Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2001 Mar;80(3):1429–1441. doi: 10.1016/S0006-3495(01)76115-2

Axial disposition of myosin heads in isometrically contracting muscles.

J Juanhuix 1, J Bordas 1, J Campmany 1, A Svensson 1, M L Bassford 1, T Narayanan 1
PMCID: PMC1301334  PMID: 11222303

Abstract

Meridional x-ray diffraction diagrams, recorded with high angular resolution, from muscles contracting at the plateau of isometric tension show that the myosin diffraction orders are clusters of peaks. These clusters are due to pronounced interference effects between the myosin diffracting units on either side of the M-line. A theoretical analysis based on the polarity of the myosin (and actin) filaments shows that it is possible to extract phase information from which the axial disposition of the myosin heads can be determined. The results show that each head in a crown pair has a distinct structural disposition. It appears that only one of the heads in the pair stereospecifically interacts with the thin filament at any one time.

Full Text

The Full Text of this article is available as a PDF (158.2 KB).

Selected References

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

  1. Bordas J., Diakun G. P., Diaz F. G., Harries J. E., Lewis R. A., Lowy J., Mant G. R., Martin-Fernandez M. L., Towns-Andrews E. Two-dimensional time-resolved X-ray diffraction studies of live isometrically contracting frog sartorius muscle. J Muscle Res Cell Motil. 1993 Jun;14(3):311–324. doi: 10.1007/BF00123096. [DOI] [PubMed] [Google Scholar]
  2. Bordas J., Lowy J., Svensson A., Harries J. E., Diakun G. P., Gandy J., Miles C., Mant G. R., Towns-Andrews E. X-ray evidence that in contracting live frog muscles there exist two distinct populations of myosin heads. Biophys J. 1995 Apr;68(4 Suppl):99S–105S. [PMC free article] [PubMed] [Google Scholar]
  3. Bordas J., Svensson A., Rothery M., Lowy J., Diakun G. P., Boesecke P. Extensibility and symmetry of actin filaments in contracting muscles. Biophys J. 1999 Dec;77(6):3197–3207. doi: 10.1016/S0006-3495(99)77150-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dobbie I., Linari M., Piazzesi G., Reconditi M., Koubassova N., Ferenczi M. A., Lombardi V., Irving M. Elastic bending and active tilting of myosin heads during muscle contraction. Nature. 1998 Nov 26;396(6709):383–387. doi: 10.1038/24647. [DOI] [PubMed] [Google Scholar]
  5. Díaz Baños F. G., Bordas J., Lowy J., Svensson A. Small segmental rearrangements in the myosin head can explain force generation in muscle. Biophys J. 1996 Aug;71(2):576–589. doi: 10.1016/S0006-3495(96)79292-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ford L. E., Huxley A. F., Simmons R. M. The relation between stiffness and filament overlap in stimulated frog muscle fibres. J Physiol. 1981 Feb;311:219–249. doi: 10.1113/jphysiol.1981.sp013582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Haselgrove J. C. X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle. J Mol Biol. 1975 Feb 15;92(1):113–143. doi: 10.1016/0022-2836(75)90094-7. [DOI] [PubMed] [Google Scholar]
  8. Holmes K. C. The swinging lever-arm hypothesis of muscle contraction. Curr Biol. 1997 Feb 1;7(2):R112–R118. doi: 10.1016/s0960-9822(06)00051-0. [DOI] [PubMed] [Google Scholar]
  9. Huxley A. F. Muscular contraction. J Physiol. 1974 Nov;243(1):1–43. [PMC free article] [PubMed] [Google Scholar]
  10. Huxley A. F., Tideswell S. Filament compliance and tension transients in muscle. J Muscle Res Cell Motil. 1996 Aug;17(4):507–511. doi: 10.1007/BF00123366. [DOI] [PubMed] [Google Scholar]
  11. Huxley A. F., Tideswell S. Rapid regeneration of power stroke in contracting muscle by attachment of second myosin head. J Muscle Res Cell Motil. 1997 Feb;18(1):111–114. doi: 10.1023/a:1018641218961. [DOI] [PubMed] [Google Scholar]
  12. Huxley H. E., Brown W. The low-angle x-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol. 1967 Dec 14;30(2):383–434. doi: 10.1016/s0022-2836(67)80046-9. [DOI] [PubMed] [Google Scholar]
