About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 486021, 7 pages
http://dx.doi.org/10.1155/2011/486021
Review Article

Thin Filament-Reconstituted Skinned Muscle Fibers for the Study of Muscle Physiology

1Laboratory for Comprehensive Bioimaging, Riken Quantitative Biology Center, OLABB, 6-2-3 Furuedai, Suita, Osaka 565-0874, Japan
2Department of Cell Physiology, The Jikei University School of Medicine, Tokyo 105-8461, Japan

Received 21 July 2011; Accepted 12 August 2011

Academic Editor: Henk Granzier

Copyright © 2011 Sayaka Higuchi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. F. Huxley and R. Niedergerke, “Structural changes in muscle during contraction: interference microscopy of living muscle fibres,” Nature, vol. 173, no. 4412, pp. 971–973, 1954. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Huxley and J. Hanson, “Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation,” Nature, vol. 173, no. 4412, pp. 973–976, 1954. View at Publisher · View at Google Scholar · View at Scopus
  3. A. M. Gordon, M. A. LaMadrid, Y. Chen, Z. Luo, and P. B. Chase, “Calcium regulation of skeletal muscle thin filament motility in vitro,” Biophysical Journal, vol. 72, no. 3, pp. 1295–1307, 1997. View at Scopus
  4. E. Homsher, D. M. Lee, C. Morris, D. Pavlov, and L. S. Tobacman, “Regulation of force and unloaded sliding speed in single thin filaments: effects of regulatory proteins and calcium,” Journal of Physiology, vol. 524, no. 1, pp. 233–243, 2000. View at Scopus
  5. R. Niederman and T. D. Pollard, “Human platelet myosin. II. In vitro assembly and structure of myosin filaments,” Journal of Cell Biology, vol. 67, no. 1, pp. 72–92, 1975. View at Scopus
  6. A. Ishijima, Y. Harada, H. Kojima, T. Funatsu, H. Higuchi, and T. Yanagida, “Single-molecule analysis of the actomyosin motor using nano-manipulation,” Biochemical and Biophysical Research Communications, vol. 199, no. 2, pp. 1057–1063, 1994. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. M. Kaya and H. Higuchi, “Nonlinear elasticity and an 8-nm working stroke of single myosin molecules in myofilaments,” Science, vol. 329, no. 5992, pp. 686–689, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. M. Suzuki, H. Fujita, and S. Ishiwata, “A new muscle contractile system composed of a thick filament lattice and a single actin filament,” Biophysical Journal, vol. 89, no. 1, pp. 321–328, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. M. Hatakenaka and I. Ohtsuki, “Effect of removal and reconstitution of troponins C and I on the 2+-activated tension development of single glycerinated rabbit skeletal muscle fibers,” European Journal of Biochemistry, vol. 205, no. 3, pp. 985–993, 1992. View at Scopus
  10. F. Shiraishi, M. Kambara, and I. Ohtsuki, “Replacement of troponin components in myofibrils,” Journal of Biochemistry, vol. 111, no. 1, pp. 61–65, 1992. View at Scopus
  11. J. M. Metzger and R. L. Moss, “Myosin light chain 2 modulates calcium-sensitive cross-bridge transitions in vertebrate skeletal muscle,” Biophysical Journal, vol. 63, no. 2, pp. 460–468, 1992. View at Scopus
  12. S. Lowey, G. S. Waller, and K. M. Trybus, “Skeletal muscle myosin light chains are essential for physiological speeds of shortening,” Nature, vol. 365, no. 6445, pp. 454–456, 1993. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. H. Higuchi and S. Ishiwata, “Disassembly kinetics of thick filaments in rabbit skeletal muscle fibers. Effects of ionic strength, 2+ concentration, pH, temperature, and cross-bridges on the stability of thick filament structure,” Biophysical Journal, vol. 47, no. 3, pp. 267–275, 1985. View at Scopus
  14. T. Funatsu, H. Higuchi, and S. Ishiwata, “Elastic filaments in skeletal muscle revealed by selective removal of thin filaments with plasma gelsolin,” Journal of Cell Biology, vol. 110, no. 1, pp. 53–62, 1990. View at Publisher · View at Google Scholar · View at Scopus
  15. H. L. M. Granzier and K. Wang, “Interplay between passive tension and strong and weak binding cross-bridges in insect indirect flight muscle: a functional dissection by gelsolin-mediated thin filament removal,” Journal of General Physiology, vol. 101, no. 2, pp. 235–270, 1993. View at Scopus
