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. 1981 Jan 1;77(1):49–64. doi: 10.1085/jgp.77.1.49

Radial forces within muscle fibers in rigor

PMCID: PMC2215413  PMID: 6970793

Abstract

Considering the widely accepted cross-bridge model of muscle contraction (Huxley. 1969. Science [Wash. D. C.]. 164:1356-1366), one would expect that attachment of angled cross-bridges would give rise to radial as well as longitudinal forces in the muscle fiber. These forces would tend, in most instances, to draw the myofilaments together and to cause the fiber to decrease in width. Using optical techniques, we have observed significant changes in the width of mechanically skinned frog muscle fibers when the fibers are put into rigor by deleting ATP from the bathing medium. Using a high molecular weight polymer polyvinylpyrrolidone (PVP-40; number average mol. wt. (Mn) = 40,000) in the bathing solution, we were able to estimate the magnitude of the radial forces by shrinking the relaxed fiber to the width observed with rigor induction. With rigor, fiber widths decreased up to approximately 10%, with shrinking being greater at shorter sarcomere spacing and at lower PVP concentrations. At higher PVP concentrations, some fibers actually swelled slightly. Radial pressures seen with rigor in 2 and 4% PVP ranged up to 8.9 x 10(3) N/m2. Upon rigor induction, fibers exerted a longitudinal force of approximately 1 x 10(5) N/m2 that was inhibited by high PVP concentrations (greater than or equal to 13%). In very high PVP concentrations (greater than or equal to 20%), fibers exerted an anomalous force, independent of ATP, which ranged up to 6 x 10(4) N/m2 at 60% PVP. Assuming that all the radial force is the result of cross- bridge attachment, we calculated that rigor cross-bridges exert a radial force of 0.2 x 1.2 x 10(-9) N per thick filament in sarcomeres near rest length. This force is of roughly the same order of magnitude as the longitudinal force per thick filament in rigor contraction or in maximal (calcium-activated) contraction of skinned fibers in ATP- containing solutions. Inasmuch as widths of fibers stretched well beyond overlap of thick and thin filaments decreased with rigor, other radially directed forces may be operating in parallel with cross-bridge forces.

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Selected References

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  1. April E. W., Wong D. Non-isovolumic behavior of the unit cell of skinned striated muscle fibers. J Mol Biol. 1976 Feb 15;101(1):107–114. doi: 10.1016/0022-2836(76)90068-1. [DOI] [PubMed] [Google Scholar]
  2. Craig R. Structure of A-segments from frog and rabbit skeletal muscle. J Mol Biol. 1977 Jan 5;109(1):69–81. doi: 10.1016/s0022-2836(77)80046-6. [DOI] [PubMed] [Google Scholar]
  3. Elliott G. F. Donnan and osmotic effects in muscle fibres without membranes. J Mechanochem Cell Motil. 1973 May;2(1):83–89. [PubMed] [Google Scholar]
  4. Godt R. E. Calcium-activated tension of skinned muscle fibers of the frog. Dependence on magnesium adenosine triphosphate concentration. J Gen Physiol. 1974 Jun;63(6):722–739. doi: 10.1085/jgp.63.6.722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Godt R. E., Maughan D. W. Swelling of skinned muscle fibers of the frog. Experimental observations. Biophys J. 1977 Aug;19(2):103–116. doi: 10.1016/S0006-3495(77)85573-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Julian F. J., Moss R. L., Sollins M. R. The mechanism for vertebrate striated muscle contraction. Circ Res. 1978 Jan;42(1):2–14. doi: 10.1161/01.res.42.1.2. [DOI] [PubMed] [Google Scholar]
  9. Kawai M., Brandt P. W. Two rigor states in skinned crayfish single muscle fibers. J Gen Physiol. 1976 Sep;68(3):267–280. doi: 10.1085/jgp.68.3.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Khan M. M., Martell A. E. Thermodynamic quantities associated with the interaction of adenosine triphosphate with metal ions. J Am Chem Soc. 1966 Feb 20;88(4):668–671. doi: 10.1021/ja00956a008. [DOI] [PubMed] [Google Scholar]
  11. Magid A., Reedy M. K. X-ray diffraction observations of chemically skinned frog skeletal muscle processed by an improved method. Biophys J. 1980 Apr;30(1):27–40. doi: 10.1016/S0006-3495(80)85074-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Maughan D. W., Godt R. E. Stretch and radial compression studies on relaxed skinned muscle fibers of the frog. Biophys J. 1979 Dec;28(3):391–402. doi: 10.1016/S0006-3495(79)85188-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Pemrick S. M., Edwards C. Differences in the charge distribution of glycerol-extracted muscle fibers in rigor, relaxation, and contraction. J Gen Physiol. 1974 Nov;64(5):551–567. doi: 10.1085/jgp.64.5.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Phillips R. C., George P., Rutman R. J. Thermodynamic studies of the formation and ionization of the magnesium(II) complexes of ADP and ATP over the pH range 5 to 9. J Am Chem Soc. 1966 Jun 20;88(12):2631–2640. doi: 10.1021/ja00964a002. [DOI] [PubMed] [Google Scholar]
  15. Squire J. M. Symmetry and three-dimensional arrangement of filaments in vertebrate striated muscle. J Mol Biol. 1974 Nov 25;90(1):153–160. doi: 10.1016/0022-2836(74)90263-0. [DOI] [PubMed] [Google Scholar]

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