Home LiteratureArticle Details
PMID: 2940083 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Is a guanine nucleotide-binding protein involved in excitation-contraction coupling in skeletal muscle?

The EMBO journal ·Vol. 5 ·No. 2 ·1986-02-00 ·Pages 259-62

Di Virgilio F, Salviati G, Pozzan T, Volpe P

Abstract

Plasma membrane depolarization causes skeletal muscle contraction by triggering Ca2+ release from an intracellular membrane network, the sarcoplasmic reticulum. A specialized portion of the sarcoplasmic reticulum, the terminal cisternae, is junctionally associated with sarcolemmal invaginations called the transverse tubules, but the mechanism by which the action potential at the level of the transverse tubules is coupled to Ca2+ release from the terminal cisternae is still mysterious. Here we show that: (i) GTP gamma S, a non-hydrolyzable analog of GTP, elicits isometric force development in skinned muscle fibre; (ii) GTP gamma S is unable to release CA2+ from isolated sarcoplasmic reticulum fractions; (iii) the threshold for tension development is shifted to higher GTP gamma S concentrations by pre-incubation with pertussis toxin. These results suggest that a GTP-binding protein is involved in coupling the action potential of transverse tubules to Ca2+ release from the terminal cisternae.

MeSH Terms
Animals Calcium/metabolism Calcium-Transporting ATPases/metabolism Cell Membrane/physiology GTP-Binding Proteins/metabolism Guanosine 5'-O-(3-Thiotriphosphate) Guanosine Triphosphate/analogs & derivatives,pharmacology Isometric Contraction/drug effects Kinetics Muscle Contraction/drug effects Muscles/drug effects,physiology Pertussis Toxin Rabbits Sarcoplasmic Reticulum/drug effects,physiology Thionucleotides/pharmacology Virulence Factors, Bordetella/pharmacology
Chemicals
Thionucleotides Virulence Factors, Bordetella Guanosine 5'-O-(3-Thiotriphosphate) Guanosine Triphosphate Pertussis Toxin GTP-Binding Proteins Calcium-Transporting ATPases Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Di Virgilio F
Salviati G
Pozzan T
Volpe P
References (35)
35 references, click to expand
  1. Slow interaction of islet-activating protein with pancreatic islets during primary culture to cause reversal of alpha-adrenergic inhibition of insulin secretion.
    J Biol Chem. 1980 Oct 25;255(20):9580-8 PMID: 6253447
  2. Chemically skinned mammalian skeletal muscle. I. The structure of skinned rabbit psoas.
    Tissue Cell. 1979;11(3):553-66 PMID: 494240
  3. Local activation of striated muscle fibres.
    J Physiol. 1958 Dec 30;144(3):426-41 PMID: 13621406
  4. Involvement of guanine nucleotide-binding protein in the gating of Ca2+ by receptors.
    Nature. 1983 Nov 3-9;306(5938):64-6 PMID: 6195532
  5. Guanine nucleotides decrease the free [Ca2+] required for secretion of serotonin from permeabilized blood platelets. Evidence of a role for a GTP-binding protein in platelet activation.
    FEBS Lett. 1984 Aug 20;174(1):90-5 PMID: 6088288
  6. The reversible delipidation of a solubilized sodium-plus-potassium ion-dependent adenosine triphosphatase from the salt gland of the spiny dogfish.
    Biochem J. 1975 Oct;151(1):61-6 PMID: 174557
  7. The messenger across the gap.
    Nature. 1985 Jul 25-31;316(6026):298-9 PMID: 2862586
  8. STUDIES OF THE TRIAD : I. Structure of the Junction in Frog Twitch Fibers.
    J Cell Biol. 1970 Nov 1;47(2):488-99 PMID: 19866746
  9. Guanine nucleotides can activate the insulin-stimulated phosphodiesterase in liver plasma membranes.
    FEBS Lett. 1983 Apr 5;154(1):87-91 PMID: 6299798
  10. Pertussis toxin inhibits fMet-Leu-Phe- but not phorbol ester-stimulated changes in rabbit neutrophils: role of G proteins in excitation response coupling.
    Proc Natl Acad Sci U S A. 1985 May;82(9):2708-12 PMID: 3157993
  11. ADP-ribosylation of the specific membrane protein by islet-activating protein, pertussis toxin, associated with inhibition of a chemotactic peptide-induced arachidonate release in neutrophils. A possible role of the toxin substrate in Ca2+-mobilizing biosignaling.
    J Biol Chem. 1984 Nov 25;259(22):13863-71 PMID: 6209272
  12. The gating behavior of a channel for Ca2+-induced Ca2+ release in fragmented sarcoplasmic reticulum.
    J Biochem. 1983 May;93(5):1271-85 PMID: 6309755
  13. Inositol 1,4,5-trisphosphate: a possible chemical link in excitation-contraction coupling in muscle.
    Proc Natl Acad Sci U S A. 1985 Sep;82(18):6352-6 PMID: 2994073
  14. The intracellular site of calcium activaton of contraction in frog skeletal muscle.
    J Gen Physiol. 1970 Jan;55(1):77-88 PMID: 5410491
  15. Inositol 1,4,5-trisphosphate induces calcium release from sarcoplasmic reticulum of skeletal muscle.
    Nature. 1985 Jul 25-31;316(6026):347-9 PMID: 2410794
  16. The inhibitory guanine nucleotide-binding regulatory component of adenylate cyclase. Properties and function of the purified protein.
    J Biol Chem. 1984 Mar 25;259(6):3568-77 PMID: 6323430
  17. Insulin and glucagon regulate the activation of two distinct membrane-bound cyclic AMP phosphodiesterases in hepatocytes.
    Biochem J. 1983 Jul 15;214(1):99-110 PMID: 6311178
  18. Inositol trisphosphate, a novel second messenger in cellular signal transduction.
    Nature. 1984 Nov 22-28;312(5992):315-21 PMID: 6095092
  19. Role of guanine nucleotide binding protein in the activation of polyphosphoinositide phosphodiesterase.
    Nature. 1985 Apr 11-17;314(6011):534-6 PMID: 2986003
  20. Inhibitors of Ca2+ release from the isolated sarcoplasmic reticulum. I. Ca2+ channel blockers.
    Biochim Biophys Acta. 1985 Jun 11;816(1):9-17 PMID: 2408667
  21. The action of caffeine on the activation of the contractile mechanism in straited muscle fibres.
    J Physiol. 1968 Jan;194(1):51-74 PMID: 5639790
  22. Pertussis toxin inhibits the rise in the intracellular concentration of free calcium that is induced by chemotactic factors in rabbit neutrophils: possible role of the "G proteins" in calcium mobilization.
    Biochem Biophys Res Commun. 1984 Oct 30;124(2):644-50 PMID: 6093808
  23. Inositol phosphate formation in fMet-Leu-Phe-stimulated human neutrophils does not require an increase in the cytosolic free Ca2+ concentration.
    Biochem J. 1985 Jul 15;229(2):361-7 PMID: 4038273
  24. Adenine nucleotide stimulation of Ca2+-induced Ca2+ release in sarcoplasmic reticulum.
    J Biol Chem. 1984 Feb 25;259(4):2365-74 PMID: 6698971
  25. Calcium release from the sarcoplasmic reticulum.
    Physiol Rev. 1977 Jan;57(1):71-108 PMID: 13441
  26. Doxorubicin induces calcium release from terminal cisternae of skeletal muscle. A study on isolated sarcoplasmic reticulum and chemically skinned fibers.
    J Biol Chem. 1985 Jun 25;260(12):7349-55 PMID: 2581966
  27. Muscarinic receptor-induced phosphoinositide hydrolysis at resting cytosolic Ca2+ concentration in PC12 cells.
    J Cell Biol. 1985 Apr;100(4):1330-3 PMID: 2984215
  28. Transducin and the cyclic GMP phosphodiesterase: amplifier proteins in vision.
    Cold Spring Harb Symp Quant Biol. 1983;48 Pt 2:841-52 PMID: 6327179
  29. LOCALIZATION OF CALCIUM-ACCUMULATING STRUCTURES IN STRIATED MUSCLE FIBERS.
    Science. 1965 Jan 8;147(3654):158-60 PMID: 14220445
  30. Regulation of tension in skinned muscle fibers: effect of high concentrations of Mg-ATP.
    Am J Physiol. 1977 Nov;233(5):C127-34 PMID: 411376
  31. Calcium accumulation by the sarcoplasmic reticulum in two populations of chemically skinned human muscle fibers. Effects of calcium and cyclic AMP.
    J Gen Physiol. 1982 Apr;79(4):603-32 PMID: 6279758
  32. Biochemical properties of hormone-sensitive adenylate cyclase.
    Annu Rev Biochem. 1980;49:533-64 PMID: 6105841
  33. Biochemical characterization, integrity, and sidedness of purified skeletal muscle triads.
    J Biol Chem. 1983 Aug 25;258(16):9867-77 PMID: 6136506
  34. Ca2+ dependence of stimulated 45Ca efflux in skinned muscle fibers.
    J Gen Physiol. 1981 Apr;77(4):419-443 PMID: 6264018
  35. The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum.
    J Gen Physiol. 1968 Nov;52(5):750-9 PMID: 5688082
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1986-02-00
Pages
259-62
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1166727
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com