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. 1998 Dec;75(6):2984–2995. doi: 10.1016/S0006-3495(98)77739-2

Volume changes of the myosin lattice resulting from repetitive stimulation of single muscle fibers.

G Rapp 1, C C Ashley 1, M A Bagni 1, P J Griffiths 1, G Cecchi 1
PMCID: PMC1299969  PMID: 9826618

Abstract

Single muscle fibers at 1 degreesC were subjected to brief tetani (20 Hz) at intervals of between 20 s and 300 s over a period of up to 2 h. A band lattice spacing increased during this period at a rate inversely dependent on the rest interval between tetani. Spacing increased rapidly during the first 10 tetani at a rate equivalent to the production of 0.04 mOsmol.liter-1 of osmolyte per contraction, then continued to expand at a much slower rate. For short rest intervals, where lattice expansion was largest, spacing increased to a limiting value between 46 and 47 nm (sarcomere length 2.2 micrometer), corresponding to accumulation of 30 mOsmol.liter-1 of osmolytes, where it remained constant until repetitive stimulation was terminated. At this limiting spacing, force was reduced by up to 30%. The effect of lattice swelling on the lattice compression that accompanies isometric force recovery from unloaded shortening was to increase the compression, similar to that observed in hypotonic media at a similar spacing. During recovery from repetitive stimulation, spacing recompressed to its original value with a half-time of 15-30 min. These findings suggest that mechanical activity produces an increase in osmotic pressure within the cell as a result of product accumulation from cross-bridge and sarcoplasmic reticulum ATPases and glycolysis.

