Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1993 Jul;466:229–243.

Myofilament sliding per ATP molecule in rabbit muscle fibres studied using laser flash photolysis of caged ATP.

T Yamada 1, O Abe 1, T Kobayashi 1, H Sugi 1
PMCID: PMC1175476  PMID: 8410692

Abstract

1. To estimate the distance of myofilament sliding per ATP molecule hydrolysed during the actin-myosin interaction in muscle, single glycerinated fibres prepared from rabbit psoas muscle were made to shorten under very small external loads (< or = 0.0005 maximum isometric force (Po), at 20-22 degrees C) by the laser flash photolysis of caged ATP (P3-1-(2-nitro) phenylethyladenosine 5'-triphosphate), a biologically inert and photolabile precursor of ATP. The laser flash-induced fibre shortening was recorded with a high-speed video system at 200 frames s-1. 2. Following the photochemical release of 75-300 microM ATP, the fibres shortened uniformly along the fibre length not only at the level of fibre segments but also at the level of sarcomeres. The fibres did not shorten appreciably in response to 50 microM ATP. 3. The initial velocity of the laser flash-induced fibre shortening increased with increasing concentration of released ATP, being 0.05 +/- 0.01, 0.12 +/- 0.04, 0.23 +/- 0.04, 0.38 +/- 0.03 and 0.95 +/- 0.08 microns s-1 (half-sarcomere)-1 (means +/- S.E.M., n = 10) with 75, 100, 150, 200 and 300 microM ATP, respectively. 4. The distance of the laser flash-induced fibre shortening also increased with increasing concentration of released ATP, being 10 +/- 2, 25 +/- 5, 65 +/- 7, 100 +/- 10 and 180 +/- 20 nm (half-sarcomere)-1 (means +/- S.E.M., n = 10) with 75, 100, 150, 200 and 300 microM ATP, respectively. 5. Comparison of the initial shortening velocities of the laser flash-induced shortening with the force-velocity relation of maximally Ca(2+)-activated fibres indicated the presence of considerable internal resistance against myofilament sliding following release of ATP. The initial velocity of shortening following the release of 300, 150 and 75 microM ATP was equal to the shortening velocity of maximally Ca(2+)-activated fibres under an external load of 0.55, 0.93 and 0.98 Po respectively. 6. These results suggest that, under nearly isometric conditions, the distance of myofilament sliding per ATP molecule hydrolysed is about 10 nm in each half-sarcomere.

Full text

PDF
229

Images in this article

235Fig. 2
on p.235
239Fig. 7
on p.239

Selected References

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

  1. Chaen S., Kometani K., Yamada T., Shimizu H. Substrate-concentration of dependences of tension, shortening velocity and ATPase activity of glycerinated single muscle fibers. J Biochem. 1981 Dec;90(6):1611–1621. doi: 10.1093/oxfordjournals.jbchem.a133636. [DOI] [PubMed] [Google Scholar]
  2. Cooke R., Bialek W. Contraction of glycerinated muscle fibers as a function of the ATP concentration. Biophys J. 1979 Nov;28(2):241–258. doi: 10.1016/S0006-3495(79)85174-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dantzig J. A., Hibberd M. G., Trentham D. R., Goldman Y. E. Cross-bridge kinetics in the presence of MgADP investigated by photolysis of caged ATP in rabbit psoas muscle fibres. J Physiol. 1991 Jan;432:639–680. doi: 10.1113/jphysiol.1991.sp018405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ferenczi M. A., Homsher E., Trentham D. R. The kinetics of magnesium adenosine triphosphate cleavage in skinned muscle fibres of the rabbit. J Physiol. 1984 Jul;352:575–599. doi: 10.1113/jphysiol.1984.sp015311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ford L. E., Huxley A. F., Simmons R. M. Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol. 1977 Jul;269(2):441–515. doi: 10.1113/jphysiol.1977.sp011911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Goldman Y. E., Hibberd M. G., McCray J. A., Trentham D. R. Relaxation of muscle fibres by photolysis of caged ATP. Nature. 1982 Dec 23;300(5894):701–705. doi: 10.1038/300701a0. [DOI] [PubMed] [Google Scholar]
  7. Goldman Y. E., Hibberd M. G., Trentham D. R. Initiation of active contraction by photogeneration of adenosine-5'-triphosphate in rabbit psoas muscle fibres. J Physiol. 1984 Sep;354:605–624. doi: 10.1113/jphysiol.1984.sp015395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goldman Y. E., Hibberd M. G., Trentham D. R. Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5'-triphosphate. J Physiol. 1984 Sep;354:577–604. doi: 10.1113/jphysiol.1984.sp015394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  10. Harada Y., Sakurada K., Aoki T., Thomas D. D., Yanagida T. Mechanochemical coupling in actomyosin energy transduction studied by in vitro movement assay. J Mol Biol. 1990 Nov 5;216(1):49–68. doi: 10.1016/S0022-2836(05)80060-9. [DOI] [PubMed] [Google Scholar]
  11. Higuchi H., Goldman Y. E. Sliding distance between actin and myosin filaments per ATP molecule hydrolysed in skinned muscle fibres. Nature. 1991 Jul 25;352(6333):352–354. doi: 10.1038/352352a0. [DOI] [PubMed] [Google Scholar]
  12. Huxley A. F., Simmons R. M. Proposed mechanism of force generation in striated muscle. Nature. 1971 Oct 22;233(5321):533–538. doi: 10.1038/233533a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Iwamoto H., Sugaya R., Sugi H. Force-velocity relation of frog skeletal muscle fibres shortening under continuously changing load. J Physiol. 1990 Mar;422:185–202. doi: 10.1113/jphysiol.1990.sp017979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaplan J. H., Forbush B., 3rd, Hoffman J. F. Rapid photolytic release of adenosine 5'-triphosphate from a protected analogue: utilization by the Na:K pump of human red blood cell ghosts. Biochemistry. 1978 May 16;17(10):1929–1935. doi: 10.1021/bi00603a020. [DOI] [PubMed] [Google Scholar]
  16. Moss R. L. The effect of calcium on the maximum velocity of shortening in skinned skeletal muscle fibres of the rabbit. J Muscle Res Cell Motil. 1982 Sep;3(3):295–311. doi: 10.1007/BF00713039. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Toyoshima Y. Y., Kron S. J., Spudich J. A. The myosin step size: measurement of the unit displacement per ATP hydrolyzed in an in vitro assay. Proc Natl Acad Sci U S A. 1990 Sep;87(18):7130–7134. doi: 10.1073/pnas.87.18.7130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Uyeda T. Q., Kron S. J., Spudich J. A. Myosin step size. Estimation from slow sliding movement of actin over low densities of heavy meromyosin. J Mol Biol. 1990 Aug 5;214(3):699–710. doi: 10.1016/0022-2836(90)90287-V. [DOI] [PubMed] [Google Scholar]
  20. Uyeda T. Q., Warrick H. M., Kron S. J., Spudich J. A. Quantized velocities at low myosin densities in an in vitro motility assay. Nature. 1991 Jul 25;352(6333):307–311. doi: 10.1038/352307a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES