Orientation changes in myosin regulatory light chains following photorelease of ATP in skinned muscle fibers

Biophysical Journal

Volumn 70, Issue 4, 1996, Pages 1847-1862

  Allen, Taylor St Claire ^a,c   Ling, Nicholas ^b,d   Irving, Malcolm ^b   Goldman, Yale E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF WAIKATO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MYOSIN LIGHT CHAIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AVIAN STOMACH; CHICKEN; FLUORESCENCE POLARIZATION; MUSCLE CELL; NONHUMAN; PHOTOLYSIS; POLARIZATION; PSOAS MUSCLE; RABBIT;

ANIMALIA; AVES; GALLUS GALLUS; ORYCTOLAGUS CUNICULUS;

EID: 0029975892     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(96)79750-3     Document Type: Article

References (71)

1. Allen, T. St. C., N. Ling, Y. E. Goldman, and M. Irving. 1992. Structural changes of myosin light chain 2 in skinned muscle fibers following photolysis of caged ATP and ADP. Biophys. J. 61:286a. (Abstr.)
2. Allen, T. St. C., N. Ling, Y. E. Goldman, and M. Irving. 1993. Kinetics of orientation changes of rhodamine probes on myosin regulatory light chains in skinned muscle fibers following photolysis of caged ATP. Biophys. J. 64:231a. (Abstr.)
3. Barabas, K., and L. Keszthelyi. 1984. Temperature dependence of ATP release from "caged" ATP. Acta Biochim. Biophys. Acad. Sci. Hung. 19:305-309.
4. Berger, C. L., J. S. Craik, D. R. Trentham, J. E. T. Corrie, and Y. E. Goldman. 1995. Fluorescence polarization from isomers of tetramethylrhodamine at SH-I in rabbit psoas muscle fibers. Biophys. J. 68: 78s-80s.
5. Brown, P. D., M. A. Ferenczi, M. Irving, and I. Dobbie. 1995. Time course of tension and intensities of the inner equatorial x-ray reflections on the photolysis of DMB-caged ATP in apyrase-treated rabbit skeletal muscle fibres. Biophys. J. 68:67a. (Abstr.)
6. Burghardt, T. P., T. Ando. and J. Borejdo. 1983. Evidence for cross-bridge order in contraction of glycerinated skeletal muscle. Proc. Natl. Acad. Sci. USA. 80:7515-7519.
7. Chase, P. B., D. A. Martyn, M. J. Kushmerick, and A. M. Gordon. 1993. Effects of inorganic phosphate analogues on stiffness and unloaded shortening of skinned muscle fibres from rabbit. J. Physiol. 460: 231-246.
8. Chen, R. F., and R. L. Bowman. 1965. Fluorescence polarization: measurement with ultraviolet-polarizing filters in a spectrophotofluorometer. Science. 147:729-732.
9. Cooke, R. 1986. The mechanism of muscle contraction. CRC Crit. Rev. Biochem. 21:53-118.
10. Cooke, R., M. S. Crowder, and D D. Thomas. 1982. Orientation of spin labels attached to cross-bridges in contracting muscle fibres. Nature. 300:776-778.
11. Corrie, J. E. T., and J. S. Craik. 1994. Synthesis and characterisation of pure isomers of iodoacetamidotetramethylrhodamine. J. Chem. Soc. Perkin Trans. 1:2967-2973.
12. Dantzig, J A., M. G. Hibberd, D. R. Trentham, and Y. E. Goldman. 1991. Cross-bridge kinetics in the presence of MgADP investigated by pho-tolysis of caged ATP in rabbit psoas muscle fibres. J. Physiol. 432: 639-680.
13. Ferenczi, M. A. 1986. Phosphate burst in permeable muscle fibers of the rabbit. Biophys. J. 50:471-477.
14. Ferenczi, M. A., E. Homsher. and D. R. Trentham, 1984. The kinetics of magnesium-adenosine triphosphate cleavage in skinned muscle fibers of the rabbit. J. Physiol. 352:575-599.
15. Fisher, A. J., C. A. Smith, J. Thoden, R. Smith, K. Sutoh, H. M. Holden, and I. Rayment. 1995. Structural studies of myosin nucleotide complexes: a revised model for the molecular basis of muscle contraction. Biophys. J. 68:19s-28s.
16. Goldman, Y. E., M. G. Hibberd, J. A. McCray, and D. R. Trentham. 1982. Relaxation of muscle fibres by photolysis of caged ATP. Nature. 300: 701-705.
17. Goldman, Y. E., M. G. Hibberd, and D. R. Trentham. 1984a, Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5′-triphosphate. J. Physiol. 354:577-604.
18. Goldman, Y. E., M. G. Hibberd, and D. R. Trentham. 1984b. Initiation of active contraction by photogeneration of adenosine-5′-triphosphate in rabbit psoas muscle fibres. J. Physiol. 354:605-624.
19. Goldman, Y. E., and R. M. Simmons. 1977. Active and rigor muscle stiffness. J. Physiol. 269:55-57P.
20. Goldman, Y. E., and R. M. Simmons. 1984. Control of sarcomere length in skinned muscle fibres of Rana temporaria during mechanical transients. J. Physiol. 350:497-518.
21. Gutfreund, H. 1972. Transients and relaxation. In Enzymes: Physical Principles John Wiley and Sons, London. 176-228.
22. Hambly, B., K. Franks, and R. Cooke. 1991. Orientation of spin-labeled light chain-2 exchanged onto myosin cross-bridges in glycerinated muscle fibers. Biophys. J. 59:127-138.
23. Hambly, B., K. Franks, and R. Cooke. 1992. Paramagnetic probes attached to a light chain on the myosin head are highly disordered in active muscle fibers. Biophys. J. 63:1306-1313.
24. Higuchi, H., and Y. E. Goldman. 1991. Sliding distance between actin and myosin filaments per ATP molecule hydrolysed in skinned muscle fibres. Nature. 352:352-354.
25. Higuchi, H., and Y. E. Goldman. 1995. Sliding distance per ATP molecule hydrolyzed by myosin heads during isotonic shortening of skinned muscle fibers. Biophys. J. 69:1491-1507.
26. Higuchi, H., T. Yanagida, and Y. E. Goldman. 1995. Compliance of thin filaments in skinned fibers of rabbit skeletal muscle. Biophys. J. 69: 1000-1010.
27. Hirose, K., C. Franzini-Armstrong, Y. E. Goldman, and J. M. Murray. 1994. Structural changes in muscle crossbridges accompanying force generation. J. Cell Biol. 127:763-778.
28. Hirose, K., T. D. Lenart, J. M. Murray, C. Franzini-Armstrong, and Y. E. Goldman. 1993. Flash and smash: rapid freezing of muscle fibers activated by photolysis of caged ATP. Biophys. J. 65:397-408.
29. Homsher, E., and N. C. Millar. 1990. Caged compounds and striated muscle contraction. Annu. Rev. Physiol. 52:875-896.
30. Hopkins, S. C., L. Phan, M. Irving, and Y. E. Goldman. 1995. Oscillations in the orientation of acetamidotetramethylrhodamine (ATR) probes on myosin regulatory light chain (RLC) caused by sinusoidal length changes in skinned muscle fibers. Biophys. J. 66:9a. (Abstr.)
31. Horiuti, K., T. Sakoda, and K. Yamada. 1992. Time course of rise of muscle stiffness at onset of contraction induced by photorelease of ATP. J. Muscle Res. Cell Motil. 13:685-691.
32. Huxley, A. F., and R. M. Simmons. 1971. Proposed mechanism of force generation in striated muscle. Nature. 233:533-538.
33. Huxley, H. E. 1969. The mechanism of muscular contraction. Science. 164:1356-1366.
34. Huxley, H. E., and W. Brown. 1967. The low-angle x-ray diagram of vertebrate skeletal muscle and its behaviour during contraction and rigor. J. Mol. Biol. 30:383-434.
35. Huxley, H. E., A. Stewart, H. Sosa, and T. Irving. 1994. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys. J. 67:2411-2421.
36. Ip, W., and J. Heuser. 1983. Direct visualization of the myosin crossbridge helices on relaxed rabbit psoas thick filaments. J. Mol. Biol. 171: 105-109.
37. Irving, M. 1996. Steady-state polarization from cylindrically-symmetric fluorophores undergoins rapid restricted motion. Biophys. J. 70: 1830-1835.
38. Irving, M., T. St. C. Allen, C. Sabido-David, J. S. Craik, B. Brandmeier, J. Kendrick-Jones, J. E. T. Corrie, D. R. Trentham, and Y. E. Goldman. 1995. Tilting of the tight-chain region of myosin during step length changes and active force generation in skeletal muscle. Nature. 375: 688-691.
39. Kensler, R. W., S. Peterson. and M. Norberg. 1994. The effects of changes in temperature or ionic strength on isolated rabbit and fish skeletal muscle thick filaments. J. Muscle Res. Cell Motil. 15:69-79.
40. Ling, N., C. Shrimpton, J. Sleep, J. Kendrick-Jones, and M. Irving. 1996. Fluorescent probes of the orientation of myosin regulatory light chains in relaxed, rigor and contracting muscle. Biophys. J. 70.1836-1846.
41. Lombardi, V. G. Piazzesi, and M. Linari. 1992. Rapid regeneration of the actin-myosin power stroke in contracting muscle. Nature. 355:638-641.
42. Lowy, J., D. Popp, and A. A. Stewart. 1991. X-ray studies of order-disorder transitions in the myosin heads of skinned rabbit psoas muscles. Biophys. J. 60:812-824.
43. Lymn, R. W., and E. W. Taylor. 1971. Mechanism of adenosine triphosphate hydrolysis by actorayosin. Biochemistry. 10:4617-4624.
44. 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.
45. Moss, R. L., G. G. Giulian, and M. L. Greaser. 1982. Physiological effects accompanying the removal of myosin LC2 from skinned skeletal muscle fibers. J. Biol. Chem. 257:8588-8591.
46. Ostap, E. M., V. A. Barnett, and D. D. Thomas. 1995. Resolution of three structural states of spin-labeled myosin in contracting muscle. Biophys. J. 69:177-188.
