The motif of human cardiac myosin-binding protein C is required for its Ca2+-dependent interaction with calmodulin

Journal of Biological Chemistry

Volumn 287, Issue 37, 2012, Pages 31596-31607

  Lu, Yanling ^a   Kwan, Ann H ^a   Jeffries, Cy M ^a,b   Guss, J Mitchell ^a   Trewhella, Jill ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b AUSTRALIAN NUCLEAR SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING MODES; CONSERVED RESIDUES; HEART MUSCLE CONTRACTIONS; ISOFORMS; MULTIPLE INTERACTIONS; N-TERMINALS; SIGNALING PATHWAYS;

BINDING ENERGY; CALCIUM; CAMS; MUSCLE; PHOSPHORYLATION;

CALMODULIN;

CALCIUM ION; CALMODULIN; GLUTAMIC ACID; LYSINE; MYOSIN BINDING PROTEIN C;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; HEART CONTRACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RADIATION SCATTERING; SIGNAL TRANSDUCTION;

ACTINS; AMINO ACID MOTIFS; CALCIUM; CALMODULIN; CARRIER PROTEINS; HUMANS; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOSINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84866054100     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.383299     Document Type: Article

References (62)

1. Geeves, M. A., and Holmes, K. C. (2005) The molecular mechanism of muscle contraction. Adv. Protein. Chem. 71, 161-193
2. Whitten, A. E., Jeffries, C. M., Harris, S. P., and Trewhella, J. (2008) Cardiac myosin-binding protein C decorates F-actin. Implications for cardiac function. Proc. Natl. Acad. Sci. U.S.A. 105, 18360-18365
3. Orlova, A., Galkin, V. E., Jeffries, C. M., Egelman, E. H., and Trewhella, J. (2011) The N-terminal domains of myosin-binding protein C can bind polymorphically to F-actin. J. Mol. Biol. 412, 379-386
4. Chin, D., and Means, A. R. (2000) Calmodulin. A prototypical calcium sensor. Trends Cell Biol. 10, 322-328
5. Vetter, S. W., and Leclerc, E. (2003) Novel aspects of calmodulin target recognition and activation. Eur. J. Biochem. 270, 404-414
6. Crivici, A., and Ikura, M. (1995) Molecular and structural basis of target recognition by calmodulin. Annu. Rev. Biophys. Biomol. Struct. 24, 85-116
7. 2+-calmodulin-dependent protein kinases. J. Biol. Chem. 259, 15587-15596
8. Schlender, K. K., and Bean, L. J. (1991) Phosphorylation of chicken cardiac C-protein by calcium/calmodulin-dependent protein kinase II. J. Biol. Chem. 266, 2811-2817
9. Yamniuk, A. P., and Vogel, H. J. (2004) Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol. Biotechnol. 27, 33-57
10. 2+ and possible function in short-term synaptic plasticity. EMBO J. 29, 680-691
11. V1.2 function but do not mediate channel dimerization. EMBO J. 29, 3924-3938
12. 2+. J. Biol. Chem. 286, 40954-40961
13. Izumi, Y., Watanabe, H., Watanabe, N., Aoyama, A., Jinbo, Y., and Hayashi, N. (2008) Solution x-ray scattering reveals a novel structure of calmodulin complexed with a binding domain peptide from the HIV-1 matrix protein p17. Biochemistry 47, 7158-7166
14. 2+/calmodulin. Nature 410, 1120-1124
15. Lu, Y., Jeffries, C. M., and Trewhella, J. (2011) Invited review. Probing the structures of muscle regulatory proteins using small-angle solution scattering. Biopolymers 95, 505-516
16. Oakley, C. E., Hambly, B. D., Curmi, P. M., and Brown, L. J. (2004) Myosinbinding protein C. Structural abnormalities in familial hypertrophic cardiomyopathy. Cell Res. 14, 95-110
17. Oakley, C. E., Chamoun, J., Brown, L. J., and Hambly, B. D. (2007) Myosinbinding protein-C. Enigmatic regulator of cardiac contraction. Int. J. Biochem. Cell Biol. 39, 2161-2166
18. Flashman, E., Redwood, C., Moolman-Smook, J., and Watkins, H. (2004) Cardiac myosin-binding protein C. Its role in physiology and disease. Circ. Res. 94, 1279-1289
19. Gautel, M., Zuffardi, O., Freiburg, A., and Labeit, S. (1995) Phosphorylation switches specific for the cardiac isoform of myosin-binding protein-C. A modulator of cardiac contraction? EMBO J. 14, 1952-1960
20. Tardiff, J. (2005) Sarcomeric proteins and familial hypertrophic cardiomyopathy. Linking mutations in structural proteins to complex cardiovascular phenotypes. Heart Fail. Rev. 10, 237-248
21. Kelly, M., and Semsarian, C. (2009) Multiple mutations in genetic cardiovascular disease. A marker of disease severity? Circ. Cardiovasc. Genet. 2, 182-190
