Top-down high-resolution mass spectrometry of cardiac myosin binding protein C revealed that truncation alters protein phosphorylation state

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 31, 2009, Pages 12658-12663

  Ge, Ying ^a   Rybakova, Inna N ^a   Xu, Qingge ^a   Moss, Richard L ^a  

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

Author keywords

Electron capture dissociation; Hypertrophic cardiomypathy

Indexed keywords

MYOSIN BINDING PROTEIN C; RECOMBINANT PROTEIN; CARRIER PROTEIN; MYOSIN-BINDING PROTEIN C;

ACCURACY; ARTICLE; BACULOVIRUS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON CAPTURE DETECTION; HEART; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; BIOSYNTHESIS; CHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY; MOLECULAR GENETICS; PHOSPHORYLATION; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; CARRIER PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 69149100342     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0813369106     Document Type: Article

References (50)

1. Winegrad S (2000) Myosin binding protein C, a potential regulator of cardiac contractility. Circ Res 86:6-7.
2. Flashman E, Redwood C, Moolman-Smook J, Watkins H (2004) Cardiac myosin binding protein C - Its role in physiology and disease. Circ Res 94:1279-1289.
3. de Tombe PP (2006) Myosin binding protein C in the heart. Circ Res 98:1234-1236.
4. Zoghbi ME, Woodhead JL, Moss RL, Craig R (2008) Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc Natl Acad Sci USA 105:2386-2390.
5. Moss RL, Razumova M, Fitzsimons DP (2004) Myosin crossbridge activation of cardiac thin filaments-Implications for myocardial function in health and disease. Circ Res 94:1290-1300.
6. Spirito P, Seidman CE, McKenna WJ, Maron BJ (1997) Medical progress - The management of hypertrophic cardiomyopathy. N Engl J Med 336:775-785.
7. Freiburg A, Gautel M (1996) A molecular map of the interactions between titin and myosin-binding protein C-Implications for sarcomeric assembly in familial hypertrophic cardiomyopathy. Euro J Biochem 235:317-323.
8. Kunst G, et al. (2000) Myosin binding protein C, a phosphorylation- dependent force regulator in muscle that controls the attachment of myosin heads by its interaction with myosin S2. Circ Res 86:51-58.
9. Razumova MV, et al. (2006) Effects of the N-terminal domains of myosin binding protein-C in an in vitro motility assay - Evidence for long-lived cross-bridges. J Biol Chem 281:35846-35854.
10. Sadayappan S, et al. (2005) Cardiac myosin-binding protein-C phosphorylation and cardiac function. Circ Res 97:1156-1163.
11. Stelzer JE, Dunning SB, Moss RL (2006) Ablation of cardiac myosin-binding protein-C accelerates stretch activation in murine skinned myocardium. Circ Res 98:1212-1218.
12. Stelzer JE, Patel JR, Walker JW, Moss RL (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.
13. Sadayappan S, et al. (2006) Cardiac myosin binding protein C phosphorylation is cardioprotective. Proc Natl Acad Sci USA 103:16918-16923.
14. Gautel M, Zuffardi O, Freiburg A, Labeit S (1995) Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C - amodulator of cardiac contraction. EMBO J 14:1952-1960.
15. Mohamed AS, Dignam JD, Schlender KK (1998) Cardiac myosin-binding protein C (MyBP-C): Identification of protein kinase A and protein kinase C phosphorylation sites. Arch Biochem Biophys 358:313-319.
16. Colson BA, et al. (2008) Protein kinase A-mediated phosphorylation of cMyBP-C increases proximity of myosin heads to actin in resting myocardium. Circ Res 103:244-251.
17. Weisberg A, Winegrad S (1996) Alteration of myosin cross bridges by phosphorylation of myosin-binding protein C in cardiac muscle. Proc Natl Acad Sci USA 93:8999-9003.
18. Gruen M, Prinz H, Gautel M (1999) CAPK-phosphorylation controls the interaction of the regulatory domain of cardiac myosin binding protein Cwith myosin-S2 in an on-off fashion. Febs Lett 453:254-259.
19. Yuan C, et al. (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.
20. Yuan C, et al. (2008) Quantitative comparison of sarcomeric phosphoproteomes of neonatal and adult rat hearts Am J Physiol Heart Circ Physiol 295:H647-H656.
21. McLafferty FW, Fridriksson EK, Horn DM, Lewis MA, Zubarev RA (1999) Biochemistry - Biomolecule mass spectrometry. Science 284:1289-1290.
22. Pesavento JJ, Mizzen CA, Kelleher NL (2006) Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry: Human histone H4. Anal Chem 78:4271-4280.
23. Mann M, Jensen ON (2003) Proteomic analysis of post-translational modifications. Nat Biotechnol 21:255-261.
24. Pesavento JJ, Bullock CR, Leduc RD, Mizzen CA, Kelleher NL (2008) Combinatorial modification of human histone H4 quantitated by two-dimensional liquid chromatography coupled with top down mass spectrometry. J Biol Chem 283:14927-14937.
25. Zabrouskov V, Ge Y, Schwartz J, Walker JW (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.
26. Mann M, Kelleher NL (2008) Precision proteomics: The case for high resolution and high mass accuracy. Proc Natl Acad Sci USA 105:18132-18138.
27. Chait BT (2006) Mass spectrometry: Bottom-up or top-down? Science 314:65-66.
28. Kjeldsen F, Savitski MM, Nielsen ML, Shi L, Zubarev RA (2007) On studying protein phosphorylation patterns using bottom-up LC-MS/MS: The case of human alpha-casein. Analyst 132:768-776.
29. Kelleher NL, et al. (1999) Top down versus bottom up protein characterization by tandem high-resolution mass spectrometry. J Am Chem Soc 121:806-812.
30. Ge Y, et al. (2002) Top down characterization of larger proteins (45 kDa) by electron capture dissociation mass spectrometry. J Am Chem Soc 124:672-678.
31. Ge Y, et al. (2003) Top down characterization of secreted proteins from Mycobacterium tuberculosis by electron capture dissociation mass spectrometry. J Am Soc Mass Spectrom 14:253-261.
32. Ge Y, et al. (2003) Detection of four oxidation sites in viral prolyl-4-hydroxylase by top-down mass spectrometry. Protein Sci 12:2320-2326.
33. Zabrouskov V, Giacomelli L, van Wijk KJ, McLafferty FW (2003) New approach for plant proteomics - Characterization of chloroplast proteins of Arabidopsis thaliana by topdown mass spectrometry. Mol Cell Proteomics 2:1253-1260.
34. Jebanathirajah JA, et al. (2005) Characterization of a new qQq-FTICR mass spectrometer for post-translational modification analysis and top-down tandem mass Spectrometry of whole proteins. J Am Soc Mass Spectrom 16:1985-1999.
35. Zabrouskov V, et al. (2006) Stepwise deamidation of ribonuclease A at five sites determined by top down mass spectrometry. Biochemistry 45:987-992.
36. Han XM, Jin M, Breuker K, McLafferty FW (2006) Extending top-down mass spectrometry to proteins with masses greater than 200 kilodaltons. Science 314:109-112.
37. Xie YM, Zhang J, Yin S, Loo JA (2006) Top-down ESI-ECD-FT-ICR mass spectrometry localizes noncovalent protein-ligand binding sites. J Am Chem Soc 128:14432-14433.
38. Siuti N, Kelleher NL (2007) Decoding protein modifications using top-down mass spectrometry. Nat Methods 4:817-821.
39. Zabrouskov V, Whitelegge JP (2007) Increased coverage in the transmembrane domain with activated-ion electron capture dissociation for top-down Fourier-transform mass spectrometry of integral membrane proteins. J Proteome Res 6:2205-2210.
40. Zubarev RA, et al. (2000) Electron capture dissociation for structural characterization of multiply charged protein cations. Anal Chem 72:563-573.
41. Senko MW, Speir JP, McLafferty FW (1994) Collisional activation of large multiply-charged ions using fourier-transform mass-spectrometry. Anal Chem 66:2801-2808.
42. Zubarev RA, Kelleher NL, McLafferty FW (1998) Electron capture dissociation of multiply charged protein cations. A nonergodic process. J Am Chem Soc 120:3265-3266.
43. Mirgorodskaya E, Roepstorff P, Zubarev RA (1999) Localization of O-glycosylation sites in peptides by electron capture dissociation in a fourier transform mass spectrometer. Anal Chem 71:4431-4436.
44. Kelleher NL, et al. (1999) Localization of labile posttranslational modifications by electron capture dissociation: The case of gamma- carboxyglutamic acid. Anal Chem 71:4250-4253.
45. Cooper HJ, Hakansson K, Marshall AG (2005) The role of electron capture dissociation in biomolecular analysis. Mass Spectrom Rev 24:201-222.
46. Govada L, et al. (2008) Crystal structure of the C1 domain of cardiac myosin binding protein-C: Implications for hypertrophic cardiomyopathy. J Mol Biol 378:387-397.
47. Whitten AE, Jeffries CM, Harris SP, Trewhella J (2008) Cardiac myosin-binding protein C decorates F-actin: Implications for cardiac function. Proc Natl Acad Sci USA 105:18360-18365.
48. Oakley CE, Chamoun J, Brown LJ, Hambly BD (2007) Myosin binding protein-C: Enigmatic regulator of cardiac contraction. Int J Biochem Cell Biol 39:2161-2166.
49. Kelleher NL, Senko MW, Siegel MM, McLafferty FW (1997) Unit resolution mass spectra of 112 kDa molecules with 3 Da accuracy. J Am Soc Mass Spectrom 8:380-383.
50. Cournoyer JJ, Lin C, O'Connor PB (2006) Detecting deamidation products in proteins by electron capture dissociation. Anal Chem 78:1264-1271.