Probing the flexibility of tropomyosin and its binding to filamentous actin using molecular dynamics simulations

Biophysical Journal

Volumn 105, Issue 8, 2013, Pages 1882-1892

  Zheng, Wenjun ^a   Barua, Bipasha ^b   Hitchcock Degregori, Sarah E ^b  

^a UNIVERSITY AT BUFFALO   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; TROPOMYOSIN;

ACTIN FILAMENT; ARTICLE; CHEMISTRY; METABOLISM; MOLECULAR DYNAMICS; PLIABILITY; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT;

ACTIN CYTOSKELETON; ACTINS; MOLECULAR DYNAMICS SIMULATION; PLIABILITY; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; TROPOMYOSIN;

EID: 84886022133     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.09.003     Document Type: Article

References (63)

1. S.C. Kwok, and R.S. Hodges Stabilizing and destabilizing clusters in the hydrophobic core of long two-stranded α-helical coiled-coils J. Biol. Chem. 279 2004 21576 21588
2. J.H. Brown, and K.H. Kim C. Cohen Deciphering the design of the tropomyosin molecule Proc. Natl. Acad. Sci. USA 98 2001 8496 8501
3. A.D. McLachlan, M. Stewart, and L.B. Smillie Sequence repeats in α-tropomyosin J. Mol. Biol. 98 1975 281 291
4. S. Minakata, and K. Maeda Y. Maéda Two-crystal structures of tropomyosin C-terminal fragment 176-273: exposure of the hydrophobic core to the solvent destabilizes the tropomyosin molecule Biophys. J. 95 2008 710 719
5. S.E. Hitchcock-DeGregori, and A. Singh What makes tropomyosin an actin binding protein? A perspective J. Struct. Biol. 170 2010 319 324
6. P. Gunning Emerging issues for tropomyosin structure, regulation, function and pathology Adv. Exp. Med. Biol. 644 2008 293 298
7. K.C. Holmes, and W. Lehman Gestalt-binding of tropomyosin to actin filaments J. Muscle Res. Cell Motil. 29 2008 213 219
8. J.H. Brown, and Z. Zhou C. Cohen Structure of the mid-region of tropomyosin: bending and binding sites for actin Proc. Natl. Acad. Sci. USA 102 2005 18878 18883
9. A. Singh, and S.E. Hitchcock-DeGregori Dual requirement for flexibility and specificity for binding of the coiled-coil tropomyosin to its target, actin Structure 14 2006 43 50
10. Y. Li, and S. Mui C. Cohen The crystal structure of the C-terminal fragment of striated-muscle α-tropomyosin reveals a key troponin T recognition site Proc. Natl. Acad. Sci. USA 99 2002 7378 7383
11. K. Murakami, and M. Stewart T. Wakabayashi Structural basis for tropomyosin overlap in thin (actin) filaments and the generation of a molecular swivel by troponin-T Proc. Natl. Acad. Sci. USA 105 2008 7200 7205
12. Y. Nitanai, and S. Minakata Y. Maéda Crystal structures of tropomyosin: flexible coiled-coil Adv. Exp. Med. Biol. 592 2007 137 151
13. P. Vibert, R. Craig, and W. Lehman Steric-model for activation of muscle thin filaments J. Mol. Biol. 266 1997 8 14
14. R. Craig, and W. Lehman Crossbridge and tropomyosin positions observed in native, interacting thick and thin filaments J. Mol. Biol. 311 2001 1027 1036
15. A. Pirani, and C. Xu W. Lehman Single particle analysis of relaxed and activated muscle thin filaments J. Mol. Biol. 346 2005 761 772
16. 2+-activated states J. Mol. Biol. 357 2006 707 717
17. K.J. Poole, and M. Lorenz K.C. Holmes 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 2006 273 284
18. W. Lehman, and R. Craig Tropomyosin and the steric mechanism of muscle regulation Adv. Exp. Med. Biol. 644 2008 95 109
19. M. Karplus, and J.A. McCammon Molecular dynamics simulations of biomolecules Nat. Struct. Biol. 9 2002 646 652
20. J.R. Moore, and X. Li W. Lehman Structural implications of conserved aspartate residues located in tropomyosin's coiled-coil core BioArchitecture 1 2011 250 255
21. X.E. Li, and W. Suphamungmee W. Lehman The flexibility of two tropomyosin mutants, D175N and E180G, that cause hypertrophic cardiomyopathy Biochem. Biophys. Res. Commun. 424 2012 493 496
22. D. Hamelberg, J. Mongan, and J.A. McCammon Accelerated molecular dynamics: a promising and efficient simulation method for biomolecules J. Chem. Phys. 120 2004 11919 11929
23. L.C. Pierce, and R. Salomon-Ferrer R.C. Walker Routine access to millisecond time scale events with accelerated molecular dynamics J. Chem. Theory Comput. 8 2012 2997 3002
24. M. Tekpinar, and W. Zheng Coarse-grained and all-atom modeling of structural states and transitions in hemoglobin Proteins 81 2013 240 252
25. X.E. Li, W. Lehman, and S. Fischer The relationship between curvature, flexibility and persistence length in the tropomyosin coiled-coil J. Struct. Biol. 170 2010 313 318
26. X.E. Li, and W. Lehman K.C. Holmes Curvature variation along the tropomyosin molecule J. Struct. Biol. 170 2010 307 312
27. X.E. Li, and K.C. Holmes S. Fischer The shape and flexibility of tropomyosin coiled coils: implications for actin filament assembly and regulation J. Mol. Biol. 395 2010 327 339
28. X.E. Li, and L.S. Tobacman W. Lehman Tropomyosin position on F-actin revealed by EM reconstruction and computational chemistry Biophys. J. 100 2011 1005 1013
29. S.E. Hitchcock-DeGregori, Y. Song, and J. Moraczewska Importance of internal regions and the overall length of tropomyosin for actin binding and regulatory function Biochemistry 40 2001 2104 2112
30. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28
31. G.J. Martyna, A. Hughes, and M.E. Tuckerman Molecular dynamics algorithms for path integrals at constant pressure J. Chem. Phys. 110 1999 3275 3290
32. M. Deserno, and C. Holm How to mesh up Ewald sums. I. A theoretical and numerical comparison of various particle mesh routines J. Chem. Phys. 109 1998 7678 7693
33. W.G. Hoover Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
34. J.C. Phillips, and R. Braun K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802
35. A.D. MacKerell, and D. Bashford M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
36. A.D. Mackerell Jr., M. Feig, and C.L. Brooks 3rd Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415
37. Y. Wang, and C.B. Harrison J.A. McCammon Implementation of accelerated molecular dynamics in NAMD Comput. Sci. Discov. 4 2011 015002
38. J.H. Brown How sequence directs bending in tropomyosin and other two-stranded α-helical coiled coils Protein Sci. 19 2010 1366 1375
39. M.H. Li, and W.J. Zheng Probing the structural and energetic basis of kinesin-microtubule binding using computational alanine-scanning mutagenesis Biochemistry 50 2011 8645 8655
40. M. Li, and W. Zheng All-atom structural investigation of kinesin-microtubule complex constrained by high-quality cryo-electron-microscopy maps Biochemistry 51 2012 5022 5032
41. + channel: a computational approach based on experimental distance restraints extracted from thermodynamic mutant cycles Biophys. J. 83 2002 2595 2609
42. M.K. Gilson, and B.H. Honig Energetics of charge-charge interactions in proteins Proteins 3 1988 32 52
43. W. Im, D. Beglov, and B. Roux Continuum Solvation Model: computation of electrostatic forces from numerical solutions to the Poisson-Boltzmann equation Comput. Phys. Commun. 111 1998 59 75
44. M.A. Olson, and L.T. Reinke Modeling implicit reorganization in continuum descriptions of protein-protein interactions Proteins 38 2000 115 119
45. M.K. Gilson, and B.H. Honig The dielectric constant of a folded protein Biopolymers 25 1986 2097 2119
46. K.A. Sharp, and B. Honig Electrostatic interactions in macromolecules: theory and applications Annu. Rev. Biophys. Biophys. Chem. 19 1990 301 332
47. K.A. Sharp, and B. Honig Calculating total electrostatic energies with the nonlinear Poisson-Boltzmann equation J. Phys. Chem. 94 1990 7684 7692
48. B. Roux Influence of the membrane potential on the free energy of an intrinsic protein Biophys. J. 73 1997 2980 2989
49. M. Nina, D. Beglov, and B. Roux Atomic radii for continuum electrostatics calculations based on molecular dynamics free energy simulations J. Phys. Chem. B 101 1997 5239 5248
50. B.R. Brooks, and R.E. Bruccoleri M. Karplus CHARMM: a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
51. J.H. Brown, and C. Cohen Regulation of muscle contraction by tropomyosin and troponin: how structure illuminates function Adv. Protein Chem. 71 2005 121 159
52. J.P. Sumida, E. Wu, and S.S. Lehrer Conserved Asp-137 imparts flexibility to tropomyosin and affects function J. Biol. Chem. 283 2008 6728 6734
53. N.J. Greenfield, T. Palm, and S.E. Hitchcock-DeGregori Structure and interactions of the carboxyl terminus of striated muscle α-tropomyosin: it is important to be flexible Biophys. J. 83 2002 2754 2766
54. N.J. Greenfield, and Y.J. Huang S.E. Hitchcock-DeGregori Solution NMR structure of the junction between tropomyosin molecules: implications for actin binding and regulation J. Mol. Biol. 364 2006 80 96
55. J.H. Brown Deriving how far structural information is transmitted through parallel homodimeric coiled-coils: a correlation analysis of helical staggers Proteins 81 2013 635 643
56. D.F. McKillop, and M.A. Geeves Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament Biophys. J. 65 1993 693 701
57. E. Behrmann, and M. Müller S. Raunser Structure of the rigor actin-tropomyosin-myosin complex Cell 150 2012 327 338
58. M. Lorenz, and K.J. Poole K.C. Holmes An atomic model of the unregulated thin filament obtained by x-ray fiber diffraction on oriented actin-tropomyosin gels J. Mol. Biol. 246 1995 108 119
59. W. Zheng, and M. Li All-atom simulations of actin-myosin interactions - a comparative study of cardiac alpha myosin, beta myosin and skeletal muscle myosin Biophys. J. 104 2013 308a
60. B. Barua, M.C. Pamula, and S.E. Hitchcock-DeGregori Evolutionarily conserved surface residues constitute actin binding sites of tropomyosin Proc. Natl. Acad. Sci. USA 108 2011 10150 10155
61. B. Barua, and P.M. Fagnant S.E. Hitchcock-DeGregori A periodic pattern of evolutionarily conserved basic and acidic residues constitutes the binding interface of actin-tropomyosin J. Biol. Chem. 288 2013 9602 9609
62. J. Moraczewska, K. Nicholson-Flynn, and S.E. Hitchcock-DeGregori The ends of tropomyosin are major determinants of actin affinity and myosin subfragment 1-induced binding to F-actin in the open state Biochemistry 38 1999 15885 15892
63. S.K. Lakkaraju, and W. Hwang Modulation of elasticity in functionally distinct domains of the tropomyosin coiled-coil Cell. Mol. Bioeng. 2 2009 57 65