22. van Dijk, S. J., Dooijes, D., dos Remedios, C., Michels, M., Lamers, J. M., Winegrad, S., Schlossarek, S., Carrier, L., ten Cate, F. J., Stienen, G. J., and van der Velden, J. (2009) Cardiac myosin-binding protein C mutations and hypertrophic cardiomyopathy haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation 119, 1473-1483
23. Gruen, M., Prinz, H., and Gautel, M. (1999) cAPK phosphorylation controls the interaction of the regulatory domain of cardiac myosin-binding protein C with myosin-S2 in an on-off fashion. FEBS Lett. 453, 254-259
24. Gruen, M., and Gautel, M. (1999) Mutations in β-myosin S2 that cause familial hypertrophic cardiomyopathy (FHC) abolish the interaction with the regulatory domain of myosin-binding protein-C. J. Mol. Biol. 286, 933-949
25. Kunst, G., Kress, K. R., Gruen, M., Uttenweiler, D., Gautel, M., and Fink, R. H. (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
26. Mohamed, A. S., Dignam, J. D., and Schlender, K. K. (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
27. Weisberg, A., and Winegrad, S. (1996) Alteration of myosin cross-bridges by phosphorylation of myosin-binding protein C in cardiac muscle. Proc. Natl. Acad. Sci. U.S.A. 93, 8999-9003
28. McClellan, G., Kulikovskaya, I., and Winegrad, S. (2001) Changes in cardiac contractility related to calcium-mediated changes in phosphorylation of myosin-binding protein C. Biophys. J. 81, 1083-1092
29. Cheng, L. H., Qin, Q. H., Ding, G. L., Yao, H., Floyd, D., Woods, D., and Yang, Q. L. (2003) Substitution of a constantly phosphorylated cardiac myosin-binding protein C in transgenic mouse heart enhances cardiac performance. Circulation 108, (Suppl IV) 90
30. Yuan, C., Guo, Y., Ravi, R., Przyklenk, K., Shilkofski, N., Diez, R., Cole, R. N., and Murphy, A. M. (2006) Myosin-binding proteinCis differentially phosphorylated upon myocardial stunning in canine and rat hearts. Evidence for novel phosphorylation sites. Proteomics 6, 4176-4186
31. Sadayappan, S., Gulick, J., Osinska, H., Barefield, D., Cuello, F., Avkiran, M., Lasko, V. M., Lorenz, J. N., Maillet, M., Martin, J. L., Brown, J. H., Bers, D. M., Molkentin, J. D., James, J., and Robbins, J. (2011) A critical function for Ser-282 in cardiac myosin-binding protein-C phosphorylation and cardiac function. Circ. Res. 109, 141-150
32. Blumenthal, D. K., Charbonneau, H., Edelman, A. M., Hinds, T. R., Rosenberg, G. B., Storm, D. R., Vincenzi, F. F., Beavo, J. A., and Krebs, E. G. (1988) Synthetic peptides based on the calmodulin-binding domain of myosin light chain kinase inhibit activation of other calmodulin-dependent enzymes. Biochem. Biophys. Res. Commun. 156, 860-865
33. Tong, C. W., Gaffin, R. D., Zawieja, D. C., and Muthuchamy, M. (2004) Roles of phosphorylation of myosin-binding protein-C and troponin I in mouse cardiac muscle twitch dynamics. J. Physiol. 558, 927-941
34. Ding, P., Huang, J., Battiprolu, P. K., Hill, J. A., Kamm, K. E., and Stull, J. T. (2010) Cardiac myosin light chain kinase is necessary for myosin regulatory light chain phosphorylation and cardiac performance in vivo. J. Biol. Chem. 285, 40819-40829
35. Sweeney, H. L., Bowman, B. F., and Stull, J. T. (1993) Myosin light-chain phosphorylation in vertebrate striated muscle. Regulation and function. Am. J. Physiol. 264, C1085-C1095
36. Zhi, G., Ryder, J. W., Huang, J., Ding, P., Chen, Y., Zhao, Y., Kamm, K. E., and Stull, J. T. (2005) Myosin light chain kinase and myosin phosphorylation effect frequency-dependent potentiation of skeletal muscle contraction. Proc. Natl. Acad. Sci. U.S.A. 102, 17519-17524
37. Solaro, R. J. (2008) Multiplex kinase signaling modifies cardiac function at the level of sarcomeric proteins. J. Biol. Chem. 283, 26829-26833
38. Ratti, J., Rostkova, E., Gautel, M., and Pfuhl, M. (2011) Structure and Interactions of myosin-binding protein C domain C0. J. Biol. Chem. 286, 12650-12658
39. Lu, Y., Kwan, A. H., Trewhella, J., and Jeffries, C. M. (2011) The C0C1 fragment of human cardiac myosin-binding protein C has common binding determinants for both actin and myosin. J. Mol. Biol. 413, 908-913
