Top-down mass spectrometry of cardiac myofilament proteins in health and disease

Proteomics - Clinical Applications

Volumn 8, Issue 7-8, 2014, Pages 554-568

  Peng, Ying ^a   Ayaz Guner, Serife ^a   Yu, Deyang ^a,b   Ge, Ying ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Electron capture dissociation; Heart failure; Myofilaments; Phosphorylation; Top down mass spectrometry; Troponin

Indexed keywords

CARDIAC MYOFILAMENT PROTEIN; CARDIAC MYOSIN BINDING PROTEIN C; CARDIAC TROPONIN C; CARDIAC TROPONIN COMPLEX; CARDIAC TROPONIN I; CARDIAC TROPONIN T; CONTRACTILE PROTEIN; MYOSIN BINDING PROTEIN C; TROPOMYOSIN; TROPONIN; TROPONIN C; TROPONIN I; TROPONIN T; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CONGESTIVE CARDIOMYOPATHY; HEART DISEASE; HEART FAILURE; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CONTRACTILITY; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MASS SPECTROMETRY; MOLECULAR MECHANICS; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; TOP DOWN MASS SPECTROMETRY; ANIMAL; HEALTH; METABOLISM; MOLECULAR GENETICS; MUSCLE FIBRIL; PROCEDURES; PROTEOMICS;

AMINO ACID SEQUENCE; ANIMALS; HEALTH; HEART FAILURE; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MYOFIBRILS; PROTEOMICS;

EID: 84906058717     PISSN: 18628346     EISSN: 18628354     Source Type: Journal    
DOI: 10.1002/prca.201400043     Document Type: Review

References (143)

1. Heidenreich, P. A., Trogdon, J. G., Khavjou, O. A., Butler, J. et al., Forecasting the future of cardiovascular disease in the United States a policy statement from the American Heart Association. Circulation 2011, 123, 933-944.
2. Krum, H., Abraham, W. T., Heart failure. Lancet 2009, 373, 941-955.
3. Mudd, J. O., Kass, D. A., Tackling heart failure in the twenty-first century. Nature 2008, 451, 919-928.
4. Bui, A. L., Horwich, T. B., Fonarow, G. C., Epidemiology and risk profile of heart failure. Nat. Rev. Cardiol. 2011, 8, 30-41.
5. McMurray, J. J., Pfeffer, M. A., Heart failure. Lancet 2005, 365, 1877-1889.
6. de Tombe, P. P., Solaro, R. J., Integration of cardiac myofilament activity and regulation with pathways signaling hypertrophy and failure. Ann. Biomed. Eng. 2000, 28, 991-1001.
7. Hamdani, N., Kooij, V., van Dijk, S., Merkus, D. et al., Sarcomeric dysfunction in heart failure. Cardiovasc. Res. 2008, 77, 649-658.
8. Solaro, R. J., Warren, C. M., Scruggs, S. B., Why is it important to analyze the cardiac sarcomere subproteome? Expert Rev. Proteomics 2010, 7, 311-314.
9. Jin, W., Brown, A. T., Murphy, A. M., Cardiac myofilaments: from proteome to pathophysiology. Proteomics Clin. Appl. 2008, 2, 800-810.
10. Yuan, C., Solaro, R. J., Myofilament proteins: from cardiac disorders to proteomic changes. Proteomics Clin. Appl. 2008, 2, 788-799.
11. Moss, R. L., Razumova, M., Fitzsimons, D. P., Myosin crossbridge activation of cardiac thin filaments-implications for myocardial function in health and disease. Circ. Res. 2004, 94, 1290-1300.
12. de Tombe, P. P., Cardiac myofilaments: mechanics and regulation. J. Biomech. 2003, 36, 721-730.
13. Takeda, S., Yamashita, A., Maeda, K., Maeda, Y., Structure of the core domain of human cardiac troponin in the Ca2+-saturated form. Nature 2003, 424, 35-41.
14. Flashman, E., Redwood, C., Moolman-Smook, J., Watkins, H., Cardiac myosin binding protein C-its role in physiology and disease. Circ. Res. 2004, 94, 1279-1289.
15. Fitzsimons, D. P., Patel, J. R., Moss, R. L., Role of myosin heavy chain composition in kinetics of force development and relaxation in rat myocardium. J. Physiol. 1998, 513, 171-183.
16. Scruggs, S. B., Solaro, R. J., The significance of regulatory light chain phosphorylation in cardiac physiology. Arch. Biochem. Biophys. 2011, 510, 129-134.
17. Moss, R. L., Fitzsimons, D. P., Myosin light chain 2 into the mainstream of cardiac development and contractility. Circ. Res. 2006, 99, 225-227.
18. Bers, D. M., Cardiac excitation-contraction coupling. Nature 2002, 415, 198-205.
19. Sumandea, M. P., Burkart, E. M., Kobayashi, T., De Tombe, P. P., Solaro, R. J., in: Sideman, S., Beyar, R. (Eds.), Cardiac Engineering: From Genes and Cells to Structure and Function 2004, New York Academy of Sciences, New York, NY, pp. 39-52.
20. Marston, S. B., Redwood, C. S., Modulation of thin filament activation by breakdown or isoform switching of thin filament proteins-physiological and pathological implications. Circ. Res. 2003, 93, 1170-1178.
21. Tardiff, J. C., Thin filament mutations developing an integrative approach to a complex disorder. Circ. Res. 2011, 108, 765-782.
22. Seidman, J. G., Seidman, C., The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 2001, 104, 557-567.
23. Smith, L. M., Kelleher, N. L., Proteoform: a single term describing protein complexity. Nat. Methods 2013, 10, 186-187.
24. Burnette, W. N., Western blotting-electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein-A. Anal. Biochem. 1981, 112, 195-203.
25. Mann, M., Can proteomics retire the western blot? J Proteome Res. 2008, 7, 3065-3065.
26. Aebersold, R., Mann, M., Mass spectrometry-based proteomics. Nature 2003, 422, 198-207.
27. Han, X. M., Aslanian, A., Yates, J. R., Mass spectrometry for proteomics. Curr. Opin. Chem. Biol. 2008, 12, 483-490.
28. Yates, J. R., Ruse, C. I., Nakorchevsky, A., Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng. 2009, 11, 49-79.
29. Aebersold, R., Cravatt, B. F., Proteomics-advances, applications and the challenges that remain. Trends Biotechnol. 2002, 20, S1-S2.
30. Gygi, S. P., Aebersold, R., Mass spectrometry and proteomics. Curr. Opin. Chem. Biol. 2000, 4, 489-494.
31. Ong, S. E., Mann, M., Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 2005, 1, 252-262.
32. Chait, B. T., Mass spectrometry: bottom-up or top-down? Science 2006, 314, 65-66.
33. Siuti, N., Kelleher, N. L., Decoding protein modifications using top-down mass spectrometry. Nat. Methods 2007, 4, 817-821.
34. Zhang, H., Ge, Y., Comprehensive analysis of protein modifications by top-down mass spectrometry. Circ. Cardiovasc. Genet. 2011, 4, 711.
35. Gregorich, Z. R., Ge, Y., Top-down proteomics in health and disease: challenges and opportunities. Proteomics 2014, 14, 1195-1210.
36. Gregorich, Z. R., Chang, Y. H., Ge, Y., Proteomics in heart failure: top-down or bottom-up? Pflugers Arch. 2014, 466, 1199-1209.
37. Sze, S. K., Ge, Y., Oh, H., McLafferty, F. W., Top-down mass spectrometry of a 29-kDa protein for characterization of any posttranslational modification to within one residue. Proc. Natl. Acad. Sci. USA 2002, 99, 1774-1779.
38. Ansong, C., Wu, S., Meng, D., Liu, X. et al., Top-down proteomics reveals a unique protein S-thiolation switch in Salmonella Typhimurium in response to infection-like conditions. Proc. Natl. Acad. Sci. USA 2013, 110, 10153-10158.
39. Ryan, C. M., Souda, P., Bassilian, S., Ujwal, R. et al., Post-translational modifications of integral membrane proteins resolved by top-down Fourier transform mass spectrometry with collisionally activated dissociation. Mol. Cell. Proteomics 2010, 9, 791-803.
40. Roth, M. J., Forbes, A. J., Boyne, M. T., Kim, Y. B. et al., Precise and parallel characterization of coding polymorphisms, alternative splicing, and modifications in human proteins by mass spectrometry. Mol. Cell. Proteomics 2005, 4, 1002-1008.
41. Senko, M. W., Speir, J. P., McLafferty, F. W., Collisional activation of large multiply charged ions using Fourier transform mass spectrometry. Anal. Chem. 1994, 66, 2801-2808.
42. Little, D. P., Speir, J. P., Senko, M. W., O'Connor, P. B., McLafferty, F. W., Infrared multiphoton dissociation of large multiply charged ions for biomolecule sequencing. Anal. Chem. 1994, 66, 2809-2815.
43. Ge, Y., Horn, D. M., McLafferty, F. W., Blackbody infrared radiative dissociation of larger (42 kDa) multiply charged proteins. Int. J. Mass Spectrom. 2001, 210, 203-214.
44. Shaw, J. B., Li, W., Holden, D. D., Zhang, Y. et al., Complete protein characterization using top-down mass spectrometry and ultraviolet photodissociation. J. Am. Chem. Soc. 2013, 135, 12646-12651.
45. Zubarev, R. A., Horn, D. M., Fridriksson, E. K., Kelleher, N. L. et al., Electron capture dissociation for structural characterization of multiply charged protein cations. Anal. Chem. 2000, 72, 563-573.
46. Syka, J. E., Coon, J. J., Schroeder, M. J., Shabanowitz, J., Hunt, D. F., Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. USA 2004, 101, 9528-9533.
47. Turecek, F., N[bond]C(alpha) bond dissociation energies and kinetics in amide and peptide radicals. Is the dissociation a non-ergodic process? J. Am. Chem. Soc. 2003, 125, 5954-5963.
48. Zhang, J., Zhang, H., Ayaz-Guner, S., Chen, Y. C. et al., Phosphorylation, but not alternative splicing or proteolytic degradation, is conserved in human and mouse cardiac troponin T. Biochemistry 2011, 50, 6081-6092.
49. Zhang, J., Guy, M. J., Norman, H. S., Chen, Y. C. et al., Top-down quantitative proteomics identified phosphorylation of cardiac troponin I as a candidate biomarker for chronic heart failure. J. Proteome Res. 2011, 10, 4054-4065.
50. Zabrouskov, V., Ge, Y., Schwartz, J., Walker, J. W., Unraveling molecular complexity of phosphorylated human cardiac troponin I by top down electron capture dissociation/electron transfer dissociation mass spectrometry. Mol. Cell. Proteomics 2008, 7, 1838-1849.
51. Ge, Y., Rybakova, I. N., Xu, Q., Moss, R. L., Top-down high-resolution mass spectrometry of cardiac myosin binding protein C revealed that truncation alters protein phosphorylation state. Proc. Natl. Acad. Sci. USA 2009, 106, 12658-12663.
52. Dong, X., Sumandea, C. A., Chen, Y.-C., Garcia-Cazarin, M. L. et al., Augmented phosphorylation of cardiac troponin I in hypertensive heart failure. J. Biol. Chem. 2012, 287, 848-857.
53. Ayaz-Guner, S., Zhang, J., Li, L., Walker, J. W., Ge, Y., In vivo phosphorylation site mapping in mouse cardiac troponin I by high resolution top-down electron capture dissociation mass spectrometry: Ser22/23 are the only sites basally phosphorylated. Biochemistry 2009, 48, 8161-8170.
54. Thomas, C. E., Kelleher, N. L., Mizzen, C. A., Mass spectrometric characterization of human histone H3: a bird's eye view. J. Proteome Res. 2006, 5, 240-247.
55. Pesavento, J. J., Mizzen, C. A., Kelleher, N. L., Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry: human histone H4. Anal. Chem. 2006, 78, 4271-4280.
56. Solaro, R. J., Henze, M., Kobayashi, T., Integration of troponin I phosphorylation with cardiac regulatory networks. Circ. Res. 2013, 112, 355-366.
57. Solaro, R. J., Rosevear, P., Kobayashi, T., The unique functions of cardiac troponin I in the control of cardiac muscle contraction and relaxation. Biochem. Biophys. Res. Commun. 2008, 369, 82-87.
58. Solaro, R. J., van der Velden, J., Why does troponin I have so many phosphorylation sites? Fact and fancy. J. Mol. Cell. Cardiol. 2010, 48, 810-816.
59. Kimura, A., Harada, H., Park, J. E., Nishi, H. et al., Mutations in the cardiac troponin I gene associated with hypertrophic cardiomyopathy. Nat. Genet. 1997, 16, 379-382.
60. Elliott, K., Watkins, H., Redwood, C. S., Altered regulatory properties of human cardiac troponin I mutants that cause hypertrophic cardiomyopathy. J. Biol. Chem. 2000, 275, 22069-22074.
61. James, J., Zhang, Y., Osinska, H., Sanbe, A. et al., Transgenic modeling of a cardiac troponin I mutation linked to familial hypertrophic cardiomyopathy. Circ. Res. 2000, 87, 805-811.
62. Layland, J., Solaro, R. J., Shah, A. M., Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc. Res. 2005, 66, 12-21.
63. Scruggs, S. B., Walker, L. A., Lyu, T., Geenen, D. L. et al., Partial replacement of cardiac troponin I with a non-phosphorylatable mutant at serines 43/45 attenuates the contractile dysfunction associated with PKC epsilon phosphorylation. J. Mol. Cell. Cardiol. 2006, 40, 465-473.
64. Wang, H., Grant, J. E., Doede, C. M., Sadayappan, S. et al., PKC-beta II sensitizes cardiac myofilaments to Ca2+ by phosphorylating troponin I on threonine-144. J. Mol. Cell. Cardiol. 2006, 41, 823-833.
65. Burkart, E. M., Sumandea, M. P., Kobayashi, T., Nili, M. et al., Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. J. Biol. Chem. 2003, 278, 11265-11272.
66. Solaro, R. J., Multiplex kinase signaling modifies cardiac function at the level of sarcomeric proteins. J. Biol. Chem. 2008, 283, 26829-26833.
67. Murphy, A. M., Another new kinase targets troponin I. Circ. Res. 2004, 95, 1043-1045.
68. Haworth, R. S., Cuello, F., Herron, T. J., Franzen, G. et al., Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function. Circ. Res. 2004, 95, 1091-1099.
69. Buscemi, N., Foster, D. B., Neverova, I., Van Eyk, J. E., p21-activated kinase increases the calcium sensitivity of rat triton-skinned cardiac muscle fiber bundles via a mechanism potentially involving novel phosphorylation of troponin I. Circ. Res. 2002, 91, 509-516.
70. Solis, R. S., Ge, Y., Walker, J. W., A preferred AMPK phosphorylation site adjacent to the inhibitory loop of cardiac and skeletal troponin I. Protein Sci. 2011, 20, 894-907.
71. Chen, S., Zhu, P., Guo, H. M., Solis, R. S. et al., Alpha1 catalytic subunit of AMPK modulates contractile function of cardiomyocytes through phosphorylation of troponin I. Life Sci. 2014, 98, 75-82.
72. Nixon, B. R., Thawornkaiwong, A., Jin, J., Brundage, E. A. et al., AMP-activated protein kinase phosphorylates cardiac troponin I at Ser-150 to increase myofilament calcium sensitivity and blunt PKA-dependent function. J. Biol. Chem. 2012, 287, 19136-19147.
73. Zhang, P. B., Kirk, J. A., Ji, W. H., dos Remedios, C. G. et al., Multiple reaction monitoring to identify site-specific troponin I phosphorylated residues in the failing human heart. Circulation 2012, 126, 1828-1837.
74. Murphy, A. M., Kogler, H., Georgakopoulos, D., McDonough, J. L. et al., Transgenic mouse model of stunned myocardium. Science 2000, 287, 488-491.
75. Biesiadecki, B. J., Tachampa, K., Yuan, C., Jin, J.-P. et al., Removal of the cardiac troponin I N-terminal extension improves cardiac function in aged mice. J. Biol. Chem. 2010, 285, 19688-19698.
76. Van Eyk, J. E., Colantonio, D. A., Przyklenk, K., Degradation of troponin I is not essential for myocardial stunning. Circulation 2001, 104, 314-314.
77. McDonough, J. L., Arrell, D. K., Gawad, Y., Van Eyk, J. E., Troponin I degradation and covalent complex formation with myocardial ischemia/reperfusion. Biophys. J. 1998, 74, A354-A354.
78. Solaro, R. J., Powers, F. M., Gao, L. Z., Gwathmey, J. K., Control of myofilament activation in heart-failure. Circulation 1993, 87, 38-43.
79. Thomas, S. A., Fallavollita, J. A., Lee, T. C., Feng, J., Canty, J. M., Absence of troponin I degradation or altered sarcoplasmic reticulum uptake protein expression after reversible ischemia in swine. Circ. Res. 1999, 85, 446-456.
80. Sherman, A. J., Klocke, F. J., Decker, R. S., Decker, M. L. et al., Myofibrillar disruption in hypocontractile myocardium showing perfusion-contraction matches and mismatches. Am. J. Physiol. Heart Circ. Physiol. 2000, 278, H1320-H1334.
81. Feng, J., Schaus, B. J., Fallavollita, J. A., Lee, T. C., Canty, J. M., Preload induces troponin I degradation independently of myocardial ischemia. Circulation 2001, 103, 2035-2037.
82. Ramirez-Correa, G. A., Jin, W., Wang, Z., Zhong, X. et al., O-linked GlcNAc modification of cardiac myofilament proteins. Circ. Res. 2008, 103, 1354-1358.
83. Labugger, R., Organ, L., Collier, C., Atar, D., Van Eyk, J. E., Extensive troponin I and T modification detected in serum from patients with acute myocardial infarction. Circulation 2000, 102, 1221-1226.
84. Labugger, R., Simpson, J. A., Quick, M., Brown, H. A. et al., Strategy for analysis of cardiac troponins in biological samples with a combination of affinity chromatography and mass spectrometry. Clin. Chem. 2003, 49, 873-879.
85. Zhang, J., Dong, X., Hacker, T. A., Ge, Y., Deciphering modifications in swine cardiac troponin I by top-down high-resolution tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 2010, 21, 940-948.
86. Xu, F., Xu, Q., Dong, X., Guy, M. et al., Top-down high-resolution electron capture dissociation mass spectrometry for comprehensive characterization of post-translational modifications in Rhesus monkey cardiac troponin I. Int. J. Mass Spectrom. 2011, 305, 95-102.
87. Messer, A. E., Jacques, A. M., Marston, S. B., Troponin phosphorylation and regulatory function in human heart muscle: dephosphorylation of Ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J. Mol. Cell. Cardiol. 2007, 42, 247-259.
88. Perry, S. V., Troponin T: genetics, properties and function. J. Muscle Res. Cell Motil. 1998, 19, 575-602.
89. Jin, J. P., Zhang, Z. L., Bautista, J. A., Isoform diversity, regulation, and functional adaptation of troponin and calponin. Crit. Rev. Eukaryot. Gene Expr. 2008, 18, 93-124.
