Reproducible ion-current-based approach for 24-Plex comparison of the tissue proteomes of hibernating versus normal myocardium in swine models

Journal of Proteome Research

Volumn 13, Issue 5, 2014, Pages 2571-2584

  Qu, Jun ^a,b   Young, Rebeccah ^b   Page, Brian J ^b   Shen, Xiaomeng ^a,b   Tata, Nazneen ^b   Li, Jun ^a,b   Duan, Xiaotao ^a,b   Fallavollita, James A ^b,c   Canty, John M ^b,c  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c VA WESTERN NEW YORK HEALTHCARE SYSTEM   (United States)

Author keywords

biomarker discovery; ion current based quantification; label free proteomics; myocardial ischemia; proteomics

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ALPHA CRYSTALLIN; ALPHA ENOLASE; ALPHA TUBULIN; BETA TUBULIN; CARNITINE PALMITOYLTRANSFERASE I; COFILIN 1; DESMIN; DESMOPLAKIN; FUMARATE HYDRATASE; GLUTATHIONE PEROXIDASE 1; GLYCOGEN SYNTHASE; HEAT SHOCK PROTEIN 27; ISOVALERYL COENZYME A DEHYDROGENASE; LAMIN C; LONG CHAIN ACYL COENZYME A DEHYDROGENASE; MACROPHAGE MIGRATION INHIBITION FACTOR; MALATE DEHYDROGENASE; MYOSIN BINDING PROTEIN C; MYOSIN HEAVY CHAIN ALPHA; PEROXIREDOXIN 1; PROPIONYL COENZYME A CARBOXYLASE; PROTEIN 14 3 3; PROTEOME; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE E1ALPHA; THIOREDOXIN; TROPONIN T; UNCLASSIFIED DRUG; VIMENTIN; VINCULIN;

AEROBIC METABOLISM; ANAEROBIC GLYCOLYSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL VIABILITY; CHEMICAL PARAMETERS; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; EXTRACTION; FALSE DISCOVERY RATE; GLYCOGEN SYNTHESIS; HEART; HEART CONTRACTION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART PROTECTION; HEART STRESS; ION CURRENT; ION CURRENT BASED PROTEOMICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; MYOCARDIAL HIBERNATION; NONHUMAN; PORCINE MODEL; PRECIPITATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; REDUCTION; REGULATORY MECHANISM; REPRODUCIBILITY; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION; ADAPTATION; ANIMAL; CARDIAC MUSCLE; COMPARATIVE STUDY; HEART MUSCLE ISCHEMIA; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PIG; PROCEDURES;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CHROMATOGRAPHY, LIQUID; HUMANS; MASS SPECTROMETRY; MODELS, ANIMAL; MYOCARDIAL ISCHEMIA; MYOCARDIUM; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SWINE; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

EID: 84899854225     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5000472     Document Type: Article

References (76)

1. 18F-2- deoxyglucose deposition and regional flow in pigs with chronically dysfunctional myocardium: Evidence for transmural variations in chronic hibernating myocardium Circulation 1997, 95, 1900-1909
2. Kelly, R. F.; Sluiter, W.; McFalls, E. O. Hibernating myocardium: is the program to survive a pathway to failure? Circ. Res. 2008, 102 (1) 3-5
3. Fallavollita, J. A.; Malm, B. J.; Canty, J. M., Jr. Hibernating myocardium retains metabolic and contractile reserve despite regional reductions in flow, function, and oxygen consumption at rest Circ. Res. 2003, 92 (1) 48-55
