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Effects of exogenously applied calponin on Ca2+-regulated force in skinned smooth muscle of the rabbit mesenteric artery

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Abstract

To help elucidate the physiological role of calponin (a thin-filament-linked regulatory protein) in smooth muscle contraction, the effects of its exogenous application were investigated on actin-activated MgATPase activity in crude actomyosin from chicken gizzard, and on contraction induced by Ca2+-dependent and -independent means in arterial smooth muscle strips skinned by saponin or β-escin. Calponin concentration dependently inhibited actin-activated MgATPase activity with a proportional increase in its binding to actomyosin and also attenuated Ca2+-induced contractions, in the presence or absence of calmodulin, in skinned arterial strips. Calponin, when phosphorylated by protein kinase C, reduced both its ability to bind to actomyosin and its inhibitory action on actomyosin MgATPase. The phosphorylated calponin also had no effect on the maximum Ca2+-induced contraction in skinned smooth muscle, suggesting that these actions of calponin are not non-specific. Calponin attenuated the Ca2+-independent contraction observed in myosin light chain thio-phosphorylated strips, or on application of trypsin-treated myosin light chain kinase. However, calponin had no effect on maintained rigor contraction. These results suggest that in vascular smooth muscle, calponin may play a physiological role in the inhibition of Ca2+-regulated force, possibly through a direct action on active actin-myosin interactions.

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References

  1. Barany M, Rokolya A, Barany K (1991) Absence of calponin phosphorylation in contracting or resting arterial smooth muscle. FEBS Lett 279:65–68

    CAS  PubMed  Google Scholar 

  2. Cassidy P, Hoar PE, Kerrick WGL (1979) Irreversible thiophosphorylation and activation of tension in functionally skinned rabbit ileum strips by [35S]ATPγS. J Biol Chem 254:11 148–11 153

    CAS  Google Scholar 

  3. Chatterjee M, Tejada M (1986) Phorbol ester-induced contraction in chemically skinned vascular smooth muscle. Am J Physiol 251:C356-C361

    CAS  PubMed  Google Scholar 

  4. Hartshorne DJ (1987) Biochemistry of the contractile process in smooth muscle. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 2nd edn. Raven, New York, pp 423–482

    Google Scholar 

  5. Horiuchi KY, Chacko S (1991) The mechanism for the inhibition of actin-activated ATPase of smooth muscle heavy meromyosin by calponin. Biochem Biophys Res Commun 176:1487–1493

    Article  CAS  PubMed  Google Scholar 

  6. Ichikawa K, Ito M, Okubo S, Konishi T, Nakano T, Mino T, Nakamura F, Naka M, Tanaka T (1993) Calponin phosphatase from smooth muscle: a possible role of type 1 protein phosphatase in smooth muscle relaxation. Biochem Biophys Res Commun 193:827–833

    Article  CAS  PubMed  Google Scholar 

  7. Ikebe M, Hartshorne DJ (1985) Effects of Ca2+ on the conformation and enzymatic activity of smooth muscle myosin. J Biol Chem 260:13 146–13 153

    CAS  Google Scholar 

  8. Ikebe M, Stepinska M, Kemp BE, Means AR, Hartshorne DJ (1987) Proteolysis of smooth muscle myosin light chain kinase. J Biol Chem 260:13828–13834

    Google Scholar 

  9. Ito T, Kanmura Y, Kuriyama H, Sasaguri T (1985) Nitroglycerine- and isoprenaline-induced vasodilatation: assessment from the actions of cyclic nucleotides. Br J Pharmacol 84:393–406

    Google Scholar 

  10. Itoh T, Kanmura Y, Kuriyama H (1986) Inorganic phosphate regulates the contraction-relaxation cycle in skinned muscles of the rabbit mesenteric artery. J Physiol (Lond) 376:231–252

    CAS  Google Scholar 

  11. Itoh T, Kanmura Y, Kuriyama H, Sumimoto K (1986) A phorbol ester has dual actions on the mechanical response in the rabbit mesenteric and porcine coronary arteries. J Physiol (Lond) 375:515–534

    CAS  Google Scholar 

  12. Itoh T, Ikebe M, Kargacin GJ, Hartshorne DJ, Kemp BE, Fay FS (1989) Effects of modulators of myosin light-chain kinase activity in single smooth muscle cells. Nature 338:164–167

    Article  CAS  PubMed  Google Scholar 

  13. Itoh T, Suzuki S, Kuriyama H (1990) Effects of pinacidil on contractile proteins in high K+-treated intact, and in β-escintreated skinned smooth muscle of the rabbit mesenteric artery. Br J Pharmacol 103:1697–1702

    Google Scholar 

  14. Kamm KE, Stull JT (1989) Regulation of smooth muscle contractile elements by second messengers. Annu Rev Physiol 51:299–313

    Article  CAS  PubMed  Google Scholar 

  15. Kobayashi S, Kitazawa T, Somlyo AV, Somlyo AP (1989) Cytosolic heparin inhibits muscarinic and α-adrenergic Ca2+ release in smooth muscle. J Biol Chem 264:17997–18004

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  17. Makuch R, Birukov K, Shirinsky V, Dabrowska R (1991) Functional interrelationship between calponin and caldesmon. Biochem J 280:33–38

