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Ca2+-induced Ca2+ desensitization of myosin light chain phosphorylation and contraction in phasic smooth muscle

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Book cover Muscle Physiology and Biochemistry

Part of the book series: Molecular and Cellular Biochemistry ((DMCB,volume 31))

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Abstract

The temporal relationship between Ca2+-induced contraction and phosphorylation of 20 kDa myosin light chain (MLC) during a step increase in Ca2+ was investigated using permeabilized phasic smooth muscle from rabbit portal vein and guinea-pig ileum at 25°C. We describe here a Ca2+-induced Ca2+] desensitization phenomenon in which a transient rise in MLC phosphorylation is followed by a transient rise in contractile force. During and after the peak contraction, the force to phosphorylation ratio remained constant. Further treatment with cytochalasin D, an actin fragmenting agent, did not affect the transient increase in phosphorylation, but blocked force development. Together, these results indicate that the transient phosphorylation causes the transient contraction and that neither inhomogeneous contractility nor reduced thin filament integrity effects the transient phosphorylation. Lastly, we show that known inhibitors to MLC kinase kinases and to a Ca2+-dependent protein phosphatase did not eliminate the desensitized contractile force. This study suggests that the Ca2+-induced Ca2+ desensitization phenomenon in phasic smooth muscle does not result from any of the known intrinsic mechanisms involved with other aspects of smooth muscle contractility. (Mol Cell Biochem 190: 91–98, 1999

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References

  1. Ebashi S: Regulation of muscle contraction. Proc Roy Soc Lond, Series B 207: 259–286, 1980

    Article  CAS  Google Scholar 

  2. Hartshorne DJ: Biochemistry of the contractile process in smooth muscle. In: L.R. Johnson (ed). Physiology of the Gastrointestinal Tract. Raven Press, New York, 1987, pp 423–482

    Google Scholar 

  3. Kamm KE, Stull JT: Regulation of smooth muscle contractile elements by second messengers. Ann Rev Physiol 51: 299–313, 1989

    Article  CAS  Google Scholar 

  4. Kitazawa T, Gaznabi AKM, Murahashi T: Regulation of Ca2+ sensitivity of smooth muscle contraction by myosin light chain phosphatase. In: K. Maruyama, Y. Nonomura, K. Kohama (eds). Calcium as Cell Signal. Igakushoin Ltd., Tokyo, 1995, pp 185–193

    Google Scholar 

  5. Himpens B, Matthijs G, Somlyo AP: Desensitization to cytoplasmic Ca2+ and Ca2+ sensitivities of guinea-pig ileum and rabbit pulmonary artery smooth muscle. J Physiol (Lond) 413: 489–503, 1989

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  7. Hai CM: Length-dependent myosin phosphorylation and contraction of arterial smooth muscle. Pflügers Arch 418: 564–571, 1991

    Article  PubMed  CAS  Google Scholar 

  8. Moreland RS, Moreland S, Murphy RA: Dependence of stress on length, Ca2+, and myosin phosphorylation in skinned smooth muscle. Am J Physiol 255: C473–C478, 1988

    PubMed  CAS  Google Scholar 

  9. Obara K, Yabu H: Effect of cytochalasin b on intestinal smooth muscle cells. Eur J Pharmacol 255: 139–147, 1994

    Article  PubMed  CAS  Google Scholar 

  10. Cooper JA: Effects of cytochalasin and phalloidin on actin. J Cell Biol 105: 1473–1478, 1987

    Article  PubMed  CAS  Google Scholar 

  11. Hashimoto Y, Soderling TR: Phosphorylation of smooth muscle myosin light chain kinase by Ca2+/calmodulin-dependent protein kinase II: Comparative study of the phosphorylation sites. Arch Biochem Biophys 278: 41–45, 1990

    Article  PubMed  CAS  Google Scholar 

  12. Ikebe M, Reardon S: Phosphorylation of smooth myosin light chain kinase by smooth muscle Ca2+/calmodulin-dependent multifunctional protein kinase. J Biol Chem 265: 8975–8978, 1990

    PubMed  CAS  Google Scholar 

  13. Tansey MG, Lubyphelps K, Kamm KE, Stull JT: Ca2+-dependent phosphorylation of myosin light chain kinase decreases the Ca2+ sensitivity of light chain phosphorylation within smooth muscle cells. J Biol Chem 269: 9912–9920, 1994

    PubMed  CAS  Google Scholar 

  14. Walsh MP, Busaan LJ, Fraser DE, Fu S Y, Pato MD, Michalak M: Characterization of the recombinant C-terminal domain of dystrophin: Phosphorylation by calmodulin-dependent protein kinase II and dephosphorylation by type 2B protein phosphatase. Biochemistry 34: 5561–5568, 1995

    Article  PubMed  CAS  Google Scholar 

  15. Murahashi T, Fujita A, Kitazawa T: Transient increase in myosin light chain (MLC) phosphorylation at constant Ca2+ in permeabilized smooth muscle. Biophys J 68: A277 (abstract), 1995

    Google Scholar 

  16. Horiuti K: Mechanism of contracture on cooling of caffeine-treated frog skeletal muscle fibres. J Physiol (Lond) 398: 131–148, 1988

