Dynamics of actomyosin interactions in relation to the cross-bridge cycle

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 359, Issue 1452, 2004, Pages 1843-1855

  Zeng, Wei ^a   Conibear, Paul B ^a   Dickens, Jane L ^a   Cowie, Ruth A ^a   Wakelin, Stuart ^a   Málnási Csizmadia, András ^b   Bagshaw, Clive R ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Dictyostelium; Fluorescence; Myopathy; Myosin; Stopped flow; Tryptophan

Indexed keywords

MUSCLE;

DICTYOSTELIUM;

EID: 13444292382     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2004.1527     Document Type: Conference Paper

References (68)

1. Bagshaw, C. R. & Trentham, D. R. 1973 The reversibility of adenosine triphosphate cleavage by myosin. Biochem. J. 133, 323-328.
2. Bagshaw, C. R. & Trentham, D. R. 1974 The characterization of myosin-product complexes and of product-release steps during the magnesium ion-dependent adenosine triphosphatase reaction. Biochem. J. 141, 331-349.
3. 2+-dependent ATPase of myosin and its proteolytic subfragments. Cold Spring Harbor Symp. Quant. Biol. 37, 127-135.
4. Bagshaw, C. R., Eccleston, J. F., Eckstein, F., Goody, R. S., Gutfreund, H. & Trentham, D. R. 1974 The magnesium ion-dependent adenosine triphosphatase of myosin. Two-step processes of adenosine triphosphate association and adenosine diphosphate dissociation. Biochem. J. 141, 351-364.
5. 2+-dependent adenosine triphosphatase activity of myosin. Proc. Natl Acad. Sci. USA 72, 2592-2596.
6. Batra, R. & Manstein, D. J. 1999 Functional characterisation of Dictyostelium myosin II with conserved tryptophanyl residue 501 mutated to tyrosine. Biol. Chem. 380, 1017-1023.
7. Batra, R., Geeves, M. A. & Manstein, D. J. 1999 Kinetic analysis of Dictyostelium discoideum myosin motor domains with glycine-to-alanine mutations in the reactive thiol region. Biochemistry 38, 6126-6134.
8. Bauer, C. B., Holden, H. M., Thoden, J. B., Smith, R. & Rayment, I. 2000 X-ray structures of the apo and MgATP-bound states of Dictyostelium discoideum myosin motor domain. J. Biol. Chem. 275, 38 494-38 499.
9. Bershitsky, S. Y., Tsaturyan, A. K., Bershitskaya, O. N., Mashanov, G. I., Brown, P., Burns, R. & Ferenczi, M. A. 1997 Muscle force is generated by myosin heads stereo-specifically attached to actin. Nature 388, 186-190.
10. Conibear, P. B., Bagshaw, C. R., Fajer, P. G., Kovacs, M. & Malnasi-Csizmadia, A. 2003 Myosin cleft movement and its coupling to actomyosin dissociation. Nature Struct. Biol. 10, 831-835.
11. Conibear, P. B., Malnasi-Csizmadia, A. & Bagshaw, C. R. 2004 The effect of F-actin on the relay helix position of myosin II, as revealed by tryptophan fluorescence, and its implications for mechanochemical coupling. Biochemistry. (In the press.)
12. 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.
13. 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.
14. 4. Biochemistry 34, 8960-8972.
15. Geeves, M. A. & Holmes, K. C. 1999 Structural mechanism of muscle contraction. A. Rev. Biochem. 68, 687-728.
16. Goody, R. S., Hofmann, W. & Mannherz, G. H. 1977 The binding constant of ATP to myosin S1 fragment. Eur. J. Biochem. 78, 317-324.
17. Gulick, A. M., Bauer, C. B., Thoden, J. B. & Rayment, I. 1997 X-ray structures of the MgADP, MgATPgS and MgAMPPNP complexes of the Dictyostelium discoideum myosin motor domain. Biochemistry 36, 11 619-11 628.
18. Holmes, K. C. & Geeves, M. A. 2000 The structural basis of muscle contraction. Phil. Trans. R. Soc. B 355, 419-431. (doi:10.1098/rstb.2000.0583)
19. Holmes, K. C., Angert, I., Kull, F. J., Jahn, W. & Schroder, R. R. 2003 Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide. Nature 425, 423-427.
20. Holmes, K. C., Schröder, R. R. , Eschenburg, S., Sweeney, H. L. & Houdusse, A. 2004 The structure of the rigor complex and its implications for the power stroke. Phil. Trans. R. Soc. B 359, 1819-1828. (doi:10.1098/rstb.2004.1566)