  13. Huxley H. E., Faruqi A. R., Kress M., Bordas J., Koch M. H. Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction. J Mol Biol. 1982 Jul 15;158(4):637–684. doi: 10.1016/0022-2836(82)90253-4. [DOI] [PubMed] [Google Scholar]
  14. Huxley H. E., Simmons R. M., Faruqi A. R., Kress M., Bordas J., Koch M. H. Changes in the X-ray reflections from contracting muscle during rapid mechanical transients and their structural implications. J Mol Biol. 1983 Sep 15;169(2):469–506. doi: 10.1016/s0022-2836(83)80062-x. [DOI] [PubMed] [Google Scholar]
  15. Huxley H. E., Simmons R. M., Faruqi A. R., Kress M., Bordas J., Koch M. H. Millisecond time-resolved changes in x-ray reflections from contracting muscle during rapid mechanical transients, recorded using synchrotron radiation. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2297–2301. doi: 10.1073/pnas.78.4.2297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Huxley H. E., Stewart A., Sosa H., Irving T. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J. 1994 Dec;67(6):2411–2421. doi: 10.1016/S0006-3495(94)80728-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huxley H. E. The mechanism of muscular contraction. Science. 1969 Jun 20;164(3886):1356–1365. doi: 10.1126/science.164.3886.1356. [DOI] [PubMed] [Google Scholar]
  18. Irving M., Lombardi V., Piazzesi G., Ferenczi M. A. Myosin head movements are synchronous with the elementary force-generating process in muscle. Nature. 1992 May 14;357(6374):156–158. doi: 10.1038/357156a0. [DOI] [PubMed] [Google Scholar]
  19. Lombardi V., Piazzesi G., Linari M. Rapid regeneration of the actin-myosin power stroke in contracting muscle. Nature. 1992 Feb 13;355(6361):638–641. doi: 10.1038/355638a0. [DOI] [PubMed] [Google Scholar]
  20. Malinchik S. B., Lednev V. V. Interpretation of the X-ray diffraction pattern from relaxed skeletal muscle and modelling of the thick filament structure. J Muscle Res Cell Motil. 1992 Aug;13(4):406–419. doi: 10.1007/BF01738036. [DOI] [PubMed] [Google Scholar]
  21. Martin-Fernandez M. L., Bordas J., Diakun G., Harries J., Lowy J., Mant G. R., Svensson A., Towns-Andrews E. Time-resolved X-ray diffraction studies of myosin head movements in live frog sartorius muscle during isometric and isotonic contractions. J Muscle Res Cell Motil. 1994 Jun;15(3):319–348. doi: 10.1007/BF00123484. [DOI] [PubMed] [Google Scholar]
  22. Rayment I., Rypniewski W. R., Schmidt-Bäse K., Smith R., Tomchick D. R., Benning M. M., Winkelmann D. A., Wesenberg G., Holden H. M. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 1993 Jul 2;261(5117):50–58. doi: 10.1126/science.8316857. [DOI] [PubMed] [Google Scholar]
  23. Rome E. M., Hirabayashi T., Perry S. V. X-ray diffraction of muscle labelled with antibody to troponin-C. Nat New Biol. 1973 Aug 1;244(135):154–155. doi: 10.1038/newbio244154a0. [DOI] [PubMed] [Google Scholar]
  24. Rome E., Offer G., Pepe F. A. X-ray diffraction of muscle labelled with antibody to C-protein. Nat New Biol. 1973 Aug 1;244(135):152–154. doi: 10.1038/newbio244152a0. [DOI] [PubMed] [Google Scholar]
  25. Squire J. M., Harford J. J., Edman A. C., Sjöström M. Fine structure of the A-band in cryo-sections. III. Crossbridge distribution and the axial structure of the human C-zone. J Mol Biol. 1982 Mar 15;155(4):467–494. doi: 10.1016/0022-2836(82)90482-x. [DOI] [PubMed] [Google Scholar]
  26. Wakabayashi K., Sugimoto Y., Tanaka H., Ueno Y., Takezawa Y., Amemiya Y. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J. 1994 Dec;67(6):2422–2435. doi: 10.1016/S0006-3495(94)80729-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Whittaker M., Wilson-Kubalek E. M., Smith J. E., Faust L., Milligan R. A., Sweeney H. L. A 35-A movement of smooth muscle myosin on ADP release. Nature. 1995 Dec 14;378(6558):748–751. doi: 10.1038/378748a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES