Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Sep;75(3):1439–1445. doi: 10.1016/S0006-3495(98)74062-7

Spontaneous oscillatory contraction without regulatory proteins in actin filament-reconstituted fibers.

H Fujita 1, S Ishiwata 1
PMCID: PMC1299818  PMID: 9726945

Abstract

Skinned skeletal and cardiac muscle fibers exhibits spontaneous oscillatory contraction (SPOC) in the presence of MgATP, MgADP, and inorganic phosphate (Pi)1 but the molecular mechanism underlying this phenomenon is not yet clear. We have investigated the role of regulatory proteins in SPOC using cardiac muscle fibers of which the actin filaments had been reconstituted without tropomyosin and troponin, according to a previously reported method (Fujita et al., 1996. Biophys. J. 71:2307-2318). That is, thin filaments in glycerinated cardiac muscle fibers were selectively removed by treatment with gelsolin. Then, by adding exogenous actin to these thin filament-free cardiac muscle fibers under polymerizing conditions, actin filaments were reconstituted. The actin filament-reconstituted cardiac muscle fibers generated active tension in a Ca(2+)-insensitive manner because of the lack of regulatory proteins. Herein we have developed a new solvent condition under which SPOC occurs, even in actin filament-reconstituted fibers: the coexistence of 2,3-butanedione 2-monoxime (BDM), a reversible inhibitor of actomyosin interactions, with MgATP, MgADP and Pi. The role of BDM in the mechanism of SPOC in the actin filament-reconstituted fibers was analogous to that of the inhibitory function of the tropomyosin-troponin complex (-Ca2+) in the control fibers. The present results suggest that SPOC is a phenomenon that is intrinsic to the actomyosin motor itself.