21. Houdusse, A., Szent-Gyorgyi, A. G. & Cohen, C. 2000 Three conformational states of scallop myosin S1. Proc. Natl Acad. Sci. USA 97, 11238-11243.
22. Huston, E. E., Grammer, J. C. & Yount, R. G. 1988 Flexibility of the myosin heavy chain: direct evidence that the region containing SH1 and SH2 can move 10 Å under the influence of nucleotide binding. Biochemistry 27, 8945-8952.
23. Huxley, A. F. 1957 Muscle structure and theories of contraction. Prog. Biophys. Biophys. Chem. 7, 255-318.
24. Huxley, A. F. & Niedergerke, R. 1954 Structural changes in muscle during contraction. Nature 173, 971-973.
25. Huxley, H. E. 1969 The mechanism of muscular contraction. Science 164, 1356-1365.
26. Huxley, H. E. 2000 Past, present and future experiments on muscle. Phil. Trans. R. Soc. B 355, 539-543. (doi:10.1098/rstb.2000.0595)
27. Huxley, H. E. & Hanson, J. 1954 Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173, 973-976.
28. Johnson, K. A. & Taylor, E. W. 1978 Intermediate states of subfragment 1 and actosubfragment 1 ATPase: reevaluation of the mechanism. Biochemistry 17, 3432-3442.
29. Kliche, W., Pfannstiel, J., Tiepold, M., Stoeva, S. & Faulstich, H. 1999 Thiol-specific cross-linkers of variable length reveal a similar separation of SH1 and SH2 in myosin subfragment 1 in the presence and absence of MgADP. Biochemistry 38, 10 307-10 317.
30. Kovacs, M., Malnasi-Csizmadia, A., Woolley, R. J. & Bagshaw, C. R. 2002 Analysis of nucleotide binding to Dictyostelium myosin II motor domains containing a single tryptophan near the active site. J. Biol. Chem. 277, 28459-28467.
31. Kuhlman, P. A. & Bagshaw, C. R. 1998 ATPase kinetics of the Dictyostelium discoideum myosin II motor domain. J. Muscle Res. Cell Motil. 19, 491-504.
32. Kurzawa, S. E., Manstein, D. J. & Geeves, M. A. 1997 Dictyostelium discoideum myosin II: characterization of functional myosin motor fragments. Biochemistry 36, 317-323.
33. Lehrer, S. S. 1997 Intramolecular pyrene excimer fluorescence: a probe of proximity and protein conformational change. Meth. Enzymol. 278, 286-295.
34. Lymn, R. W. & Taylor, E. W. 1971 Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10, 4617-4624.
35. Malnasi-Csizmadia, A., Woolley, R. J. & Bagshaw, C. R. 2000 Resolution of conformational states of Dictyostelium myosin II motor domain using tryptophan (W501) mutants: implications for the open-closed transition identified by crystallography. Biochemistry 39, 16135-16146.
36. Malnasi-Csizmadia, A., Pearson, D. S., Kovacs, M., Woolley, R. J., Geeves, M. A. & Bagshaw, C. R. 2001 Kinetic resolution of a conformational transition and the ATP hydrolysis step using relaxation methods with a Dictyostelium myosin II mutant containing a single tryptophan residue. Biochemistry 40, 12 727-12 737.
37. Mandelkow, E. M. & Mandelkow, E. 1973 Fluorimetric studies on the influence of metal ions and chelators on the interaction between myosin and ATP. FEBS Lett. 33, 161-166.
38. Mannherz, H. G., Schenck, H. & Goody, R. S. 1974 Synthesis of ATP from ADP and inorganic phosphate at the myosin-subfragment 1 active site. Eur. J. Biochem. 48, 287-295.
39. Martinsson, T., Oldfors, A., Darin, N., Berg, K., Tajsharghi, H., Kyllerman, M. & Wahlstrom, J. 2000 Autosomal dominant myopathy: missense mutation (Glu-706 → Lys) in the myosin heavy chain IIa gene. Proc. Natl Acad. Sci. USA 97, 14614-14619.
40. Millar, N. C. & Geeves, M. A. 1988 Protein fluorescence changes associated with ATP and adenosine 5′-[γ-thio]-triphosphate binding to skeletal muscle myosin subfragment 1 and actomyosin subfragment 1. Biochem. J. 249, 735-743.
41. Miller, L., Coppedge, J. & Reisler, E. 1982 The reactive SH1 and SH2 cysteines in myosin subfragment 1 are cross-linked at similar rates with reagents of different length. Biochem. Biophys. Res. Commun. 106, 117-122.
42. Onishi, H., Konishi, K., Fujiwara, K., Hayakawa, K., Tanokura, M., Martinez, H. M. & Morales, M. F. 2000 On the tryptophan residue of smooth muscle myosin that responds to binding of nucleotide. Proc. Natl Acad. Sci. USA 97, 11 203-11 208.
