Myosin Regulatory Domain Orientation in Skeletal Muscle Fibers: Application of Novel Electron Paramagnetic Resonance Spectral Decomposition and Molecular Modeling Methods

Biophysical Journal

Volumn 86, Issue 5, 2004, Pages 3030-3041

  Baumann, Bruce A J ^a,b   Liang, Hua ^a,b   Sale, Ken ^a,b,d   Hambly, Brett D ^c   Fajer, Piotr G ^a,b  

^a FLORIDA STATE UNIVERSITY   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF SYDNEY   (Australia)

^d SANDIA NATIONAL LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; MYOSIN;

ACCURACY; ACTIN FILAMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECOMPOSITION; ELECTRON SPIN RESONANCE; MAGNETIC FIELD; MOLECULAR MODEL; MONTE CARLO METHOD; MUSCLE FORCE; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; RABBIT; REGULATORY MECHANISM; SKELETAL MUSCLE; STOICHIOMETRY;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 2142702352     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74352-0     Document Type: Article

References (58)

1. Adhikari, B., J. Somerset, J. T. Stull, and P. G. Fajer. 1999. Dynamic modulation of the regulatory domain of myosin heads by pH, ionic strength, and RLC phosphorylation in synthetic myosin filaments. Biochemistry. 38:3127-3132.
2. Adhikari, B. B., and P. G. Fajer. 1996. Myosin head orientation and mobility during isometric contraction: effects of osmotic compression. Biophys. J. 70:1872-1880.
3. Allen, T. S., D. C. Sabido, N. Ling, M. Irving, and Y. E. Goldman. 1995. Transients of fluorescence polarization in skeletal muscle fibers labeled with rhodamine on the regulatory light chain. Biophys. J. 68:81S-86S.
4. Allen, T. S., N. Ling, M. Irving, and Y. E. Goldman. 1996. Orientation changes in myosin regulatory light chains following photorelease of ATP in skinned muscle fibers. Biophys. J. 70:1847-1862.
5. Arata, T. 1990. Orientation of spin-labeled light chain 2 of myosin heads in muscle fibers. J. Mol. Biol. 214:471-478.
6. Baker, J. E., I. Brust-Mascher, S. Ramachandran, L. E. LaConte, and D. D. Thomas. 1998. A large and distinct rotation of the myosin light chain domain occurs upon muscle contraction. Proc. Natl. Acad. Sci. USA. 95:2944-2949.
7. Baumann, B. A., B. D. Hambly, K. Hideg, and P. G. Fajer. 2001. The regulatory domain of the myosin head behaves as a rigid lever. Biochemistry. 40:7868-7873.
8. Bell, M. G., R. E. Dale, U. A. van der Heide, and Y. E. Goldman. 2002. Polarized fluorescence depletion reports orientation distribution and rotational dynamics of muscle cross-bridges. Biophys. J. 83:1050-1073.
9. Boey, W., W. Huang, B. Bennetts, J. Sparrow, C. G. dos Remedios, and B. D. Hambly. 1994. Fluorescence resonance energy transfer within the regulatory light chain of myosin. Eur. J. Biochem. 219:603-610.
10. Brown, L. J., N. Klonis, W. H. Sawyer, P. G. Fajer, and B. D. Hambly. 2001. Independent movement of the regulatory and catalytic domains of myosin heads revealed by phosphorescence anisotropy. Biochemistry. 40:8283-8291.
11. Burgess, S., M. Walker, F. Wang, J. R. Sellers, H. D. White, P. J. Knight, and J. Trinick. 2002. The pre-power stroke conformation of myosin V. J. Cell Biol. 159:983-991.
12. Chen, L. F., H. Winkler, M. K. Reedy, M. C. Reedy, and K. A. Taylor. 2002. Molecular modeling of averaged rigor crossbridges from tomograms of insect flight muscle. J. Struct. Biol. 138:92-104.
13. Chen, Y. H., J. T. Yang, and H. M. Martinez. 1972. Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion. Biochemistry. 11:4120-4131.
14. Corrie, J. E., B. D. Brandmeier, R. E. Ferguson, D. R. Trentham, J. Kendrick-Jones, S. C. Hopkins, U. A. van der Heide, Y. E. Goldman, C. Sabido-David, R. E. Dale, S. Criddle, and M. Irving. 1999. Dynamic measurement of myosin light-chain-domain tilt and twist in muscle contraction. Nature. 400:425-430.
15. Dominguez, R., Y. Freyzon, K. M. Trybus, and C. Cohen. 1998. 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. 94:559-571.
