Proteomics analysis of the cardiac myofilament subproteome reveals dynamic alterations in phosphatase subunit distribution

Molecular and Cellular Proteomics

Volumn 9, Issue 3, 2010, Pages 497-509

  Yin, Xiaoke ^a   Cuello, Friederike ^a   Mayr, Ursula ^a   Hao, Zhiqi ^b   Hornshaw, Martin ^b   Ehler, Elisabeth ^a   Avkiran, Metin ^a   Mayr, Manuel ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Thermo Fisher Scientific   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ENDOTHELIN 1; ISOPRENALINE; MYOSIN BINDING PROTEIN C; MYOSIN LIGHT CHAIN; MYOSIN PHOSPHATASE 1; MYOSIN PHOSPHATASE 2; MYOSIN VI; PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN SUBUNIT; TROPONIN C; TROPONIN T; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; BETA ADRENERGIC STIMULATION; CELL ISOLATION; CELL NUCLEUS; CELL STIMULATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; HEART MUSCLE CELL; IMMUNOBLOTTING; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; RAT; RIBOSOME; SARCOMERE; TANDEM MASS SPECTROMETRY;

ADRENERGIC BETA-AGONISTS; ANIMALS; CELLS, CULTURED; ENDOTHELIN-1; ISOPROTERENOL; MALE; MICE; MICROFILAMENTS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; NEUROTRANSMITTER AGENTS; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTEIN PHOSPHATASE 1; PROTEIN PHOSPHATASE 2; PROTEOME; PROTEOMICS; RATS; SARCOMERES; TANDEM MASS SPECTROMETRY;

RODENTIA;

EID: 77649109602     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900275-MCP200     Document Type: Article

References (40)

1. Haworth, R. S., Cuello, F., Herron, T. J., Franzen, G., Kentish, J. C., Gautel, M., and Avkiran, M. (2004) Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function. Circ. Res. 95, 1091-1099
2. Vahebi, S., Kobayashi, T., Warren, C. M., de Tombe, P. P., and Solaro, R. J. (2005) Functional effects of rho-kinase-dependent phosphorylation of specific sites on cardiac troponin. Circ. Res. 96, 740-747
3. Cuello, F., Bardswell, S. C., Haworth, R. S., Yin, X., Lutz, S., Wieland, T., Mayr, M., Kentish, J. C., and Avkiran, M. (2007) Protein kinase D selectively targets cardiac troponin I and regulates myofilament Ca2+ sensitivity in ventricular myocytes. Circ. Res. 100, 864-873
4. Cazorla, O., Szilagyi, S., Vignier, N., Salazar, G., Krämer, E., Vassort, G., Carrier, L., and Lacampagne, A. (2006) Length and protein kinase A modulations of myocytes in cardiac myosin binding protein C-deficient mice. Cardiovasc. Res. 69, 370-380
5. Stelzer, J. E., Patel, J. R., Walker, J. W., and Moss, R. L. (2007) Differential roles of cardiac myosin-binding protein C and cardiac troponin I in the myofibrillar force responses to protein kinase A phosphorylation. Circ. Res. 101, 503-511
6. Tong, C. W., Stelzer, J. E., Greaser, M. L., Powers, P. A., and Moss, R. L. (2008) Acceleration of crossbridge kinetics by protein kinase A phosphorylation of cardiac myosin binding protein C modulates cardiac function. Circ. Res. 103, 974-982
7. Stelzer, J. E., Patel, J. R., and Moss, R. L. (2006) Acceleration of stretch activation in murine myocardium due to phosphorylation of myosin regulatory light chain. J. Gen. Physiol. 128, 261-272
8. Olsson, M. C., Patel, J. R., Fitzsimons, D. P., Walker, J. W., and Moss, R. L. (2004) Basal myosin light chain phosphorylation is a determinant of Ca2+ sensitivity of force and activation dependence of the kinetics of myocardial force development. Am. J. Physiol. Heart Circ. Physiol. 287, H2712-H2718
9. Scruggs, S. B., Hinken, A. C., Thawornkaiwong, A., Robbins, J., Walker, L. A., de Tombe, P. P., Geenen, D. L., Buttrick, P. M., and Solaro, R. J. (2009) Ablation of ventricular myosin regulatory light chain phosphorylation in mice causes cardiac dysfunction in situ and affects neighboring myofilament protein phosphorylation. J. Biol. Chem. 284, 5097-5106
10. Labugger, R., McDonough, J. L., Neverova, I., and Van Eyk, J. E. (2002) Solubilization, two-dimensional separation and detection of the cardiac myofilament protein troponin T. Proteomics 2, 673-678
11. Zabrouskov, V., Ge, Y., Schwartz, J., and Walker, J. W. (2008) Unraveling molecular complexity of phosphorylated human cardiac troponin I by top down electron capture dissociation/electron transfer dissociation mass spectrometry. Mol. Cell. Proteomics 7, 1838-1849
12. White, M. Y., Cordwell, S. J., McCarron, H. C., Prasan, A. M., Craft, G., Hambly, B. D., and Jeremy, R. W. (2005) Proteomics of ischemia/reperfusion injury in rabbit myocardium reveals alterations to proteins of essential functional systems. Proteomics 5, 1395-1410
13. Yuan, C., Guo, Y., Ravi, R., Przyklenk, K., Shilkofski, N., Diez, R., Cole, R. N., and Murphy, A. M. (2006) Myosin binding protein C is differentially phosphorylated upon myocardial stunning in canine and rat hearts - evidence for novel phosphorylation sites. Proteomics 6, 4176-4186
14. Burkart, E. M., Sumandea, M. P., Kobayashi, T., Nili, M., Martin, A. F., Homsher, E., and Solaro, R. J. (2003) Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. J. Biol. Chem. 278, 11265-11272
15. van der Velden, J., Merkus, D., Klarenbeek, B. R., James, A. T., Boontje, N. M., Dekkers, D. H., Stienen, G. J., Lamers, J. M., and Duncker, D. J. (2004) Alterations in myofilament function contribute to left ventricular dysfunction in pigs early after myocardial infarction. Circ. Res. 95, e85-95
16. van der Velden, J., Narolska, N. A., Lamberts, R. R., Boontje, N. M., Borbély, A., Zaremba, R., Bronzwaer, J. G., Papp, Z., Jaquet, K., Paulus, W. J., and Stienen, G. J. (2006) Functional effects of protein kinase C-mediated myofilament phosphorylation in human myocardium. Cardiovasc. Res. 69, 876-887
17. Yuan, C., and Solaro, R. J. (2008) Myofilament proteins: From cardiac disorders to proteomic changes. Proteomics Clin. Appl. 2, 788-799
18. Jin, W., Brown, A. T., and Murphy, A. M. (2008) Cardiac myofilaments: from proteome to pathophysiology. Proteomics Clin. Appl. 2, 800-810
19. Arrell, D. K., Neverova, I., Fraser, H., Marbán, E., and Van Eyk, J. E. (2001) Proteomic analysis of pharmacologically preconditioned cardiomyocytes reveals novel phosphorylation of myosin light chain 1. Circ. Res. 89, 480-487
20. Syka, J. E., Coon, J. J., Schroeder, M. J., Shabanowitz, J., and Hunt, D. F. (2004) Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 101, 9528-9533
21. Sugden, P. H. (2003) An overview of endothelin signaling in the cardiac myocyte. J. Mol. Cell. Cardiol. 35, 871-886
22. Solaro, R. J. (2008) Multiplex kinase signaling modifies cardiac function at the level of sarcomeric proteins. J. Biol. Chem. 283, 26829-26833
23. Messerli, J. M., Eppenberger-Eberhardt, M. E., Rutishauser, B. M., Schwarb, P., von Arx, P., Koch-Schneidemann, S., Eppenberger, H. M., and Perriard, J. C. (1993) Remodelling of cardiomyocyte cytoarchitecture visualized by three-dimensional (3D) confocal microscopy. Histochemistry 100, 193-202
24. Snabaitis, A. K., D'Mello, R., Dashnyam, S., and Avkiran, M. (2006) A novel role for protein phosphatase 2A in receptor-mediated regulation of the cardiac sarcolemmal Na+/H+ exchanger NHE1. J. Biol. Chem. 281, 20252-20262
25. Sidibe, A., Yin, X., Tarelli, E., Xiao, Q., Zampetaki, A., Xu, Q., and Mayr, M. (2007) Integrated membrane protein analysis of mature and embryonic stem cell-derived smooth muscle cells using a novel combination of CyDye/biotin labeling. Mol. Cell. Proteomics 6, 1788-1797
26. Mayr, M., Chung, Y. L., Mayr, U., McGregor, E., Troy, H., Baier, G., Leitges, M., Dunn, M. J., Griffiths, J. R., and Xu, Q. (2004) Loss of PKCδ alters cardiac metabolism. Am. J. Physiol. Heart Circ. Physiol. 287, H937-H945
27. Yan, J. X., Wait, R., Berkelman, T., Harry, R. A., Westbrook, J. A., Wheeler, C. H., and Dunn, M. J. (2000) A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 21, 3666-3672
28. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
29. Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S., Schweigerer, L., Fotsis, T., and Mann, M. (1996) Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379, 466-469
30. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392
31. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
32. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567
33. Gharib, M., Marcantonio, M., Lehmann, S. G., Courcelles, M., Meloche, S., Verreault, A., and Thibault, P. (2009) Artifactual sulfation of silver-stained proteins: implications for the assignment of phosphorylation and sulfation sites. Mol. Cell. Proteomics 8, 506-518
34. Arrell, D. K., Neverova, I., and Van Eyk, J. E. (2001) Cardiovascular proteomics: evolution and potential. Circ. Res. 88, 763-773
35. Agnetti, G., Kane, L. A., Guarnieri, C., Caldarera, C. M., and Van Eyk, J. E. (2007) Proteomic technologies in the study of kinases: novel tools for the investigation of PKC in the heart. Pharmacol. Res. 55, 511-522
36. Liu, X., Ramjiganesh, T., Chen, Y. H., Chung, S. W., Hall, S. R., Schissel, S. L., Padera, R. F., Jr., Liao, R., Ackerman, K. G., Kajstura, J., Leri, A., Anversa, P., Yet, S. F., Layne, M. D., and Perrella, M. A. (2009) Disruption of striated preferentially expressed gene locus leads to dilated cardiomyopathy in mice. Circulation 119, 261-268
37. Virshup, D. M., and Shenolikar, S. (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol. Cell 33, 537-545
38. Mayr, M., Zhang, J., Greene, A. S., Gutterman, D., Perloff, J., and Ping, P. (2006) Proteomics-based development of biomarkers in cardiovascular disease: mechanistic, clinical, and therapeutic insights. Mol. Cell. Proteomics 5, 1853-1864
39. Mayr, M., Metzler, B., Chung, Y. L., McGregor, E., Mayr, U., Troy, H., Hu, Y., Leitges, M., Pachinger, O., Griffiths, J. R., Dunn, M. J., and Xu, Q. (2004) Ischemic preconditioning exaggerates cardiac damage in PKCδ null mice. Am. J. Physiol. Heart Circ. Physiol. 287, H946-H956
40. Mayr, M., Liem, D., Zhang, J., Li, X., Avliyakulov, N. K., Yang, J. I., Young, G., Vondriska, T. M., Ladroue, C., Madhu, B., Griffiths, J. R., Gomes, A., Xu, Q., and Ping, P. (2009) Proteomic and metabolomic analysis of cardioprotection: Interplay between protein kinase C epsilon and delta in regulating glucose metabolism of murine hearts. J. Mol. Cell. Cardiol. 46, 268-277