Skip residues modulate the structural properties of the myosin rod and guide thick filament assembly

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

Volumn 112, Issue 29, 2015, Pages E3806-E3815

  Taylor, Keenan C ^a   Buvoli, Massimo ^b   Korkmaz, Elif Nihal ^a   Buvoli, Ada ^b   Zheng, Yuqing ^a   Heinze, Nathan T ^a   Cui, Qiang ^a   Leinwand, Leslie A ^b   Rayment, Ivan ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Cardiac skeleta myopathies; Coiled coils; Molecular dynamics; Myosin; Protein structure

Indexed keywords

AMINO ACID; MYOSIN; MYOSIN HEAVY CHAIN BETA; TROPOMYOSIN; CARDIAC MYOSIN; MUTANT PROTEIN; MYH7 PROTEIN, HUMAN; MYOSIN HEAVY CHAIN; MYOSIN SUBFRAGMENT;

ARTICLE; MOLECULAR DYNAMICS; MYOFILAMENT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; CHEMISTRY; GENE DELETION; HUMAN; METABOLISM; MOLECULAR GENETICS; PLIABILITY; PROTEIN SECONDARY STRUCTURE; SARCOMERE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; AMINO ACIDS; CARDIAC MYOSINS; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MYOSIN HEAVY CHAINS; MYOSIN SUBFRAGMENTS; PLIABILITY; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; REPETITIVE SEQUENCES, AMINO ACID; SARCOMERES; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84937460118     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505813112     Document Type: Article

References (56)