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Selected References

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  1. ABBOTT B. C., BASKIN R. J. Volume changes in frog muscle during contraction. J Physiol. 1962 May;161:379–391. doi: 10.1113/jphysiol.1962.sp006893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen D. G., Westerblad H., Lännergren J. The role of intracellular acidosis in muscle fatigue. Adv Exp Med Biol. 1995;384:57–68. doi: 10.1007/978-1-4899-1016-5_5. [DOI] [PubMed] [Google Scholar]
  3. April E. W., Brandt P. W., Elliott G. F. The myofilament lattice: studies on isolated fibers. II. The effects of osmotic strength, ionic concentration, and pH upon the unit-cell volume. J Cell Biol. 1972 Apr;53(1):53–65. doi: 10.1083/jcb.53.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BLINKS J. R. INFLUENCE OF OSMOTIC STRENGTH ON CROSS-SECTION AND VOLUME OF ISOLATED SINGLE MUSCLE FIBRES. J Physiol. 1965 Mar;177:42–57. doi: 10.1113/jphysiol.1965.sp007574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bagni M. A., Cecchi G., Griffiths P. J., Maéda Y., Rapp G., Ashley C. C. Lattice spacing changes accompanying isometric tension development in intact single muscle fibers. Biophys J. 1994 Nov;67(5):1965–1975. doi: 10.1016/S0006-3495(94)80679-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baskin R. J., Paolini P. J. Muscle volume changes. J Gen Physiol. 1966 Jan;49(3):387–404. doi: 10.1085/jgp.49.3.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brenner B., Yu L. C. Characterization of radial force and radial stiffness in Ca(2+)-activated skinned fibres of the rabbit psoas muscle. J Physiol. 1991 Sep;441:703–718. doi: 10.1113/jphysiol.1991.sp018774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cecchi G., Bagni M. A., Griffiths P. J., Ashley C. C., Maeda Y. Detection of radial crossbridge force by lattice spacing changes in intact single muscle fibers. Science. 1990 Dec 7;250(4986):1409–1411. doi: 10.1126/science.2255911. [DOI] [PubMed] [Google Scholar]
  9. Cecchi G., Griffiths P. J., Bagni M. A., Ashley C. C., Maeda Y. Time-resolved changes in equatorial x-ray diffraction and stiffness during rise of tetanic tension in intact length-clamped single muscle fibers. Biophys J. 1991 Jun;59(6):1273–1283. doi: 10.1016/S0006-3495(91)82342-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Curtin N. A. Buffer power and intracellular pH of frog sartorius muscle. Biophys J. 1986 Nov;50(5):837–841. doi: 10.1016/S0006-3495(86)83524-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Curtin N. A., Gilbert C., Kretzschmar K. M., Wilkie D. R. The effect of the performance of work on total energy output and metabolism during muscular contraction. J Physiol. 1974 May;238(3):455–472. doi: 10.1113/jphysiol.1974.sp010537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dawson M. J., Gadian D. G., Wilkie D. R. Contraction and recovery of living muscles studies by 31P nuclear magnetic resonance. J Physiol. 1977 Jun;267(3):703–735. doi: 10.1113/jphysiol.1977.sp011835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Godt R. E., Maughan D. W. On the composition of the cytosol of relaxed skeletal muscle of the frog. Am J Physiol. 1988 May;254(5 Pt 1):C591–C604. doi: 10.1152/ajpcell.1988.254.5.C591. [DOI] [PubMed] [Google Scholar]
  14. Godt R. E., Nosek T. M. Changes of intracellular milieu with fatigue or hypoxia depress contraction of skinned rabbit skeletal and cardiac muscle. J Physiol. 1989 May;412:155–180. doi: 10.1113/jphysiol.1989.sp017609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lee J. A., Westerblad H., Allen D. G. Changes in tetanic and resting [Ca2+]i during fatigue and recovery of single muscle fibres from Xenopus laevis. J Physiol. 1991 Feb;433:307–326. doi: 10.1113/jphysiol.1991.sp018427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Mobley B. A., Eisenberg B. R. Sizes of components in frog skeletal muscle measured by methods of stereology. J Gen Physiol. 1975 Jul;66(1):31–45. doi: 10.1085/jgp.66.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nagesser A. S., Van der Laarse W. J., Elzinga G. ATP formation and ATP hydrolysis during fatiguing, intermittent stimulation of different types of single muscle fibres from Xenopus laevis. J Muscle Res Cell Motil. 1993 Dec;14(6):608–618. doi: 10.1007/BF00141558. [DOI] [PubMed] [Google Scholar]
  19. Nagesser A. S., van der Laarse W. J., Elzinga G. Lactate efflux from fatigued fast-twitch muscle fibres of Xenopus laevis under various extracellular conditions. J Physiol. 1994 Nov 15;481(Pt 1):139–147. doi: 10.1113/jphysiol.1994.sp020425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Neering I. R., Quesenberry L. A., Morris V. A., Taylor S. R. Nonuniform volume changes during muscle contraction. Biophys J. 1991 Apr;59(4):926–933. doi: 10.1016/S0006-3495(91)82306-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Perrin D. D., Sayce I. G. Computer calculation of equilibrium concentrations in mixtures of metal ions and complexing species. Talanta. 1967 Jul;14(7):833–842. doi: 10.1016/0039-9140(67)80105-x. [DOI] [PubMed] [Google Scholar]
  22. Schoenberg M. Geometrical factors influencing muscle force development. II. Radial forces. Biophys J. 1980 Apr;30(1):69–77. doi: 10.1016/S0006-3495(80)85077-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tanokura M., Imaizumi M., Yamada K. A calorimetric study of Ca2+ binding by the parvalbumin of the toad (Bufo): distinguishable binding sites in the molecule. FEBS Lett. 1986 Dec 1;209(1):77–82. doi: 10.1016/0014-5793(86)81087-0. [DOI] [PubMed] [Google Scholar]
  24. Veech R. L., Lawson J. W., Cornell N. W., Krebs H. A. Cytosolic phosphorylation potential. J Biol Chem. 1979 Jul 25;254(14):6538–6547. [PubMed] [Google Scholar]

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