16. Eads, T. M., D. D. Thomas, and R. H. Austin. 1984. Microsecond rotational motions of eosin-labeled myosin measured by time-resolved anisotropy of absorption and phosphorescence. J. Mol. Biol. 179:55-81.
17. Fajer, P. G., E. A. Fajer, N. J. Brunsvold, and D. D. Thomas. 1988. Effects of AMPPNP on the orientation and rotational dynamics of spin-labeled muscle cross-bridges. Biophys. J. 53:513-524.
18. Fajer, P. G., E. A. Fajer, and D. D. Thomas. 1990. Myosin heads have a broad orientational distribution during isometric muscle contraction: time-resolved EPR studies using caged ATP. Proc. Natl. Acad. Sci. USA. 87:5538-5542.
19. Fajer, P. G. 1994a. Determination of spin-label orientation within the myosin head. Proc. Natl. Acad. Sci. USA. 91:937-941.
20. Fajer, P. G. 1994b. Method for the determination of myosin head orientation from EPR spectra. Biophys. J. 66:2039-2050.
21. Hambly, B. D., K. Franks, and R. Cooke. 1991. Orientation of spin-labeled light chain-2 exchanged onto myosin cross-bridge in glycerinated muscle fibers. Biophys. J. 59:127-138.
22. Hambly, B. D., F. Kathleen, and R. Cooke. 1992. Paramagnetic probes attached to a light chain on the myosin head are highly disordered in active muscle fibers. Biophys. J. 63:1306-1313.
23. Highsmith, S., and D. Eden. 1990. Ligand-induced myosin subfragment 1 global conformational change. Biochemistry. 29:4087-4093.
24. 2+ sensitivities of isometric tension, stiffness, and velocity of shortening in skinned skeletal muscle fibers. J. Gen. Physiol. 95:477-498.
25. Holmes, K. C., I. Angert, F. J. Kull, W. Jahn, and R. R. Schroder. 2003. Electron cryomicroscopy shows how strong binding of myosin to actin releases nucleotide. Nature. 425:423-427.
26. Hopkins, S. C., C. Sabido-David, J. E. Corrie, M. Irving, and Y. E. Goldman. 1998. Fluorescence polarization transients from rhodamine isomers on the myosin regulatory light chain in skeletal muscle fibers. Biophys. J. 74:3093-3110.
27. Houdusse, A., and C. Cohen. 1996. Structure of the regulatory domain of scallop myosin at 2Å resolution: implications for regulation. Structure. 4:21-32.
28. Hustedt, E. J., A. I. Smirnov, C. F. Laub, C. E. Cobb, and A. H. Beth. 1997. Molecular distances from dipolar coupled spin-labels: the global analysis of multifrequency continuous wave electron paramagnetic resonance data. Biophys. J. 72:1861-1877.
29. Huxley, A. F. 1974. Muscular contraction. J. Physiol. 243:1-43.
30. Huxley, H. E. 1969. The mechanism of muscular contraction. Science. 164:1356-1365.
31. Irving, M. 1993. Birefringence changes associated with isometric contraction and rapid shortening steps in frog skeletal muscle fibres. J. Physiol. 472:127-156.
32. Irving, M., T. S. Allen, C. Sabido-David, J. Craik, B. D. Brandmeier, J. Kendrick-Jones, J. E. Corrie, D. R. Trentham, and Y. E. Goldman. 1995. Tilting of the light-chain region of myosin during step length changes and active force generation in skeletal muscle. Nature. 375:688-691.
33. Jontes, J. D., E. M. Wilson-Kubalek, and R. A. Milligan. 1995. A 32° tail swing in brush border myosin I on ADP release. Nature. 378:751-753.
34. Ling, N., C. Shrimpton, J. Sleep, J. Kendrick-Jones, and M. Irving. 1996. Fluorescent probes of the orientation of myosin regulatory light chains in relaxed, rigor, and contracting muscle. Biophys. J. 70:1836-1846.
35. Metzger, J. M., and R. L. Moss. 1992. Myosin light chain 2 modulates calcium-sensitive cross-bridge transitions in vertebrate skeletal muscle. Biophys. J. 63:460-468.
36. Moss, R. L., G. G. Giulian, and M. L. Greaser. 1982. Physiological effects accompanying the removal of myosin LC2 from skinned skeletal muscle fibers. J. Biol. Chem. 257:8588-8591.
37. Offer, G., and P. Knight. 1996. The structure of the head-tail junction of the myosin molecule. J. Mol. Biol. 256:407-416.
38. Palm, T., K. Sale, L. Brown, H. Li, B. Hambly, and P. G. Fajer. 1999. Intradomain distances in the regulatory domain of the myosin head in prepower and postpower stroke states-fluorescence energy transfer. Biochemistry. 38:13026-13034.
39. Pollard, T. D., D. Bhandari, P. Maupin, D. Wachsstock, A. G. Weeds, and H. G. Zot. 1993. Direct visualization by electron microscopy of the weakly bound intermediates in the actomyosin adenosine triphosphatase cycle. Biophys. J. 64:454-471.
40. Potter, J. D. 1982. Preparation of troponin and its subunits. Methods Enzymol. 85B:241-263.
41. Rayment, I., H. M. Holden, M. Whittaker, C. B. Yohn, M. Lorenz, K. C. Holmes, and R. A. Milligan. 1993a. Structure of the actin-myosin complex and its implications for muscle contraction. Science. 261:58-65.
42. Rayment, I., W. R. Rypniewski, K. Schmidt-Base, R. Smith, D. R. Tomchick, M. M. Benning, D. A. Winkelmann, G. Wesenberg, and H. M. Holden. 1993b. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 261:50-65.
43. Reedy, M. K., K. C. Holmes, and R. T. Tregear. 1965. Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature. 207:1276-1279.
44. Sabido-David, C., B. D. Brandmeier, J. Craik, J. E. Corrie, D. R. Trentham, and M. Irving. 1998a. Steady-state fluorescence polarization studies of the orientation of myosin regulatory light chains in single skeletal muscle fibers using pure isomers of iodoacetamidotetramethylrhodamine. Biophys. J. 74:3083-3092.
45. Sabido-David, C., S. C. Hopkins, L. D. Saraswat, S. Lowey, Y. E. Goldman, and M. Irving. 1998b. Orientation changes of fluorescent probes at five sites on the myosin regulatory light chain during contraction of single skeletal muscle fibres. J. Mol. Biol. 279:387-402.
46. Sale, K., C. Sar, K. A. Sharp, K. Hideg, and P. G. Fajer. 2002. Structural determination of spin-label immobilization and orientation: a Monte Carlo minimization approach. J. Magn. Reson. 156:104-112.
47. Shih, W. M., Z. Gryczynski, J. R. Lakowicz, and J. A. Spudich. 2000. A FRET-based sensor reveals large ATP hydrolysis-induced conformational changes and three distinct states of the molecular motor myosin. Cell. 102:683-694.
48. Thomas, D. D., and R. Cooke. 1980. Orientation of spin-labeled myosin heads in glycerinated muscle fibers. Biophys. J. 32:891-906.
49. Tonomura, Y., P. Appel, and M. Morales. 1966. On the molecular weight of myosin II. Biochemistry. 5:515-521.
50. Toste, A. P., and R. Cooke. 1979. Interactions of contractile proteins with free and immobilized Cibracron Blue F3GA. Anal. Biochem. 95:317-328.
51. Volkmann, N., D. Hanein, G. Ouyang, K. M. Trybus, D. J. DeRosier, and S. Lowey. 2000. Evidence for cleft closure in actomyosin upon ADP release. Nat. Struct. Biol. 7:1147-1155.
52. Wagner, P. D. 1982. Preparation and fractionation of myosin light chains and exchange of the essential light chains. Methods Enzymol. 85:72-81.
53. Wray, J., P. Vibert, and C. Cohen. 1978. Actin filaments in muscle: pattern of myosin and tropomyosin/troponin attachments. J. Mol. Biol. 124:501-521.
54. Wray, J. S., and K. C. Holmes. 1981. X-ray diffraction studies of muscle. Annu. Rev. Physiol. 43:553-565.
55. Xiao, M., H. Li, G. E. Snyder, R. Cooke, R. G. Yount, and P. R. Selvin. 1998. Conformational changes between the active-site and regulatory light chain of myosin as determined by luminescence resonance energy transfer: the effect of nucleotides and actin. Proc. Nad. Acad. Sci. USA. 95:15309-15314.
56. Xiao, M., J. G. Reifenberger, A. L. Wells, C. Baldacchino, L. Q. Chen, P. Ge, H. L. Sweeney, and P. R. Selvin. 2003. An actin-dependent conformational change in myosin. Nat. Struct. Biol. 10:402-408.
57. Xu, J., and D. D. Root. 1998. Domain motion between the regulatory light chain and the nucleotide site in skeletal myosin. J. Struct. Biol. 123:150-161.
58. Zhao, L., J. Gollub, and R. Cooke. 1996. Orientation of paramagnetic probes attached to gizzard regulatory light chain bound to myosin heads in rabbit skeletal muscle. Biochemistry. 35:10158-10165.