1. Craig R (1977) Structure of A-segments from frog and rabbit skeletal muscle. J Mol Biol 109(1):69-81.
2. Gautel M (2011) The sarcomeric cytoskeleton: Who picks up the strain? Curr Opin Cell Biol 23(1):39-46.
3. Craig R, Woodhead JL (2006) Structure and function of myosin filaments. Curr Opin Struct Biol 16(2):204-212.
4. Al-Khayat HA, Kensler RW, Squire JM, Marston SB, Morris EP (2013) Atomic model of the human cardiac muscle myosin filament. Proc Natl Acad Sci USA 110(1):318-323.
5. McLachlan AD, Karn J (1982) Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature 299(5880):226-231.
6. Sohn RL, et al. (1997) A 29 residue region of the sarcomeric myosin rod is necessary for filament formation. J Mol Biol 266(2):317-330.
7. Thompson RC, Buvoli M, Buvoli A, Leinwand LA (2012) Myosin filament assembly requires a cluster of four positive residues located in the rod domain. FEBS Lett 586(19):3008-3012.
8. Parry DA, Fraser RD, Squire JM (2008) Fifty years of coiled-coils and alpha-helical bundles: A close relationship between sequence and structure. JStructBiol163(3):258-269.
9. Offer G (1990) Skip residues correlate with bends in the myosin tail. J Mol Biol 216(2): 213-218.
10. Straussman R, Squire JM, Ben-Ya'acov A, Ravid S (2005) Skip residues and charge interactions in myosin II coiled-coils: Implications for molecular packing. J Mol Biol 353(3):613-628.
11. Atkinson SJ, Stewart M (1991) Expression in Escherichia coli of fragments of the coiled-coil rod domain of rabbit myosin: Influence of different regions of the molecule on aggregation and paracrystal formation. J Cell Sci 99(Pt 4):823-836.
12. Klenchin VA, Frye JJ, Jones MH, Winey M, Rayment I (2011) Structure-function analysis of the C-terminal domain of CNM67, a core component of the Saccharomyces cerevisiae spindle pole body. J Biol Chem 286(20):18240-18250.
13. Frye J, Klenchin VA, Rayment I (2010) Structure of the tropomyosin overlap complex from chicken smooth muscle: Insight into the diversity of N-terminal recognition. Biochemistry 49(23):4908-4920.
14. Nitanai Y, Minakata S, Maeda K, Oda N, Maéda Y (2007) Crystal structures of tropomyosin: Flexible coiled-coil. Adv Exp Med Biol 592:137-151.
15. Deiss S, et al. (2014) Your personalized protein structure: Andrei N. Lupas fused to GCN4 adaptors. J Struct Biol 186(3):380-385.
16. Crick FHC (1953) The Fourier transform of a coiled-coil. Acta Crystallogr 6:685-689.
17. Grigoryan G, Degrado WF (2011) Probing designability via a generalized model of helical bundle geometry. J Mol Biol 405(4):1079-1100.
18. O'Shea EK, Klemm JD, Kim PS, Alber T (1991) X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science 254(5031):539-544.
19. Gromiha MM, Parry DA (2004) Characteristic features of amino acid residues in coiledcoil protein structures. Biophys Chem 111(2):95-103.
20. Buvoli M, Buvoli A, Leinwand LA (2012) Effects of pathogenic proline mutations on myosin assembly. J Mol Biol 415(5):807-818.
21. Al-Khayat HA, Kensler RW, Morris EP, Squire JM (2010) Three-dimensional structure of the M-region (bare zone) of vertebrate striated muscle myosin filaments by singleparticle analysis. J Mol Biol 403(5):763-776.
22. White GE, Erickson HP (2006) Sequence divergence of coiled coils - Structural rods, myosin filament packing, and the extraordinary conservation of cohesins. J Struct Biol 154(2):111-121.
23. Chew MW, Squire JM (1995) Packing of alpha-helical coiled-coil myosin rods in vertebrate muscle thick filaments. J Struct Biol 115(3):233-249.
24. Brown JH, et al. (2001) Deciphering the design of the tropomyosin molecule. Proc Natl Acad Sci USA 98(15):8496-8501.
25. Brown JH (2010) How sequence directs bending in tropomyosin and other two-stranded alpha-helical coiled coils. Protein Sci 19(7):1366-1375.
26. Li XE, Holmes KC, Lehman W, Jung H, Fischer S (2010) The shape and flexibility of tropomyosin coiled coils: Implications for actin filament assembly and regulation. J Mol Biol 395(2):327-339.
27. Zheng W, Barua B, Hitchcock-DeGregori SE (2013) Probing the flexibility of tropomyosin and its binding to filamentous actin using molecular dynamics simulations. Biophys J 105(8):1882-1892.
28. Chernyatina AA, Guzenko D, Strelkov SV (2015) Intermediate filament structure: The bottom-up approach. Curr Opin Cell Biol 32:65-72.
29. Strelkov SV, Burkhard P (2002) Analysis of alpha-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation. J Struct Biol 137(1-2):54-64.
30. McLachlan AD (1983) Analysis of gene duplication repeats in the myosin rod. J Mol Biol 169(1):15-30.
31. Houmeida A, Holt J, Tskhovrebova L, Trinick J (1995) Studies of the interaction between titin and myosin. J Cell Biol 131(6 Pt 1):1471-1481.
32. McLachlan AD, Karn J (1983) Periodic features in the amino acid sequence of nematode myosin rod. J Mol Biol 164(4):605-626.
33. Ricketson D, Johnston CA, Prehoda KE (2010) Multiple tail domain interactions stabilize nonmuscle myosin II bipolar filaments. Proc Natl Acad Sci USA 107(49): 20964-20969.
34. Luther PK, Munro PM, Squire JM (1981) Three-dimensional structure of the vertebrate muscle A-band. III. M-region structure and myosin filament symmetry. J Mol Biol 151(4):703-730.
35. Squire JM (1973) General model of myosin filament structure. 3. Molecular packing arrangements in myosin filaments. J Mol Biol 77(2):291-323.
36. Postma AV, et al. (2011) Mutations in the sarcomere gene MYH7 in Ebstein anomaly. Circ Cardiovasc Genet 4(1):43-50.
37. Cullup T, et al. (2012) Mutations in MYH7 cause Multi-minicore Disease (MmD) with variable cardiac involvement. Neuromuscul Disord 22(12):1096-1104.
38. Tasca G, et al. (2012) New phenotype and pathology features in MYH7-related distal myopathy. Neuromuscul Disord 22(7):640-647.
39. Imai Y, Matsushima Y, Sugimura T, Terada M (1991) A simple and rapid method for generating a deletion by PCR. Nucleic Acids Res 19(10):2785.
40. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 229(1):105-124.
41. Rayment I (1997) Reductive alkylation of lysine residues to alter crystallization properties of proteins. Methods Enzymol 276:171-179.
42. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276(Pt A):307-326.
43. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Cryst 40(Pt 4):658-674.
44. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macro-molecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
45. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
46. Li DW, Brüschweiler R (2010) NMR-based protein potentials. Angew Chem Int Ed Engl 49(38):6778-6780.
47. Beauchamp KA, Lin YS, Das R, Pande VS (2012) Are protein force fields getting better? A systematic benchmark on 524 diverse NMR measurements. J Chem Theory Comput 8(4):1409-1414.
48. Case DA, et al. (2012) AMBER 12 (Univ of California, San Francisco, CA). Available at ambermd.org/doc12/Amber12.pdf. Accessed June 26, 2015.
49. Götz AW, et al. (2012) Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized Born. J Chem Theory Comput 8(5):1542-1555.
50. Lee MS, Salsbury FR, Brooks CL (2002) Novel generalized Born methods. J Chem Phys 116(24):10606-10614.
51. Mongan J, Simmerling C, McCammon JA, Case DA, Onufriev A (2007) Generalized Born model with a simple, robust molecular volume correction. J Chem Theory Comput 3(1):156-169.
52. Ryckaert JP, Ciccotti G, Berendsen HJC (1977) Numerical-integration of Cartesian equations of motion of a system with constraints: Molecular-dynamics of N-alkanes. J Comput Phys 23(3):327-341.
53. rd (2008) Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J Phys Chem B 112(30):9020-9041.
54. Andrea TA, Swope WC, Andersen HC (1983) The role of long ranged forces in determining the structure and properties of liquid water. J Chem Phys 79(9):4576-4584.
55. Maass AH, Buvoli M (2007) Cardiomyocyte preparation, culture, and gene transfer. Methods Mol Biol 366:321-330.
56. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671-675.