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Tetrahexylammonium ions increase Ca2+ sensitivity of contraction of guinea-pig ileal smooth muscle

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Effects of tetraalkylammonium ions, having tetraalkyl chains of increasing length from ethyl to octyl, on inositol-trisphosphate (InsP 3)-induced Ca2+ release and contractile mechanics were examined in guinea-pig skinned ileal smooth muscle longitudinal strips. Although tetrahexylammonium ions (THexA) appeared to be the most potent inhibitor of Ca2+ release among the tetraalkylammonium ions examined, an additional and more prominent effect was found, i.e., the contraction induced by Ca2+ release showed a large sustained component in the presence of THexA. Potentiation of the contraction by THexA (above 30 μM) was also observed in skinned fibers in which the sarcoplasmic reticulum function was destroyed by treatment with A23187. The potentiating effect of THexA was the most potent by far among the tetraalkylammonium ions examined and was elicited by Ca2+-dependent and GTP-binding-protein-independent mechanisms. The potentiation was not due to activation of myosin light-chain kinase. The selective inhibitors of myosin light-chain kinase, protein kinase C and calmodulin reduced THexA-induced potentiation of contraction only at concentrations above 30 μM, at which non-specific effects are likely. Furthermore, relaxation induced by changing pCa from 4.5 to 8.5 was not affected by 1 mM THexA, suggesting that the potentiating effect is not mainly due to inhibition of myosin light-chain phosphatase. In conclusion, THexA sensitizes guinea-pig skinned ileal smooth muscle to Ca2+ in a structure-selective manner. This sensitization appears not to be mediated mainly by a GTP-binding protein, by activation of myosin light-chain kinase or protein kinase C, by enhanced Ca2+ binding to calmodulin, or by inhibition of myosin light-chain phosphatase.

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References

  1. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361:315–325

    Article  PubMed  Google Scholar 

  2. Chadwick CC, Saito A, Fleisher S (1990) Isolation and characterisation of the inositol trisphosphate receptor from smooth muscle. Proc Natl Acad Sci USA 87:2132–2136

    PubMed  Google Scholar 

  3. Collins EM, Walsh MP, Morgan KG (1992) Contraction of single vascular smooth muscle cells by phenylephrine at constant [Ca]i. Am J Physiol 252:H754-H762

    Google Scholar 

  4. Coronado R, Miller C (1979) Voltage-dependent caesium blockade of a cation channel from fragmented sarcoplasmic reticulum. Nature 280:807–810

    Google Scholar 

  5. Coronado R, Miller C (1980) Decamethonium and hexamethonium block K+ channels of sarcoplasmic reticulum. Nature 284:495–497

    Google Scholar 

  6. Gong MC, Fuglsang A, Alessi D, Kobayashi S, Cohen P, Somlyo AV, Somlyo AP (1992) Arachidonic acid inhibits myosin light-chain phosphatase and sensitizes smooth muscle to calcium. J Biol Chem 267:21492–21498

    PubMed  Google Scholar 

  7. Herrman-Frank A, Darling E, Meissner G (1991) Functional characterisation of the Ca2+-gated Ca2+-release channel of vascular smooth muscle sarcoplasmic reticulum. Pflügers Arch 418:353–359

    Google Scholar 

  8. Hidaka Y, Kobayashi R (1992) Pharmacology of protein kinase inhibitors. Annu Rev Pharmacol Toxicol 32:377–397

    Article  PubMed  Google Scholar 

  9. Hirata K, Kikuchi A, Sasaki T, Kuroda S, Kaibuchi K, Matsuura Y, Seki H, Saida K, Takai Y (1992) Involvement of rho p21 in the GTP-enhanced calcium ion sensitivity of smooth muscle contraction. J Biol Chem 267:8719–8722

    PubMed  Google Scholar 

  10. Ikebe M, Inagaki M, Naka M, Hidaka H (1988) Correlation of conformation and phosphorylation and dephosphorylation of smooth muscle myosin. J Biol Chem 263:10698–10704

    PubMed  Google Scholar 

  11. Itoh T, Kanmura Y, Kuriyama H (1985) A23187 increases calcium permeability of store sites more than of surface membranes in the rabbit mesenteric artery. J Physiol (Lond) 359:467–484

    Google Scholar 

  12. Katsuyama H, Morgan KG (1993) Mechanisms of Ca2+-independent contraction in single permeabilized ferret aorta cells. Circ Res 72:651–657

    PubMed  Google Scholar 

  13. Kitazawa T, Somlyo AP (1990) Desensitization and muscarinic resensitization of force and myosin light chain phosphorylation to cytoplasmic Ca2+ in smooth muscle. Biochem Biophys Res Commun 172:1291–1297

    PubMed  Google Scholar 

  14. Kitazawa T, Gaylin BD, Denney GH, Somlyo AP (1991) Gprotein-mediated Ca2+ sensitization of smooth muscle contraction through myosin light chain phosphorylation. J Biol Chem 266:1708–1715

    PubMed  Google Scholar 

  15. Kobayashi S, Kitazawa T, Somlyo AV, Somlyo AP (1989) Cytosolic heparin inhibits muscarinic and α-adrenargic Ca2+ release in smooth muscle: physiological role of inositol 1,4,5-trisphosphate in pharmacomechanical coupling. J Biol Chem 264:17997–18004

    PubMed  Google Scholar 

  16. Kuroda S, Kikuchi A, Hirata K, Masuda T, Kishi K, Sasaki T, Takai Y (1992) Cooperative function of rho GDS and rho GDI to regulate rho p21 activation in smooth muscle. Biochem Biophys Res Commun 185473:473–480

    Google Scholar 

  17. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    PubMed  Google Scholar 

  18. Martell AE, Smith RE (1974–1982) Critical stability constants, vol 1–5. Plenum, New York

    Google Scholar 

  19. McKinley D, Meissner G (1978) Evidence for a K+, Na+ permeable channel in sarcoplasmic reticulum. J Membrane Biol 44:159–186

    Google Scholar 

  20. Miller C (1978) Voltage-gated cation conductance channel from fragmented sarcoplasmic reticulum: steady state electrical properties. J Membrane Biol 40:1–23

    Google Scholar 

  21. Miller C (1982) Bis-quaternary ammonium blockers as structural probes of the sarcoplasmic reticulum K+ channel. J Gen Physiol 79:869–891

    Article  PubMed  Google Scholar 

  22. Missiaen L, Desmedt H, Droogmans G, Himpens B, Casteels R (1992) Calcium ion homeostasis in smooth muscle. Pharmacol Ther 56:191–231

    Article  PubMed  Google Scholar 

  23. Muallem S, Schoeffied M, Pandol S, Sachs G (1985) Inositol trisphosphate modification of ion transport in rough endoplasmic reticulum. Proc Natl Acad Sci USA 82:4433–4437

    PubMed  Google Scholar 

  24. Ngai PK, Carruthers CA, Walsh MP (1984) Isolation of the native form of chicken gizzard myosin light-chain kinase. Biochem 1218:863–870

    Google Scholar 

  25. Nishimura J, Kolber M, Breemen C van (1988) Norepinephrine and GTPγS increase myofilament Ca2+ sensitivity in α-toxin permeabilized arterial smooth muscle. Biochem Biophys Res Commun 157:677–683

    PubMed  Google Scholar 

  26. Palade P, Dettbarn C, Volpe P, Alderson B, Otero AS (1989) Direct inhibition of inositol-1,4,5-trisphosphate-induced Ca2+ release from brain microsomes by K+ channel blockers. Mol Pharmacol 36:664–672

    PubMed  Google Scholar 

  27. Persechini A, Hartshorne DJ (1981) Phosphorylation of smooth muscle myosin: evidence for cooperativity between the myosin heads. Science 213:1383–1385

    PubMed  Google Scholar 

  28. Ralston AW, Hoerr CW (1942) Studies on high molecular weight aliphatic amines and their salts. VI. Electrical conductivities of aqueous solutions of the hydrochlorides of octyl-, decyl-, tetra-decyl- and hexadecylamines. J Am Chem Soc 64:772–776

    Google Scholar 

  29. Rhee SG, Choi KD (1992) Regulation of inositol phospholipid-specific phospholipase C isozymes. J Biol Chem 267:12393–12396

    PubMed  Google Scholar 

  30. Shah J, Pant HC (1988) Potassium-channel blockers inhibit inositol trisphosphate-induced calcium release in the microsomal fractions isolated from the rat brain. Biochem J 250:617–620

    PubMed  Google Scholar 

  31. Somlyo AP (1985) Excitation-contraction coupling and the ultrastructure of smooth muscle. Circ Res 57:497–508

    PubMed  Google Scholar 

  32. Uyama Y, Imaizumi Y, Watanabe M (1992) Effects of cyclopiazonic acid, a novel Ca2+-ATPase inhibitor, on contractile responses in skinned ileal smooth muscle. Br J Pharmacol 106:208–214

    PubMed  Google Scholar 

  33. Walsh MP, Hinkins S, Dabrowska R, Hartshorne DJ (1983) Smooth muscle myosin light-chain kinase. Methods Enzymol 99:279–288

    PubMed  Google Scholar 

  34. Walsh MP, Valentine KA, Ngai PK, Carruthers CA, Hollenberg MD (1984) Ca2+-dependent hydrophobic interaction chromatography: isolation of a novel Ca2+-binding protein and protein kinase C from bovine brain. Biochem J 224:117–127

    PubMed  Google Scholar 

  35. Winder SJ, Walsh MP (1990) Smooth muscle calponin: inhibition of actomyosin MgATPase and regulation by phosphorylation. J Biol Chem 265:10148–10155

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Chemical Pharmacology, Faculty of Pharmaceutical Sciences, Nagoya City University, 3-1 Tanabedori, Mizohoku, 467, Nagoya, Japan

    Yoshiaki Uyama, Katsuhiko Muraki, Yuji Imaizumi & Minoru Watanabe

  2. Department of Medical Biochemistry, Faculty of Medicine, University of Calgary, T2N 4N1, Calgary, Alberta, Canada

    Michael P. Walsh

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  1. Yoshiaki Uyama
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  2. Katsuhiko Muraki
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  3. Michael P. Walsh
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  4. Yuji Imaizumi
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  5. Minoru Watanabe
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Uyama, Y., Muraki, K., Walsh, M.P. et al. Tetrahexylammonium ions increase Ca2+ sensitivity of contraction of guinea-pig ileal smooth muscle. Pflugers Arch. 426, 363–370 (1994). https://doi.org/10.1007/BF00388298

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  • DOI: https://doi.org/10.1007/BF00388298

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