Direct modeling of X-ray diffraction pattern from contracting skeletal muscle

Biophysical Journal

Volumn 95, Issue 6, 2008, Pages 2880-2894

  Koubassova, Natalia A ^a   Bershitsky, Sergey Y ^b   Ferenczi, Michael A ^c   Tsaturyan, Andrey K ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b INSTITUTE OF IMMUNOLOGY AND PHYSIOLOGY   (Russian Federation)

^c NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN;

ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; PROTEIN CONFORMATION; RABBIT; SKELETAL MUSCLE; STEREOISOMERISM; TEMPERATURE; X RAY DIFFRACTION;

ANIMALS; MODELS, MOLECULAR; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MYOSINS; PROTEIN CONFORMATION; RABBITS; STEREOISOMERISM; SUBSTRATE SPECIFICITY; TEMPERATURE; X-RAY DIFFRACTION;

EID: 55549097137     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.120832     Document Type: Article

References (48)

1. Huxley, H. E. 1996. A personal view of muscle and motility mechanisms. Annu. Rev. Physiol. 58:1-19.
2. Piazzesi, G., M. Reconditi, M. Linari, L. Lucii, Y.B. Sun, T. Narayanan, P. Boesecke, V. Lombardi, and M. Irving. 2002. Mechanism of force generation by myosin heads in skeletal muscle. Nature. 415:659-662.
3. Dobbie, I., M. Linari, G. Piazzesi, M. Reconditi, N. Koubassova, M. A. Ferenczi, V. Lombardi, and M. Irving. 1998. Elastic bending and active tilting of myosin heads during muscle contraction. Nature. 396:383-387.
4. Takezawa, Y., D. S. Kim, M. Ogino, Y. Sugimoto, T. Kobayashi, T. Arata, and K. Wakabayashi. 1999. Backward movements of cross-bridges by application of stretch and by binding of MgADP to skeletal muscle fibers in the rigor state as studied by x-ray diffraction. Biophys. J. 76:1770-1783.
5. Juanhuix, J., J. Bordas, J. Campmany, A. Svensson, M. L. Bassford, and T. Narayanan. 2001. Axial disposition of myosin heads in isometrically contracting muscles. Biophys. J. 80:1429-1441.
6. Kraft, T., T. Mattei, A. Radocaj, B. Piep, C. Nocula, M. Furch, and B. Brenner. 2002. Structural features of cross-bridges in isometrically contracting skeletal muscle. Biophys. J. 82:2536-2547.
7. Oshima, K., Y. Takezawa, Y. Sugimoto, T. Kobayashi, T. C. Irving, and K. Wakabayashi. 2007. Axial dispositions and conformations of myosin crossbridges along thick filaments in relaxed and contracting states of vertebrate striated muscles by X-ray fiber diffraction. J. Mol. Biol. 367:275-301.
8. Huxley, H. E., M. Reconditi, A. Stewart, and T. Irving. 2006. X-ray interference studies of crossbridge action in muscle contraction: evidence from quick releases. J. Mol. Biol. 363:743-761.
9. Malinchik, S. B., and V. V. Lednev. 1992. Interpretation of the X-ray diffraction pattern from relaxed skeletal muscle and modelling of the thick filament structure. J. Muscle Res. Cell Motil. 13:406-419.
10. Malinchik, S., S. Xu, and L. C. Yu. 1997. Temperature-induced structural changes in the myosin thick filament of skinned rabbit psoas muscle. Biophys. J. 73:2304-2312.
11. Hudson, L., J. J. Harford, R. C. Denny, and J. M. Squire. 1997. 3D structure of fish muscle myosin filaments. J. Struct. Biol. 137:154-163.
12. Al-Khayat, H. A., L. Hudson, M. K. Reedy, T. C. Irving, and J. M. Squire. 2003. Myosin head con.guration in relaxed insect flight muscle: x-ray modeled resting cross-bridges in a pre-powerstroke state are poised for actin binding. Biophys. J. 85:1063-1079.
13. Al-Khayat, H. A., and J. M. Squire. 2006. Refined structure of bony fish muscle myosin filaments from low-angle X-ray diffraction data. J. Struct. Biol. 155:218-229.
14. Gu, J., S. Xu, and L. C. Yu. 2002. A model of cross-bridge attachment to actin in the A·M·ATP state based on x-ray diffraction from permeabilized rabbit psoas muscle. Biophys. J. 82:2123-2133.
15. Yagi, N., H. Iwamoto, J. Wakayama, and K. Inoue. 2005. Structural changes of actin-bound myosin heads after a quick length change in frog skeletal muscle. Biophys. J. 89:1150-1164.
16. Yagi, N., H. Iwamoto, and K. Inoue. 2006. Structural changes of crossbridges on transition from isometric to shortening state in frog skeletal muscle. Biophys. J. 91:4110-4120.
17. Holmes, K. C., I. Angert, F. J. Kull, W. Jahn, and R. R. Schroeder. 2003. Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide. Nature. 425:423-427.
18. Koubassova, N. A., and A. K. Tsaturyan. 2002. Direct modeling of x-ray diffraction pattern from skeletal muscle in rigor. Biophys. J. 83:1082-1097.
19. Iwamoto, H., J. Wakayama, T. Fujisawa, and N. Yagi. 2003. Static and dynamic x-ray diffraction recordings from living mammalian and amphibian skeletal muscles. Biophys. J. 85:2492-2506.
20. Holmes, K. C. 1997. The swinging lever arm hypothesis of muscle contraction. Curr. Biol. 7:112-118.
21. Houdusse, A., A. G. Szent-Gyorgyi, and C. Cohen. 2000. Three conformational states of scallop myosin S1. Proc. Natl. Acad. Sci. USA. 97:11238-11243.
