Coupling between phosphate release and force generation in muscle actomyosin

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 359, Issue 1452, 2004, Pages 1913-1920

  Takagi, Y ^a,b   Shuman, H ^a   Goldman, Y E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Actomyosin phosphate; Force generation; Muscle contraction; Optical trap; Single molecule

Indexed keywords

MUSCLE;

EID: 13444280378     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2004.1561     Document Type: Conference Paper

References (71)

1. Bowater, R., Webb, M. R. & Ferenczi, M. A. 1989 Measurement of the reversibility of ATP binding to myosin in calcium-activated skinned fibers from rabbit skeletal muscle. Oxygen exchange between water and ATP released to the solution J. Biol. Chem. 264, 7193-7201.
2. Bowater, R., Zimmerman, R. W. & Webb, M. R. 1990 Kinetics of ATP and inorganic phosphate release during hydrolysis of ATP by rabbit skeletal actomyosin subfragment 1. J. Biol. Chem. 265, 171-176.
3. Conibear, P. B., Bagshaw, C. R., Fajer, P. G., Kovács, M. & Málnási-Csizmadia, A. 2003 Myosin cleft movement and its coupling to actomyosin dissociation. Nature Struct. Biol. 10, 831-835.
4. Cooke, R. 1997 Actomyosin interaction in striated muscle. Physiol. Rev. 77, 671-697.
5. Cooke, R. 1999 Myosin structure: does the tail wag the dog? Curr. Biol. 9, R773-R775.
6. Coureux, P.-D., Wells, A. L., Menetrey, J., Yengo, C. M., Morris, C. A., Sweeney, H. L. & Houdusse, A. 2003 A structural state of the myosin V motor without bound nucleotide. Nature 425, 419-423.
7. Cremo, C. R. & Geeves, M. A. 1998 Interaction of actin and ADP with the head domain of smooth muscle myosin: implications for strain-dependent ADP release in smooth muscle. Biochemistry 37, 1969-1978.
8. Dantzig, J. A. & Goldman, Y. E. 1985 Suppression of muscle contraction by vanadate. Mechanical and ligand binding studies on glycerol-extracted rabbit fibers. J. Gen. Physiol. 86, 305-327.
9. Dantzig, J. A., Goldman, Y. E., Millar, N. C., Lacktis, J. & Homsher, E. 1992 Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J. Physiol. 451, 247-278.
10. Dominguez, R., Freyzon, Y., Trybus, K. M. & Cohen, C. 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.
11. Finer, J. T., Simmons, R. M. & Spudich, J. A. 1994 Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368, 113-119.
12. 4. Biochemistry 34, 8960-8972.
13. Fortune, N. S., Geeves, M. A. & Ranatunga, K. W. 1991 Tension responses to rapid pressure release in glycerinated rabbit muscle fibers. Proc. Natl Acad. Sci. USA 88, 7323-7327.
14. Fortune, N. S., Geeves, M. A. & Ranatunga, K. W. 1994 Contractile activation and force generation in skinned rabbit muscle fibres: effects of hydrostatic pressure. J. Physiol. 474, 283-290.
15. Geeves, M. A. & Holmes, K. C. 1999 Structural mechanism of muscle contraction. A. Rev. Biochem. 68, 687-728.
16. Goldman, Y. E. 1998 Wag the tail: structural dynamics of actomyosin. Cell 93, 1-4.
17. Goldman, Y. E. & Brenner, B. 1987 Special topic: molecular mechanism of muscle contraction. General introduction. A. Rev. Physiol. 49, 629-636.
18. Goldman, Y. E., Hibberd, M. G., McCray, J. A. & Trentham, D. R. 1982 Relaxation of muscle fibres by photolysis of caged ATP. Nature 300, 701-705.
19. Goldman, Y. E., Hibberd, M. G. & Trentham, D. R. 1984a Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5′-triphosphate. J. Physiol. 354, 577-604.
20. Goldman, Y. E., Hibberd, M. G. & Trentham, D. R. 1984b Initiation of active contraction by photogeneration of adenosine-5′-triphosphate in rabbit psoas muscle fibres. J. Physiol. 354, 605-624.
21. Guilford, W. H., Dupuis, D. E., Kennedy, G., Wu, J., Patlak, J. B. & Warshaw, D. M. 1997 Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap. Biophys. J. 72, 1006-1021.
22. Hibberd, M. G., Dantzig, J. A., Trentham, D. R. & Goldman, Y. E. 1985a Phosphate release and force generation in skeletal muscle fibers. Science 228, 1317-1319.
23. Hibberd, M. G., Webb, M. R., Goldman, Y. E. & Trentham, D. R. 1985b Oxygen exchange between phosphate and water accompanies calcium-regulated ATPase activity of skinned fibers from rabbit skeletal muscle. J. Biol. Chem. 260, 3496-3500.
24. Holmes, K. C. 1997 The swinging lever-arm hypothesis of muscle contraction. Curr. Biol. 7, R112-R118.
25. Holmes, K. C., Angert, I., Kull, F. J., Jahn, W. & Schröder, R. R. 2003 Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide. Nature 425, 423-427.
26. Horiuti, K., Kagawa, K. & Yamada, K. 1994 The initial contraction of skinned muscle fibers on photorelease of ATP in the presence of ADP. Jpn. J. Physiol. 44, 675-691.
27. Houdusse, A. & Sweeney, H. L. 2001 Myosin motors, missing structures and hidden springs. Curr. Opin. Struct. Biol. 11, 182-194.
28. Houdusse, A., Kalabokis, V. N., Himmel, D., Szent-Györgyi, A. G. & Cohen, C. 1999 Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97, 459-470.
29. Houdusse, A., Szent-Györgyi, A. G. & Cohen, C. 2000 Three conformational states of scallop myosin S1. Proc. Natl Acad. Sci. USA 97, 11 238-11 243.
30. Huxley, A. F. 1974 Muscular contraction. J. Physiol. 243, 1-43.
31. Irving, M., Lombardi, V., Piazzesi, G. & Ferenczi, M. A. 1992 Myosin head movements are synchronous with the elementary force-generating process in muscle. Nature 357, 156-158.
32. Irving, M., Allen, T. S., Sabido-David, C., Craik, J. S., Brandmeier, B., Kendrick-Jones, J., Corrie, J. E. T., 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.
33. Kawai, M. & Halvorson, H. R. 1991 Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned fibers of rabbit psoas muscle. Biophys. J. 59, 329-342.
34. Kawai, M. & Zhao, Y. 1993 Cross-bridge scheme and force per cross-bridge state in skinned rabbit psoas muscle fibers. Biophys. J. 65, 638-651.
35. Lionne, C., Brune, M., Webb, M. R., Travers, F. & Barman, T. 1995 Time resolved measurements show that phosphate release is the rate limiting step on myofibrillar ATPases. FEBS Lett. 364, 59-62.
36. Lionne, C., Iorga, B., Candau, R., Piroddi, N., Webb, M. R., Belus, A., Travers, F. & Barman, T. 2002 Evidence that phosphate release is the rate-limiting step on the overall ATPase of psoas myofibrils prevented from shortening by chemical cross-linking. Biochemistry 41, 13 297-13 308.
37. Lymn, R. W. & Taylor, E. W. 1971 Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10, 4617-4624.
38. Millar, N. C. & Homsher, E. 1990 The effect of phosphate and calcium on force generation in glycerinated rabbit skeletal muscle fibers: a steady-state and transient kinetic study. J. Biol. Chem. 265, 20 234-20 240.
39. Molloy, J. E., Burns, J. E., Kendrick-Jones, J., Tregear, R. T. & White, D. C. 1995 Movement and force produced by a single myosin head. Nature 378, 209-212.
40. Ostap, E. M., Barnett, V. A. & Thomas, D. D. 1995 Resolution of three structural states of spin-labeled myosin in contracting muscle. Biophys. J. 69, 177-188.
41. Pate, E. & Cooke, R. 1989 Addition of phosphate to active muscle fibers probes actomyosin states within the power-stroke. Pflügers Arch. 414, 73-81.
42. Pate, E., Naber, N., Matuska, M., Franks-Skiba, K. & Cooke, R. 1997 Opening of the myosin nucleotide triphosphate binding domain during the ATPase cycle. Biochemistry 36, 12 155-12 166.
43. Piazzesi, G., Lombardi, V., Ferenczi, M. A., Thirlwell, H., Dobbie, I. & Irving, M. 1995 Changes in the X-ray diffraction pattern from single, intact muscle fibers produced by rapid shortening and stretch. Biophys. J. 68(Suppl.), 92S-96S.
44. Ranatunga, K. W. 1999 Effects of inorganic phosphate on endothermic force generation in muscle. Proc. R. Soc. B 266, 1381-1385. (doi:10.1098/rspb.1999. 0791)
45. Rayment, I., Holden, H. M., Whittaker, M., Yohn, C. B., Lorenz, M., Holmes, K. C. & Milligan, R. A. 1993a Structure of the actin-myosin complex and its implications for muscle contraction. Science 261, 58-65.
46. Rayment, I., Rypniewski, W. R., Schmidt-Base, K., Smith, R., Tomchick, D. R., Benning, M. M., Winkelmann, D. A., Wesenberg, G. & Holden, H. M. 1993b Three-dimensional structure of myosin subfragment-1, a molecular motor. Science 261, 50-58.
47. Rayment, I., Smith, C. & Yount, R. G. 1996 The active site of myosin A. Rev. Physiol. 58, 671-702.
48. Reubold, T. F., Eschenburg, S., Becker, A., Kull, F. J. & Manstein, D. J. 2003 A structural model for actin-induced nucleotide release in myosin. Nature Struct. Biol. 10, 826-830.
49. Schröder, R. R., Manstein, D. J., Jahn, W., Holden, H., Rayment, I., Holmes, K. C. & Spudich, J. A. 1993 Three-dimensional atomic model of F-actin decorated with Dictyostetium myosin S1. Nature 364, 171-174.
50. Siemankowski, R. F., Wiseman, M. O. & White, H. D. 1985 ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc. Natl Acad. Sci. USA 82, 658-662.
51. Sleep, J. A. & Hutton, R. L. 1980 Exchange between inorganic phosphate and adenosine 5′-triphosphate in the medium by actomyosin subfragment 1. Biochemistry 19, 1276-1283.
52. Sleep, J. A., Irving, M. & Burton, K. 2004 The ATP hydrolysis and phosphate release steps control the time course of force development in skeletal muscle. J. Physiol. (In the press.)
53. Smith, C. A. & Rayment, I. 1996 X-ray structure of the magnesium (II)·ADP·vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry 35, 5404-5417.
54. Spudich, J. A. 2001 The myosin swinging cross-bridge model. Nature Rev. Mol. Cell Biol. 2, 387-392.
55. Steffen, W., Smith, D. & Sleep, J. 2003 The working stroke upon myosin-nucleotide complexes binding to actin. Proc. Natl Acad. Sci. USA 100, 6434-6439.
56. Takagi, Y., Goldman, Y. E. & Shuman, H. 2000 Single molecule force of myosin II measured with a novel optical trap system that eliminates linkage compliance. Biophys. J. 78, 235A.
57. Takagi, Y., Homsher, E. E., Goldman, Y. E. & Shuman, H. 2002 Probing the transduction mechanism of rabbit skeletal myosin II under isometric condition using an optical trap. Biophys. J. 82, 373A.
58. Takagi, Y., Homsher, E. E., Goldman, Y. E. & Shuman, H. 2004 ATP and phosphate dependence of single rabbit skeletal actomyosin interactions under differing loads. Biophys. J. 86, 54A.
59. 2+-activated contracting insect flight muscle. Cell 99, 421-431.
60. Tesi, C., Colomo, F., Nencini, S., Piroddi, N. & Poggesi, C. 2000 The effect of inorganic phosphate on force generation in single myofibrils from rabbit skeletal muscle. Biophys. J. 78, 3081-3092.
61. Tesi, C., Colomo, F., Piroddi, N. & Poggesi, C. 2002 Characterization of the cross-bridge force-generating step using inorganic phosphate and BDM in myofibrils from rabbit skeletal muscles. J. Physiol. 541, 187-199.
62. Thirlwell, H., Corrie, J. E. T., Reid, G. P., Trentham, D. R. & Ferenczi, M. A. 1994 Kinetics of relaxation from rigor of permeabilized fast-twitch skeletal fibers from the rabbit using a novel caged ATP and apyrase. Biophys. J. 67, 2436-2447.
63. Trentham, D. R., Bardsley, R. G. & Eccleston, J. F. 1972 Elementary processes of the magnesium ion-dependent adenosine triphosphatase activity of heavy meromyosin. Biochemistry 126, 635-644.
64. Tsaturyan, A. K., Bershitsky, S. Y., Burns, R. & Ferenczi, M. A. 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.
65. Ulbrich, M. & Rüegg, J. C. 1976 Is the chemomechanical energy transformation reversible? Pflügers Arch. 363, 219-222.
66. Vale, R. D. 1996 Switches, latches, and amplifiers: common themes of G proteins and molecular motors. J. Cell Biol. 135, 291-302.
67. 2+ on the kinetics of phosphate release in skeletal muscle. J. Biol. Chem. 267, 2459-2466.
68. i binding to a force-generating state. J. Biol. Chem. 261, 15 557-15 564.
69. White, H. D. & Taylor, E. W. 1976 Energetics and mechanism of actomyosin adenosine triphosphatase. Biochemistry 15, 5818-5826.
70. White, H. D., Belknap, B. & Webb, M. R. 1997 Kinetics of nucleoside triphosphate cleavage and phosphate release steps by associated rabbit skeletal actomyosin, measured using a novel fluorescent probe for phosphate. Biochemistry 36, 11 828-11 836.
71. Yengo, C. M., De La Cruz, E. M., Chrin, L. R., Gaffney II, D. P. & Berger, C. L. 2002 Actin-induced closure of the actin-binding cleft of smooth muscle myosin. J. Biol. Chem. 277, 24 114-24 119.