  16. T. Funatsu, E. Kono, H. Higuchi et al., “Elastic filaments in situ in cardiac muscle: deep-etch replica analysis in combination with selective removal of actin and myosin filaments,” Journal of Cell Biology, vol. 120, no. 3, pp. 711–724, 1993. View at Publisher · View at Google Scholar · View at Scopus
  17. H. L. M. Granzier and K. Wang, “Passive tension and stiffness of vertebrate skeletal and insect flight muscles: the contribution of weak cross-bridges and elastic filaments,” Biophysical Journal, vol. 65, no. 5, pp. 2141–2159, 1993. View at Scopus
  18. T. Funatsu, T. Anazawa, and S. Ishiwata, “Structural and functional reconstruction of thin filaments in skeletal muscle,” Journal of Muscle Research and Cell Motility, vol. 15, no. 2, pp. 158–171, 1994. View at Scopus
  19. H. Fujita, K. Yasuda, S. Niitsu, T. Funatsu, and S. Ishiwata, “Structural and functional reconstitution of thin filaments in the contractile apparatus of cardiac muscle,” Biophysical Journal, vol. 71, no. 5, pp. 2307–2318, 1996. View at Scopus
  20. T. F. Robinson and S. Winegrad, “Variation of thin filament length in heart muscle,” Nature, vol. 267, no. 5606, pp. 74–75, 1977. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Kawai and S. Ishiwata, “Use of thin filament reconstituted muscle fibres to probe the mechanism of force generation,” Journal of Muscle Research and Cell Motility, vol. 27, no. 5–7, pp. 455–468, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. D. W. Maughan and R. E. Godt, “A quantitative analysis of elastic, entropic, electrostatic, and osmotic forces within relaxed skinned muscle fibers,” Biophysics of Structure and Mechanism, vol. 7, no. 1, pp. 17–40, 1980.
  23. M. J. Dawson, D. G. Gadian, and D. R. Wilkie, “Muscular fatigue investigated by phosphorus nuclear magnetic resonance,” Nature, vol. 274, no. 5674, pp. 861–866, 1978. View at Scopus
  24. K. A. P. Edman and A. R. Mattiazzi, “Effects of fatigue and altered pH on isometric force and velocity of shortening at zero load in frog muscle fibres,” Journal of Muscle Research and Cell Motility, vol. 2, no. 3, pp. 321–334, 1981. View at Scopus
  25. H. Fujita and S. Ishiwata, “Tropomyosin modulates pH dependence of isometric tension,” Biophysical Journal, vol. 77, no. 3, pp. 1540–1546, 1999. View at Scopus
  26. S. P. Robertson and W. G. Kerrick, “The effects of pH on 2+-activated force in frog skeletal muscle fibers,” Pflugers Archiv European Journal of Physiology, vol. 380, no. 1, pp. 41–45, 1979. View at Scopus
  27. P. B. Chase and M. J. Kushmerick, “Effects of pH on contraction of rabbit fast and slow skeletal muscle fibers,” Biophysical Journal, vol. 53, no. 6, pp. 935–946, 1988. View at Scopus
  28. K. W. Ranatunga, “Endothermic force generation in skinned cardiac muscle from rat,” Journal of Muscle Research and Cell Motility, vol. 20, no. 5-6, pp. 489–496, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. E. Goldman, J. A. McCray, and K. W. Ranatunga, “Transient tension changes initiated by laser temperature jumps in rabbit psoas muscle fibres,” Journal of Physiology, vol. 392, pp. 71–95, 1987. View at Scopus
  30. H. Fujita and M. Kawai, “Temperature effect on isometric tension is mediated by regulatory proteins tropomyosin and troponin in bovine myocardium,” Journal of Physiology, vol. 539, part 1, pp. 267–276, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Fukuda, H. Fujita, T. Fujita, and S. Ishiwata, “Spontaneous tension oscillation in skinned bovine cardiac muscle,” Pflugers Archiv European Journal of Physiology, vol. 433, no. 1-2, pp. 1–8, 1996. View at Publisher · View at Google Scholar
  32. H. Fujita and S. Ishiwata, “Spontaneous oscillatory contraction without regulatory proteins in actin filament-reconstituted fibers,” Biophysical Journal, vol. 75, no. 3, pp. 1439–1445, 1998.
  33. K. Sato, M. Ohtaki, Y. Shimamoto, and S. Ishiwata, “A theory on auto-oscillation and contraction in striated muscle,” Progress in Biophysics and Molecular Biology, vol. 105, no. 3, pp. 199–207, 2011. View at Publisher · View at Google Scholar · View at PubMed
  34. N. S. Fortune, M. A. Geeves, and K. W. Ranatunga, “Contractile activation and force generation in skinned rabbit muscle fibres: effects of hydrostatic pressure,” Journal of Physiology, vol. 474, no. 2, pp. 283–290, 1994.
  35. J. A. Dantzig, Y. E. Goldman, N. C. Millar, J. Lacktis, and E. Homsher, “Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres,” Journal of Physiology, vol. 451, pp. 247–278, 1992.
  36. E. Homsher and N. C. Millar, “Caged compounds and striated muscle contraction,” Annual Review of Physiology, vol. 52, pp. 875–896, 1990.
  37. K. Horiuti, K. Kagawa, and K. Yamada, “Transient contraction of muscle fibers on photorelease of ATP at intermediate concentrations of 2+,” Biophysical Journal, vol. 67, no. 5, pp. 1925–1932, 1994.
  38. J. A. Dantzig, M. G. Hibberd, D. R. Trentham, and Y. E. Goldman, “Cross-bridge kinetics in the presence of MgADP investigated by photolysis of caged ATP in rabbit psoas muscle fibres,” Journal of Physiology, vol. 432, pp. 639–680, 1991.
  39. G. Piazzesi, F. Francini, M. Linari, and V. Lombardi, “Tension transients during steady lengthening of tetanized muscle fibres of the frog,” Journal of Physiology, vol. 445, pp. 659–711, 1992.
  40. G. Piazzesi, M. Linari, M. Reconditi, F. Vanzi, and V. Lombardi, “Cross-bridge detachment and attachment following a step stretch imposed on active single frog muscle fibres,” Journal of Physiology, vol. 498, no. 2, part 1, pp. 3–15, 1997.
  41. M. Linari, V. Lombardi, and G. Piazzesi, “Cross-bridge kinetics studied with staircase shortening in single fibres from frog skeletal muscle,” Journal of Muscle Research and Cell Motility, vol. 18, no. 1, pp. 91–101, 1997. View at Publisher · View at Google Scholar
  42. H. Fujita, D. Sasaki, S. Ishiwata, and M. Kawai, “Elementary steps of the cross-bridge cycle in bovine myocardium with and without regulatory proteins,” Biophysical Journal, vol. 82, no. 2, pp. 915–928, 2002.
  43. H. Fujita, X. Lu, M. Suzuki, S. Ishiwata, and M. Kawai, “The effect of tropomyosin on force and elementary steps of the cross-bridge cycle in reconstituted bovine myocardium,” Journal of Physiology, vol. 556, part 2, pp. 637–649, 2004. View at Publisher · View at Google Scholar · View at PubMed
  44. M. Kawai and H. R. Halvorson, “Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned fibers of rabbit psoas muscle,” Biophysical Journal, vol. 59, no. 2 I, pp. 329–342, 1991.
  45. X. Lu, M. K. Bryant, K. E. Bryan, P. A. Rubenstein, and M. Kawai, “Role of the N-terminal negative charges of actin in force generation and cross-bridge kinetics in reconstituted bovine cardiac muscle fibres,” Journal of Physiology, vol. 564, part 1, pp. 65–82, 2005. View at Publisher · View at Google Scholar · View at PubMed
  46. A. D. McLachlan and M. Stewart, “The 14 fold periodicity in α tropomyosin and the interaction with actin,” Journal of Molecular Biology, vol. 103, no. 2, pp. 271–293, 1976.
  47. M. Kawai, X. Lu, S. E. Hitchcock-Degregori, et al., “Tropomyosin period 3 is essential for enhancement of isometric tension in thin filament-reconstituted bovine myocardium,” Journal of Biophysics, vol. 2009, Article ID 380967, 17 pages, 2009. View at Publisher · View at Google Scholar · View at PubMed
  48. F. Bai, A. Weis, A. K. Takeda, et al., “Enhanced active cross-bridges during diastole: molecular pathogenesis of tropomyosin's HCM mutations,” Biophysical Journal, vol. 10, no. 4, pp. 1013–1023, 2011.
  49. X. Lu, D. H. Heeley, L. B. Smillie, and M. Kawai, “The role of tropomyosin isoforms and phosphorylation in force generation in thin-filament reconstituted bovine cardiac muscle fibres,” Journal of Muscle Research and Cell Motility, vol. 31, no. 2, pp. 93–109, 2010. View at Publisher · View at Google Scholar · View at PubMed
  50. S. Labeit and B. Kolmerer, “Titins: giant proteins in charge of muscle ultrastructure and elasticity,” Science, vol. 270, no. 5234, pp. 293–296, 1995.
  51. R. Horowits, E. S. Kempner, M. E. Bisher, and R. J. Podolsky, “A physiological role for titin and nebulin in skeletal muscle,” Nature, vol. 323, no. 6084, pp. 160–164, 1986.
  52. H. Fujita, D. Labeit, B. Gerull, S. Labeit, and H. L. Granzier, “Titin isoform-dependent effect of calcium on passive myocardial tension,” American Journal of Physiology, vol. 287, no. 6, pp. H2528–H2534, 2004. View at Publisher · View at Google Scholar · View at PubMed
  53. D. Labeit, K. Watanabe, C. Witt et al., “Calcium-dependent molecular spring elements in the giant protein titin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 23, pp. 13716–13721, 2003. View at Publisher · View at Google Scholar · View at PubMed