47. Peckham, M., M. A. Ferenczi, and M. Irving. 1994. A birefringence study of changes in myosin orientation during relaxation of skinned muscle fibers induced by photolytic ATP release. Biophys. J. 67:1141-1148.
48. Poole, K. J. V., Y. Maeda, G. Rapp, and R. S. Goody. 1991. Dynamic x-ray diffraction measurements following photolytic relaxation and activation of skinned rabbit psoas fibres. Adv. Biophys. 27:63-75.
49. Poole, K. J. V., G. Rapp, Y. Maéda, and R. S. Goody. 1988. The time course of changes in the equatorial diffraction patterns from different muscle types on photolysis of caged-ATP. In Advances In Experimental Medicine and Biological Molecular Mechanism of Muscle Contraction, Vol. 226. H. Sugi and G. Pollack, editors. Plenum Press, New York. 391-404.
50. Press, W. H., S. A. Teukolsky. W. T. Vetterling, and B. P. Flannery. 1992. Nonlinear models. In Numerical Recipes in C: The Art of Scientific Computing, 2nd ed. Cambridge University Press, New York. 683-688.
51. Rader, C. M., and B. Gold. 1967. Digital filter design techniques in the frequency domain. Proc. IEEE. 55:149-171.
52. Rayment, I., H. M. Holden, M. Whittaker, C. B. Yohn, M. Lorenz, K. C. Holmes, and R. A. Milligan. 1993. Structure of the actin-myosin complex and its implications for muscle contraction. Science. 261:58-65.
53. Reedy, M. K., R. S. Goody, W. Hofmann, and G. Rosenbaum. 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 fibres fixed in rigor, in ATP and in AMPPNP. J. Muscle Res. Cell Motil. 4:25-53.
54. 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.
55. Sabido-David, C., J. S. Craik, B. Brandmeier, J. E. T. Corrie, D. R. Trentham, N. Ling, and M. Irving. 1994. Orientation of acetamidotetramethylrhodamine (ATR) isomers covalently bound to regulatory light chains in rabbit psoas muscle fibers. Biophys. J. 66:234a. (Abstr.)
56. Savitzky, A., and M. J. E. Golay. 1964. Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 36:1627-1639.
57. Sosa, H., D. Popp, G. Ouyang, and H. E. Huxley. 1994. Ultrastructure of skeletal muscle fibers studied by a plunge quick freezing method: myofilament lengths. Biophys. J. 67:283-292.
58. Tanner, J. W., D. D. Thomas, and Y. E. Goldman. 1992. Transients in orientation of a fluorescent cross-bridge probe following photolysis of caged nucleotides in skeletal muscle fibres. J. Mol. Biol. 223:185-203.
59. Taylor, K. A., M. C. Reedy, L. Cordova, and M. K. Reedy. 1989. Three-dimensional image reconstruction of insect flight muscle. II. The rigor actin layer. J. Cell. Biol. 109:1103-1123.
60. Thirlwell, H., J. E. T. Corrie, G. P. Reid, D. R. Trentham, and M. A. Ferenczi. 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.
61. Thirlwell, H., J. A. Sleep, and M. A. Ferenczi. 1995. Inhibition of unloaded shortening velocity in permeabilized muscle fibres by caged ATP compounds. J. Muscle Res. Cell Motil. 16:131-137.
62. Thomas, D. D. 1987. Spectroscopic probes of muscle cross-bridge rotation. Anna. Rev. Physiol. 49:691-709.
63. Thomas, D. D., and R. Cooke. 1980. Orientation of spin-labeled myosin heads in glycerinated muscle fibers. Biophys. J. 32:891-906.
64. Tsukita, S., and M. Yano. 1985. Actomyosin structure in contracting muscle detected by rapid freezing. Nature. 317:182-184.
65. Vibert, P., and C. Cohen. 1988. Domains, motions and regulation in the myosin head. J. Muscle Res. Cell Motil. 9:296-305.
66. Wakabayashi, K., Y. Sugimoto, H. Tanaka, Y. Ueno. Y. Takezawa, and Y Amemiya. 1994. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys. J. 67 2422-2435.
67. Walker, J. W., G. P. Reid, J. A. McCray, and D. R. Trentham. 1988. Photolabile 1-(2-Nitrophenyl)ethyl phosphate esters of adenine nucleotide analogues. Synthesis and mechanism of photolysis. J. Am. Chem. Soc. 110.7170-7177.
68. Weber, G. 1952. Polarization of the fluorescence of macromolecules 1. Theory and experimental method. Biochemistry. 51:145-155.
69. White, H. D , and E. W. Taylor 1976. Energetics and mechanism of actomyosin adenosine triphosphatase. Biochemistry. 15:5818-5826.
70. Yanagida, T., T. Arata, and F. Oosawa. 1985. Sliding distance of actin filament induced by a myosin crossbridge during one ATP hydrolysis cycle. Nature. 316:366-369.
71. Yount, R. G. 1975. ATP analogs. Adv. Enzymol. 43:1-56.