    CAS  PubMed  Google Scholar 

  18. Moss RL (1992) Ca2+ regulation of mechanical properties of striated muscle. Circ Res 70:865–884

    CAS  PubMed  Google Scholar 

  19. Naka M, Kureishi Y, Muroga Y, Takahashi K, Ito M, Tanaka T (1990) Modulation of smooth muscle calponin by protein kinase C and calmodulin. Biochem Biophys Res Commun 171:933–937

    Article  CAS  PubMed  Google Scholar 

  20. Nishida W, Abe M, Takahashi K, Hiwada K (1990) Do thin filaments of smooth muscle contain calponin? FEBS Lett 268:165–168

    Article  CAS  PubMed  Google Scholar 

  21. Nishimura J, Moreland S, Ahn HY, Kawase T, Moreland RS, van Breemen C (1992) Endothelin increases myofilament Ca2+ sensitivity in α-toxin-permeabilized rabbit mesenteric artery. Circ Res 71:951–959

    CAS  PubMed  Google Scholar 

  22. Pohl J, Walsh MP, Gerthoffer WT (1991) Calponin and caldesmon phosphorylation in canine tracheal smooth muscle (abstract). Biophys J 59:58a

    Google Scholar 

  23. Rasmussen H, Takuwa Y, Park S (1987) Protein kinase C in the regulation of smooth muscle contraction. FASEB J 1:177–185

    CAS  PubMed  Google Scholar 

  24. Shirinsky VP, Biryukov KG, Hettasch JM, Sellers JR (1992) Inhibition of the relative movement of actin and myosin by caldesmon and calponin. J Biol Chem 267:15886–15892

    CAS  PubMed  Google Scholar 

  25. Sobieszek A, Small JV (1976) Myosin-linked calcium regulation in vertebrate smooth muscle. J Mol Biol 102:75–92

    Article  CAS  PubMed  Google Scholar 

  26. Stull JT, Gallagher PJ, Herring BP, Kamm KE (1991) Vascular smooth muscle contractile elements. Hypertension 17:723–732

    CAS  PubMed  Google Scholar 

  27. Szpacenko A, Wagner J, Dabrowska R, Rüegg JC (1985) Caldesmon-induced inhibition of ATPase activity of actomyosin and contraction of skinned fibres of chicken gizzard smooth muscle. FEBS Lett 192:9–12

    Article  CAS  PubMed  Google Scholar 

  28. Taggart MJ, Marston SB (1988) The effects of vascular smooth muscle caldesmon on force production by ‘desensitised’ skeletal muscle fibres. FEBS Lett 242:171–174

    Article  CAS  PubMed  Google Scholar 

  29. Takahashi K, Hiwada K, Kokubu T (1986) Isolation and characterization of a 34 000 dalton calmodulin- and F-actin-binding protein from chicken gizzard smooth muscle. Biochem Biophys Res Commun 141:20–26

    Article  CAS  PubMed  Google Scholar 

  30. Takahashi K, Hiwada K, Kokubu T (1987) Occurrence of anti-gizzard P34k antibody cross-reactive components in bovine smooth muscles and non-smooth muscle tissues. Life Sci 41:291–296

    Article  CAS  PubMed  Google Scholar 

  31. Takahashi K, Hiwada K, Kokubu T (1988) Vascular smooth muscle calponin. Hypertension 11:620–626

    CAS  PubMed  Google Scholar 

  32. Tanaka T, Naka M, Hidaka H (1980) Activation of myosin light chain kinase by trypsin. Biochem Biophys Res Commun 92:313–318

    Article  CAS  PubMed  Google Scholar 

  33. Walsh MP (1990) Smooth muscle caldesmon. In: Sperelakis N, Wood JD (eds) Frontiers in smooth muscle research. Liss, New York, pp 127–140

    Google Scholar 

  34. Walsh MP, Bridenbaugh R, Kerrick WGL, Hartshorne DJ (1983) Gizzard Ca2+-independent myosin light chain kinase: evidence in favor of the phosphorylation theory. Fed Proc 42:45–50

    CAS  PubMed  Google Scholar 

  35. Winder SJ, Walsh MP (1990) Smooth muscle calponin. J Biol Chem 265:10148–10155

    CAS  PubMed  Google Scholar 

  36. Winder SJ, Pato MD, Walsh MP (1992) Purification and characterization of calponin phosphatase from smooth muscle. Biochem J 286:197–203

    CAS  PubMed  Google Scholar 

  37. Yazawa M, Sakuma M, Yagi K (1980) Calmodulins from muscles of marine invertebrates, scallop and sea anemone. J Biochem (Tokyo) 87:1313–1320

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacology, Faculty of Medicine, Kyushu University, 812, Fukuoka, Japan

    Takeo Itoh, Satoshi Suzuki & Akito Suzuki

  2. Department of Molecular and Cellular Pharmacology, Mie University School of Medicine, Edobashi, Tsu, 514, Mie, Japan

    Fumiaki Nakamura, Michiko Naka & Toshio Tanaka

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  1. Takeo Itoh
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  2. Satoshi Suzuki
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  3. Akito Suzuki
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  4. Fumiaki Nakamura
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  5. Michiko Naka
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  6. Toshio Tanaka
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Itoh, T., Suzuki, S., Suzuki, A. et al. Effects of exogenously applied calponin on Ca2+-regulated force in skinned smooth muscle of the rabbit mesenteric artery. Pflügers Arch 427, 301–308 (1994). https://doi.org/10.1007/BF00374538

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  • DOI: https://doi.org/10.1007/BF00374538

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