Measurement of nucleotide release kinetics in single skeletal muscle myofibrils during isometric and isovelocity contractions using fluorescence microscopy

Biophysical Journal

Volumn 73, Issue 4, 1997, Pages 2033-2042

  Chaen, Shigeru ^a   Shirakawa, Ibuki ^a   Bagshaw, Clive R ^b   Sugi, Haruo ^a  

^a TEIKYO UNIVERSITY   (Japan)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CALCIUM ION;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; KINETICS; MUSCLE CONTRACTION; MUSCLE FIBRIL; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; PHOTOLYSIS; RABBIT; SARCOMERE; SKELETAL MUSCLE; VELOCITY;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0030759147     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78233-X     Document Type: Article

References (56)

1. Anazawa, T., K. Yasuda, and S. Ishiwata. 1992. Spontaneous oscillation of tension and sarcomere length in skeletal myofibrils. Microscopic measurement and analysis. Biophys. J. 61:1099-1108.
2. Bagshaw, C. R. 1993. Muscle Contraction, 2nd Ed. Chapman and Hall, London.
3. Bagshaw, C. R. 1997. Use of fluorescent nucleotides. In Current Methods in Muscle Physiology: Advantages, Problems and Limitations. H. Sugi, editor. Oxford University Press, Oxford. In press.
4. Bagshaw, C. R., M. Matuska, and J. A. Spudich. 1992. Measurement of ATP turnover by single, immobilized myosin filaments. J. Muscle Res. Cell Motil. 13:266-267.
5. Bartoo, M. L., V. I. Popov, L. A. Fearn, and G. H. Pollack. 1993. Active tension generation in isolated skeletal myofibrils. J. Muscle Res. Cell Motil. 14:498-510.
6. Bremel, R. D., and A. Weber. 1972. Cooperation with actin filament in vertebrate skeletal muscle. Nature New Biol. 238:97-101.
7. Chaen, S., I. Shirakawa, I., C. R. Bagshaw, and H. Sugi. 1996. Measurement of ATP turnover in single contracting myofibrils using a fluorescent ATP analogue. J. Muscle Res. Cell Motil. 17:280. (Abstr.)
8. Colomo, F., N. Piroddi, C. Poggesi, and C. Tesi. 1995. Myofibrillar contribution to passive tension in striated muscle. Biophys. J. 68:344S. (Abstr.)
9. Conibear, P. B., and C. R. Bagshaw. 1996. Measurement of nucleotide exchange kinetics with isolated synthetic myosin filaments using flash photolysis. FEBS Lett. 380:13-16.
10. Conibear, P. B., D. S. Jeffreys, C. K. Seehra, R. J. Eaton, and C. R. Bagshaw. 1996. Kinetic and spectroscopic characterization of fluorescent ribose-modified ATP analogs upon interaction with skeletal muscle myosin subfragment 1. Biochemistry. 35:2299-2308.
11. Conibear, P. B., C. K. Seehra, C. R. Bagshaw, and D. Gingell. 1995. Observation of ATP turnover during in vitro motility assays. Biochem. Soc. Trans. (Lond.). 23:4005. (Abstr.)
12. Cooke, R. 1986. The mechanism of muscle contraction. CRC Crit. Rev. Biochem. 21:53-118.
13. Cooke, R., and W. Bialek. 1979. Contraction of glycerinated muscle fibers as a function of MgATP concentration. Biophys. J. 28:241-258.
14. Cooke, R., K. Franks, G. B. Luciani, and E. Pate. 1988. The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J. Physiol. (Lond.). 398:77-97.
15. Cooke, R., H. White, and E. Pate. 1994. A model of the release of myosin heads from actin in rapidly contracting muscle fibers. Biophys. J. 66: 778-788.
16. Cremo, C. R., J. M. Neuron, and R. G. Yount. 1990. Interaction of myosin subfragment 1 with fluorescent ribose-modified nucleotides: a comparison of vanadate trapping and SH1-SH2 cross-linking. Biochemistry. 29:3309-3319.
17. Eccleston, J. F., K. Oiwa, M. A. Ferenczi, M. Anson, J. E. T. Corrie, A. Yamada, H. Nakayama, and D. R. Trentham. 1996. Ribose-linked sulfoindocyanine conjugates of ATP: Cy3-EDA-ATP and Cy5-EDA-ATP. Biophys. J. 70:A159.
18. Fenn, W. O. 1923. A quantitative comparison between the energy liberated and the work performed by the isolated sartorius muscle of the frog. J. Physiol. (Lond.). 58:175-203.
19. Fenn, W. O. 1924. The relation between the work performed and the energy liberated in muscular contraction. J. Physiol. (Lond.). 58: 373-395.
20. Ferenczi, M. A., S. K. A. Woodward, and J. F. Eccleston. 1989. The rate of Mant-ADP release from cross-bridges of single skeletal muscle fibers. Biophys. J. 55:441a.
21. 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.
22. Ford, L. E., A. F. Huxley, and R. M. Simmons. 1977. Tension responses to sudden length changes in stimulated frog muscle fibres near slack length. J. Physiol. (Lond.). 269:441-515.
23. Friedman, A. L., and Y. E. Goldman. 1996. Mechanical characterization of skeletal muscle myofibrils. Biophys. J. 71:2774-2785.
24. Funatsu, T., Y. Harada, M. Tokunaga, K. Saito, and T. Yanagida. 1995. Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature. 374:555-559.
25. Glyn, H., and J. Sleep. 1985. Dependence of adenosine triphosphatase activity of rabbit psoas muscle fibers and myofibrils on substrate concentration. J. Physiol. (Lond.). 365:259-276.
26. Goldman, Y. E. 1987. Kinetics of the actomyosin ATPase in muscle fibers. Annu. Rev. Physiol. 49:637-654.
27. Herrmann, C., C. Lionne, F. Travers, and T. Barman. 1994. Correlation of actoS1, myofibrillar, and muscle fiber ATPases. Biochemistry. 33: 4148-4154.
28. Herrmann, C., J. Sleep, P. Chaussepied, F. Travers, and T. Barman. 1993. A structural and kinetic study on myofibrils prevented from shortening by chemical cross-linking. Biochemistry. 32:7255-7263.
29. Hibberd, M. G., and D. R. Trentham. 1986. Relationship between chemical and mechanical events during muscular contraction. Annu. Rev. Biophys. Biophys. Chem. 15:119-161.
30. Hill, A. V. 1964. The effect of load on the heat of shortening of muscle. Proc. R. Soc. Lond. B Biol. Sci. 159:297-318.
31. Hiratsuka, T. 1983. New ribose-modified fluorescent analogs of adenine and guanine nucleotides available as substrates for various enzymes. Biochem. Biophys. Acta. 742:496-508.
32. Homsher, E. 1987. Muscle enthalpy production and its relationship to actomyosin ATPase. Annu. Rev. Physiol. 49:673-690.
33. Homsher, E., M. Irving, and A. Wallner. 1981. High-energy phosphate metabolism and energy liberation associated with rapid shortening in frog skeletal muscle. J. Physiol. (Lond.). 321:423-436.
34. 2+-activated myofibrillar ATPase: transient kinetics and the titration of its active sites. Biochemistry. 31:1564-1569.
35. Huxley, A. F. 1957. Muscle structure and theories of contraction. Prog. Biophys. Biophys. Chem. 7:255-318.
36. Huxley, A. F. 1973. A note suggesting that the cross-bridge attachment during muscle contraction may take place in two stages. Proc. R. Soc. Lond. B. 183:83-86.
37. Kushmerick, M. J., and R. E. Davies. 1969. The chemical energetics of muscle contraction. II. The chemistry, efficiency and power of maximally working sartorius muscles. Proc. R. Soc. Lond. B Biol. Sci. 174:315-353.
