Electron microscopy and 3D reconstruction of F-actin decorated with cardiac myosin-binding protein C (cMyBP-C)

Journal of Molecular Biology

Volumn 410, Issue 2, 2011, Pages 214-225

  Mun, Ji Young ^a   Gulick, James ^b   Robbins, Jeffrey ^b   Woodhead, John ^a   Lehman, William ^c   Craig, Roger ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cardiac contraction; cardiac muscle; cardiac regulation; muscle regulation; muscle structure

Indexed keywords

CURVED DNA; DOUBLE STRANDED DNA; ESCHERICHIA COLI PROTEIN; HU PROTEIN; INTEGRATION HOST FACTOR;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; ESCHERICHIA COLI; GAP JUNCTION; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; PROTEIN DNA BINDING; SALT DEPENDENT THERMODYNAMICS; THERMODYNAMICS;

VERTEBRATA;

EID: 79958708378     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.05.010     Document Type: Article

References (53)

1. Offer, G., Moos, C. & Starr, R. (1973). A new protein of the thick filaments of vertebrate skeletal myofibrils. Extraction, purification and characterization. J. Mol. Biol. 74, 653-676.
2. Bennett, P. M., Furst, D. O. & Gautel, M. (1999). The C-protein (myosin binding protein C) family: regulators of contraction and sarcomere formation? Rev. Physiol. Biochem. Pharmacol. 138, 203-234.
3. 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.
4. Barefield, D. & Sadayappan, S. (2010). Phosphorylation and function of cardiac myosin binding protein-C in health and disease. J. Mol. Cell. Cardiol. 48, 866-875.
5. Craig, R. & Offer, G. (1976). The location of C-protein in rabbit skeletal muscle. Proc. R. Soc. London, Ser. B, 192, 451-461.
6. Luther, P. K., Bennett, P. M., Knupp, C., Craig, R., Padron, R., Harris, S. P. et al. (2008). Understanding the organisation and role of myosin binding protein C in normal striated muscle by comparison with MyBP-C knockout cardiac muscle. J. Mol. Biol. 384, 60-72.
7. Bennett, P., Craig, R., Starr, R. & Offer, G. (1986). The ultrastructural location of C-protein, X-protein and H-protein in rabbit muscle. J. Muscle Res. Cell Motil. 7, 550-567.
8. Einheber, S. & Fischman, D. A. (1990). Isolation and characterization of a cDNA clone encoding avian skeletal muscle C-protein: an intracellular member of the immunoglobulin superfamily. Proc. Natl Acad. Sci. USA, 87, 2157-2161.
9. Jia, W., Shaffer, J. F., Harris, S. P. & 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.
10. Yasuda, M., Koshida, S., Sato, N. & Obinata, T. (1995). Complete primary structure of chicken cardiac C-protein (MyBP-C) and its expression in developing striated muscles. J. Mol. Cell. Cardiol. 27, 2275-2286.
11. Gautel, M., Zuffardi, O., Freiburg, A. & 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.
12. Watkins, H., Conner, D., Thierfelder, L., Jarcho, J. A., MacRae, C., McKenna, W. J. et al. (1995). Mutations in the cardiac myosin binding protein-C gene on chromosome 11 cause familial hypertrophic cardiomyopathy. Nat. Genet. 11, 434-437.
13. Vikstrom, K. L. & Leinwand, L. A. (1996). Contractile protein mutations and heart disease. Curr. Opin. Cell Biol. 8, 97-105.
14. Dhandapany, P. S., Sadayappan, S., Xue, Y., Powell, G. T., Rani, D. S., Nallari, P. et al. (2009). A common MYBPC3 (cardiac myosin binding protein C) variant associated with cardiomyopathies in South Asia. Nat. Genet. 41, 187-191.
15. Gurnett, C. A., Desruisseau, D. M., McCall, K., Choi, R., Meyer, Z. I., Talerico, M. et al. (2010). Myosin binding protein C1: a novel gene for autosomal dominant distal arthrogryposis type 1. Hum. Mol. Genet. 19, 1165-1173.
16. Lin, Z., Lu, M. H., Schultheiss, T., Choi, J., Holtzer, S., DiLullo, C. et al. (1994). Sequential appearance of muscle-specific proteins in myoblasts as a function of time after cell division: evidence for a conserved myoblast differentiation program in skeletal muscle. Cell Motil. Cytoskeleton, 29, 1-19.
17. Sadayappan, S., Osinska, H., Klevitsky, R., Lorenz, J. N., Sargent, M., Molkentin, J. D. et al. (2006). Cardiac myosin binding protein C phosphorylation is cardioprotective. Proc. Natl Acad. Sci. USA, 103, 16918-16923.
18. 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.
19. Levine, R., Weisberg, A., Kulikovskaya, I., McClellan, G. & Winegrad, S. (2001). Multiple structures of thick filaments in resting cardiac muscle and their influence on cross-bridge interactions. Biophys. J. 81, 1070-1082. (Pubitemid 32721475)
20. Zoghbi, M. E., Woodhead, J. L., Moss, R. L. & Craig, R. (2008). Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc. Natl Acad. Sci. USA, 105, 2386-2390.
21. Starr, R. & Offer, G. (1978). The interaction of Cprotein with heavy meromyosin and subfragment-2. Biochem. J. 171, 813-816. (Pubitemid 8348760)
22. Gruen, M., Prinz, H. & 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. (Pubitemid 29326658)
23. Moos, C., Mason, C. M., Besterman, J. M., Feng, I. N. & Dubin, J. H. (1978). The binding of skeletal muscle C-protein to F-actin, and its relation to the interaction of actin with myosin subfragment-1. J. Mol. Biol. 124, 571-586.
24. Moos, C. (1981). Fluorescence microscope study of the binding of added C protein to skeletal muscle myofibrils. J. Cell Biol. 90, 25-31.
25. Shaffer, J. F., Kensler, R. W. & Harris, S. P. (2009). The myosin-binding protein C motif binds to F-actin in a phosphorylation-sensitive manner. J. Biol. Chem. 284, 12318-12327.
26. Yamamoto, K. (1986). The binding of skeletal muscle C-protein to regulated actin. FEBS Lett. 208, 123-127.
27. Razumova, M. V., Shaffer, J. F., Tu, A. Y., Flint, G. V., Regnier, M. & Harris, S. P. (2006). Effects of the N-terminal domains of myosin binding protein-C in an in vitro motility assay: evidence for long-lived crossbridges. J. Biol. Chem. 281, 35846-35854.
28. Kulikovskaya, I., McClellan, G., Flavigny, J., Carrier, L. & Winegrad, S. (2003). Effect of MyBP-C binding to actin on contractility in heart muscle. J. Gen. Physiol. 122, 761-774.
29. Rybakova, I. N., Greaser, M. L. & Moss, R. L. (2011). Myosin binding protein C interaction with actin: characterization and mapping of the binding site. J. Biol. Chem. 286, 2008-2016.
30. Luther, P., Winkler, H., Taylor, K., Zoghbi, M. E., Craig, R., Padrón, R., et al. (2011). Myosin binding protein C bridges myosin and actin filaments in intact muscle. Proc. Natl Acad. Sci. USA. In press.
31. Squire, J. M., Luther, P. K. & Knupp, C. (2003). Structural evidence for the interaction of C-protein (MyBP-C) with actin and sequence identification of a possible actin-binding domain. J. Mol. Biol. 331, 713-724.
32. Saber, W., Begin, K. J., Warshaw, D. M. & VanBuren, P. (2008). Cardiac myosin binding protein-C modulates actomyosin binding and kinetics in the in vitro motility assay. J. Mol. Cell. Cardiol. 44, 1053-1061.
33. Previs, M. J., Previs, S. B., Robbins, J. & Warshaw, D. M. (2011). Cardiac myosin binding protein-C (MyBP-C) impedes actin filament motility on native mouse ventricular thick filaments only within the C-zone. Biophys. J. 100, 370a.