Full Text

The Full Text of this article is available as a PDF (162.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anazawa T., Yasuda K., Ishiwata S. Spontaneous oscillation of tension and sarcomere length in skeletal myofibrils. Microscopic measurement and analysis. Biophys J. 1992 May;61(5):1099–1108. doi: 10.1016/S0006-3495(92)81919-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cooke R., Pate E. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J. 1985 Nov;48(5):789–798. doi: 10.1016/S0006-3495(85)83837-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dantzig J. A., Goldman Y. E., Millar N. C., Lacktis J., Homsher E. Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J Physiol. 1992;451:247–278. doi: 10.1113/jphysiol.1992.sp019163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ebashi S., Endo M. Calcium ion and muscle contraction. Prog Biophys Mol Biol. 1968;18:123–183. doi: 10.1016/0079-6107(68)90023-0. [DOI] [PubMed] [Google Scholar]
  5. Fabiato A., Fabiato F. Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere length-tension relation of skinned cardiac cells. J Gen Physiol. 1978 Nov;72(5):667–699. doi: 10.1085/jgp.72.5.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fujita H., Yasuda K., Niitsu S., Funatsu T., Ishiwata S. Structural and functional reconstitution of thin filaments in the contractile apparatus of cardiac muscle. Biophys J. 1996 Nov;71(5):2307–2318. doi: 10.1016/S0006-3495(96)79465-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fukuda N., Fujita H., Fujita T., Ishiwata S. Spontaneous tension oscillation in skinned bovine cardiac muscle. Pflugers Arch. 1996 Nov-Dec;433(1-2):1–8. doi: 10.1007/s004240050241. [DOI] [PubMed] [Google Scholar]
  8. Funatsu T., Higuchi H., Ishiwata S. Elastic filaments in skeletal muscle revealed by selective removal of thin filaments with plasma gelsolin. J Cell Biol. 1990 Jan;110(1):53–62. doi: 10.1083/jcb.110.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Funatsu T., Kono E., Higuchi H., Kimura S., Ishiwata S., Yoshioka T., Maruyama K., Tsukita S. Elastic filaments in situ in cardiac muscle: deep-etch replica analysis in combination with selective removal of actin and myosin filaments. J Cell Biol. 1993 Feb;120(3):711–724. doi: 10.1083/jcb.120.3.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Greene L. E., Eisenberg E. Cooperative binding of myosin subfragment-1 to the actin-troponin-tropomyosin complex. Proc Natl Acad Sci U S A. 1980 May;77(5):2616–2620. doi: 10.1073/pnas.77.5.2616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Higuchi H., Takemori S. Butanedione monoxime suppresses contraction and ATPase activity of rabbit skeletal muscle. J Biochem. 1989 Apr;105(4):638–643. doi: 10.1093/oxfordjournals.jbchem.a122717. [DOI] [PubMed] [Google Scholar]
  12. Horiuti K., Higuchi H., Umazume Y., Konishi M., Okazaki O., Kurihara S. Mechanism of action of 2, 3-butanedione 2-monoxime on contraction of frog skeletal muscle fibres. J Muscle Res Cell Motil. 1988 Apr;9(2):156–164. doi: 10.1007/BF01773737. [DOI] [PubMed] [Google Scholar]
  13. Horiuti K. Some properties of the contractile system and sarcoplasmic reticulum of skinned slow fibres from Xenopus muscle. J Physiol. 1986 Apr;373:1–23. doi: 10.1113/jphysiol.1986.sp016032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ishiwata S., Anazawa T., Fujita T., Fukuda N., Shimizu H., Yasuda K. Spontaneous tension oscillation (SPOC) of muscle fibers and myofibrils minimum requirements for SPOC. Adv Exp Med Biol. 1993;332:545–556. doi: 10.1007/978-1-4615-2872-2_49. [DOI] [PubMed] [Google Scholar]
  15. Ishiwata S., Okamura N., Shimizu H., Anazawa T., Yasuda K. Spontaneous oscillatory contraction (SPOC) of sarcomeres in skeletal muscle. Adv Biophys. 1991;27:227–235. doi: 10.1016/0065-227x(91)90022-6. [DOI] [PubMed] [Google Scholar]
  16. Iwazumi T., Pollack G. H. The effect of sarcomere non-uniformity on the sarcomere length-tension relationship of skinned fibers. J Cell Physiol. 1981 Mar;106(3):321–337. doi: 10.1002/jcp.1041060302. [DOI] [PubMed] [Google Scholar]
  17. Kawai M. The role of orthophosphate in crossbridge kinetics in chemically skinned rabbit psoas fibres as detected with sinusoidal and step length alterations. J Muscle Res Cell Motil. 1986 Oct;7(5):421–434. doi: 10.1007/BF01753585. [DOI] [PubMed] [Google Scholar]
  18. Kondo H., Ishiwata S. Uni-directional growth of F-actin. J Biochem. 1976 Jan;79(1):159–171. doi: 10.1093/oxfordjournals.jbchem.a131043. [DOI] [PubMed] [Google Scholar]
  19. Kurokawa H., Fujii W., Ohmi K., Sakurai T., Nonomura Y. Simple and rapid purification of brevin. Biochem Biophys Res Commun. 1990 Apr 30;168(2):451–457. doi: 10.1016/0006-291x(90)92342-w. [DOI] [PubMed] [Google Scholar]
  20. Li T., Sperelakis N., Teneick R. E., Solaro R. J. Effects of diacetyl monoxime on cardiac excitation-contraction coupling. J Pharmacol Exp Ther. 1985 Mar;232(3):688–695. [PubMed] [Google Scholar]
  21. Linke W. A., Bartoo M. L., Pollack G. H. Spontaneous sarcomeric oscillations at intermediate activation levels in single isolated cardiac myofibrils. Circ Res. 1993 Oct;73(4):724–734. doi: 10.1161/01.res.73.4.724. [DOI] [PubMed] [Google Scholar]
  22. McKillop D. F., Fortune N. S., Ranatunga K. W., Geeves M. A. The influence of 2,3-butanedione 2-monoxime (BDM) on the interaction between actin and myosin in solution and in skinned muscle fibres. J Muscle Res Cell Motil. 1994 Jun;15(3):309–318. doi: 10.1007/BF00123483. [DOI] [PubMed] [Google Scholar]
  23. Okamura N., Ishiwata S. Spontaneous oscillatory contraction of sarcomeres in skeletal myofibrils. J Muscle Res Cell Motil. 1988 Apr;9(2):111–119. doi: 10.1007/BF01773733. [DOI] [PubMed] [Google Scholar]
  24. Seow C. Y., Ford L. E. Exchange of ATP for ADP on high-force cross-bridges of skinned rabbit muscle fibers. Biophys J. 1997 Jun;72(6):2719–2735. doi: 10.1016/S0006-3495(97)78915-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shimizu H., Fujita T., Ishiwata S. Regulation of tension development by MgADP and Pi without Ca2+. Role in spontaneous tension oscillation of skeletal muscle. Biophys J. 1992 May;61(5):1087–1098. doi: 10.1016/S0006-3495(92)81918-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Spudich J. A., Watt S. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem. 1971 Aug 10;246(15):4866–4871. [PubMed] [Google Scholar]
  27. Stephenson D. G., Williams D. A. Calcium-activated force responses in fast- and slow-twitch skinned muscle fibres of the rat at different temperatures. J Physiol. 1981 Aug;317:281–302. doi: 10.1113/jphysiol.1981.sp013825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Swartz D. R., Moss R. L., Greaser M. L. Calcium alone does not fully activate the thin filament for S1 binding to rigor myofibrils. Biophys J. 1996 Oct;71(4):1891–1904. doi: 10.1016/S0006-3495(96)79388-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sweitzer N. K., Moss R. L. The effect of altered temperature on Ca2(+)-sensitive force in permeabilized myocardium and skeletal muscle. Evidence for force dependence of thin filament activation. J Gen Physiol. 1990 Dec;96(6):1221–1245. doi: 10.1085/jgp.96.6.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Weber A., Murray J. M. Molecular control mechanisms in muscle contraction. Physiol Rev. 1973 Jul;53(3):612–673. doi: 10.1152/physrev.1973.53.3.612. [DOI] [PubMed] [Google Scholar]
  31. Yasuda K., Anazawa T., Ishiwata S. Microscopic analysis of the elastic properties of nebulin in skeletal myofibrils. Biophys J. 1995 Feb;68(2):598–608. doi: 10.1016/S0006-3495(95)80221-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yasuda K., Shindo Y., Ishiwata S. Synchronous behavior of spontaneous oscillations of sarcomeres in skeletal myofibrils under isotonic conditions. Biophys J. 1996 Apr;70(4):1823–1829. doi: 10.1016/S0006-3495(96)79747-3. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES