Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1989 Oct 1;94(4):769–781. doi: 10.1085/jgp.94.4.769

Kinetics of contraction initiated by flash photolysis of caged adenosine triphosphate in tonic and phasic smooth muscles

PMCID: PMC2228968  PMID: 2559141

Abstract

Laser flash photolysis of caged adenosine triphosphate (ATP), in the presence of Ca2+, was used to examine the time course of isometric force development from rigor states in glycerinated tonic (rabbit trachealis) and phasic (guinea-pig ileum and portal vein) smooth muscles. Photolytic liberation of ATP from caged ATP initiated force development, at 20 degrees C, with half-time (t1/2) of 5.4 s in trachealis and 1.2-2.2 s in the phasic muscles. Prior to photolysis, some muscles were phosphorylated with ATP plus okadaic acid (an inhibitor of myosin light-chain phosphatase) or thiophosphorylated with ATP gamma S to fully activate the regulatory system, before turning on the contractile apparatus. In these prephosphorylated muscles, force development, after caged ATP photolysis, was more rapid than in the unphosphorylated muscles, but the t1/2 values for trachealis (0.8-1.1 s) were still longer than for ileum and portal-vein muscles (0.20-0.25 s). The results suggest that both the contractile machinery and the regulatory system are slower in the tonic than in the phasic smooth muscles. The time course of force development for each muscle type was sigmoidal, with an initial delay (td) of approximately 10% of the t1/2 value. Some possible chemical and mechanical origins of the delay are discussed.

Full Text

The Full Text of this article is available as a PDF (802.7 KB).

Selected References

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

  1. Arheden H., Arner A., Hellstrand P. Cross-bridge behaviour in skinned smooth muscle of the guinea-pig taenia coli at altered ionic strength. J Physiol. 1988 Sep;403:539–558. doi: 10.1113/jphysiol.1988.sp017263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bezanilla F. A high capacity data recording device based on a digital audio processor and a video cassette recorder. Biophys J. 1985 Mar;47(3):437–441. doi: 10.1016/S0006-3495(85)83935-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bialojan C., Rüegg J. C., Takai A. Effects of okadaic acid on isometric tension and myosin phosphorylation of chemically skinned guinea-pig taenia coli. J Physiol. 1988 Apr;398:81–95. doi: 10.1113/jphysiol.1988.sp017030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brenner B., Eisenberg E. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Natl Acad Sci U S A. 1986 May;83(10):3542–3546. doi: 10.1073/pnas.83.10.3542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Butler T. M., Siegman M. J., Mooers S. U. Chemical energy usage during shortening and work production in mammalian smooth muscle. Am J Physiol. 1983 Mar;244(3):C234–C242. doi: 10.1152/ajpcell.1983.244.3.C234. [DOI] [PubMed] [Google Scholar]
  6. Cassidy P., Hoar P. E., Kerrick W. G. Irreversible thiophosphorylation and activation of tension in functionally skinned rabbit ileum strips by [35S]ATP gamma S. J Biol Chem. 1979 Nov 10;254(21):11148–11153. [PubMed] [Google Scholar]
  7. Erdödi F., Rokolya A., Di Salvo J., Bárány M., Bárány K. Effect of okadaic acid on phosphorylation-dephosphorylation of myosin light chain in aortic smooth muscle homogenate. Biochem Biophys Res Commun. 1988 May 31;153(1):156–161. doi: 10.1016/s0006-291x(88)81202-6. [DOI] [PubMed] [Google Scholar]
  8. Gerthoffer W. T., Murphy R. A. Myosin phosphorylation and regulation of cross-bridge cycle in tracheal smooth muscle. Am J Physiol. 1983 Mar;244(3):C182–C187. doi: 10.1152/ajpcell.1983.244.3.C182. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  12. Himpens B., Matthijs G., Somlyo A. V., Butler T. M., Somlyo A. P. Cytoplasmic free calcium, myosin light chain phosphorylation, and force in phasic and tonic smooth muscle. J Gen Physiol. 1988 Dec;92(6):713–729. doi: 10.1085/jgp.92.6.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Himpens B., Somlyo A. P. Free-calcium and force transients during depolarization and pharmacomechanical coupling in guinea-pig smooth muscle. J Physiol. 1988 Jan;395:507–530. doi: 10.1113/jphysiol.1988.sp016932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Horiuti K. Mechanism of contracture on cooling of caffeine-treated frog skeletal muscle fibres. J Physiol. 1988 Apr;398:131–148. doi: 10.1113/jphysiol.1988.sp017034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kamm K. E., Stull J. T. Activation of smooth muscle contraction: relation between myosin phosphorylation and stiffness. Science. 1986 Apr 4;232(4746):80–82. doi: 10.1126/science.3754063. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Moreland R. S., Moreland S., Murphy R. A. Dependence of stress on length, Ca2+, and myosin phosphorylation in skinned smooth muscle. Am J Physiol. 1988 Oct;255(4 Pt 1):C473–C478. doi: 10.1152/ajpcell.1988.255.4.C473. [DOI] [PubMed] [Google Scholar]
  18. Paul R. J., Doerman G., Zeugner C., Rüegg J. C. The dependence of unloaded shortening velocity on Ca++, calmodulin, and duration of contraction in "chemically skinned" smooth muscle. Circ Res. 1983 Sep;53(3):342–351. doi: 10.1161/01.res.53.3.342. [DOI] [PubMed] [Google Scholar]
  19. Singer H. A., Murphy R. A. Maximal rates of activation in electrically stimulated swine carotid media. Circ Res. 1987 Mar;60(3):438–445. doi: 10.1161/01.res.60.3.438. [DOI] [PubMed] [Google Scholar]
  20. Somlyo A. P., Somlyo A. V. Vascular smooth muscle. I. Normal structure, pathology, biochemistry, and biophysics. Pharmacol Rev. 1968 Dec;20(4):197–272. [PubMed] [Google Scholar]
  21. Somlyo A. V., Goldman Y. E., Fujimori T., Bond M., Trentham D. R., Somlyo A. P. Cross-bridge kinetics, cooperativity, and negatively strained cross-bridges in vertebrate smooth muscle. A laser-flash photolysis study. J Gen Physiol. 1988 Feb;91(2):165–192. doi: 10.1085/jgp.91.2.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Somlyo A. V., Somlyo A. P. Electromechanical and pharmacomechanical coupling in vascular smooth muscle. J Pharmacol Exp Ther. 1968 Jan;159(1):129–145. [PubMed] [Google Scholar]
  23. Umemoto S., Bengur A. R., Sellers J. R. Effect of multiple phosphorylations of smooth muscle and cytoplasmic myosins on movement in an in vitro motility assay. J Biol Chem. 1989 Jan 25;264(3):1431–1436. [PubMed] [Google Scholar]
  24. Warshaw D. M., Rees D. D., Fay F. S. Characterization of cross-bridge elasticity and kinetics of cross-bridge cycling during force development in single smooth muscle cells. J Gen Physiol. 1988 Jun;91(6):761–779. doi: 10.1085/jgp.91.6.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yagi S., Becker P. L., Fay F. S. Relationship between force and Ca2+ concentration in smooth muscle as revealed by measurements on single cells. Proc Natl Acad Sci U S A. 1988 Jun;85(11):4109–4113. doi: 10.1073/pnas.85.11.4109. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES