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. 1995 Feb 15;306(Pt 1):199–204. doi: 10.1042/bj3060199

Interaction of calponin with actin and its functional implications.

J Kołakowski 1, R Makuch 1, D Stepkowski 1, R Dabrowska 1
PMCID: PMC1136501  PMID: 7864810

Abstract

Titration of F-actin with calponin causes the formation of two types of complexes. One, at saturation, contains a lower ratio of calponin to actin (0.5:1) and is insoluble at physiological ionic strength. The another is soluble, with a higher ratio of calponin to actin (1:1). Electron microscopy revealed that the former complex consists of paracrystalline bundles of actin filaments, whereas the latter consists of separate filaments. Ca(2+)-calmodulin causes dissociation of bundles with simultaneous increase in the number of separate calponin-containing filaments. Further increase in the calmodulin concentration results in full release of calponin from actin filaments. In motility assays, calponin, when added together with ATP to actin filaments complexed with immobilized myosin, evoked a decrease in both the number and velocity of moving actin filaments. Addition of calponin to actin filaments before their binding to myosin resulted in a formation of actin filament bundles which were dissociated by ATP.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abe M., Takahashi K., Hiwada K. Effect of calponin on actin-activated myosin ATPase activity. J Biochem. 1990 Nov;108(5):835–838. doi: 10.1093/oxfordjournals.jbchem.a123289. [DOI] [PubMed] [Google Scholar]
  2. Crosbie R. H., Chalovich J. M., Reisler E. Interaction of caldesmon and myosin subfragment 1 with the C-terminus of actin. Biochem Biophys Res Commun. 1992 Apr 15;184(1):239–245. doi: 10.1016/0006-291x(92)91184-r. [DOI] [PubMed] [Google Scholar]
  3. Drabikowski W., Nonomura Y. The interaction of troponin with F-action and its abolition by tropomyosin. Biochim Biophys Acta. 1968 May 6;160(1):129–131. doi: 10.1016/0005-2795(68)90075-5. [DOI] [PubMed] [Google Scholar]
  4. Fürst D. O., Cross R. A., De Mey J., Small J. V. Caldesmon is an elongated, flexible molecule localized in the actomyosin domains of smooth muscle. EMBO J. 1986 Feb;5(2):251–257. doi: 10.1002/j.1460-2075.1986.tb04206.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gong B. J., Mabuchi K., Takahashi K., Nadal-Ginard B., Tao T. Characterization of wild type and mutant chicken gizzard alpha calponin expressed in E. coli. J Biochem. 1993 Oct;114(4):453–456. doi: 10.1093/oxfordjournals.jbchem.a124197. [DOI] [PubMed] [Google Scholar]
  6. Gopalakrishna R., Anderson W. B. Ca2+-induced hydrophobic site on calmodulin: application for purification of calmodulin by phenyl-Sepharose affinity chromatography. Biochem Biophys Res Commun. 1982 Jan 29;104(2):830–836. doi: 10.1016/0006-291x(82)90712-4. [DOI] [PubMed] [Google Scholar]
  7. Graceffa P., Adam L. P., Lehman W. Disulphide cross-linking of smooth-muscle and non-muscle caldesmon to the C-terminus of actin in reconstituted and native thin filaments. Biochem J. 1993 Aug 15;294(Pt 1):63–67. doi: 10.1042/bj2940063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Haeberle J. R. Calponin decreases the rate of cross-bridge cycling and increases maximum force production by smooth muscle myosin in an in vitro motility assay. J Biol Chem. 1994 Apr 29;269(17):12424–12431. [PubMed] [Google Scholar]
  9. Houk T. W., Jr, Ue K. The measurement of actin concentration in solution: a comparison of methods. Anal Biochem. 1974 Nov;62(1):66–74. doi: 10.1016/0003-2697(74)90367-4. [DOI] [PubMed] [Google Scholar]
  10. Kron S. J., Toyoshima Y. Y., Uyeda T. Q., Spudich J. A. Assays for actin sliding movement over myosin-coated surfaces. Methods Enzymol. 1991;196:399–416. doi: 10.1016/0076-6879(91)96035-p. [DOI] [PubMed] [Google Scholar]
  11. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  12. Lehman W. The effect of calcium on the aggregation of chicken gizzard thin filaments. J Muscle Res Cell Motil. 1986 Dec;7(6):537–549. doi: 10.1007/BF01753570. [DOI] [PubMed] [Google Scholar]
  13. Lehrer S. S., Betteridge D. R., Graceffa P., Wong S., Seidel J. C. Comparison of the fluorescence and conformational properties of smooth and striated tropomyosin. Biochemistry. 1984 Apr 10;23(8):1591–1595. doi: 10.1021/bi00303a001. [DOI] [PubMed] [Google Scholar]
  14. Levine B. A., Moir A. J., Perry S. V. The interaction of troponin-I with the N-terminal region of actin. Eur J Biochem. 1988 Mar 1;172(2):389–397. doi: 10.1111/j.1432-1033.1988.tb13899.x. [DOI] [PubMed] [Google Scholar]
  15. Makuch R., Birukov K., Shirinsky V., Dabrowska R. Functional interrelationship between calponin and caldesmon. Biochem J. 1991 Nov 15;280(Pt 1):33–38. doi: 10.1042/bj2800033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Makuch R., Kołakowski J., Dabrowska R. The importance of C-terminal amino acid residues of actin to the inhibition of actomyosin ATPase activity by caldesmon and troponin I. FEBS Lett. 1992 Feb 10;297(3):237–240. doi: 10.1016/0014-5793(92)80546-s. [DOI] [PubMed] [Google Scholar]
  17. Marston S. B. Properties of calponin isolated from sheep aorta thin filaments. FEBS Lett. 1991 Nov 4;292(1-2):179–182. doi: 10.1016/0014-5793(91)80862-w. [DOI] [PubMed] [Google Scholar]
  18. Mezgueldi M., Fattoum A., Derancourt J., Kassab R. Mapping of the functional domains in the amino-terminal region of calponin. J Biol Chem. 1992 Aug 5;267(22):15943–15951. [PubMed] [Google Scholar]
  19. Miki M., Walsh M. P., Hartshorne D. J. The mechanism of inhibition of the actin-activated myosin MgATPase by calponin. Biochem Biophys Res Commun. 1992 Sep 16;187(2):867–871. doi: 10.1016/0006-291x(92)91277-w. [DOI] [PubMed] [Google Scholar]
  20. Naka M., Kureishi Y., Muroga Y., Takahashi K., Ito M., Tanaka T. Modulation of smooth muscle calponin by protein kinase C and calmodulin. Biochem Biophys Res Commun. 1990 Sep 28;171(3):933–937. doi: 10.1016/0006-291x(90)90773-g. [DOI] [PubMed] [Google Scholar]
  21. Nishida W., Abe M., Takahashi K., Hiwada K. Do thin filaments of smooth muscle contain calponin? A new method for the preparation. FEBS Lett. 1990 Jul 30;268(1):165–168. doi: 10.1016/0014-5793(90)80999-y. [DOI] [PubMed] [Google Scholar]
  22. Noda S., Ito M., Watanabe S., Takahashi K., Maruyama K. Conformational changes of actin induced by calponin. Biochem Biophys Res Commun. 1992 May 29;185(1):481–487. doi: 10.1016/s0006-291x(05)81010-1. [DOI] [PubMed] [Google Scholar]
  23. North A. J., Gimona M., Cross R. A., Small J. V. Calponin is localised in both the contractile apparatus and the cytoskeleton of smooth muscle cells. J Cell Sci. 1994 Mar;107(Pt 3):437–444. doi: 10.1242/jcs.107.3.437. [DOI] [PubMed] [Google Scholar]
  24. North A. J., Gimona M., Lando Z., Small J. V. Actin isoform compartments in chicken gizzard smooth muscle cells. J Cell Sci. 1994 Mar;107(Pt 3):445–455. doi: 10.1242/jcs.107.3.445. [DOI] [PubMed] [Google Scholar]
  25. Pope B. J., Wagner P. D., Weeds A. G. Heterogeneity of myosin heavy chains in subfragment-1 isoenzymes rabbit skeletal myosin. J Mol Biol. 1977 Jan 25;109(3):470–473. doi: 10.1016/s0022-2836(77)80024-7. [DOI] [PubMed] [Google Scholar]
  26. Shirinsky V. P., Biryukov K. G., Hettasch J. M., Sellers J. R. Inhibition of the relative movement of actin and myosin by caldesmon and calponin. J Biol Chem. 1992 Aug 5;267(22):15886–15892. [PubMed] [Google Scholar]
  27. Stepkowski D., Szczesna D., Wrotek M., Kakol I. Factors influencing interaction of phosphorylated and dephosphorylated myosin with actin. Biochim Biophys Acta. 1985 Oct 18;831(3):321–329. doi: 10.1016/0167-4838(85)90114-1. [DOI] [PubMed] [Google Scholar]
  28. Takahashi K., Hiwada K., Kokubu T. Isolation and characterization of a 34,000-dalton calmodulin- and F-actin-binding protein from chicken gizzard smooth muscle. Biochem Biophys Res Commun. 1986 Nov 26;141(1):20–26. doi: 10.1016/s0006-291x(86)80328-x. [DOI] [PubMed] [Google Scholar]
  29. Takahashi K., Nadal-Ginard B. Molecular cloning and sequence analysis of smooth muscle calponin. J Biol Chem. 1991 Jul 15;266(20):13284–13288. [PubMed] [Google Scholar]
  30. Talbot J. A., Hodges R. S. Comparative studies on the inhibitory region of selected species of troponin-I. The use of synthetic peptide analogs to probe structure-function relationships. J Biol Chem. 1981 Dec 10;256(23):12374–12378. [PubMed] [Google Scholar]
  31. Vancompernolle K., Gimona M., Herzog M., Van Damme J., Vandekerckhove J., Small V. Isolation and sequence of a tropomyosin-binding fragment of turkey gizzard calponin. FEBS Lett. 1990 Nov 12;274(1-2):146–150. doi: 10.1016/0014-5793(90)81350-w. [DOI] [PubMed] [Google Scholar]
  32. Wills F. L., McCubbin W. D., Kay C. M. Characterization of the smooth muscle calponin and calmodulin complex. Biochemistry. 1993 Mar 9;32(9):2321–2328. doi: 10.1021/bi00060a025. [DOI] [PubMed] [Google Scholar]
  33. Winder S. J., Walsh M. P. Calponin: thin filament-linked regulation of smooth muscle contraction. Cell Signal. 1993 Nov;5(6):677–686. doi: 10.1016/0898-6568(93)90029-l. [DOI] [PubMed] [Google Scholar]
  34. Winder S. J., Walsh M. P. Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation. J Biol Chem. 1990 Jun 15;265(17):10148–10155. [PubMed] [Google Scholar]

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