Myosin head configuration in relaxed insect flight muscle: X-ray modeled resting cross-bridges in a pre-powerstroke state are poised for actin binding

Biophysical Journal

Volumn 85, Issue 2, 2003, Pages 1063-1079

  Al Khayat, Hind A ^a   Hudson, Liam ^a   Reedy, Michael K ^b   Irving, Thomas C ^c   Squire, John M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE; MYOSIN; MYOSIN LIGHT CHAIN; NUCLEOTIDE;

ARTICLE; CALCULATION; FLIGHT MUSCLE; INSECT; MUSCLE CONTRACTION; MYOFILAMENT; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; X RAY DIFFRACTION;

HEXAPODA; INSECTA;

EID: 0042092511     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74545-7     Document Type: Article

References (75)

1. Brent, R. P. 1973. Algorithms for Minimisation without Derivatives. Prentice-Hall, Englewood Cliffs, NJ. Chapter 5.
2. Bullard, B., and K. Leonard. 1996. Modular proteins of insect muscle. Adv. Biophys. 33:211-221.
3. Cantino, M. E., L. D. Brown, M. Chew, P. K. Luther, and J. M. Squire. 2000. A-band architecture in vertebrate skeletal muscle: polarity of the myosin head array. J. Muscle Res. Cell Motil. 21:681-690.
4. 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.
5. Clayton, J. D., R. M. Cripps, J. C. Sparrow, and B. Bullard. 1998. Interaction of troponin-H and glutathione S-transferase-2 in the indirect flight muscles of Drosophila melanogaster. J. Muscle Res. Cell Motil. 19:117-127.
6. 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.
7. Eakins, F., H. A. AL-Khayat, R. W. Kensler, E. P. Morris, and J. M. Squire. 2002. 3D Structure of fish muscle myosin filaments. J. Struct. Biol. 137:154-163.
8. Ferguson, C., A. Lakey, A. Hutchings, G. W. Butcher, K. R. Leonard, and B. Bullard. 1994. Cytoskeletal proteins of insect muscle: location of zeelins in Lethocerus flight and leg muscle. J. Cell Sci. 107:1115-1129.
9. Freundlich, A., and J. M. Squire. 1983. Three-dimensional structure of the insect (Lethocerus) flight muscle M-band. J. Mol. Biol. 169:439-453.
10. Güth, K., and R. Wojciechowski. 1986. Perfusion cuvette for the simultaneous measurement of mechanical, optical and energetic parameters of skinned muscle fibres. Pflugers Arch. 407:552-557.
11. Harford, J., and J. M. Squire. 1997. Time-resolved diffraction studies of muscle using synchrotron radiation. Rep. Prog. Phys. 60:1723-1787.
12. Harford, J., and J. M. Squire. 1986. "Crystalline" myosin cross-bridge array in relaxed bony fish muscle. Low-angle x-ray diffraction from plaice fin muscle and its interpretation. Biophys. J. 50:145-155.
13. Harford, J. J., and J. M. Squire. 1992. Evidence for structurally different attached states of myosin cross-bridges on actin during contraction of fish muscle. Biophys. J. 63:387-396.
14. Haselgrove, J. C. 1975. X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle. J. Mol. Biol. 92:113-143.
15. Heinrich, B. 1993. The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation. Harvard University Press, Cambridge, MA.
16. Hibberd, M. G., and D. R. Trentham. 1986. Relationships between chemical and mechanical events during muscular contraction. Ann. Rev. Biophys. & Biophys. Chem. 15:119-161.
17. Holmes, K. C. 1996. Muscle proteins - their actions and interactions. Curr. Opin. Struct. Biol. 6:781-789.
18. Holmes, K. C. 1998. Picture story. A powerful stroke. Nat. Struct. Biol. 5:940-942.
19. Holmes, K. C., D. Popp, W. Gebhard, and W. Kabsch. 1990. Atomic model of the actin filament. Nature. 347:44-49.
20. Hopkins, S. C., C. Sabido-David, U. A. van der Heide, R. E. Ferguson, B. D. Brandmeier, R. E. Dale, J. Kendrick-Jones, J. E. Corrie, D. R. Trentham, M. Irving, and Y. E. Goldman. 2002. Orientation changes of the myosin light chain domain during filament sliding in active and rigor muscle. J. Mol. Biol. 318:1275-1291.
21. Houdusse, A., V. N. Kalabokis, D. Himmel, A. G. Szent-Gyorgyi, and C. Cohen. 1999. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: A novel conformation of the myosin head. Cell. 97:459-470.
22. Houdusse, A., and H. L. Sweeney. 2001. Myosin motors: missing structures and hidden springs. Curr. Opin. Struct. Biol. 11:182-194.
23. Houdusse, A., A. G. Szent-Gyorgyi, and C. Cohen. 2000. Three conformational states of scallop myosin SI. Proc. Natl. Acad. Sci. USA. 97:11238-11243.
24. Hudson, L. 1997. Ultrastructure of the A band unit cell in relaxed muscle. Ph.D. thesis. London University, London.
25. Hudson, L., J. J. Harford, R. C. Denny, and J. M. Squire. 1997. Myosin head configuration in relaxed fish muscle: resting state myosin heads must swing axially by up to 150 Å or turn upside down to reach rigor. J. Mol. Biol. 273:440-455.
26. Huxley, H. E. 1969. The mechanism of muscular contraction. Science. 164:1356-1366.
27. Huxley, H. E., and W. Brown. 1967. The low-angle x-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J. Mol. Biol. 30:383-434.
28. Irving, M., G. Piazzesi, L. Lucii, Y. B. Sun, J. J. Harford, I. M. Dobbie, M. A. Ferenczi, M. Reconditi, and V. Lombardi. 2000. Conformation of the myosin motor during force generation in skeletal muscle. Nat. Struct. Biol. 7:482-485.
29. Irving, T. C., R. Fischetti, G. Rosenbaum, and G. B. Bunker. 2000. Fibre diffraction using the BioCAT undulator beamline at the Advanced Photon Source. Nuclear Instruments and Methods. 448:250-254.
30. Irving, T. C., and D. W. Maughan. 2000. In vivo x-ray diffraction of indirect flight muscle from Drosophila melanogaster. Biophys. J. 78:2511-2515.
31. Josephson, R. K., J. G. Malamud, and D. R. Stokes. 2000. Asynchronous muscle: a primer. J. Exp. Biol. 203:2713-2722.
32. Kensler, R. W., and M. Stewart. 1989. An ultrastructural study of crossbridge arrangement in the fish skeletal muscle thick filament. J. Cell Sci. 94:391-401.
33. Levine, R. J. C. 1993. Evidence for overlapping myosin heads on relaxed thick filaments of fish, frog, and scallop striated muscles. J. Struct. Biol. 110:99-110.
34. Levine, R. J. C. 1997. Differences in myosin head arrangement on relaxed thick filaments from Lethocerus and rabbit muscles. J. Muscle Res. Cell Motil. 18:529-543.
35. Linari, M., G. Piazzesi, I. Dobbie, N. Koubassova, M. Reconditi, T. Narayanan, O. Diat, M. Irving, and V. Lombardi. 2000. Interference fine structure and sarcomere length dependence of the axial x-ray pattern from active single muscle fibers. Proc. Natl. Acad. Sci. USA. 97:7226-7231.
36. Luther, P. K., and J. M. Squire. 1980. Three-dimensional structure of the vertebrate muscle A-band. II. The myosin filament superlattice. J. Mol. Biol. 141:409-439.
37. Luther, P. K., J. M. Squire, and P. L. Forey. 1996. Evolution of myosin filament arrangements in vertebrate skeletal muscle. J. Morphol. 229:325-335.
38. Lymn, R. W., and E. W. Taylor. 1971. Mechanism of adenosine triphosphate hydrolysis of actomyosin. Biochemistry. 10:4617-4624.