43. Park, S. & Burghardt, T. P. 2000 Isolating and localizing ATP-sensitive tryptophan emission in skeletal myosin subfragment 1. Biochemistry 39, 11 732-11 741.
44. Ranatunga, K. W., Coupland, M. E. & Mutungi, G. 2002 An asymmetry in the phosphate dependence of tension transients induced by length perturbation in mammalian (rabbit psoas) muscle fibres. J. Physiol. 542, 899-910.
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. 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.
48. Ritchie, M. D., Geeves, M. A., Woodward, S. K. & Manstein, D. J. 1993 Kinetic characterization of a cytoplasmic myosin motor domain expressed in Dictyostelium discoideum. Proc. Natl Acad. Sci. USA 90, 8619-8623.
49. Ruppel, K. M. & Spudich, J. A. 1996 Structure-function analysis of the motor domain of myosin. A. Rev. Cell Dev. Biol. 12, 543-573.
50. Sasaki, N., Shimada, T. & Sutoh, K. 1998 Mutational analysis of the switch II loop of Dictyostelium myosin II. J. Biol. Chem. 273, 20 334-20 340.
51. Sasaki, N., Ohkura, R. & Sutoh, K. 2003 Dictyostelium myosin II mutations that uncouple the converter swing and ATP hydrolysis cycle. Biochemistry 42, 90-95.
52. Shih, W. M., Gryczynski, Z., Lakowicz, J. R. & Spudich, J. A. 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.
53. Shimada, T., Sasaki, N., Ohkura, R. & Sutoh, K. 1997 Alanine scanning mutagenesis of the switch I region in the ATPase site of Dictyostelium discoideum myosin II. Biochemistry 36, 14 037-14 043.
54. 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.
55. 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.
56. Steffen, W. & Sleep, J. 2004 Using optical tweezers to relate the chemical and mechanical cross-bridge cycles. Phil. Trans. R. Soc. B 359, 1857-1865. (doi:10.1098/rstb.2004.1558)
57. 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.
58. Suzuki, Y., Yasunaga, T., Ohkura, R., Wakabayashi, T. & Sutoh, K. 1998 Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature 396, 380-383.
59. Tajsharghi, H., Thornell, L. E., Darin, N., Martinsson, T., Kyllerman, M., Wahlstrom, J. & Oldfors, A. 2002 Myosin heavy chain IIa gene mutation E706K is pathogenic and its expression increases with age. Neurology 58, 780-786.
60. Taylor, E. W. 1977 Transient phase of adenosine triphosphate hydrolysis by myosin, heavy meromyosin, and subfragment 1. Biochemistry 16, 732-739.
61. Trybus, K. M. & Taylor, E. W. 1982 Transient kinetics of adenosine 5′-diphosphate and adenosine 5′-(β, γ-imidotriphosphate) binding to subfragment 1 and actosubfragment 1. Biochemistry 21, 1284-1294.
62. Urbanke, C. & Wray, J. 2001 A fluorescence temperature-jump study of conformational transitions in myosin subfragment 1. Biochem. J. 358, 165-173.
63. Wachter, R. M. & Remington, S. J. 1999 Sensitivity of the yellow variant of green fluorescent protein to halides and nitrate. Curr. Biol. 9, R628-629.
64. Wakelin, S. & Bagshaw, C. R. 2003 A prism combination for near isotropic fluorescence excitation by total internal reflection. J. Microsc. 209, 143-148.
65. Wakelin, S., Conibear, P. B., Woolley, R. J., Floyd, D. N., Bagshaw, C. R., Kovacs, M. & Malnasi-Csizmadia, A. 2002 Engineering Dictyostelium discoideum myosin II for the introduction of site-specific probes. J. Muscle Res. Cell Motil. 24, 673-683.
66. Xiao, M., Reifenberger, J. G., Wells, A. L., Baldacchino, C., Chen, L. Q., Ge, P., Sweeney, H. L. & Selvin, P. R. 2003 An actin-dependent conformational change in myosin. Nature Struct. Biol. 10, 402-408.
67. Yengo, C. M., Chrin, L. R., Rovner, A. S. & Berger, C. L. 2000 Tryptophan 512 is sensitive to conformational changes in the rigid relay loop of smooth muscle myosin during the MgATPase cycle. J. Biol. Chem. 275, 25481-25487.
68. Yount, R. G., Lawson, D. & Rayment, I. 1995 Is myosin a 'back door' enzyme? Biophys. J. 68, 44S-47S.