4. Fallavollita, J. A. Spatial heterogeneity in fasting and insulin-stimulated 18F-2-deoxyglucose uptake in pigs with hibernating myocardium Circulation 2000, 102 (8) 908-914
5. McFalls, E. O.; Baldwin, D.; Palmer, B.; Marx, D.; Jaimes, D.; Ward, H. B. Regional glucose uptake within hypoperfused swine myocardium as measured by positron emission tomography Am. J. Physiol. 1997, 272 (1) H343-H349
6. Wiggers, H.; Noreng, M.; Paulsen, P. K.; Bottcher, M.; Egeblad, H.; Nielsen, T. T.; Botker, H. E. Energy stores and metabolites in chronic reversibly and irreversibly dysfunctional myocardium in humans J. Am. Coll. Cardiol. 2001, 37 (1) 100-108
7. Van Eyk, J. E. Overview: the maturing of proteomics in cardiovascular research Circ. Res. 2011, 108 (4) 490-8
8. Agnetti, G.; Husberg, C.; Van Eyk, J. E. Divide and conquer: the application of organelle proteomics to heart failure Circ. Res. 2011, 108 (4) 512-526
9. Stastna, M.; Abraham, M. R.; Van Eyk, J. E. Cardiac stem/progenitor cells, secreted proteins, and proteomics FEBS Lett. 2009, 583 (11) 1800-1807
10. Zhang, H.; Ge, Y. Comprehensive analysis of protein modifications by top-down mass spectrometry Circ.: Cardiovasc. Genet. 2011, 4 (6) 711
11. Zhang, J.; Guy, M. J.; Norman, H. S.; Chen, Y. C.; Xu, Q.; Dong, X.; Guner, H.; Wang, S.; Kohmoto, T.; Young, K. H.; Moss, R. L.; Ge, Y. Top-down quantitative proteomics identified phosphorylation of cardiac troponin I as a candidate biomarker for chronic heart failure J. Proteome Res. 2011, 10 (9) 4054-4065
12. Zhang, J.; Zhang, H.; Ayaz-Guner, S.; Chen, Y. C.; Dong, X.; Xu, Q.; Ge, Y. Phosphorylation, but not alternative splicing or proteolytic degradation, is conserved in human and mouse cardiac troponin T Biochemistry 2011, 50 (27) 6081-6092
13. Kelly, R. F.; Cabrera, J. A.; Ziemba, E. A.; Crampton, M.; Anderson, L. B.; McFalls, E. O.; Ward, H. B. Continued depression of maximal oxygen consumption and mitochondrial proteomic expression despite successful coronary artery bypass grafting in a swine model of hibernation J. Thorac. Cardiovasc. Surg. 2011, 141 (1) 261-268
14. Lilley, K. S.; Razzaq, A.; Dupree, P. Two-dimensional gel electrophoresis: recent advances in sample preparation, detection and quantitation Curr. Opin. Chem. Biol. 2002, 6 (1) 46-50
15. Ong, S. E.; Blagoev, B.; Kratchmarova, I.; Kristensen, D. B.; Steen, H.; Pandey, A.; Mann, M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 2002, 1 (5) 376-386
16. Gygi, S. P.; Rist, B.; Gerber, S. A.; Turecek, F.; Gelb, M. H.; Aebersold, R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags Nat. Biotechnol. 1999, 17 (10) 994-999
17. DeSouza, L.; Diehl, G.; Rodrigues, M. J.; Guo, J.; Romaschin, A. D.; Colgan, T. J.; Siu, K. W. Search for cancer markers from endometrial tissues using differentially labeled tags iTRAQ and cICAT with multidimensional liquid chromatography and tandem mass spectrometry J. Proteome Res. 2005, 4 (2) 377-386
18. Wang, G.; Wu, W. W.; Zeng, W.; Chou, C. L.; Shen, R. F. Label-free protein quantification using LC-coupled ion trap or FT mass spectrometry: Reproducibility, linearity, and application with complex proteomes J. Proteome Res. 2006, 5 (5) 1214-1223
19. Domon, B.; Aebersold, R. Options and considerations when selecting a quantitative proteomics strategy Nat. Biotechnol. 2010, 28 (7) 710-721
20. Duan, X.; Young, R. F.; Straubinger, R. M.; Page, B. J.; Cao, J.; Wang, H.; Yu, Y.; Canty, J. M., 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. 2009, 8 (6) 2838-2850
21. Tu, C.; Li, J.; Bu, Y.; Hangauer, D.; Qu, J. An ion-current-based, comprehensive and reproducible proteomic strategy for comparative characterization of the cellular responses to novel anti-cancer agents in a prostate cell model J. Proteomics 2012, 77, 187-201
22. Ono, M.; Shitashige, M.; Honda, K.; Isobe, T.; Kuwabara, H.; Matsuzuki, H.; Hirohashi, S.; Yamada, T. Label-free quantitative proteomics using large peptide data sets generated by nanoflow liquid chromatography and mass spectrometry Mol. Cell. Proteomics 2006, 5 (7) 1338-1347
23. Page, B.; Young, R.; Iyer, V.; Suzuki, G.; Lis, M.; Korotchkina, K.; Patel, M.; Blumenthal, K.; Fallavollita, J. A.; Canty, J. M., Jr. Persistent regional downregulation in mitochondrial enzymes and upregulation of stress proteins in swine with chronic hibernating myocardium Circ. Res. 2008, 102, 103-112
24. Calvo, S. E.; Mootha, V. K. The mitochondrial proteome and human disease Annu. Rev. Genomics Hum. Genet. 2010, 11, 25-44
25. Bildl, W.; Haupt, A.; Muller, C. S.; Biniossek, M. L.; Thumfart, J. O.; Huber, B.; Fakler, B.; Schulte, U. Extending the dynamic range of label-free mass spectrometric quantification of affinity purifications Mol. Cell. Proteomics 2012, 11 (2) M111 007955
26. Schindler, J.; Nothwang, H. G. Aqueous polymer two-phase systems: effective tools for plasma membrane proteomics Proteomics 2006, 6 (20) 5409-5417
27. Bindoff, L. Mitochondria and the heart Eur. Heart J. 2003, 24 (3) 221-224
28. Leth-Larsen, R.; Lund, R. R.; Ditzel, H. J. Plasma membrane proteomics and its application in clinical cancer biomarker discovery Mol. Cell. Proteomics 2010, 9 (7) 1369-1382
29. Carr, S. A.; Anderson, L. Protein quantitation through targeted mass spectrometry: the way out of biomarker purgatory? Clin. Chem. 2008, 54 (11) 1749-1752
30. Rifai, N.; Gillette, M. A.; Carr, S. A. Protein biomarker discovery and validation: the long and uncertain path to clinical utility Nat. Biotechnol. 2006, 24 (8) 971-983
31. Diamandis, E. P. Cancer biomarkers: can we turn recent failures into success? JNCI, J. Natl. Cancer Inst. 2010, 102 (19) 1462-1467
32. Diz, A. P.; Carvajal-Rodriguez, A.; Skibinski, D. O. Multiple hypothesis testing in proteomics: a strategy for experimental work Mol. Cell. Proteomics 2011, 10 (3) M110 004374
33. Karp, N. A.; McCormick, P. S.; Russell, M. R.; Lilley, K. S. Experimental and statistical considerations to avoid false conclusions in proteomics studies using differential in-gel electrophoresis Mol. Cell. Proteomics 2007, 6 (8) 1354-1364
34. Margolin, A. A.; Ong, S. E.; Schenone, M.; Gould, R.; Schreiber, S. L.; Carr, S. A.; Golub, T. R. Empirical Bayes analysis of quantitative proteomics experiments PLoS One 2009, 4 (10) e7454
35. Qu, J.; Lesse, A. J.; Brauer, A. L.; Cao, J.; Gill, S. R.; Murphy, T. F. Proteomic expression profiling of Haemophilus influenzae grown in pooled human sputum from adults with chronic obstructive pulmonary disease reveal antioxidant and stress responses Anal. Chem. 2010, 10, 162
36. Malm, B. J.; Suzuki, G.; Canty, J. M., Jr.; Fallavollita, J. A. Variability of contractile reserve in hibernating myocardium: Dependence on the method of stimulation Cardiovasc. Res. 2002, 56, 422-433
37. Page, B. J.; Young, R. F.; Suzuki, G.; Fallavollita, J. A.; Canty, J. M., Jr. The physiological significance of a coronary stenosis differentially affects contractility and mitochondrial function in viable chronically dysfunctional myocardium Basic Res. Cardiol. 2013, 108 (4) 354
38. Unlu, M.; Morgan, M. E.; Minden, J. S. Difference gel electrophoresis: a single gel method for detecting changes in protein extracts Electrophoresis 1997, 18 (11) 2071-2077
39. Sadygov, R. G.; Maroto, F. M.; Huhmer, A. F. ChromAlign: A two-step algorithmic procedure for time alignment of three-dimensional LC-MS chromatographic surfaces Anal. Chem. 2006, 78 (24) 8207-8217
40. Nilsson, T.; Mann, M.; Aebersold, R.; Yates, J. R., 3rd; Bairoch, A.; Bergeron, J. J. Mass spectrometry in high-throughput proteomics: ready for the big time Nat. Methods 2010, 7 (9) 681-685
41. Tu, C.; Li, J.; Jiang, X.; Sheflin, L. G.; Pfeffer, B. A.; Behringer, M.; Fliesler, S. J.; Qu, J. Ion-current-based Proteomic Profiling of the Retina in a Rat Model of Smith-Lemli-Opitz Syndrome Mol. Cell. Proteomics 2013, 12 (12) 3583-3598
42. Dicker, L.; Lin, X.; Ivanov, A. R. Increased power for the analysis of label-free LC-MS/MS proteomics data by combining spectral counts and peptide peak attributes Mol. Cell. Proteomics 2010, 9 (12) 2704-2718
43. Griffin, N. M.; Yu, J.; Long, F.; Oh, P.; Shore, S.; Li, Y.; Koziol, J. A.; Schnitzer, J. E. Label-free, normalized quantification of complex mass spectrometry data for proteomic analysis Nat. Biotechnol. 2010, 28 (1) 83-89
44. Qu, J.; Jusko, W. J.; Straubinger, R. M. Utility of cleavable isotope-coded affinity-tagged reagents for quantification of low-copy proteins induced by methylprednisolone using liquid chromatography/tandem mass spectrometry Anal. Chem. 2006, 78 (13) 4543-4552
45. Premstaller, A.; Oberacher, H.; Walcher, W.; Timperio, A. M.; Zolla, L.; Chervet, J. P.; Cavusoglu, N.; van Dorsselaer, A.; Huber, C. G. High-performance liquid chromatography-electrospray ionization mass spectrometry using monolithic capillary columns for proteomic studies Anal. Chem. 2001, 73 (11) 2390-2396
46. Shen, Y.; Zhang, R.; Moore, R. J.; Kim, J.; Metz, T. O.; Hixson, K. K.; Zhao, R.; Livesay, E. A.; Udseth, H. R.; Smith, R. D. Automated 20 kpsi RPLC-MS and MS/MS with chromatographic peak capacities of 1000-1500 and capabilities in proteomics and metabolomics Anal. Chem. 2005, 77 (10) 3090-3100
47. Qu, J.; Straubinger, R. M. Improved sensitivity for quantification of proteins using triply charged cleavable isotope-coded affinity tag peptides Rapid Commun. Mass Spectrom. 2005, 19 (19) 2857-2864