39. Miller, A., and R. T. Tregear. 1972. The structure of insect fibrillar flight muscle in the presence and absence of ATP. J. Mol. Biol. 70:85-104.
40. Milligan, R. A., and P. F. Flicker. 1987. Structural relationships of actin, myosin, and tropomyosin revealed by cryo-electron microscopy. J. Cell Biol. 105:29-39
41. Moore, J. R., M. H. Dickinson, J. O. Vigoreaux, and D. W. Maughan. 2000. The effect of removing the N-terminal extension of the Drosophila myosin regulatory light chain upon flight ability and the contractile dynamics of the indirect flight muscle. Biophys. J. 78:1431-1440.
42. Morris, E. P., J. M. Squire, and G. W. Fuller. 1991. The 4-stranded helical arrangement of myosin heads on insect (Lethocerus) flight muscle thick filaments. J. Struct. Biol. 107:237-249.
43. Nelder, J. A., and R. Mead. 1965. The simplex method for function minimisation. Comput. J. 7:308-313.
44. Padron, R., L. Alamo, J. Murgich, and R. Craig. 1998. Towards an atomic model of the thick filaments of muscle. J. Mol. Biol. 275:35-41.
45. Piazzesi, G., M. Reconditi, I. Dobbie, M. Linari, P. Boesecke, O. Diat, M. Irving, and V. Lombardi. 1999. Changes in conformation of myosin heads during the development of isometric contraction and rapid shortening in single frog muscle fibres. J. Physiol. 514:305-312.
46. Press, W. H., S. Teukolsky, T. Vettering, and B. Flannery. 1992. Numerical Recipes in C, 2nd ed. Cambridge Univ. Press, Cambridge, UK.
47. Pringle, J. W. S. 1967. The contractile mechanism of insect fibrillar muscle. Prog. Biophys. Mol. Biol. 17:1-60.
48. Rayment, I., and H. M. Holden. 1993. Myosin subfragment-1: structure and function of a molecular motor. Curr. Opin. Struct. Biol. 3:944-952.
49. Rayment, I., H. M. Holden, M. Whittaker, C. B. Yohn, M. Lorenz, K. C. Holmes, and R. A. Milligan. 1993b. Structure of the actin-myosin complex and its implications for muscle contraction. Science. 261:58-65.
50. Rayment, I., W. R. Rypniewsky, K. Schmidt-Bäse, R. Smith, D. R. Tomchick, M. M. Benning, D. A. Winkelmann, G. Wesenbergand, and H. M. Holden. 1993a. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 261:50-58.
51. Reedy, M. C., B. Bullard, and J. O. Vigoreaux. 2000. Flightin is essential for thick filament assembly and sarcomere stability in Drosophila flight muscles. J. Cell Biol. 151:1483-1500.
52. Reedy, M. C., M. K. Reedy, and R. S. Goody. 1983. Co-ordinated electron microscopy and X-ray studies of glycerinated insect flight muscle. II. Electron microscopy and image reconstruction of muscle fibres fixed in rigor, in ATP and in AMPPNP. J. Muscle Res. Cell Motil. 4:55-81.
53. Reedy, M. C., M. K. Reedy, and R. S. Goody. 1987. The structure of insect flight muscle in the presence of AMPPNP. J. Muscle Res. Cell Motil. 8:473-503.
54. Reedy, M. C., M. K. Reedy, K. R. Leonard, and B. Bullard. 1994. Gold/Fab immuno electron microscopy localization of troponin H and troponin T in Lethocerus flight muscle. J. Mol. Biol. 239:52-67.
55. 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. 207:1276-1280.
56. Reedy, M. K., K. R. Leonard, R. Freeman, and T. Arad. 1981. Thick myofilament mass determination by electron scattering measurements with the scanning transmission electron microscope. J. Muscle Res. Cell Motil. 2:45-64.
57. Reedy, M. K., C. Lucaveche, N. Naber, and R. Cooke. 1992. Insect crossbridges, relaxed by spin-labeled nucleotide, show well-ordered 90 degrees state by X-ray diffraction and electron microscopy, but spectra of electron paramagnetic resonance probes report disorder. J. Mol. Biol. 227:678-697.
58. Reedy, M. K., C. Lucaveche, M. C. Reedy, and B. Somasundaram. 1993. Experiments on rigor crossbridge action and filament sliding in insect flight muscle. Adv. Exp. Med. Biol. 332:33-44; Discussion 44-46.
59. Reedy, M. K., J. M. Squire, B. A. J. Baumann, A. Stewart, and T. C. Irving. 2000. X-ray fibre diffraction of the indirect flight muscle of Lethocerus indicus. In Advanced Photon Source User Activity: Report 2000. Argonne National Laboratory, Argonne, IL.
60. Schlichting, I., and J. S. Wray. 1986. Behaviour of cross-bridges in non-overlap frog muscle in the presence and absence of ATP. J. Muscle Res. Cell Motil. 7:79-80.
61. Schmitz, H., C. Lucaveche, M. K. Reedy, and K. A. Taylor. 1994. Oblique section 3-D reconstruction of relaxed insect flight muscle reveals the cross-bridge lattice in helical registration. Biophys. J. 67:1620-1633.
62. Schmitz, H., M. C. Reedy, M. K. Reedy, R. T. Tregear, and K. A. Taylor. 1997. Tomographic three-dimensional reconstruction of insect flight muscle partially relaxed by AMPPNP and ethylene glycol. J. Cell Biol. 139:695-707.
63. Squire, J. M. 1998. Time-resolved X-ray diffraction. In Current Methods In Muscle Physiology. H. Sugi, editor. Oxford University Press, Oxford, UK. 241-285.
64. Squire, J. M. 2000. Fibre and muscle diffraction. In Structure and Dynamics of Biomolecules. E. Fanchon, E. Geissler, L.-L. Hodeau, J.-R. Regnard, and P. Timmins, editors. Oxford University Press, Oxford, UK. 272-301.
65. Squire, J. M., M. Cantino, M. Chew, R. Denny, J. Harford, L. Hudson, and P. Luther. 1998. Myosin rod-packing schemes in vertebrate muscle thick filaments. J. Struct. Biol. 122:128-138.
66. Squire, J. M., J. J. Harford, A. C. Edman, and M. Sjostrom. 1982. Fine structure of the A-band in cryo-sections. III. Cross-bridge distribution and the axial structure of the human C-zone. J. Mol. Biol. 155:467-494.
67. Steffen, W., D. Smith, R. Simmons, and J. Sleep. 2001. Mapping the actin filament with myosin. Proc. Natl. Acad. Sci. USA. 98:14949-14954.
68. Stewart, M., and R. W. Kensler. 1986. Arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle. J. Mol. Biol. 192:831-851.
69. 2+-activated contracting insect flight muscle. Cell. 99:421-431.
70. Tregear, R. T., and M. L. Clarke. 1984. On the possibility of interaction between neighbouring crossbridges. Adv. Exp. Med. Biol. 170:177-184.
71. Tregear, R. T., R. J. Edwards, T. C. Irving, K. J. V. Poole, M. C. Reedy, H. Schmitz, E. Towns-Andrews, and M. K. Reedy. 1998a. Cross-bridges attach to helically restricted actin target zones in stretch-activated insect flight muscle. Biophys. J. 74:A22.
72. Tregear, R. T., R. J. Edwards, T. C. Irving, K. J. V. Poole, M. C. Reedy, H. Schmitz, E. Towns-Andrews, and M. K. Reedy. 1998b. X-ray diffraction indicates that active cross-bridges bind to actin target zones in insect flight muscle. Biophys. J. 74:1439-1451.
73. Wendt, T., and K. Leonard. 1999. Structure of the insect troponin complex. J. Mol. Biol. 285:1845-1856.
74. Wendt, T. G., D. Taylor, K. M. Trybus, T. Messier, and K. A. Taylor. 2000. Electron crystallography reveals the "off" state of smooth muscle myosin. Biophys. J. 78:792A.
75. Xu, S., J. Gu, T. Rhodes, B. Belknap, G. Rosenbaum, G. Offer, H. White, and L. C. Yu. 1999. The M.ADP.P(i) state is required for helical order in the thick filaments of skeletal muscle. Biophys. J. 77:2665-2676.