    CAS  Google Scholar 

  17. Kitazawa T, Gaylinn BD, Denney GH, Somlyo AP: G-protein-mediated Ca2+-sensitization of smooth muscle contraction through myosin light chain phosphorylation. J Biol Chem 266: 1708–1715, 1991

    PubMed  CAS  Google Scholar 

  18. Masuo M, Reardon S, Ikebe M, Kitazawa T: A novel mechanism for the Ca2+-sensitizing effect of protein kinase C on vascular smooth muscle: Inhibition of myosin light chain phosphatase. J Gen Physiol 104: 265–286, 1994

    Article  PubMed  CAS  Google Scholar 

  19. Tokumitsu H, Chijiwa T, Hagiwara M, Mizutani A, Terasawa M, Hidaka H: KN-62, l-[N,0-bis(5-isoquinolinesulfonyl)-N-methyl-L-tyrosyl]-4-phenylpiperazine, a specific inhibitor of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 265: 4315–4320, 1990

    PubMed  CAS  Google Scholar 

  20. Sumi M, Kiuchi K, Ishikawa T, Ishii A, Higawara M, Nagatsu T, Hidaka H: The newly synthesized selective Ca2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem Biophys Res Commun 181: 968–975, 1991

    Article  PubMed  CAS  Google Scholar 

  21. Kerrick WG, Hoar PE: Relationship between ATPase activity, Ca2+, and force in α-toxin and ß-escin-treated smooth muscle. Can J Physiol Pharmacol 72: 1361–1367, 1994

    Article  PubMed  CAS  Google Scholar 

  22. Trinklemulcahy L, Siegman MJ, Butler TM: Metabolic characteristics of oα-toxin permeabilized smooth muscle. Am J Physiol 266: C1673–C1683, 1994

    CAS  Google Scholar 

  23. Nishizuka Y: The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334: 661–665, 1988

    Article  PubMed  CAS  Google Scholar 

  24. Gailly P, Boland B, Paques C, Himpens B, Casteels R, Gillis JM: Post-Receptor pathway of the ATP-induced relaxation in smooth muscle of the mouse vas deferens. Br J Pharmacol 110: 326–330, 1993

    Article  PubMed  CAS  Google Scholar 

  25. Payne ME, Fong Y-L, Ono T, Colbran RJ, Kemp BE, Soderling TR, Means AR: Calcium/calmodulin-dependent protein kinase II: Characterization of distinct calmodulin binding and inhibitory domains. J Biol Chem 263: 7190–7195, 1988

    PubMed  CAS  Google Scholar 

  26. Waxham MN, Malenka RC, Kelly PT, Mauk MD: Calcium/calmodulin-dependent protein kinase II regulates hippocampal synaptic trans mission. Brain Res 609: 1–8, 1993

    Article  PubMed  CAS  Google Scholar 

  27. Ishida A, Kameshita I, Okuno S, Kitani T, Fujisawa H: A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 212: 806–812, 1995

    Article  PubMed  CAS  Google Scholar 

  28. Enan E, Matsumura F: Specific inhibition of calcineurin by type II synthetic pyrethroid insecticides. Biochem Pharmacol 43: 1777–1784, 1992

    Article  PubMed  CAS  Google Scholar 

  29. Dabrowska R, Hinkins S, Walsh MP, Hartshorne DJ: The binding of smooth muscle myosin light chain kinase to actin. Biochem Biophys Res Commun 107: 1524–1531, 1982

    Article  PubMed  CAS  Google Scholar 

  30. Khromov A, Somlyo AV, Trentham DR, Zimmermann B, Somlyo AP: The role of MgADP in force maintenance by dephosphorylated cross-bridge in smooth muscle: a flash photolysis study. Biophys J 69: 2611–2622, 1995

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Physiology and Biophysics, Georgetown University School of Medicine, Washington, DC, USA

    Tetsuya Murahashi, Akikazu Fujita & Toshio Kitazawa

Authors
  1. Tetsuya Murahashi
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  2. Akikazu Fujita
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  3. Toshio Kitazawa
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Editor information

Editors and Affiliations

  1. Department of Pharmacology, Niigata University School of Medicine, No. 757, Asahimachi-dori 1, Niigata 951, Japan

    Shoichi Imai

  2. Faculty of Medicine, Kyushu University, 812-82, Fukuoka, Japan

    Iwao Ohtsuki

  3. Saitama Medical School, 350-04, Moroyamamachi, Saitama, Japan

    Makoto Endo

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© 1999 Springer Science+Business Media Dordrecht

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Murahashi, T., Fujita, A., Kitazawa, T. (1999). Ca2+-induced Ca2+ desensitization of myosin light chain phosphorylation and contraction in phasic smooth muscle. In: Imai, S., Ohtsuki, I., Endo, M. (eds) Muscle Physiology and Biochemistry. Molecular and Cellular Biochemistry, vol 31. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5543-8_12

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  • DOI: https://doi.org/10.1007/978-1-4615-5543-8_12

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-7534-0

  • Online ISBN: 978-1-4615-5543-8

  • eBook Packages: Springer Book Archive

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