38. Lionne, C. M. Brune, M. R. Webb, F. Travers, and T. Barman. 1995. Time resolved measurements show that phosphate release is the rate limiting step on myofibrillar ATPases. FEBS Lett. 364:59-62.
39. Lionne, C., F. Travers, and T. Barman. 1996. Mechanochemical coupling in muscle: attempts to measure simultaneously shortening and ATPase rates in myofibrils. Biophys. J. 70:887-895.
40. Ma, Y.-Z., and E. W. Taylor. 1994. Kinetic mechanism of myofibril ATPase. Biophys. J. 66:1542-1553.
41. Mujumdar, R. B., L. A. Ernst, S. R. Mujumdar, C. J. Lewis, and A. S. Waggoner. 1993. Cyanine dye labeling reagent: sulphoindocyanine succinimidyl esters. Bioconj. Chem. 4:105-111.
42. Myburgh, K. H., K. Franks-Siba, and R. Cooke. 1995. Nucleotide turnover rate measured in fully relaxed rabbit skeletal muscle myofibrils. J. Gen. Physiol. 106:957-973.
43. Ohno, T., and T. Kodama. 1991. Kinetics of adenosine triphosphate hydrolysis by shortening myofibrils from rabbit psoas muscle. J. Physiol. (Lond.). 441:685-702.
44. Oiwa, K., M. Anson, A. Yamada, J. F. Eccleston, J. E. T. Corrie, M. A. Ferenczi, D. R. Trentham, and H. Nakayama. 1996. Microscopic observations of Cy3-EDA-ATP and Cy5-EDA-ATP binding to myosin filaments in vitro. Biophys. J. 70:A159.
45. Rall, J. A., E. Homsher, A. Wallner, and W. F. H. M. Mommaerts. 1976. A temporal dissociation of energy liberation and high energy phosphate splitting during shortening in frog skeletal muscles. J. Gen. Physiol. 68:13-27.
46. Saito, K., M. Tokunaga, H. Yokota, and T. Yanagida. 1995. ATPase reaction during sliding of actin filaments. Biophysics (Jpn. Biophys. Soc.). 35:S208. (Abstr.)
47. Siemankowski, R. F., M. O. Wiseman, and H. D. White. 1995. ADP dissociation from actomyosin subfragment1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc. Natl. Acad. Sci. USA. 82:628-662.
48. Sleep, J. A. 1981. Single turnovers of adenosine 5′-triphosphate by myofibrils and actomyosin subfragment 1. Biochemistry. 20:5043-5051.
49. Sowerby, A. J., C. K. Seehra, M. Lee, and C. R. Bagshaw. 1993. Turnover of fluorescent nucleotide triphosphates by isolated immobilized myosin filaments. Transient kinetics on the zeptomole scale. J. Mol. Biol. 243:114-123.
50. Sugi, H. 1992. Molecular mechanism of actin-myosin interaction in muscle contraction. In Muscle Contraction and Cell Motility: Molecular and Cellular Aspects. H. Sugi, editor. Springer-Verlag, Berlin and Heidelberg. 132-171.
51. Sugi, H. 1997. Muscle mechanics I and II. In Current Methods in Muscle Physiology: Advantages, Problems and Limitations. H. Sugi, editor. Oxford University Press, Oxford. In press.
52. Taylor, E. W. 1979. Mechanism of actomyosin ATPase and the problem of muscle contraction. CRC Crit. Rev. Biochem. 6:103-164.
53. Thirwell, 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.
54. Warshaw, D. M., J. M. Desrosiers, S. S. Work, and K. M. Trybus. 1990. Smooth muscle myosin cross-bridge interactions modulate actin filament sliding in vitro. J. Cell. Biol. 111:453-463.
55. Woodward, S. K. A., J. F. Eccleston, and M. A. Geeves. 1991. Kinetics of the interaction of 2′(3′)-O-(N-methylanthraniloyl)-ATP with myosin subfragment 1 and actomyosin subfragment 1: characterization of two actoS1ADP complexes. Biochemistry. 30:422-430.
56. Yamada, T., O. Abe, T. Kobayashi, and H. Sugi. 1993. Myofilament sliding per ATP molecule in rabbit skeletal fibres using laser flash photolysis of caged ATP. J. Physiol. (Lond.). 466:229-243.