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PMID: 9746533 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

MgADP promotes a catch-like state developed through force-calcium hysteresis in tonic smooth muscle.

Biophysical journal ·Vol. 75 ·No. 4 ·1998-10-00 ·Pages 1926-34

Khromov A, Somlyo AV, Somlyo AP

Abstract

Tonic rabbit femoral artery and phasic rabbit ileum smooth muscles permeabilized with Triton X-100 were activated either by increasing [Ca2+] from pCa > 8.0 to pCa 6.0 (calcium-ascending protocol) or contracted at pCa 6.0 before lowering [Ca2+] (calcium-descending protocol). The effects of, respectively, high [MgATP]/low [MgADP] [10 mM MgATP + creatine phosphate (CP) + creatine kinase (CK)] or low [MgATP]/[MgADP] (2 mM MgATP, 0 CP, 0 CK) on the "force-[Ca]" relationships were determined. In femoral artery at low, but not at high, [MgATP]/[MgADP] the force and the ratio of stiffness/force at pCa 7.2 were significantly higher under the calcium-descending than calcium-ascending protocols (54% vs. 3% of Po, the force at pCa 6.0) (force hysteresis); the levels of regulatory myosin light chain (MLC20) phosphorylation (9 +/- 2% vs. 10 +/- 2%) and the velocities of unloaded shortening V0 (0.02 +/- 0.004 l/s with both protocols) were not significantly different. No significant force hysteresis was detected in rabbit ileum under either of these experimental conditions. [MgADP], measured in extracts of permeabilized femoral artery strips by two methods, was 130-140 microM during maintained force under the calcium-descending protocol. Exogenous CP (10 mM) applied during the descending protocol reduced endogenous [MgADP] to 46 +/- 10 microM and abolished force hysteresis: residual force at low [Ca2+] was 17 +/- 5% of maximal force. We conclude that the proportion of force-generating nonphosphorylated (AMdp) relative to phosphorylated cross-bridges is higher on the Ca2+-descending than on the Ca2+-ascending force curve in tonic smooth muscle, that this population of positively strained dephosphorylated cross-bridges has a high affinity for MgADP, and that the dephosphorylated AMdp . MgADP state makes a significant contribution to force maintenance at low levels of MLC20 phosphorylation.

