R.M., Pask H.T., Severson D.L. Calcium ions and the regulation of pyruvate dehydrogenase. Biochem Soc Symp 1974, 75-88.
60. Saga A., Karibe A., Otomo J., Iwabuchi K., Takahashi T., Kanno H., et al. Lamin A/C gene mutations in familial cardiomyopathy with advanced atrioventricular block and arrhythmia. Tohoku J Exp Med 2009, 218:309-316.
61. Delmar M., McKenna W.J. The cardiac desmosome and arrhythmogenic cardiomyopathies from gene to disease. Circ Res 2010, 107:700-714.
62. Odening K.E., Choi B.R., Liu G.X., Hartmann K., Ziv O., Chaves L., et al. Estradiol promotes sudden cardiac death in transgenic long QT type 2 rabbits while progesterone is protective. Heart Rhythm 2012, 9:823-832.
63. Liu G.X., Choi B.R., Ziv O., Li W., de Lange E., Qu Z., et al. Differential conditions for early after-depolarizations and triggered activity in cardiomyocytes derived from transgenic LQT1 and LQT2 rabbits. J Physiol 2012, 590:1171-1180.