48. America, A. H.; Cordewener, J. H. Comparative LC-MS: a landscape of peaks and valleys Proteomics 2008, 8 (4) 731-749
49. Makarov, A.; Denisov, E.; Kholomeev, A.; Balschun, W.; Lange, O.; Strupat, K.; Horning, S. Performance evaluation of a hybrid linear ion trap/orbitrap mass spectrometer Anal. Chem. 2006, 78 (7) 2113-2120
50. Gorshkov, M. V.; Good, D. M.; Lyutvinskiy, Y.; Yang, H.; Zubarev, R. A. Calibration function for the Orbitrap FTMS accounting for the space charge effect J. Am. Soc. Mass Spectrom. 2010, 21 (11) 1846-1851
51. Duan, X.; Engler, F. A.; Qu, J. Electron transfer dissociation coupled to an Orbitrap analyzer may promise a straightforward and accurate sequencing of disulfide-bridged cyclic peptides: a case study J. Mass Spectrom. 2010, 45 (12) 1477-1482
52. Tu, C.; Li, J.; Young, R.; Page, B. J.; Engler, F.; Halfon, M. S.; Canty, J. M., Jr.; Qu, J. Combinatorial peptide ligand library treatment followed by a dual-enzyme, dual-activation approach on a nanoflow liquid chromatography/ orbitrap/electron transfer dissociation system for comprehensive analysis of swine plasma proteome Anal. Chem. 2011, 83 (12) 4802-4813
53. Duan, X.; Dai, L.; Chen, S. C.; Balthasar, J. P.; Qu, J. Nano-scale liquid chromatography/mass spectrometry and on-the-fly orthogonal array optimization for quantification of therapeutic monoclonal antibodies and the application in preclinical analysis J. Chromatogr., A 2012, 1251, 63-73
54. White, F. M. The potential cost of high-throughput proteomics Sci. Signal. 2011, 4 (160) pe8
55. Xia, Q.; Wang, T.; Taub, F.; Park, Y.; Capestany, C. A.; Lamont, R. J.; Hackett, M. Quantitative proteomics of intracellular Porphyromonas gingivalis Proteomics 2007, 7 (23) 4323-4337
56. Canty, J. M., Jr.; Suzuki, G. Myocardial perfusion and contraction in acute ischemia and chronic ischemic heart disease J Mol Cell Cardiol 2012, 52 (4) 822-831
57. Lim, H.; Fallavollita, J. A.; Hard, R.; Kerr, C. W.; Canty, J. M., Jr. Profound apoptosis-mediated regional myocyte loss and compensatory hypertrophy in pigs with hibernating myocardium Circulation 1999, 100, 2380-2386
58. Canty, J. M., Jr.; Fallavollita, J. A. Hibernating myocardium J. Nucl Cardiol. 2005, 12 (1) 104-119
59. Hu, Q.; Suzuki, G.; Young, R. F.; Page, B. J.; Fallavollita, J. A.; Canty, J. M., Jr. Reductions in mitochondrial O(2) consumption and preservation of high-energy phosphate levels after simulated ischemia in chronic hibernating myocardium Am. J. Physiol.: Heart Circ. Physiol. 2009, 297 (1) H223-H232
60. Kassiotis, C.; Rajabi, M.; Taegtmeyer, H. Metabolic reserve of the heart: the forgotten link between contraction and coronary flow Prog. Cardiovasc. Dis. 2008, 51 (1) 74-88
61. McFalls, E. O.; Sluiter, W.; Schoonderwoerd, K.; Manintveld, O. C.; Lamers, J. M.; Bezstarosti, K.; van Beusekom, H. M.; Sikora, J.; Ward, H. B.; Merkus, D.; Duncker, D. J. Mitochondrial adaptations within chronically ischemic swine myocardium J. Mol. Cell. Cardiol. 2006, 41, 980-988