90. Wei, B., Jin, J. P., Troponin T isoforms and posttranscriptional modifications: evolution, regulation and function. Arch. Biochem. Biophys. 2011, 505, 144-154.
91. Sumandea, M. P., deTombe, P. P., Solaro, R. J., PKC dependent regulation of myofilament function through cardiac troponin T phosphorylation. Circulation 2003, 108, 592.
92. He, X., Liu, Y., Sharma, V., Dirksen, R. T. et al., ASK1 associates with troponin T and induces troponin T phosphorylation and contractile dysfunction in cardiomyocytes. Am. J. Pathol. 2003, 163, 243-251.
93. Vahebi, S., Kobayashi, T., Warren, C. M., de Tombe, P. P., Solaro, R. J., Functional effects of Rho-kinase-dependent phosphorylation of specific sites on cardiac troponin. Circ. Res. 2005, 96, 740-747.
94. Pfleiderer, P., Sumandea, M., Rybin, V., Wang, C., Steinberg, S., Raf-1: a novel cardiac troponin T kinase. J. Muscle Res. Cell Motil. 2009, 30, 67-72.
95. Sumandea, M. P., Pyle, W. G., Kobayashi, T., de Tombe, P. P., Solaro, R. J., Identification of a functionally critical protein kinase C phosphorylation residue of cardiac troponin T. J. Biol. Chem. 2003, 278, 35135-35144.
96. Katrukha, I. A., Gusev, N. B., Enigmas of cardiac troponin T phosphorylation. J. Mol. Cell. Cardiol. 2013, 65, 156-158.
97. Gusev, N. B., Dobrovolskii, A. B., Severin, S. E., Isolation and some properties of troponin-T kinase from rabbit skeletal-muscle. Biochem. J. 1980, 189, 219-226.
98. Moir, A. J. G., Cole, H. A., Perry, S. V., Phosphorylation sites of troponin-T from white skeletal-muscle and effects of interaction with troponin-C on their phosphorylation by phosphorylase kinase. Biochem. J. 1977, 161, 371-382.
99. Communal, C., Sumandea, M., de Tombe, P., Narula, J. et al., Functional consequences of caspase activation in cardiac myocytes. Proc. Natl. Acad. Sci. USA 2002, 99, 6252-6256.
100. Feng, H.-Z., Biesiadecki, B. J., Yu, Z.-B., Hossain, M. M., Jin, J. P., Restricted N-terminal truncation of cardiac troponin T: a novel mechanism for functional adaptation to energetic crisis. J. Physiol. 2008, 586, 3537-3550
101. Zhang, Z. L., Biesiadecki, B. J., Jin, J. P., Selective deletion of the NH2-terminal variable region of cardiac troponin T in ischemia reperfusion by myofibril-associated mu-calpain cleavage. Biochemistry 2006, 45, 11681-11694.
102. Solis, R. S., Ge, Y., Walker, J. W., Single amino acid sequence polymorphisms in rat cardiac troponin revealed by top-down tandem mass spectrometry. J. Muscle Res. Cell Motil. 2008, 29, 203-212.
103. Gusev, N. B., Barskaya, N. V., Verin, A. D., Duzhenkova, I. V. et al., Some Properties of Cardiac Troponin-T Structure. Biochem. J. 1983, 213, 123-129.
104. Gunning, P., in: Gunning, P. (Ed.), Tropomyosin, New York 2008.
105. Perry, S. V., Vertebrate tropomyosin: distribution, properties and function. J. Muscle Res. Cell Motil. 2001, 22, 5-49.
106. Jagatheesan, G., Rajan, S., Wieczorek, D. F., Investigations into tropomyosin function using mouse models. J. Mol. Cell. Cardiol. 2010, 48, 893-898.
107. Denz, C. R., Narshi, A., Zajdel, R. W., Dube, D. K., Expression of a novel cardiac-specific tropomyosin isoform in humans. Biochem. Biophys. Res. Commun. 2004, 320, 1291-1297.
108. Wieczorek, D. F., Smith, C. W. J., Nadalginard, B., The rat alpha-tropomyosin gene generates a minimum of 6 different messenger-Rnas coding for striated, smooth, and nonmuscle isoforms by alternative splicing. Mol. Cell. Biol. 1988, 8, 679-694.
109. Nadal-Ginard, B., Muscle cell differentiation and alternative splicing. Curr. Opin. Cell. Biol. 1990, 2, 1058-1064.
110. Leesmiller, J. P., Helfman, D. M., The molecular-basis for tropomyosin isoform diversity. Bioessays 1991, 13, 429-437.
111. Rajan, S., Jagatheesan, G., Karam, C. N., Alves, M. L. et al., Molecular and functional characterization of a novel cardiac-specific human tropomyosin isoform. Circulation 2010, 121, 410-418.
112. Marston, S. B., Copeland, O. N., Messer, A. E., MacNamara, E. et al., Tropomyosin isoform expression and phosphorylation in the human heart in health and disease. J. Muscle Res. Cell Motil. 2013, 34, 189-197.
113. Peng, Y., Yu, D. Y., Gregorich, Z., Chen, X. et al., In-depth proteomic analysis of human tropomyosin by top-down mass spectrometry. J. Muscle Res. Cell Motil. 2013, 34, 199-210.
114. Gunning, P. W., Schevzov, G., Kee, A. J., Hardeman, E. C., Tropomyosin isoforms: divining rods for actin cytoskeleton function. Trends Cell Biol. 2005, 15, 333-341.
115. Gunning, P., O'Neill, G., Hardeman, E., Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiol. Rev. 2008, 88, 1-35.
116. Wieczorek, D. F., Jagatheesan, G., Rajan, S., in: Peter, G. (Ed.), Tropomyosin, Spring Science, New York 2008, pp. 132-139.
117. Vahebi, S., Ota, A., Li, M., Warren, C. M., de Tombe, P. P. et al., p38-MAPK induced dephosphorylation of alpha-tropomyosin is associated with depression of myocardial sarcomeric tension and ATPase activity. Circ. Res. 2007, 100, 408-415.
118. Schulz, E. M., Correll, R. N., Sheikh, H. N., Lofrano-Alves, M. S. et al., Tropomyosin dephosphorylation results in compensated cardiac hypertrophy. J. Biol. Chem. 2012, 287, 44478-44489.
119. Peng, Y., Chen, X., Zhang, H., Xu, Q. G. et al., Top-down targeted proteomics for deep sequencing of tropomyosin isoforms. J. Proteome Res. 2013, 12, 187-198.
120. Mak, A., Smillie, L. B., Barany, M., Specific phosphorylation at serine-283 of alpha-tropomyosin from skeletal and rabbit skeletal and cardiac-muscle. Proc. Natl. Acad. Sci. USA 1978, 75, 3588-3592.
121. Heeley, D. H., Watson, M. H., Mak, A. S., Dubord, P., Smillie, L. B., Effect of phosphorylation on the interaction and functional properties of rabbit striated muscle alpha alpha-tropomyosin. J. Biol. Chem. 1989, 264, 2424-2430.
122. Barefield, D., Sadayappan, S., Phosphorylation and function of cardiac myosin binding protein-C in health and disease. J. Mol. Cell. Cardiol. 2010, 48, 866-875.
123. Spirito, P., Seidman, C. E., McKenna, W. J., Maron, B. J., Medical progress-the management of hypertrophic cardiomyopathy. N. Engl. J. Med. 1997, 336, 775-785.
124. Winegrad, S., Myosin binding protein C, a potential regulator of cardiac contractility. Circ. Res. 2000, 86, 6-7.
125. de Tombe, P. P., Myosin binding protein C in the heart. Circ. Res. 2006, 98, 1234-1236.
126. Sadayappan, S., Gulick, J., Osinska, H., Martin, L. A. et al., Cardiac myosin-binding protein-C phosphorylation and cardiac function. Circ. Res. 2005, 97, 1156-1163.
