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PMID: 7647245 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Parallel inhibition of active force and relaxed fiber stiffness by caldesmon fragments at physiological ionic strength and temperature conditions: additional evidence that weak cross-bridge binding to actin is an essential intermediate for force generation.

Biophysical journal ·Vol. 68 ·No. 6 ·1995-06-00 ·Pages 2404-18

Kraft T, Chalovich JM, Yu LC, Brenner B

Abstract

Previously we showed that stiffness of relaxed fibers and active force generated in single skinned fibers of rabbit psoas muscle are inhibited in parallel by actin-binding fragments of caldesmon, an actin-associated protein of smooth muscle, under conditions in which a large fraction of cross-bridges is weakly attached to actin (ionic strength of 50 mM and temperature of 5 degrees C). These results suggested that weak cross-bridge attachment to actin is essential for force generation. The present study provides evidence that this is also true for physiological ionic strength (170 mM) at temperatures up to 30 degrees C, suggesting that weak cross-bridge binding to actin is generally required for force generation. In addition, we show that the inhibition of active force is not a result of changes in cross-bridge cycling kinetics but apparently results from selective inhibition of weak cross-bridge binding to actin. Together with our previous biochemical, mechanical, and structural studies, these findings support the proposal that weak cross-bridge attachment to actin is an essential intermediate on the path to force generation and are consistent with the concept that isometric force mainly results from an increase in strain of the attached cross-bridge as a result of a structural change associated with the transition from a weakly bound to a strongly bound actomyosin complex. This mechanism is different from the processes responsible for quick tension recovery that were proposed by Huxley and Simmons (Proposed mechanism of force generation in striated muscle. Nature. 233:533-538.) to represent the elementary mechanism of force generation.

MeSH Terms
Actins/metabolism Animals Calmodulin-Binding Proteins/isolation & purification,metabolism,pharmacology Chymotrypsin Gizzard, Avian In Vitro Techniques Kinetics Mathematics Microscopy, Confocal Models, Biological Muscle Contraction/drug effects Muscle Fibers, Skeletal/cytology,drug effects,physiology Muscle, Skeletal/cytology,drug effects,physiology Muscle, Smooth Peptide Fragments/metabolism,pharmacology Protein Binding Rabbits Turkeys
Chemicals
Actins Calmodulin-Binding Proteins Peptide Fragments Chymotrypsin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kraft T
Department of General Physiology, University of Ulm, Germany.
Chalovich J M
Yu L C
Brenner B
References (64)
64 references, click to expand
  1. Tension responses to sudden length change in stimulated frog muscle fibres near slack length.
    J Physiol. 1977 Jul;269(2):441-515 PMID: 302333
  2. The effects of temperature and salts on myosin subfragment-1 and F-actin association.
    Arch Biochem Biophys. 1977 Apr 30;180(2):404-8 PMID: 879794
  3. Characterization of the myosin adenosine triphosphate (M.ATP) crossbridge in rabbit and frog skeletal muscle fibers.
    Biophys J. 1988 Jul;54(1):135-48 PMID: 3261996
  4. Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibers.
    Biophys J. 1983 Jan;41(1):99-102 PMID: 6824759
  5. The rates of formation and dissociation of actin-myosin complexes. Effects of solvent, temperature, nucleotide binding and head-head interactions.
    Biochem J. 1982 May 1;203(2):453-60 PMID: 7115298
  6. Energetics and mechanism of actomyosin adenosine triphosphatase.
    Biochemistry. 1976 Dec 28;15(26):5818-26 PMID: 12793
  7. Theoretical formalism for the sliding filament model of contraction of striated muscle. Part I.
    Prog Biophys Mol Biol. 1974;28:267-340 PMID: 4617248
  8. Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction.
    Proc Natl Acad Sci U S A. 1988 May;85(9):3265-9 PMID: 2966401
  9. State-dependent radial elasticity of attached cross-bridges in single skinned fibres of rabbit psoas muscle.
    J Physiol. 1993 Feb;461:283-99 PMID: 16993186
  10. The relation of muscle biochemistry to muscle physiology.
    Annu Rev Physiol. 1980;42:293-309 PMID: 6996582
  11. Direct visualization by electron microscopy of the weakly bound intermediates in the actomyosin adenosine triphosphatase cycle.
    Biophys J. 1993 Feb;64(2):454-71 PMID: 8457671
  12. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution.
    Proc Natl Acad Sci U S A. 1986 May;83(10):3542-6 PMID: 2939452
  13. Three-dimensional structure of myosin subfragment-1: a molecular motor.
    Science. 1993 Jul 2;261(5117):50-8 PMID: 8316857
  14. Cooperative binding of myosin subfragment-1 to the actin-troponin-tropomyosin complex.
    Proc Natl Acad Sci U S A. 1980 May;77(5):2616-20 PMID: 6930656
  15. Stiffness of skinned rabbit psoas fibers in MgATP and MgPPi solution.
    Biophys J. 1986 Oct;50(4):685-91 PMID: 3022835
  16. Force and ATPase rate in skinned skeletal muscle fibers.
    Fed Proc. 1982 May;41(7):2232-7 PMID: 6210577
  17. Structural changes in the actomyosin cross-bridges associated with force generation.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5252-6 PMID: 8506374
  18. Effects of pH on contraction of rabbit fast and slow skeletal muscle fibers.
    Biophys J. 1988 Jun;53(6):935-46 PMID: 2969265
  19. Analysis of numerical methods for computer simulation of kinetic processes: development of KINSIM--a flexible, portable system.
    Anal Biochem. 1983 Apr 1;130(1):134-45 PMID: 6688159
  20. Relationship between regulated actomyosin ATPase activity and cooperative binding of myosin to regulated actin.
    Cell Biophys. 1988 Jan-Jun;12:59-71 PMID: 2453286
  21. Relaxation of muscle fibers with adenosine 5'-[gamma-thio]triphosphate (ATP[gamma S]) and by laser photolysis of caged ATP[gamma S]: evidence for Ca2+-dependent affinity of rapidly detaching zero-force cross-bridges.
    Proc Natl Acad Sci U S A. 1988 Sep;85(18):6716-20 PMID: 3413119
  22. Changes in the X-ray reflections from contracting muscle during rapid mechanical transients and their structural implications.
    J Mol Biol. 1983 Sep 15;169(2):469-506 PMID: 6604821
  23. Mechanism of adenosine triphosphate hydrolysis by actomyosin.
    Biochemistry. 1971 Dec 7;10(25):4617-24 PMID: 4258719
  24. Crosslinked myosin subfragment 1: a stable analogue of the subfragment-1.ATP complex.
    Proc Natl Acad Sci U S A. 1983 Aug;80(16):4909-13 PMID: 6576363
  25. Pressure-relaxation studies of pyrene-labelled actin and myosin subfragment 1 from rabbit skeletal muscle. Evidence for two states of acto-subfragment 1.
    Biochem J. 1985 Dec 1;232(2):351-6 PMID: 4091793
  26. Molecular structure of F-actin and location of surface binding sites.
    Nature. 1990 Nov 15;348(6298):217-21 PMID: 2234090
  27. Measurement of the fraction of myosin heads bound to actin in rabbit skeletal myofibrils in rigor.
    J Mol Biol. 1981 Jul 15;149(4):659-74 PMID: 6273587
  28. Muscle contraction and free energy transduction in biological systems.
    Science. 1985 Mar 1;227(4690):999-1006 PMID: 3156404
  29. Orientational disorder and motion of weakly attached cross-bridges.
    Biophys J. 1991 Sep;60(3):642-9 PMID: 1657230
  30. Rapid dissociation and reassociation of actomyosin cross-bridges during force generation: a newly observed facet of cross-bridge action in muscle.
    Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10490-4 PMID: 1835789
  31. Kinetic and thermodynamic properties of the ternary complex between F-actin, myosin subfragment 1 and adenosine 5'-[beta, gamma-imido]triphosphate.
    Eur J Biochem. 1982 Nov 15;128(2-3):547-55 PMID: 7151795
  32. All myosin heads form bonds with actin in rigor rabbit skeletal muscle.
    Biochemistry. 1980 May 13;19(10):2265-9 PMID: 6103713
  33. Proposed mechanism of force generation in striated muscle.
    Nature. 1971 Oct 22;233(5321):533-8 PMID: 4939977
  34. Kinetic studies on the association and dissociation of myosin subfragment 1 and actin.
    J Biol Chem. 1991 Jan 5;266(1):294-302 PMID: 1845966
  35. Muscle structure and theories of contraction.
    Prog Biophys Biophys Chem. 1957;7:255-318 PMID: 13485191
  36. Calcium-sensitive binding of heavy meromyosin to regulated actin in the presence of ATP.
    J Biol Chem. 1981 Dec 25;256(24):12647-50 PMID: 6458606
  37. Atomic model of the actin filament.
    Nature. 1990 Sep 6;347(6288):44-9 PMID: 2395461
  38. Kinetic studies of the cooperative binding of subfragment 1 to regulated actin.
    Proc Natl Acad Sci U S A. 1980 Dec;77(12):7209-13 PMID: 6938966
  39. Three-dimensional atomic model of F-actin decorated with Dictyostelium myosin S1.
    Nature. 1993 Jul 8;364(6433):171-4 PMID: 8321290
  40. Myosin head movements are synchronous with the elementary force-generating process in muscle.
    Nature. 1992 May 14;357(6374):156-8 PMID: 1579164
  41. Structure of the actin-myosin complex in the presence of ATP.
    Proc Natl Acad Sci U S A. 1985 May;82(10):3247-51 PMID: 3858821
  42. The cross-bridge cycle in muscle. Mechanical, biochemical, and structural studies on single skinned rabbit psoas fibers to characterize cross-bridge kinetics in muscle for correlation with the actomyosin-ATPase in solution.
    Basic Res Cardiol. 1986;81 Suppl 1:1-15 PMID: 2947559
  43. Effect of caldesmon on the ATPase activity and the binding of smooth and skeletal myosin subfragments to actin.
    J Biol Chem. 1988 Feb 5;263(4):1878-85 PMID: 2962997
  44. Parallel inhibition of active force and relaxed fiber stiffness in skeletal muscle by caldesmon: implications for the pathway to force generation.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5739-43 PMID: 2062853
  45. Smooth muscle caldesmon. Rapid purification and F-actin cross-linking properties.
    J Biol Chem. 1984 Oct 25;259(20):12873-80 PMID: 6092349
  46. Interaction of myosin subfragments with F-actin.
    Biochemistry. 1978 Dec 12;17(25):5431-9 PMID: 153150
  47. Characterization of radial force and radial stiffness in Ca(2+)-activated skinned fibres of the rabbit psoas muscle.
    J Physiol. 1991 Sep;441:703-18 PMID: 1816390
  48. Dynamic interaction between actin and myosin subfragment 1 in the presence of ADP.
    Biochemistry. 1989 Jul 11;28(14):5864-71 PMID: 2528376
  49. Binding of gizzard smooth muscle myosin subfragment 1 to actin in the presence and absence of adenosine 5'-triphosphate.
    Biochemistry. 1983 Feb 1;22(3):530-5 PMID: 6838810
  50. Actin mediated regulation of muscle contraction.
    Pharmacol Ther. 1992;55(2):95-148 PMID: 1289901
  51. X-ray evidence for two structural states of the actomyosin cross-bridge in muscle fibers.
    Proc Natl Acad Sci U S A. 1984 Apr;81(8):2364-8 PMID: 6585803
  52. Passive tension and stiffness of vertebrate skeletal and insect flight muscles: the contribution of weak cross-bridges and elastic filaments.
    Biophys J. 1993 Nov;65(5):2141-59 PMID: 8298040
  53. Effect of Ca2+ on weak cross-bridge interaction with actin in the presence of adenosine 5'-[gamma-thio]triphosphate).
    Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11362-6 PMID: 1454820
  54. Electron cryomicroscopy of acto-myosin-S1 during steady-state ATP hydrolysis.
    Biophys J. 1994 May;66(5):1563-72 PMID: 8061205
  55. Structures of actomyosin crossbridges in relaxed and rigor muscle fibers.
    Biophys J. 1989 Mar;55(3):441-53 PMID: 2930830
  56. Mechanism of actomyosin adenosine triphosphatase. Evidence that adenosine 5'-triphosphate hydrolysis can occur without dissociation of the actomyosin complex.
    Biochemistry. 1979 Sep 4;18(18):3895-909 PMID: 158378
  57. Dissociation of the actin.subfragment 1 complex by adenyl-5'-yl imidodiphosphate, ADP, and PPi.
    J Biol Chem. 1980 Jan 25;255(2):543-8 PMID: 6243280
  58. Characterization of a caldesmon fragment that competes with myosin-ATP binding to actin.
    Biophys J. 1993 Aug;65(2):892-8 PMID: 8218912
  59. The dissociation constant of the actin-heavy meromyosin subfragment-1 complex.
    Biochemistry. 1975 Aug 26;14(17):3868-73 PMID: 126077
  60. Photolysis of a photolabile precursor of ATP (caged ATP) induces microsecond rotational motions of myosin heads bound to actin.
    Proc Natl Acad Sci U S A. 1989 Nov;86(22):8753-7 PMID: 2554328
  61. Cooperation within actin filament in vertebrate skeletal muscle.
    Nat New Biol. 1972 Jul 26;238(82):97-101 PMID: 4261616
  62. Mechanism of action of troponin . tropomyosin. Inhibition of actomyosin ATPase activity without inhibition of myosin binding to actin.
    J Biol Chem. 1981 Jan 25;256(2):575-8 PMID: 6450206
  63. Localization and characterization of a 7.3-kDa region of caldesmon which reversibly inhibits actomyosin ATPase activity.
    J Biol Chem. 1992 Aug 15;267(23):16644-50 PMID: 1386604
  64. Structure of the actin-myosin complex and its implications for muscle contraction.
    Science. 1993 Jul 2;261(5117):58-65 PMID: 8316858
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
DOI
10.1016/S0006-3495(95)80423-6
Published
1995-06-00
Pages
2404-18
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1282151
Subset
IM
Grants
NIAMS NIH HHS · AR40540 · United States
External Links
PubMed source DOI: 10.1016/S0006-3495(95)80423-6 PMC Full Text View journal details
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