Three-dimensional structure of nucleotide-bearing crossbridges in situ: Oblique section reconstruction of insect flight muscle in AMPPNP at 23°C

Journal of Molecular Biology

Volumn 264, Issue 2, 1996, Pages 302-322

  Winkler, Hanspeter ^a,c   Reedy, Mary C ^a   Reedy, Michael K ^a   Tregear, Richard ^b   Taylor, Kenneth A ^a,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Actin; Myosin; Nucleotide triphosphate; Troponin

Indexed keywords

MUSCLE PROTEIN; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN; TROPONIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FLIGHT MUSCLE; MUSCLE CELL; MUSCLE STIFFNESS; MUSCLE STRENGTH; MUSCLE TONE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE; SARCOMERE; SARCOMERE LENGTH; X RAY DIFFRACTION;

ANIMALIA; INSECTA;

EID: 0030606281     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0642     Document Type: Article

References (61)

1. Bagshaw, C. (1993). Muscle Contraction. Chapman & Hall, London.
2. Barrington-Leigh, J., Holmes, K. C., Mannherz, H. G., Rosenbaum, G., Eckstein, F. & Goody, R. S. (1972). Effects of ATP analogs on the low-angle X-ray diffraction pattern of insect flight muscle. Cold Spring Harbor Symp. Quant. Biol. 37, 443-447.
3. Barrington-Leigh, J., Goody, R. S., Hofmann, W., Holmes, K. C., Rosenbaum, G. & Tregear, R. T. (1977). The interpretation of X-ray diffraction from glycerinated flight muscle fibre bundles: new theoretical and experimental approaches. In Insect Flight Muscle: Proceedings of the Oxford Symposium (Tregear, R. T., ed.), pp. 137-146, Elsevier, Amsterdam.
4. Beinbrech, G. (1977). Electron micrography of Lethocerus muscle in the presence of nucleotides. In Insect Flight Muscle: Proceedings of the Oxford Symposium (Tregear, R. T., ed.), pp. 147-160, Elsevier, Amsterdam.
5. Beinbrech, G., Kuhn, H. J., Herzig, J. W. & Rueff, J. C. (1976). Evidence for two attached myosin crossbridge states of different potential energy. Cytobiologie, 12, 385-396.
6. Biosca, J. A., Green, L. E. & Eisenberg, E. (1988). Binding of ADP and 5′adenylyl imidodiphosphate to rabbit muscle myofibrils. J. Biol. Chem. 263, 14231-14235.
7. Biosca, J. A., Eisenberg, E., Reedy, M. C. & Reedy, M. K. (1990). Binding of ADP and adenosine 5′[β, γ-imido]triphosphate to insect flight muscle fibrils. Eur. J. Biochem. 189, 395-399.
8. Fajer, P. G., Fajer, E. A., Brunsvold, N. J. & Thomas, D. D. (1988). Effects of AMPPNP on the orientation and rotational dynamics of spin-labeled muscle crossbridges. Biophys. J. 53, 513-524.
9. Fisher, A., Smith, C., Thoden, J., Smith, R., Sutoh, K., Holden, H. & Rayment, I. (1995). Structural studies of myosin: nucleotide complexes: a revised model for the molecular basis of muscle contraction. Biophys. J. 68, 19S-34S.
10. Freundlich, A. & Squire, J. M. (1983). Three-dimensional structure of the insect (Lethocerus) flight muscle M-band. J. Mol. Biol. 169, 439-453.
11. Goody, R. S., Holmes, K. C., Mannherz, H. G., Tregear, R. T. & Rosenbaum, G. (1975). Cross-bridge conformation as revealed by X-ray diffraction studies of insect flight muscle with ATP analogs. Biophys. J. 15, 687-705.
12. Goody, R. S., Barrington-Leigh, J., Mannherz, H. G., Tregear, R. T. & Rosenbaum, G. (1976). X-ray titration of binding of beta, gamma,-imido-ATP to myosin in insect flight muscle. Nature, 262, 613-615.
13. Goody, R. S., Reedy, M. C., Hofmann, W., Holmes, K. C. & Reedy, M. K. (1985). Binding of myosin subfragment 1 to glycerinated insect flight muscle in the rigor state. Biophys. J. 47, 151-169.
14. Green, L. E. & Eisenberg, E. (1978). Formation of ternary complex: actin, 5′-adenylyl imidodiphosphate, and the subfragments of myosin. Proc. Natl Acad. Sci. USA, 75, 54-58.
15. Green, L. E. & Eisenberg, E. (1980). Dissociation of the actin subfragment-1 complex by adenyl-5′-yl imidodiphosphate, ADP and PPi. J. Biol. Chem. 255, 543-548.
16. Henderson, R., Baldwin, J. M., Downing, K. H., Lepault, J. & Zemlin, F. (1986). Structure of purple membrane from Halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5 Å resolution. Ultramicrosopy, 19, 147-178.
17. Holmes, K. C., Goody, R. S., Mannherz, H. G., Barrington-Leigh, J. & Rosenbaum, G. (1976). An investigation of the cross-bridge cycle using ATP analogs and low-angle X-ray diffraction from glycerinated fibres of insect flight muscle. In Molecular Basis of Motility (Heilmeyer, L., Guegg, J. C. & Gieland, T., eds), pp. 26-41, 1975 Colloquium-Mosbach.
18. Holmes, K. C., Tregear, R. T. & Barrington-Leigh, J. (1980). Interpretation of the low angle X-ray diffraction from insect muscle in rigor. Proc. Roy. Soc. Lond. [Biol.], 207, 13-33.
19. Holmes, K. C., Popp, D., Gebhard, W. & Kabsch, W. (1990). Atomic model of the actin filament. Nature, 347, 44-49.
20. Huxley, H. E. & Brown, W. (1967). The low-angle X-ray diagram of vertebrate striated muscle and its behavior during contraction and rigor. J. Mol. Biol. 30, 383-434.
21. Huxley, H. E., Simmons, R. M., Faruqi, A. R., Kress, M., Bordas, J. & Koch, M. H. J. (1983). Changes in the X-ray reflexions from contracting muscle during rapid mechanical transients and their structural implications. J. Mol. Biol. 169, 469-506.
22. Irving, M., Lombardi, V., Piazzesi, G. & Ferenczi, M. A. (1992). Myosin head movements are synchronous with the elementary force-generating process in muscle. Nature, 355, 156-158.
23. Irving, M., St. Claire Allen, T., Sabido-David, C., Craik, J. S., Brandmeier, B., Kendrick-Jones, J., Corrie, J. E., Trentham, D. R. & Goldman, Y. E. (1995). Tilting of the light-chain region of myosin during step length changes and active force generation in skeletal muscle. Nature, 375, 688-691.
24. Jones, T. A., Zou, J.-Y., Cowan, S. W., & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47, 110-119.
25. Jontes, J., Wilson-Kubalek, E. & Milligan, R. (1995). A 32° tail swing in brush border myosin I on ADP release. Nature, 378, 751-753.
26. Kuhn, H. J. (1973). Transformation of chemical energy into mechanical energy by glycerol-extracted fibres of insect flight muscle in the absence of nucleosidetriphosphate - hydrolysis. Experientia, 29, 1086-1088.
27. Lovell, S. J., Knight, P. J. & Harrington, W. F. (1981). Fraction of myosin heads bound to thin filaments in rigor fibrils from insect flight and vertebrate muscles. Nature, 293, 664-666.
28. Luther, P. K. & Squire, J. M. (1980). Three-dimensional structure of the vertebrate muscle A-band. J. Mol. Biol. 141, 409-439.
29. Malloy, J. E., Burns, J. E., Kendrick-Jones, J., Tregear, R. T. & White, D. C. S. (1995). Movement and force produced by a single myosin head. Nature, 378, 209-212.
30. Marston, S. B., Rodger, C. D. & Tregear, R. T. (1976). Changes in muscle crossbridges when β, γ-imido-ATP binds to myosin. J. Mol. Biol. 104, 263-276.
31. Marston, S. B., Tregear, R. T., Rodger, C. D. & Clarke, M. L. (1979). Coupling between the enzymatic site of myosin and the mechanical output of muscle. J. Mol. Biol. 128, 111-126.
32. Miller, A. & Tregear, R. T. (1972). The structure of insect fibrillar flight muscle in the presence and absence of ATP. J. Mol. Biol. 70, 85-104.
33. Rayment, I., Rypniewski, W. R., Schmidt-Baese, K., Smith, R., Tomchick, D. R., Benning, M. M., Winkelmann, D. A., Wesenberg, G. & Holden, H. M. (1993a). Three-dimensional structure of myosin subfragment-1: a molecular motor. Science, 261, 50-58.
34. Rayment, I., Holden, H. M., Whittaker, M. C., Yohn, B., Lorenz, M., Holmes, K. C. & Milligan, R. A. (1993b). Structure of the actin-myosin complex and its implications for muscle contraction. Science, 261, 58-65.
35. Reedy, M. C., Reedy, M. K. & Goody, R. S. (1983). Co-ordinated electron microscopy and X-ray studies of glycerinated insect flight muscle. II. Electron microscopy and image reconstruction of muscle fibers fixed in rigor, in ATP and in AMPPNP. J. Muscle Res. Cell Motil. 4, 55-81.
36. Reedy, M. C., Reedy, M. K. & Goody, R. S. (1987). The structure of insect flight muscle in the presence of AMPPNP. J. Muscle Res. Cell Motil. 8, 473-503.
37. Reedy, M. C., Reedy, M. K. & Tregear, R. T. (1988a). Two attached non-rigor crossbridge forms. Advan. Exp. Med. Biol. 226, 5-15.
38. Reedy, M. C., Reedy, M. K. & Tregear, R. T. (1988b). Two attached non-rigor crossbridge forms in insect flight muscle. J. Mol. Biol. 204, 357-383.
39. Reedy, M. C., Reedy, M. K., Leonard, K. & Bullard, B. (1994). Gold/Fab immuno electron microscopy localization of troponin H and troponin T in Lethocerus flight muscle. J. Mol. Biol. 239, 52-67.
40. Reedy, M. K. (1968). Ultrastructure of insect flight muscle. I. Screw sense and structural grouping in the rigor cross-bridge lattice. J. Mol. Biol. 31, 155-176.
41. Reedy, M. K. & Reedy, M. C. (1985). Rigor crossbridge structure in tilted single filament layers and flared-X formations from insect flight muscle. J. Mol. Biol. 185, 145-176.
42. Reedy, M. K., Holmes, K. C. & Tregear, R. T. (1965). Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature, 207, 1276-1280.
43. Reedy, M. K., Goody, R. S., Hofmann, W. & Rosenbaum, G. (1983). Co-ordinated electron microscopy and X-ray studies of glycerinated insect flight muscle. I. X-ray diffraction monitoring during preparation for electron microscopy of muscle fibers fixed in rigor, in ATP and in AMPPNP. J. Muscle Res. Cell Motil. 4, 25-53.
44. Schmitz, H., Reedy, M. C., Reedy, M. K., Tregear, R. T., Winkler, H. & Taylor, K. A. (1996). Electron tomography of insect flight muscle in rigor and AMPPNP at 23°C. J. Mol. Biol. 264, 279-301.
45. Schoenberg, M. (1989). Effect of adenosine triphosphate analogs on skeletal muscle fibers in rigor. Biophys. J. 56, 33-41.
46. Schoenberg, M. (1993). Equilibrium muscle crossbridge behavior: the interaction of myosin crossbridges with actin. Advan. Biophys. 29, 55-73.
47. Sleep, J. & Glyn, H. (1986). Inhibition of myofibrillar and actomyosin subfragment 1 adenosinetriphosphatase by adenosine 5′-diphosphate, pyrophosphate, and adenyl-5′-yl imidodiphosphate. Biochemistry, 25, 1949-1954.
48. Taylor, K. A. & Crowther, R. A. (1991). A protocol for 3-D image reconstruction from a single image of an oblique section. Ultramicroscopy, 38, 85-103.
49. Taylor, K. A. & Crowther, R. A. (1992). 3-D reconstruction from the Fourier transform of a single superlattice image of an oblique section. Ultramicroscopy, 41, 153-167.
50. Taylor, K. A., Reedy, M. C., Córdova, L. & Reedy, M. K. (1984). Three-dimensional reconstruction of rigor insect flight muscle from tilted thin sections. Nature, 310, 285-291.
51. Taylor, K. A., Reedy, M. C., Córdova, L. & Reedy, M. K. (1989a). Three-dimensional image reconstruction of insect flight muscle. I. The rigor myac layer. J. Cell Biol. 109, 1085-1102.
52. Taylor, K. A., Reedy, M. C., Córdova, L. & Reedy, M. K. (1989b). Three-dimensional image reconstruction of insect flight muscle. II. The rigor actin layer. J. Cell Biol. 109, 1103-1123.
53. Taylor, K. A., Reedy, M. C., Reedy, M. K. & Crowther, R. A. (1993). Crossbridges in the complete unit cell of rigor insect flight muscle imaged by 3-D reconstruction from oblique sections. J. Mol. Biol. 233, 86-108.
54. Thomas, D. D. & Cooke, R. (1980). Orientation of spin-labeled myosin heads in glycerinated muscle fibers. Biophys. J. 32, 891-906.
55. Thomas, D. D., Cooke, R. & Barnett, V. A. (1983). Orientation and rotational mobility of spin-labeled myosin heads in insect flight muscle in rigor. J. Muscle Res. Cell Motil. 4, 367-378.
56. Tregear, R. T., Wakabayashi, K., Iwamoto, H., Reedy, M. C., Reedy, M. K., Sugi, H. & Amemiya, Y. (1990). X-ray diffraction and electron microscopy from Lethocerus flight muscle partially relaxed by adenylylimidodiphosphate and ethylene glycol. J. Mol. Biol. 214, 129-141.
57. Whittaker, M., Wilson-Kubalek, E., Smith, J., Faust, L., Milligan, R. & Sweeney, L. (1995). A 35-Å movement of smooth muscle myosin on ADP release. Nature, 378, 748-751.
58. Winkler, H. & Taylor, K. A. (1994). 3-D reconstruction by combining data from sections cut oblique to different unit cell axes. Ultramicroscopy, 55, 357-371.
59. Wray, J. S. (1979). Filament geometry and the activation of insect flight muscles. Nature, 280, 325-326.
60. Wray, J. S. (1984). Crossbridge states in invertebrate muscles. In Contractile Mechanisms in Muscle (Pollack, G. H. & Sugi, H., eds), pp. 185-192, Plenum Press, New York.
61. Xie, X., Harrison, D. H., Schlichting, I., Sweet, R. M., Kalabokis, V. N., Szent-Gyorgyi, A. G. & Cohen, C. (1994). Structure of the regulatory domain of scallop myosin at 2.8 Å resolution. Nature, 368, 306-312.