127. Sadayappan, S., Osinska, H., Klevitsky, R., Lorenz, J. N. et al., Cardiac myosin binding protein C phosphorylation is cardioprotective. Proc. Natl. Acad. Sci. USA 2006, 103, 16918-16923.
128. Colson, B. A., Bekyarova, T., Locher, M. R., Fitzsimons, D. P. et al., Protein kinase A-mediated phosphorylation of cMyBP-C increases proximity of myosin heads to actin in resting myocardium. Circ. Res. 2008, 103, 244-251.
129. Weisberg, A., Winegrad, S., Alteration of myosin cross bridges by phosphorylation of myosin-binding protein C in cardiac muscle. Proc. Natl. Acad. Sci. USA 1996, 93, 8999-9003.
130. Mohamed, A. S., Dignam, J. D., Schlender, K. K., Cardiac myosin-binding protein C (MyBP-C): identification of protein kinase A and protein kinase C phosphorylation sites. Arch. Biochem. Biophys. 1998, 358, 313-319.
131. Yuan, C., Guo, Y. R., Ravi, R., Przyklenk, K. et al., Myosin binding protein C is differentially phosphorylated upon myocardial stunning in canine and rat hearts-evidence for novel phosphorylation sites. Proteomics 2006, 6, 4176-4186.
132. Kooij, V., Holewinski, R. J., Murphy, A. M., Van Eyk, J. E., Characterization of the cardiac myosin binding protein-C phosphoproteome in healthy and failing human hearts. J. Mol. Cell. Cardiol. 2013, 60, 116-120.
133. Govindan, S., McElligott, A., Muthusamy, S., Nair, N. et al., Cardiac myosin binding protein-C is a potential diagnostic biomarker for myocardial infarction. J. Mol. Cell. Cardiol. 2012, 52, 154-164.
134. Sadayappan, S., Cardiac myosin binding protein-C: a potential early-stage, cardiac-specific biomarker of ischemia-reperfusion injury. Biomarkers Med. 2012, 6, 69-72.
135. Witayavanitkul, N., Ait Mou, Y., Kuster, D.W., Khairallah, R.J. et al., Myocardial infarction-induced N-terminal fragment of cardiac myosin-binding protein C (cMyBP-C) impairs myofilament function in human myocardium. J. Biol. Chem. 2014, 289, 8818-8827.
136. Gautel, M., Zuffardi, O., Freiburg, A., Labeit, S., Phosphorylation Switches Specific for the cardiac isoform of myosin binding protein-C-a modulator of cardiac contraction. EMBO J. 1995, 14, 1952-1960.
137. Tian, Z., Tolic, N., Zhao, R., Moore, R. J. et al., Enhanced top-down characterization of histone post-translational modifications. Genome Biol. 2012, 13, R86.
138. Tran, J. C., Zamdborg, L., Ahlf, D. R., Lee, J. E. et al., Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature 2011, 480, 254-258.
139. Chen, X., Ge, Y., Ultrahigh pressure fast size exclusion chromatography for top-down proteomics. Proteomics 2013, 13, 2563-2566.
140. Zhao, D. S., Gregorich, Z. R., Ge, Y., High throughput screening of disulfide-containing proteins in a complex mixture. Proteomics 2013, 13, 3256-3260.
141. Guner, H., Close, P. L., Cai, W. X., Zhang, H. et al., MASH suite: a user-friendly and versatile software interface for high-resolution mass spectrometry data interpretation and visualization. J. Am. Soc. Mass Spectrom. 2014, 25, 464-470.
142. Liu, X., Inbar, Y., Dorrestein, P. C., Wynne, C. et al., Deconvolution and database search of complex tandem mass spectra of intact proteins. Mol. Cell. Proteomics 2010, 9, 2772-2782.
143. Meng, F. Y., Cargile, B. J., Miller, L. M., Forbes, A. J. et al., Informatics and multiplexing of intact protein identification in bacteria and the archaea. Nat. Biotechnol. 2001, 19, 952-957.