An Unstable Head-Rod Junction May Promote Folding into the Compact Off-State Conformation of Regulated Myosins

Journal of Molecular Biology

Volumn 375, Issue 5, 2008, Pages 1434-1443

  Brown, Jerry H ^a   Yang, Yuting ^a   Reshetnikova, Ludmilla ^a   Gourinath, S ^a,b   Süveges, Dániel ^c   Kardos, József ^c   Hóbor, Fruzsina ^c   Reutzel, Robbie ^a   Nyitray, László ^c   Cohen, Carolyn ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b JAWAHARLAL NEHRU UNIVERSITY   (India)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

myosin subfragment 2; off state; thermal stability; X ray diffraction; helical coiled coil

Indexed keywords

MYOSIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; THERMOSTABILITY; THIN FILAMENT; X RAY DIFFRACTION;

EID: 37549054688     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.11.071     Document Type: Article

References (50)

1. Huxley H.E. The mechanism of muscular contraction. Science 164 (1969) 1356-1365
2. Yang Y., Gourinath S., Kovács 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
3. Woodhead J.L., Zhao F.Q., Craig R., Egelman E.H., Alamo L., and Padron R. Atomic model of a myosin filament in the relaxed state. Nature 436 (2005) 1195-1199
4. Rayment I., Rypniewski W.R., Schmidt-Bäse 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
5. Houdusse A., Kalabokis V.N., Himmel D., Szent-Györgyi 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
6. Geeves M.A., and Holmes K.C. The molecular mechanism of muscle contraction. Adv. Protein Chem. 71 (2005) 161-193
7. Brown J.H., and Cohen C. Regulation of muscle contraction by tropomyosin and troponin: how structure illuminates function. In: Squire J.M., and Parry D.A. (Eds). Fibrous Proteins and Related Structures vol. 71 (2005), Elsevier/Academic Press, San Diego, CA
8. Sellers J.R. Regulation of cytoplasmic and smooth muscle myosin. Curr. Opin. Cell Biol. 3 (1991) 98-104
9. Szent-Gyorgyi A.G. Regulation of contraction by calcium binding myosins. Biophys. Chem. 59 (1996) 357-363
10. Adelstein R.S., and Eisenberg E. Regulation and kinetics of the actin-myosin-ATP interaction. Annu. Rev. Biochem. 49 (1980) 921-956
11. Lauzon A.M., Tyska M.J., Rovner A.S., Freyzon Y., Warshaw D.M., and Trybus K.M. Coiled-coil unwinding at the smooth muscle myosin head-rod junction is required for optimal mechanical performance. Biophys. J. 80 (2001) 1900-1904
12. 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
13. Stafford W.F., Jacobsen M.P., Woodhead J., Craig R., O'Neall-Hennessey E., and Szent-Gyorgyi A.G. Calcium-dependent structural changes in scallop heavy meromyosin. J. Mol. Biol. 307 (2001) 137-147
14. Burgess S., Yu R., Walker M.L., Trinick J., Chalovich J.M., and Knight P.J. Structure of smooth muscle myosin in the switched-off state. Biophys. J. 82 (2002) 356a
15. Houdusse A., and Cohen C. Structure of the regulatory domain of scallop myosin at 2 Å resolution: implications for regulation. Structure 4 (1996) 21-32
16. Houdusse A., Szent-Györgyi A.G., and Cohen C. Three conformational states of scallop S1. Proc. Natl Acad. Sci. USA 97 (2000) 11238-11243
17. Himmel D.M., Gourinath S., Reshetnikova L., Shen Y., Szent-Györgyi A.G., and Cohen C. Crystallographic findings on the internally-uncoupled and near-rigor states of myosin: further insights into the mechanics of the motor. Proc. Natl Acad. Sci. USA 99 (2002) 12645-12650
18. Gourinath S., Himmel D.M., Brown J.H., Reshetnikova L., Szent-Györgyi A.G., and Cohen C. Crystal structure of scallop myosin S1 in the pre-power stroke state to 2.6 Å resolution: flexibility and function in the head. Structure 11 (2003) 1621-1627
19. Risal D., Gourinath S., Himmel D.M., Szent-Györgyi A.G., and Cohen C. Myosin S1 structures reveal a novel nucleotide conformation and a complex salt bridge that helps couple nucleotide and actin binding. Proc. Natl Acad. Sci. USA 101 (2004) 8930-8935
20. 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
21. Blankenfeldt W., Thoma N.H., Wray J.S., Gautel M., and Schlichting I. Crystal structures of human cardiac β-myosin II S2-Δ provide insight into the functional role of the S2 subfragment. Proc. Natl Acad. Sci. USA 103 (2006) 17713-17717
22. 2+ to a canonical EF-hand of a conventional myosin. J. Biol. Chem. 280 (2005) 41458-41464
23. Aurora R., and Rose G.D. Helix capping. Protein Sci. 7 (1998) 21-38
24. Richardson J.S., and Richardson D.C. Amino acid preferences for specific locations at the ends of alpha helices. Science 240 (1988) 1648-1652
25. Chakrabarty T., Yengo C., Baldacchino C., Chen L.Q., Sweeney H.L., and Selvin P.R. Does the S2 rod of myosin II uncoil upon two-headed binding to actin? A leucine-zippered HMM study. Biochemistry 42 (2003) 12886-12892
26. Offer G., and Knight P. The structure of the head-tail junction of the myosin molecule. J. Mol. Biol. 256 (1996) 407-416
27. Strelkov S.V., and Burkhard P. Analysis of alpha-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation. J. Struct. Biol. 137 (2002) 54-64
28. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Crystallogr., Sect. A 32 (1976) 922-923
29. Collaborative Computational Project, Number 4. The CCP4 Suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
30. Málnási-Csizmadia A., Shimony E., Hegyi G., Szent-Györgyi A.G., and Nyitray L. Dimerization of the head-rod junction of scallop myosin. Biochem. Biophys. Res. Commun. 252 (1998) 595-601
31. Trybus K.M., Freyzon Y., Faust L.Z., and Sweeney H.L. Spare the rod, spoil the regulation: necessity for a myosin rod. Proc. Natl Acad. Sci. USA 94 (1997) 48-52
32. Meier M., Lustig A., Aebi U., and Burkhard P. Removing an interhelical salt bridge abolishes coiled-coil formation in a de novo designed peptide. J. Struct. Biol. 137 (2002) 65-72
33. Burkhard P., Ivaninskii S., and Lustig A. Improving coiled-coil stability by optimizing ionic interactions. J. Mol. Biol. 318 (2002) 901-910
34. Musafia B., Buchner V., and Arad D. Complex salt bridges in proteins: statistical analysis of structure and function. J. Mol. Biol. 254 (1995) 761-770
35. 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
36. 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
37. Jung H., Burgess S.A., Colegrave M., Patel H., Chantler P.D., Chalovich J.M., et al. Comparative Studies of the Folded Structures of Scallop Striated and Vertebrate Smooth Muscle Myosins. (2004) Biophysical Society 48th Annual Meeting, Baltimore
38. Tama F., Feig M., Liu J., Brooks III C.L., and Taylor K.A. The requirement for mechanical coupling between head and S2 domains in smooth muscle myosin ATPase regulation and its implications for dimeric motor function. J. Mol. Biol. 345 (2005) 837-854
39. Jung H., and Craig R. Head-head interaction is a common structural motif in regulated myosin II molecules. Biophys. J. 92 (2007) 491a
40. Kovács M., Toth J., Hetenyi C., Málnási-Csizmadia A., and Sellers J.R. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279 (2004) 35557-35563
41. Allingham J.S., Smith R., and Rayment I. The structural basis of blebbistatin inhibition and specificity for myosin II. Nat. Struct. Mol. Biol. 12 (2005) 378-379
42. Kovács M., Thirumurugan K., Knight P.J., and Sellers J.R. Load-dependent mechanism of nonmuscle myosin 2. Proc. Natl Acad. Sci. USA 104 (2007) 9994-9999
43. Goldstein R.A. Amino-acid interactions in psychrophiles, mesophiles, thermophiles, and hyperthermophiles: insights from the quasi-chemical approximation. Protein Sci. 16 (2007) 1887-1895
44. Odronitz F., and Kollmar M. Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol. 8 (2007) R196
45. Otwinowski Z., and Minor W. Processing of x-ray diffraction data collected in oscillation mode. Methods in Enzymology vol. 276 (1997), Academic Press, New York 307-326
46. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., and Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 61 (2005) 458-464
47. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
48. Jones T.A., Zou J.-Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr., Sect. A: Found. Crystallogr. 47 (1991) 110-119
49. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallogr., Sect. A: Found. Crystallogr. 50 (1994) 157-163
50. Hodi Z., Nemeth A.L., Radnai L., Hetenyi C., Schlett K., Bodor A., et al. Alternatively spliced exon B of myosin Va is essential for binding the tail-associated light chain shared by dynein. Biochemistry 45 (2006) 12582-12595