MeSH Terms
Adenosine Diphosphate/metabolism,pharmacology Animals Calcium/metabolism Cell Membrane Permeability Chelating Agents Diazonium Compounds Femoral Artery/physiology Ileum/physiology In Vitro Techniques Muscle Contraction/physiology Muscle, Smooth/drug effects,physiology Muscle, Smooth, Vascular/drug effects,physiology Octoxynol Phenoxyacetates Phosphorylation Photolysis Rabbits
Chemicals
Chelating Agents Diazonium Compounds Phenoxyacetates diazo-2 Adenosine Diphosphate Octoxynol Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Khromov A
Department of Molecular Physiology and Biological Physics, University of Virginia Health Sciences Center, Charlottesville, Virginia 22906-0011, USA.
Somlyo A V
Somlyo A P
References (32)
32 references, click to expand
  1. Phosphagen content, breakdown during contraction, and O2 consumption in rat portal vein.
    Am J Physiol. 1983 Mar;244(3):C250-8 PMID: 6829748
  2. Tension responses of chemically skinned fibre bundles of the guinea-pig taenia caeci under varied ionic environments.
    J Physiol. 1981 Nov;320:449-67 PMID: 6976434
  3. Effects of calcium and substrate on force-velocity relation and energy turnover in skinned smooth muscle of the guinea-pig.
    J Physiol. 1985 Mar;360:347-65 PMID: 3872937
  4. The effects of ADP and phosphate on the contraction of muscle fibers.
    Biophys J. 1985 Nov;48(5):789-98 PMID: 3878160
  5. Determinants of Ca2+-dependent stress maintenance in skinned swine carotid media.
    Am J Physiol. 1986 Dec;251(6 Pt 1):C892-903 PMID: 3098110
  6. Slowing of crossbridge cycling rate in mammalian smooth muscle occurs without evidence of an increase in internal load.
    Prog Clin Biol Res. 1987;245:289-301 PMID: 3685015
  7. 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):165-92 PMID: 3373178
  8. Cytoplasmic free calcium, myosin light chain phosphorylation, and force in phasic and tonic smooth muscle.
    J Gen Physiol. 1988 Dec;92(6):713-29 PMID: 3216188
  9. G-protein-mediated Ca2+ sensitization of smooth muscle contraction through myosin light chain phosphorylation.
    J Biol Chem. 1991 Jan 25;266(3):1708-15 PMID: 1671041
  10. Myosin light chain phosphatase activities and the effects of phosphatase inhibitors in tonic and phasic smooth muscle.
    J Biol Chem. 1992 Jul 25;267(21):14662-8 PMID: 1321813
  11. Cooperative activation of myosin by light chain phosphorylation in permeabilized smooth muscle.
    Am J Physiol. 1992 Jul;263(1 Pt 1):C210-9 PMID: 1386187
  12. The effects of MgADP on cross-bridge kinetics: a laser flash photolysis study of guinea-pig smooth muscle.
    J Physiol. 1993 Jan;460:247-71 PMID: 8487195
  13. Cross-bridge cycling at rest and during activation. Turnover of myosin-bound ADP in permeabilized smooth muscle.
    J Biol Chem. 1994 Mar 11;269(10):7316-22 PMID: 8125947
  14. Myosin isoforms in smooth muscle: how may they affect function and structure?
    J Muscle Res Cell Motil. 1993 Dec;14(6):557-63 PMID: 8126215
  15. Flash photolysis studies of relaxation and cross-bridge detachment: higher sensitivity of tonic than phasic smooth muscle to MgADP.
    J Muscle Res Cell Motil. 1993 Dec;14(6):666-77 PMID: 8126226
  16. What is special about smooth muscle? The significance of covalent crossbridge regulation.
    FASEB J. 1994 Mar 1;8(3):311-8 PMID: 8143937
  17. Metabolic characteristics of alpha-toxin-permeabilized smooth muscle.
    Am J Physiol. 1994 Jun;266(6 Pt 1):C1673-83 PMID: 8023897
  18. Relaxation from rigor of skinned trabeculae of the guinea pig induced by laser photolysis of caged ATP.
    Biophys J. 1994 Apr;66(4):1115-28 PMID: 8038383
  19. Signal transduction and regulation in smooth muscle.
    Nature. 1994 Nov 17;372(6503):231-6 PMID: 7969467
  20. Effect of physiological ADP concentrations on contraction of single skinned fibers from rabbit fast and slow muscles.
    Am J Physiol. 1995 Feb;268(2 Pt 1):C480-9 PMID: 7864087
  21. Phosphocreatine and creatine kinase in energetic metabolism of the porcine carotid artery.
    J Vasc Res. 1995 Jan-Feb;32(1):24-30 PMID: 7873707
  22. The creatine kinase equilibrium, free [ADP] and myosin ATPase in vascular smooth muscle cross-bridges.
    J Theor Biol. 1995 Mar 21;173(2):207-11 PMID: 7739220
  23. The role of MgADP in force maintenance by dephosphorylated cross-bridges in smooth muscle: a flash photolysis study.
    Biophys J. 1995 Dec;69(6):2611-22 PMID: 8599668
  24. Nucleotide binding by actomyosin as a determinant of relaxation kinetics of rabbit phasic and tonic smooth muscle.
    J Physiol. 1996 May 1;492 ( Pt 3):669-73 PMID: 8734980
  25. ADP release produces a rotation of the neck region of smooth myosin but not skeletal myosin.
    Nat Struct Biol. 1996 Sep;3(9):796-802 PMID: 8784354
  26. Basal intracellular free Mg2+ concentration in smooth muscle cells of guinea pig tenia cecum: intracellular calibration of the fluorescent indicator furaptra.
    Biophys J. 1997 Dec;73(6):3358-70 PMID: 9414246
  27. Interaction of actin and ADP with the head domain of smooth muscle myosin: implications for strain-dependent ADP release in smooth muscle.
    Biochemistry. 1998 Feb 17;37(7):1969-78 PMID: 9485324
  28. The amount and compartmentalization of adenosine diphosphate in muscle.
    Biochim Biophys Acta. 1962 Dec 17;65:443-60 PMID: 13988021
  29. Differences in cellular contractile protein contents among porcine smooth muscles: evidence for variation in the contractile system.
    J Gen Physiol. 1978 Sep;72(3):369-80 PMID: 702112
  30. The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres.
    J Physiol. 1979 Jun;291:143-59 PMID: 314510
  31. Myosin phosphorylation and the cross-bridge cycle in arterial smooth muscle.
    Science. 1981 Jan 30;211(4481):495-7 PMID: 6893872
  32. Phosphagen and metabolite content during contraction in porcine carotid artery.
    Am J Physiol. 1983 May;244(5):C385-90 PMID: 6846527
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
1998-10-00
Pages
1926-34
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1299863
Subset
IM
Grants
NHLBI NIH HHS · HL19242 · United States
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