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. 1988 Dec;407:231–241. doi: 10.1113/jphysiol.1988.sp017412

Time-resolved X-ray diffraction studies on the effect of slow length changes on tetanized frog skeletal muscle.

Y Amemiya 1, H Iwamoto 1, T Kobayashi 1, H Sugi 1, H Tanaka 1, K Wakabayashi 1
PMCID: PMC1191200  PMID: 3267188

Abstract

1. The mechanism of the enhancement and the deficit of isometric force by slow length changes in frog skeletal muscle was studied with the time-resolved X-ray diffraction technique, using intense X-rays of synchrotron radiation. 2. When a tetanized muscle was slowly stretched by 4% from sarcomere lengths 2.3-2.4 microns, the force rose to a peak during stretch and then decreased to a steady level 10-15% higher than that immediately before stretch. 3. The intensity of the 1,1 equatorial reflection decreased nearly linearly during stretch and then again increased after the completion of stretch, reaching a steady level 12 +/- 5% (mean +/- S.D., n = 11) lower than that immediately before stretch. The above 1,1 intensity change was roughly a mirror image of the force change. 4. The intensity of the 1,0 equatorial reflection showed no marked changes in response to a slow stretch, except for an initial transient increase observed occasionally. 5. If a tetanized muscle was slowly released by 4% from sarcomere lengths 2.3-2.4 microns, the steady force attained after the completion of release was lower than that immediately before release. 6. The 1,1 intensity increased slightly during release, while the 1,0 intensity did not change significantly. 7. The half-width of both the 1,0 and the 1,1 reflections did not change appreciably in response to slow length changes. 8. Slow length changes always produced changes in the spacing between the reflections as expected from the constant-volume behaviour of the myofilament lattice. 9. These results indicate that a slow stretch produces disordering of the myofilament lattice in such a way that the thin filaments are displaced from trigonal positions in the thick filament lattice. The resulting increase in the overall repulsion forces between the filaments may lead to the enhanced isometric force after stretch.

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Selected References

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

  1. ABBOTT B. C., AUBERT X. M. The force exerted by active striated muscle during and after change of length. J Physiol. 1952 May;117(1):77–86. [PMC free article] [PubMed] [Google Scholar]
  2. DELEZE J. B. The mechanical properties of the semitendinosus muscle at lengths greater than its length in the body. J Physiol. 1961 Sep;158:154–164. [PMC free article] [PubMed] [Google Scholar]
  3. Edman K. A., Elzinga G., Noble M. I. Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J Physiol. 1978 Aug;281:139–155. doi: 10.1113/jphysiol.1978.sp012413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Edman K. A. The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol. 1979 Jun;291:143–159. doi: 10.1113/jphysiol.1979.sp012804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Elliott G. F., Lowy J., Millman B. M. Low-angle x-ray diffraction studies of living striated muscle during contraction. J Mol Biol. 1967 Apr 14;25(1):31–45. doi: 10.1016/0022-2836(67)90277-x. [DOI] [PubMed] [Google Scholar]
  6. HUXLEY H. E. X-ray analysis and the problem of muscle. Proc R Soc Lond B Biol Sci. 1953 Mar 11;141(902):59–62. doi: 10.1098/rspb.1953.0017. [DOI] [PubMed] [Google Scholar]
  7. Haselgrove J. C., Huxley H. E. X-ray evidence for radial cross-bridge movement and for the sliding filament model in actively contracting skeletal muscle. J Mol Biol. 1973 Jul 15;77(4):549–568. doi: 10.1016/0022-2836(73)90222-2. [DOI] [PubMed] [Google Scholar]
  8. Huxley H. E. Structural difference between resting and rigor muscle; evidence from intensity changes in the lowangle equatorial x-ray diagram. J Mol Biol. 1968 Nov 14;37(3):507–520. doi: 10.1016/0022-2836(68)90118-6. [DOI] [PubMed] [Google Scholar]
  9. Julian F. J., Sollins M. R. Variation of muscle stiffness with force at increasing speeds of shortening. J Gen Physiol. 1975 Sep;66(3):287–302. doi: 10.1085/jgp.66.3.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Maréchal G., Plaghki L. The deficit of the isometric tetanic tension redeveloped after a release of frog muscle at a constant velocity. J Gen Physiol. 1979 Apr;73(4):453–467. doi: 10.1085/jgp.73.4.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Matsubara I., Elliott G. F. X-ray diffraction studies on skinned single fibres of frog skeletal muscle. J Mol Biol. 1972 Dec 30;72(3):657–669. doi: 10.1016/0022-2836(72)90183-0. [DOI] [PubMed] [Google Scholar]
  12. Matsubara I., Yagi N. Movements of cross-bridges during and after slow length changes in active frog skeletal muscle. J Physiol. 1985 Apr;361:151–163. doi: 10.1113/jphysiol.1985.sp015638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Matsuda T., Podolsky R. J. Ordering of the myofilament lattice in muscle fibers. J Mol Biol. 1986 May 20;189(2):361–365. doi: 10.1016/0022-2836(86)90516-4. [DOI] [PubMed] [Google Scholar]
  14. Podolsky R. J., St Onge H., Yu L., Lymn R. W. X-ray diffraction of actively shortening muscle. Proc Natl Acad Sci U S A. 1976 Mar;73(3):813–817. doi: 10.1073/pnas.73.3.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Sugi H., Tsuchiya T. Enhancement of mechanical performance in frog muscle fibres after quick increases in load. J Physiol. 1981;319:239–252. doi: 10.1113/jphysiol.1981.sp013904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sugi H., Tsuchiya T. Stiffness changes during enhancement and deficit of isometric force by slow length changes in frog skeletal muscle fibres. J Physiol. 1988 Dec;407:215–229. doi: 10.1113/jphysiol.1988.sp017411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Tanaka H., Tanaka M., Sugi H. The effect of sarcomere length and stretching on the rate of ATP splitting in glycerinated rabbit psoas muscle fibers. J Biochem. 1979 Nov;86(5):1587–1593. doi: 10.1093/oxfordjournals.jbchem.a132676. [DOI] [PubMed] [Google Scholar]

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