Three-Dimensional Reconstruction of Tarantula Myosin Filaments Suggests How Phosphorylation May Regulate Myosin Activity

Journal of Molecular Biology

Volumn 384, Issue 4, 2008, Pages 780-797

  Alamo, Lorenzo ^a   Wriggers, Willy ^b   Pinto, Antonio ^a   Bártoli, Fulvia ^a   Salazar, Leiria ^a   Zhao, Fa Qing ^c   Craig, Roger ^c   Padrón, Raúl ^a  

^a INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

cryo EM; myosin regulation; myosin regulatory light chain; phosphorylation; thick filament

Indexed keywords

ACTIN; MYOSIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARACHNID; ARTICLE; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; MUSCLE CONTRACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; VERTEBRATE;

TARANTULA; VERTEBRATA;

EID: 56249115186     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.10.013     Document Type: Article

References (88)

1. Craig R., and Padrón R. Molecular structure of the sarcomere. In: Engel A.G., and Franzini-Armstrong C. (Eds). Myology (2004), McGraw-Hill, New York, NY 129-166
2. Lehman W., and Szent-Gyorgyi A.G. Regulation of muscular contraction. Distribution of actin control and myosin control in the animal kingdom. J. Gen. Physiol. 66 (1975) 1-30
3. Vibert P., Craig R., and Lehman W. Steric-model for activation of muscle thin filaments. J. Mol. Biol. 266 (1997) 8-14
4. Poole K.J., Lorenz M., Evans G., Rosenbaum G., Pirani A., Craig R., et al. 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
5. Szent-Gyorgyi A.G. Regulation by myosin: how calcium regulates some myosins, past and present. Adv. Exp. Med. Biol. 592 (2007) 253-264
6. Sweeney H.L., Bowman B.F., and Stull J.T. Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function. Am. J. Physiol. 264 (1993) C1085-C1095
7. Sellers J.R. Phosphorylation-dependent regulation of Limulus myosin. J. Biol. Chem. 256 (1981) 9274-9278
8. Craig R., Padrón R., and Kendrick-Jones J. Structural changes accompanying phosphorylation of tarantula muscle myosin filaments. J. Cell Biol. 105 (1987) 1319-1327
9. 2+ regulation. Proc. Natl Acad. Sci. USA 74 (1977) 129-133
10. Rayment I., Rypniewski W.R., Schmidt-Base K., Smith R., Tomchick D.R., Benning M.M., et al. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261 (1993) 50-58
11. Sweeney H.L., and Houdusse A. Mammalian muscle myosin. In: Engel A.G., and Franzini-Armstrong C. (Eds). Myology (2004), McGraw-Hill, New York, NY 167-186
12. Kwon H., Goodwin E.B., Nyitray L., Berliner E., O'Neall-Hennessey E., Melandri F.D., and Szent-Gyorgyi A.G. Isolation of the regulatory domain of scallop myosin: role of the essential light chain in calcium binding. Proc. Natl Acad. Sci. USA 87 (1990) 4771-4775
13. Nelson W.D., Blakely S.E., Nesmelov Y.E., and Thomas D.D. Site-directed spin labeling reveals a conformational switch in the phosphorylation domain of smooth muscle myosin. Proc. Natl Acad. Sci. USA 102 (2005) 4000-4005
14. Wendt T., Taylor D., Messier T., Trybus K.M., and Taylor K.A. Visualization of head-head interactions in the inhibited state of smooth muscle myosin. J. Cell Biol. 147 (1999) 1385-1390
15. Wendt T., Taylor D., Trybus K.M., and Taylor K. Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2. Proc. Natl Acad. Sci. USA 98 (2001) 4361-4366
16. Liu J., Wendt T., Taylor D., and Taylor K. Refined model of the 10S conformation of smooth muscle myosin by cryo-electron microscopy 3D image reconstruction. J. Mol. Biol. 329 (2003) 963-972
17. Burgess S.A., Yu S., Walker M.L., Hawkins R.J., Chalovich J.M., and Knight P.J. Structures of smooth muscle myosin and heavy meromyosin in the folded, shutdown state. J. Mol. Biol. 372 (2007) 1165-1178
18. Woodhead J.L., Zhao F.Q., Craig R., Egelman E.H., Alamo L., and Padrón R. Atomic model of a myosin filament in the relaxed state. Nature 436 (2005) 1195-1199
19. Jung H.S., Burgess S.A., Billington N., Colegrave M., Patel H., Chalovich J.M., et al. Conservation of the regulated structure of folded myosin 2 in species separated by at least 600 million years of independent evolution. Proc. Natl Acad. Sci. USA 105 (2008) 6022-6026
20. Jung H.S., Komatsu S., Ikebe M., and Craig R. Head-head and head-tail interaction: a general mechanism for switching off myosin II activity in cells. Mol. Biol. Cell 19 (2008) 3234-3242
21. Zoghbi M.E., Woodhead J.L., Moss R.L., and Craig R. Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc. Natl Acad. Sci. USA 105 (2008) 2386-2390
22. Zhao F.Q., Woodhead J.L., and Craig R. Head-head interaction characterizes the relaxed state of scallop and Limulus muscle myosin filaments. Biophys. J. 94 (2008) 630
23. Craig R., and Woodhead J.L. Structure and function of myosin filaments. Curr. Opin. Struct. Biol. 16 (2006) 204-212
24. Sellers J.R., and Knight P.J. Folding and regulation in myosins II and V. J. Muscle Res. Cell Motil. 28 (2008) 363-370
25. Levine R.J., Chantler P.D., Kensler R.W., and Woodhead J.L. Effects of phosphorylation by myosin light chain kinase on the structure of Limulus thick filaments. J. Cell Biol. 113 (1991) 563-572
26. Levine R.J., Kensler R.W., Yang Z., Stull J.T., and Sweeney H.L. Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments. Biophys. J. 71 (1996) 898-907
27. Espinoza-Fonseca L.M., Kast D., and Thomas D.D. Molecular dynamics simulations reveal a disorder-to-order transition on phosphorylation of smooth muscle myosin. Biophys. J. 93 (2007) 2083-2090
28. Ikebe M., and Morita J. Identification of the sequence of the regulatory light chain required for the phosphorylation-dependent regulation of actomyosin. J. Biol. Chem. 266 (1991) 21339-21342
29. Egelman E.H. A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85 (2000) 225-234
30. Burgess S., Walker M., Knight P.J., Sparrow J., Schmitz S., Offer G., et al. Structural studies of arthrin: monoubiquitinated actin. J. Mol. Biol. 341 (2004) 1161-1173
31. Pomfret A.J., Rice W.J., and Stokes D.L. Application of the iterative helical real-space reconstruction method to large membranous tubular crystals of P-type ATPases. J. Struct. Biol. 157 (2007) 106-116
32. Maita T., Chen J.I., and Matsuda G. Amino-acid sequence of the 20 000-molecular-weight light chain of chicken gizzard-muscle myosin. Eur. J. Biochem. 117 (1981) 417-424
33. Rost B., Yachdav G., and Liu J. The PredictProtein server. Nucleic Acids Res. 32 (2004) W321-W326
34. Cuff J.A., Clamp M.E., Siddiqui A.S., Finlay M., and Barton G.J. JPred: a consensus secondary structure prediction server. Bioinformatics 14 (1998) 892-893
35. McGuffin L.J., Bryson K., and Jones D.T. The PSIPRED protein structure prediction server. Bioinformatics 16 (2000) 404-405
36. Combet C., Blanchet C., Geourjon C., and Deleage G. NPS@: network protein sequence analysis. Trends Biochem. Sci. 25 (2000) 147-150
37. Karplus K., Karchin R., Barrett C., Tu S., Cline M., Diekhans M., et al. What is the value added by human intervention in protein structure prediction?. Proteins 45(S5) (2001) 86-91
38. Geourjon C., and Deleage G. SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput. Appl. Biosci. 11 (1995) 681-684
39. Cheng J., Randall A.Z., Sweredoski M.J., and Baldi P. SCRATCH: a protein structure and structural feature prediction server. Nucleic Acids Res. 33 (2005) W72-W76
40. Bystroff C., Thorsson V., and Baker D. HMMSTR: a hidden Markov model for local sequence-structure correlations in proteins. J. Mol. Biol. 301 (2000) 173-190
41. Kneller D.G., Cohen F.E., and Langridge R. Improvements in protein secondary structure prediction by an enhanced neural network. J. Mol. Biol. 214 (1990) 171-182
42. Kelley L.A., MacCallum R.M., and Sternberg M.J. Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299 (2000) 499-520
43. Bennett-Lovsey R.M., Herbert A.D., Sternberg M.J., and Kelley L.A. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70 (2008) 611-625
44. Kemp B.E., and Pearson R.B. Protein kinase recognition sequence motifs. Trends Biochem. Sci. 15 (1990) 342-346
45. Blankenfeldt W., Thoma N.H., Wray J.S., Gautel M., and Schlichting I. Crystal structures of human cardiac beta-myosin II S2-Delta provide insight into the functional role of the S2 subfragment. Proc. Natl Acad. Sci. USA 103 (2006) 17713-17717
46. Hidalgo C., Craig R., Ikebe M., and Padrón R. Mechanism of phosphorylation of the regulatory light chain of myosin from tarantula striated muscle. J. Muscle Res. Cell Motil. 22 (2001) 51-59
47. Wriggers W., and Chacon P. Modeling tricks and fitting techniques for multiresolution structures. Structure 9 (2001) 779-788
48. Dominguez R., Freyzon Y., Trybus K.M., and Cohen C. Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state. Cell 94 (1998) 559-571
49. Houdusse A., Szent-Gyorgyi A.G., and Cohen C. Three conformational states of scallop myosin S1. Proc. Natl Acad. Sci. USA 97 (2000) 11238-11243
50. Yang Y., Gourinath S., Kovacs M., Nyitray L., Reutzel R., Himmel D.M., et al. Rigor-like structures from muscle myosins reveal key mechanical elements in the transduction pathways of this allosteric motor. Structure 15 (2007) 553-564
51. Houdusse A., Kalabokis V.N., Himmel D., Szent-Gyorgyi A.G., and Cohen C. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97 (1999) 459-470
52. Crowther R.A., Padrón R., and Craig R. Arrangement of the heads of myosin in relaxed thick filaments from tarantula muscle. J. Mol. Biol. 184 (1985) 429-439
53. Li Y., Brown J.H., Reshetnikova L., Blazsek A., Farkas L., Nyitray L., and Cohen C. Visualization of an unstable coiled coil from the scallop myosin rod. Nature 424 (2003) 341-345
54. Brown J.H., Yang Y., Reshetnikova L., Gourinath S., Suveges D., Kardos J., et al. An unstable head-rod junction may promote folding into the compact off-state conformation of regulated myosins. J. Mol. Biol. 375 (2008) 1434-1443
55. Zoghbi M.E., Woodhead J.L., Craig R., and Padrón R. Helical order in tarantula thick filaments requires the "closed" conformation of the myosin head. J. Mol. Biol. 342 (2004) 1223-1236
56. Xu S., Offer G., Gu J., White H.D., and Yu L.C. Temperature and ligand dependence of conformation and helical order in myosin filaments. Biochemistry 42 (2003) 390-401
57. Xu S., Gu J., White H., Offer G., and Yu L. Structural effects on myosin of three ATPase inhibitors. Biophys. J. 88 (2005) 124a
58. Xu S., White H.D., Offer G.W., and Yu L.C. Stabilisation of the helical order of myosin filaments by blebbistatin. Biophys. J. 94 (2008) 624
59. Zhao F.Q., Padrón R., and Craig R. Blebbistatin stabilizes the helical order of myosin filaments by promoting the switch 2 closed state. Biophys. J. 95 (2008) 3322-3329
60. Sweeney H.L., Yang Z., Zhi G., Stull J.T., and Trybus K.M. Charge replacement near the phosphorylatable serine of the myosin regulatory light chain mimics aspects of phosphorylation. Proc. Natl Acad. Sci. USA 91 (1994) 1490-1494
61. Zhi G., Ryder J.W., Huang J., Ding P., Chen Y., Zhao Y., et al. Myosin light chain kinase and myosin phosphorylation effect frequency-dependent potentiation of skeletal muscle contraction. Proc. Natl Acad. Sci. USA 102 (2005) 17519-17524
62. Geisterfer-Lowrance A.A., Kass S., Tanigawa G., Vosberg H.P., McKenna W., Seidman C.E., and Seidman J.G. A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation. Cell 62 (1990) 999-1006