40. Jeffries, C. M., Lu, Y., Hynson, R. M., Taylor, J. E., Ballesteros, M., Kwan, A. H., and Trewhella, J. (2011) Human cardiac myosin-binding protein C. Structural flexibility within an extended modular architecture. J. Mol. Biol. 414, 735-748
41. Jeffries, C. M., Whitten, A. E., Harris, S. P., and Trewhella, J. (2008) Smallangle x-ray scattering reveals the N-terminal domain organization of cardiac myosin-binding protein C. J. Mol. Biol. 377, 1186-1199
42. Chow, J. Y., Jeffries, C. M., Kwan, A. H., Guss, J. M., and Trewhella, J. (2010) Calmodulin disrupts the structure of the HIV-1MAprotein. J. Mol. Biol. 400, 702-714
43. André, I., Kesvatera, T., Jönsson, B., Akerfeldt, K. S., and Linse, S. (2004) The role of electrostatic interactions in calmodulin-peptide complex formation. Biophys. J. 87, 1929-1938
44. Ababou, A., Rostkova, E., Mistry, S., Le Masurier, C., Gautel, M., and Pfuhl, M. (2008) Myosin-binding protein C positioned to play a key role in regulation of muscle contraction. Structure and interactions of domain C1. J. Mol. Biol. 384, 615-630
45. Franke, D., and Svergun, D. I. (2009) DAMMIF, a program for rapid ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346
46. Ababou, A., Gautel, M., and Pfuhl, M. (2007) Dissecting the N-terminal myosin binding site of human cardiac myosin-binding protein C. Structure and myosin binding of domain C2. J. Biol. Chem. 282, 9204-9215
47. Govada, L., Carpenter, L., da Fonseca, P. C., Helliwell, J. R., Rizkallah, P., Flashman, E., Chayen, N. E., Redwood, C., and Squire, J. M. (2008) Crystal structure of the C1 domain of cardiac myosin-binding protein-C. Implications for hypertrophic cardiomyopathy. J. Mol. Biol. 378, 387-397
48. Weljie, A. M., and Vogel, H. J. (2000) Tryptophan fluorescence of calmodulin binding domain peptides interacting with calmodulin containing unnatural methionine analogues. Protein Eng. 13, 59-66
49. Muiño, P. L., and Callis, P. R. (2009) Solvent effects on the fluorescence quenching of tryptophan by amides via electron transfer. Experimental and computational studies. J. Phys. Chem. B 113, 2572-2577
50. Howarth, J. W., Ramisetti, S., Nolan, K., Sadayappan, S., and Rosevear, P. R. (2012) Structural insight into the unique cardiac myosin-binding protein-C motif.Apartially folded domain. J. Biol. Chem. 287, 8254-8262
51. Yap, K. L., Kim, J., Truong, K., Sherman, M., Yuan, T., and Ikura, M. (2000) Calmodulin target database. J. Struct. Funct. Genomics 1, 8-14
52. Rhoads, A. R., and Friedberg, F. (1997) Sequence motifs for calmodulin recognition. FASEB J. 11, 331-340
53. Chattopadhyaya, R., Meador, W. E., Means, A. R., and Quiocho, F. A. (1992) Calmodulin structure refined at 1.7 Å resolution. J. Mol. Biol. 228, 1177-1192
54. Petoukhov, M. V., Konarev, P. V., Kikhney, A. G., and Svergun, D. I. (2007) ATSAS 2.1. Toward automated and web-supported small-angle scattering data analysis. J. Appl. Crystallogr. 40, S223-S228
55. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
56. Heidorn, D. B., and Trewhella, J. (1988) Comparison of the crystal and solution structures of calmodulin and troponin C. Biochemistry 27, 909-915
57. 2+-bound calmodulin forms a compact globular structure on binding four trifluoperazine molecules in solution. Biochem. J. 347, 211-215
58. Jia, W., Shaffer, J. F., Harris, S. P., and Leary, J. A. (2010) Identification of novel protein kinase A phosphorylation sites in the m-domain of human and murine cardiac myosin-binding protein-C using mass spectrometry analysis. J. Proteome Res. 9, 1843-1853
59. Rybakova, I. N., Greaser, M. L., and Moss, R. L. (2011) Myosin-binding protein C interaction with actin. J. Biol. Chem. 286, 2008-2016
60. Harris, S. P., Lyons, R. G., and Bezold, K. L. (2011) In the thick of it. HCM-causing mutations in myosin-binding proteins of the thick filament. Circ. Res. 108, 751-764
61. Colbran, R. J. (2004) Targeting of calcium/calmodulin-dependent protein kinase II. Biochem. J. 378, 1-16
62. Stull, J. T., Kamm, K. E., and Vandenboom, R. (2011) Myosin light chain kinase and the role of myosin light chain phosphorylation in skeletal muscle. Arch. Biochem. Biophys. 510, 120-128