22. Huxley, H. E., and M. Kress. 1985. Crossbridge behaviour during muscle contraction. J. Muscle Res. Cell Motil. 6:153-161.
23. 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.
24. Bershitsky, S. Y., A. K. Tsaturyan, O. N. Bershitskaya, G. I. Machanov, P. Brown, R. Burns, and M. A. Ferenczi. 1997. Muscle force is generated by myosin heads stereospecifically attached to actin. Nature. 388:186-190.
25. Tsaturyan, A. K., S. Y. Bershitsky, R. Burns, and M. A. Ferenczi. 1999. Structural changes in the actin-myosin cross-bridges associated with force generation induced by temperature jump in permeabilized frog muscle fibers. Biophys. J. 77:354-372.
26. Brenner, B., E. Mahlmann, T. Mattei, and T. Kraft. 2005. Driving filament sliding: weak binding cross-bridge states, strong binding cross-bridge states, and the power stroke. Adv. Exp. Med. Biol. 565:75-91.
27. Ferenczi, M. A., S. Y. Bershitsky, N. Koubassova, V. Siththanandan, W. I. Helsby, P. Panine, M. Roessle, T. Narayanan, and A. K. Tsaturyan. 2005. The "roll and lock" mechanism of force generation in muscle. Structure. 13:131-141.
28. 2+-activated contracting insect flight muscle. Cell. 99:421-431.
29. Bershitsky, S. Y., A. K. Tsaturyan, O. Bershitskaya, G. Mashanov, P. Brown, M. Webb, and M. A. Ferenczi. 1996. Mechanical and structural properties underlying contraction of skeletal muscle fibers after partial 1-ethyl-3-[3-dimethylamino)propyl]carbodiimide cross-linking. Biophys. J. 71:1462-1474.
30. Bershitsky, S. Y., and A. K. Tsaturyan. 2002. The elementary force generation process probed by temperature and length perturbations in muscle fibres from the rabbit. J. Physiol. 540:971-988.
31. Cantino, M., and J. Squire. 1986. Resting myosin cross-bridge configuration in frog muscle thick filaments. J. Cell Biol. 102:610-618.
32. 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.
33. 2+-activated states. J. Mol. Biol. 357:707-717.
34. Poole, K. J., M. Lorenz, G. Evans, G. Rosenbaum, A. Pirani, R. Craig, L. S. Tobacman, W. Lehman, and K. C. Holmes. 2006. 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. 155:273-284.
35. Vainstein, B. K. 1963. Diffraction of X-Rays by Chain Molecules. Izdatelstvo Akademii Nauk SSSR, Moscow.
36. Huxley, H. E., A. R. Faruqi, M. Kress, J. Bordas, and M. H. Koch. 1982. Time-resolved X-ray diffraction studies of the myosin layerline reflections during muscle contraction. J. Mol. Biol. 158:637-684.
37. Yagi, N. 1996. Labelling of thin filaments by myosin heads in contracting and rigor vertebrate skeletal muscles. Acta Crystallogr. D. 52:1169-1173.
38. Tsaturyan, A. K. 2002. Diffraction on partially decorated helices. Acta Crystallogr. A. 58:292-294.
39. Linari, M., I. Dobbie, M. Reconditi, N. Koubassova, M. Irving, G. Piazzesi, and V. Lombardi. 1998. The stiffness of skeletal muscle in isometric contraction and rigor:. the fraction of myosin heads bound to actin. Biophys. J. 74:2459-2473.
40. Bershitsky, S. Yu., and A. K. Tsaturyan. 1989. Effect of joule temperature jump on tension and stiffness of skinned rabbit muscle fibers. Biophys. J. 56:809-816.
41. Bordas, J., G. P. Diakun, F. G. Diaz, J. E. Harries, R. A. Lewis, J. Lowy, G. R. Mant, M. L. Martin-Fernandez, and E. Towns-Andrews. 1993. Two-dimensional time-resolved X-ray diffraction studies of live isometrically contracting frog sartorius muscle. J. Muscle Res. Cell Motil. 14:311-324.
42. Linari, M., M. Caremani, C. Piperio, P. Brandt, and V. Lombardi. 2007. Stiffness and fraction of myosin motors responsible for active force in permeabilized muscle fibers from rabbit psoas. Biophys. J. 92:2476-2490.
43. Holmes, K. C., R. T. Tregear, and J. Barrington-Leigh. 1980. Interpretation of the low angle X-ray diffraction from insect flight muscle in rigor. Proc. R. Soc. Lond. B. Biol. Sci. 207:13-33.
44. Piazzesi, G., M. Reconditi, N. Koubassova, V. Decostre, M. Linari, L. Lucii, and V. Lombardi. 2003. Temperature dependence of the force-generating process in single fibres from frog skeletal muscle. J. Physiol. 549:93-106.
45. Iwamoto, H., K. Oiwa, T. Suzuki, and T. Fujisawa. 2001. X-ray diffraction evidence for the lack of stereospecific protein interactions in highly activated actomyosin complex. J. Mol. Biol. 305:863-874.
46. Linari, M., E. Brunello, M. Reconditi, Y.-B. Sun, P. Panine, T. Narayanan, G. Piazzesi, V. Lombardi, and M. Irving. 2005. The structural basis of the increase in isometric force production with temperature in frog skeletal muscle. J. Physiol. 567:459-469.
47. Siththanandan, V. B., J. L. Donnelly, and M. A. Ferenczi. 2006. Effect of strain on actomyosin kinetics in isometric muscle fibers. Biophys. J. 90:3653-3665.
48. 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.