63. Huxley H.E., and Brown W. The low-angle x-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J. Mol. Biol. 30 (1967) 383-434
64. McLachlan A.D., and Karn J. Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature 299 (1982) 226-231
65. Decker B., and Kellermayer M.S. Periodically arranged interactions within the myosin filament backbone revealed by mechanical unzipping. J. Mol. Biol. 377 (2008) 307-310
66. Ikebe M. Regulation of the function of mammalian myosin and its conformational change. Biochem. Biophys. Res. Commun. 369 (2008) 157-164
67. Metzger J.M., Greaser M.L., and Moss R.L. Variations in cross-bridge attachment rate and tension with phosphorylation of myosin in mammalian skinned skeletal muscle fibers. Implications for twitch potentiation in intact muscle. J. Gen. Physiol. 93 (1989) 855-883
68. Barany K., Barany M., Gillis J.M., and Kushmerick M.J. Phosphorylation-dephosphorylation of the 18,000-dalton light chain of myosin during the contraction-relaxation cycle of frog muscle. J. Biol. Chem. 254 (1979) 3617-3623
69. Kemp B.E., and Stull J.T. Myosin light chain kinases. In: Kemp B.E. (Ed). Peptides and Protein Phosphorylation (1990), CRC, Boca Raton, FL 115-133
70. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
71. Egelman E.H. The iterative helical real space reconstruction method: surmounting the problems posed by real polymers. J. Struct. Biol. 157 (2007) 83-94
72. Egelman E.H. Single-particle reconstruction from EM images of helical filaments. Curr. Opin. Struct. Biol. 17 (2007) 556-561
73. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199
74. Padrón R., Alamo L., Guerrero J.R., Granados M., Uman P., and Craig R. Three-dimensional reconstruction of thick filaments from rapidly frozen, freeze-substituted tarantula muscle. J. Struct. Biol. 115 (1995) 250-257
75. Padrón R., Alamo L., Murgich J., and Craig R. Towards an atomic model of the thick filaments of muscle. J. Mol. Biol. 275 (1998) 35-41
76. Offer G., Knight P.J., Burgess S.A., Alamo L., and Padrón R. A new model for the surface arrangement of myosin molecules in tarantula thick filaments. J. Mol. Biol. 298 (2000) 239-260
77. Gulick A.M., Bauer C.B., Thoden J.B., and Rayment I. X-ray structures of the MgADP, MgATPgammaS, and MgAMPPNP complexes of the Dictyostelium discoideum myosin motor domain. Biochemistry 36 (1997) 11619-11628
78. 4-. Biochemistry 34 (1995) 8960-8972
79. Bauer C.B., Holden H.M., Thoden J.B., Smith R., and Rayment I. X-ray structures of the apo and MgATP-bound states of Dictyostelium discoideum myosin motor domain. J. Biol. Chem. 275 (2000) 38494-38499
80. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
81. Chacon P., and Wriggers W. Multi-resolution contour-based fitting of macromolecular structures. J. Mol. Biol. 317 (2002) 375-384
82. Wriggers W., Chacon P., Kovacs J., Tama T., and Birmanns S. Topology representing neural networks reconcile biomolecular shape, structure, and dynamics. Neurocomputing 56 (2004) 365-379
83. Darst S.A., Opalka N., Chacon P., Polyakov A., Richter C., Zhang G., and Wriggers W. Conformational flexibility of bacterial RNA polymerase. Proc. Natl Acad. Sci. USA 99 (2002) 4296-4301
84. Opalka N., Chlenov M., Chacon P., Rice W.J., Wriggers W., and Darst S.A. Structure and function of the transcription elongation factor GreB bound to bacterial RNA polymerase. Cell 114 (2003) 335-345
85. Zhang L., and Hermans J. Hydrophilicity of cavities in proteins. Proteins 24 (1996) 433-438
86. Gerstein M., and Krebs W. A database of macromolecular motions. Nucleic Acids Res. 26 (1998) 4280-4290
87. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graphics 14 (1996) 33-38
88. Baker N.A., Sept D., Joseph S., Holst M.J., and McCammon J.A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98 (2001) 10037-10041