34. Weith, A., Sadayappan, S., VanBuren, P., Robbins, J. & Warshaw, D. M. (2010). N-terminal fragments of cardiac myosin binding protein-C inhibit actomyosin motility by tethering actin. Biophys. J. 98, 756a.
35. Weith, A., Gulick, J., VanBuren, P., Robbins, J. & Warshaw, D. M. (2011). N-terminal fragment of cardiac myosin binding protein-C (cMyBP-C) reduces actomyosin power output in the laser trap assay. Biophys. J. 100, 454a.
36. Whitten, A. E., Jeffries, C. M., Harris, S. P. & Trewhella, J. (2008). Cardiac myosin-binding protein C decorates F-actin: implications for cardiac function. Proc. Natl Acad. Sci. USA, 105, 18360-18365.
37. Kensler, R. W., Shaffer, J. F. & Harris, S. P. (2011). Binding of the N-terminal fragment C0-C2 of cardiac MyBP-C to cardiac F-actin. J. Struct. Biol. 174, 44-51.
38. Sadayappan, S., Greis, K. D. & Robbins, J. (2008). Phosphorylation-dependent proteolysis and pathogenesis of cardiac myosin binding protein-C. J. Mol. Cell. Cardiol. 44, S44.
39. Oda, T., Iwasa, M., Aihara, T., Maeda, Y. & Narita, A. (2009). The nature of the globular- to fibrous-actin transition. Nature, 457, 441-445.
40. Fisher, S. J., Helliwell, J. R., Khurshid, S., Govada, L., Redwood, C., Squire, J. M. & Chayen, N. E. (2008). An investigation into the protonation states of the C1 domain of cardiac myosin-binding protein C. Acta Crystallogr., Sect. D: Biol. Crystallogr. 64, 658-664. (Pubitemid 351872067)
41. Karsai, A., Harris, S. P. & Kellermayer, M. (2011). The motif of myosin binding protein-C is mechanically weak and extensible. Biophys. J. 100, 453a-454a.
42. Jeffries, C. M., Whitten, A. E., Harris, S. P. & Trewhella, J. (2008). Small-angle X-ray scattering reveals the N-terminal domain organization of cardiac myosin binding protein C. J. Mol. Biol. 377, 1186-1199.
43. Orlova, A., Galkin, V. E., Jeffries, C. M., Trewhella, J. & Egelman, E. H. (2010). Binding of N-terminus fragments of cardiac myosin-binding C-protein to actin. Biophys. J. 98, 157a.
44. Poole, K. J., Lorenz, M., Evans, G., Rosenbaum, G., Pirani, A., Craig, R. et al. (2006). A comparison of muscle thin filament models obtained from electron microscopy reconstructions and low-angle X-ray fibre diagrams from non-overlap muscle. J. Struct. Biol. 155, 273-284.
45. Vibert, P., Craig, R. & Lehman, W. (1997). Stericmodel for activation of muscle thin filaments. J. Mol. Biol. 266, 8-14.
46. Sousa, D., Cammarato, A., Jang, K., Graceffa, P., Tobacman, L. S., Li, X. E. & Lehman, W. (2010). Electron microscopy and persistence length analysis of semi-rigid smooth muscle tropomyosin strands. Biophys. J. 99, 862-868.
47. Li, X. E., Tobacman, L. S., Mun, J. Y., Craig, R., Fischer, S. & Lehman, W. (2011). Tropomyosin position on Factin revealed by EM reconstruction and computational chemistry. Biophys. J. 100, 1005-1013.
48. Pardee, J. D. & Spudich, J. A. (1982). Purification of muscle actin. Methods Enzymol. 85, 164-181.
49. Craig, R. & Lehman, W. (2001). Crossbridge and tropomyosin positions observed in native, interacting thick and thin filaments. J. Mol. Biol. 311, 1027-1036.
50. Lehman, W., Hatch, V., Korman, V., Rosol, M., Thomas, L., Maytum, R. et al. (2000). Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments. J. Mol. Biol. 302, 593-606.
51. Owen, C. H., Morgan, D. G. & DeRosier, D. J. (1996). Image analysis of helical objects: the Brandeis Helical Package. J. Struct. Biol. 116, 167-175.
52. Egelman, E. H. (2000). A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy, 85, 225-234.
53. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. & Ferrin, T. E. (2004). UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.