62. Rajabi, M.; Kassiotis, C.; Razeghi, P.; Taegtmeyer, H. Return to the fetal gene program protects the stressed heart: a strong hypothesis Heart Fail Rev. 2007, 12 (3-4) 331-343
63. Kim, S. J.; Peppas, A.; Hong, S. K.; Yang, G.; Huang, Y.; Diaz, G.; Sadoshima, J.; Vatner, D. E.; Vatner, S. F. Persistent stunning induces myocardial hibernation and protection: flow/function and metabolic mechanisms Circ. Res. 2003, 92 (11) 1233-1239
64. McFalls, E. O.; Kelly, R. F.; Hu, Q.; Mansoor, A.; Lee, J.; Kuskowski, M.; Sikora, J.; Ward, H. B.; 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 2007, 293 (5) H2945-H2951
65. Han, X. J.; Chae, J. K.; Lee, M. J.; You, K. R.; Lee, B. H.; Kim, D. G. Involvement of GADD153 and cardiac ankyrin repeat protein in hypoxia-induced apoptosis of H9c2 cells J. Biol. Chem. 2005, 280 (24) 23122-23129
66. Miller, E. J.; Li, J.; Leng, L.; McDonald, C.; Atsumi, T.; Bucala, R.; Young, L. H. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart Nature 2008, 451 (7178) 578-582
67. Qi, D.; Hu, X.; Wu, X.; Merk, M.; Leng, L.; Bucala, R.; Young, L. H. Cardiac macrophage migration inhibitory factor inhibits JNK pathway activation and injury during ischemia/reperfusion J. Clin. Invest. 2009, 119 (12) 3807-3816
68. Koga, K.; Kenessey, A.; Powell, S. R.; Sison, C. P.; Miller, E. J.; Ojamaa, K. Macrophage migration inhibitory factor provides cardioprotection during ischemia/reperfusion by reducing oxidative stress Antioxid. Redox Signaling 2011, 14 (7) 1191-1202
69. Li, H. W.; Gao, Y. X.; Qi, Y. F.; Katovich, M. J.; Jiang, N.; Braseth, L. N.; Scheuer, D. A.; Shi, P.; Sumners, C. Macrophage migration inhibitory factor in hypothalamic paraventricular nucleus neurons decreases blood pressure in spontaneously hypertensive rats FASEB J. 2008, 22 (9) 3175-3185
70. Garcia-Gras, E.; Lombardi, R.; Giocondo, M. J.; Willerson, J. T.; Schneider, M. D.; Khoury, D. S.; Marian, A. J. Suppression of canonical Wnt/beta-catenin signaling by nuclear plakoglobin recapitulates phenotype of arrhythmogenic right ventricular cardiomyopathy J. Clin. Invest. 2006, 116 (7) 2012-2021
71. Dhalla, N. S.; Saini-Chohan, H. K.; Rodriguez-Leyva, D.; Elimban, V.; Dent, M. R.; Tappia, P. S. Subcellular remodelling may induce cardiac dysfunction in congestive heart failure Cardiovasc. Res. 2009, 81 (3) 429-438
72. White, E. Mechanical modulation of cardiac microtubules Pfluegers Arch. 2011, 462 (1) 177-184
73. Collins, J. F.; Pawloski-Dahm, C.; Davis, M. G.; Ball, N.; Dorn, G. W., 2nd; Walsh, R. A. The role of the cytoskeleton in left ventricular pressure overload hypertrophy and failure J. Mol. Cell Cardiol. 1996, 28 (7) 1435-1443
74. Rappaport, L.; Samuel, J. L. Microtubules in cardiac myocytes Int. Rev. Cytol. 1988, 113, 101-143
75. Hein, S.; Kostin, S.; Heling, A.; Maeno, Y.; Schaper, J. The role of the cytoskeleton in heart failure Cardiovasc. Res. 2000, 45 (2) 273-278
76. Fassett, J. T.; Hu, X.; Xu, X.; Lu, Z.; Zhang, P.; Chen, Y.; Bache, R. J. AMPK Attenuates Microtubule Proliferation in Cardiac Hypertrophy Am. J. Physiol.: Heart Circ. Physiol 2013, 304, H749-H758