The effects of MgADP on cross-bridge kinetics: a laser flash photolysis study of guinea-pig smooth muscle (original) (raw)

Abstract

1. The effects of MgADP on cross-bridge kinetics were investigated using laser flash photolysis of caged ATP (P3-1(2-nitrophenyl) ethyladenosine 5'-triphosphate), in guinea-pig portal vein smooth muscle permeabilized with Staphylococcus aureus alpha-toxin. Isometric tension and in-phase stiffness transitions from rigor state were monitored upon photolysis of caged ATP. The estimated concentration of ATP released from caged ATP by high-pressure liquid chromatography (HPLC) was 1.3 mM. 2. The time course of relaxation initiated by photolysis of caged ATP in the absence of Ca2+ was well fitted during the initial 200 ms by two exponential functions with time constants of, respectively, tau 1 = 34 ms and tau 2 = 1.2 s and relative amplitudes of 0.14 and 0.86. Multiple exponential functions were needed to fit longer intervals; the half-time of the overall relaxation was 0.8 s. The second order rate constant for cross-bridge detachment by ATP, estimated from the rate of initial relaxation, was 0.4-2.3 x 10(4) M-1 s-1. 3. MgADP dose dependently reduced both the relative amplitude of the first component and the rate constant of the second component of relaxation. Conversely, treatment of muscles with apyrase, to deplete endogenous ADP, increased the relative amplitude of the first component. In the presence of MgADP, in-phase stiffness decreased during force maintenance, suggesting that the force per cross-bridge increased. The apparent dissociation constant (Kd) of MgADP for the cross-bridge binding site, estimated from its concentration-dependent effect on the relative amplitude of the first component, was 1.3 microM. This affinity is much higher than the previously reported values (50-300 microM for smooth muscle; 18-400 microM for skeletal muscle; 7-10 microM for cardiac muscle). It is possible that the high affinity reflects the properties of a state generated during the co-operative reattachment cycle, rather than that of the rigor bridge. 4. The rate constant of MgADP release from cross-bridges, estimated from its concentration-dependent effect on the rate constant of the second (tau 2) component, was 0.35-7.7 s-1. To the extent that reattachment of cross-bridges could slow relaxation even during the initial 200 ms, this rate constant may be an underestimate. 5. Inorganic phosphate (Pi, 30 mM) did not affect the rate of relaxation during the initial approximately 50 ms, but accelerated the slower phase of relaxation, consistent with a cyclic cross-bridge model in which Pi increases the proportion of cross-bridges in detached ('weakly bound') states.(ABSTRACT TRUNCATED AT 400 WORDS)

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  1. Arheden H., Hellstrand P. Force response to rapid length change during contraction and rigor in skinned smooth muscle of guinea-pig taenia coli. J Physiol. 1991 Oct;442:601–630. doi: 10.1113/jphysiol.1991.sp018811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arner A., Hellstrand P., Rüegg J. C. Influence of ATP, ADP and AMPPNP on the energetics of contraction in skinned smooth muscle. Prog Clin Biol Res. 1987;245:43–57. [PubMed] [Google Scholar]
  3. Butler T. M., Siegman M. J., Mooers S. U., Narayan S. R. Myosin-product complex in the resting state and during relaxation of smooth muscle. Am J Physiol. 1990 Jun;258(6 Pt 1):C1092–C1099. doi: 10.1152/ajpcell.1990.258.6.C1092. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Cooke R., Pate E. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J. 1985 Nov;48(5):789–798. doi: 10.1016/S0006-3495(85)83837-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Driska S. P., Stein P. G., Porter R. Myosin dephosphorylation during rapid relaxation of hog carotid artery smooth muscle. Am J Physiol. 1989 Feb;256(2 Pt 1):C315–C321. doi: 10.1152/ajpcell.1989.256.2.C315. [DOI] [PubMed] [Google Scholar]
  8. Eisenberg E., Greene L. E. The relation of muscle biochemistry to muscle physiology. Annu Rev Physiol. 1980;42:293–309. doi: 10.1146/annurev.ph.42.030180.001453. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Greene L. E., Sellers J. R. Effect of phosphorylation on the binding of smooth muscle heavy meromyosin X ADP to actin. J Biol Chem. 1987 Mar 25;262(9):4177–4181. [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. Hai C. M., Murphy R. A. Ca2+, crossbridge phosphorylation, and contraction. Annu Rev Physiol. 1989;51:285–298. doi: 10.1146/annurev.ph.51.030189.001441. [DOI] [PubMed] [Google Scholar]
  13. Hellstrand P., Paul R. J. Phosphagen content, breakdown during contraction, and O2 consumption in rat portal vein. Am J Physiol. 1983 Mar;244(3):C250–C258. doi: 10.1152/ajpcell.1983.244.3.C250. [DOI] [PubMed] [Google Scholar]
  14. Hibberd M. G., Dantzig J. A., Trentham D. R., Goldman Y. E. Phosphate release and force generation in skeletal muscle fibers. Science. 1985 Jun 14;228(4705):1317–1319. doi: 10.1126/science.3159090. [DOI] [PubMed] [Google Scholar]
  15. Hibberd M. G., Trentham D. R. Relationships between chemical and mechanical events during muscular contraction. Annu Rev Biophys Biophys Chem. 1986;15:119–161. doi: 10.1146/annurev.bb.15.060186.001003. [DOI] [PubMed] [Google Scholar]
  16. Horiuti K., Somlyo A. V., Goldman Y. E., Somlyo A. P. Kinetics of contraction initiated by flash photolysis of caged adenosine triphosphate in tonic and phasic smooth muscles. J Gen Physiol. 1989 Oct;94(4):769–781. doi: 10.1085/jgp.94.4.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Iino M. Tension responses of chemically skinned fibre bundles of the guinea-pig taenia caeci under varied ionic environments. J Physiol. 1981 Nov;320:449–467. doi: 10.1113/jphysiol.1981.sp013961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ishijima A., Doi T., Sakurada K., Yanagida T. Sub-piconewton force fluctuations of actomyosin in vitro. Nature. 1991 Jul 25;352(6333):301–306. doi: 10.1038/352301a0. [DOI] [PubMed] [Google Scholar]
  19. Itoh T., Kanmura Y., Kuriyama H. Inorganic phosphate regulates the contraction-relaxation cycle in skinned muscles of the rabbit mesenteric artery. J Physiol. 1986 Jul;376:231–252. doi: 10.1113/jphysiol.1986.sp016151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Johnson R. E., Adams P. H. ADP binds similarly to rigor muscle myofibrils and to actomyosin-subfragment one. FEBS Lett. 1984 Aug 20;174(1):11–14. doi: 10.1016/0014-5793(84)81067-4. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Kitazawa T., Kobayashi S., Horiuti K., Somlyo A. V., Somlyo A. P. Receptor-coupled, permeabilized smooth muscle. Role of the phosphatidylinositol cascade, G-proteins, and modulation of the contractile response to Ca2+. J Biol Chem. 1989 Apr 5;264(10):5339–5342. [PubMed] [Google Scholar]
  23. Lind I., Ahnert-Hilger G., Fuchs G., Gratzl M. Purification of alpha-toxin from Staphylococcus aureus and application to cell permeabilization. Anal Biochem. 1987 Jul;164(1):84–89. doi: 10.1016/0003-2697(87)90371-x. [DOI] [PubMed] [Google Scholar]
  24. Lymn R. W., Taylor E. W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry. 1971 Dec 7;10(25):4617–4624. doi: 10.1021/bi00801a004. [DOI] [PubMed] [Google Scholar]
  25. Marston S. B., Taylor E. W. Comparison of the myosin and actomyosin ATPase mechanisms of the four types of vertebrate muscles. J Mol Biol. 1980 Jun 5;139(4):573–600. doi: 10.1016/0022-2836(80)90050-9. [DOI] [PubMed] [Google Scholar]
  26. Marston S. The nucleotide complexes of myosin in glycerol-extracted muscle fibres. Biochim Biophys Acta. 1973 May 30;305(2):397–412. doi: 10.1016/0005-2728(73)90186-2. [DOI] [PubMed] [Google Scholar]
  27. Nishimura J., van Breemen C. Possible involvement of actomyosin ADP complex in regulation of Ca2+ sensitivity in alpha-toxin permeabilized smooth muscle. Biochem Biophys Res Commun. 1989 Nov 30;165(1):408–415. doi: 10.1016/0006-291x(89)91085-1. [DOI] [PubMed] [Google Scholar]
  28. Rosenfeld S. S., Taylor E. W. The ATPase mechanism of skeletal and smooth muscle acto-subfragment 1. J Biol Chem. 1984 Oct 10;259(19):11908–11919. [PubMed] [Google Scholar]
  29. Rosenfeld S. S., Taylor E. W. The dissociation of 1-N6-ethenoadenosine diphosphate from regulated actomyosin subfragment 1. J Biol Chem. 1987 Jul 25;262(21):9994–9999. [PubMed] [Google Scholar]
  30. Schoenberg M., Eisenberg E. ADP binding to myosin cross-bridges and its effect on the cross-bridge detachment rate constants. J Gen Physiol. 1987 Jun;89(6):905–920. doi: 10.1085/jgp.89.6.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sellers J. R. Mechanism of the phosphorylation-dependent regulation of smooth muscle heavy meromyosin. J Biol Chem. 1985 Dec 15;260(29):15815–15819. [PubMed] [Google Scholar]
  32. Siegman M. J., Butler T. M., Mooers S. U., Davies R. E. Chemical energetics of force development, force maintenance, and relaxation in mammalian smooth muscle. J Gen Physiol. 1980 Nov;76(5):609–629. doi: 10.1085/jgp.76.5.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Siemankowski R. F., Wiseman M. O., White H. D. ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc Natl Acad Sci U S A. 1985 Feb;82(3):658–662. doi: 10.1073/pnas.82.3.658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sleep J. A., Hutton R. L. Exchange between inorganic phosphate and adenosine 5'-triphosphate in the medium by actomyosin subfragment 1. Biochemistry. 1980 Apr 1;19(7):1276–1283. doi: 10.1021/bi00548a002. [DOI] [PubMed] [Google Scholar]
  35. Somlyo A. P., Somlyo A. V. Flash photolysis studies of excitation-contraction coupling, regulation, and contraction in smooth muscle. Annu Rev Physiol. 1990;52:857–874. doi: 10.1146/annurev.ph.52.030190.004233. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Takahashi M., Sohma H., Morita F. The steady state intermediate of scallop smooth muscle myosin ATPase and effect of light chain phosphorylation. A molecular mechanism for catch contraction. J Biochem. 1988 Jul;104(1):102–107. doi: 10.1093/oxfordjournals.jbchem.a122402. [DOI] [PubMed] [Google Scholar]