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Effect of ATP on actin filament stiffness

Nature volume 347, pages 95–99 (1990)Cite this article

Abstract

ACTIN is an adenine nucleotide-binding protein and an ATPase1. The bound adenine nucleotide stabilizes the protein against denaturation2 and the ATPase activity, although not required for actin polymerization, affects the kinetics of this assembly (see ref. 3 for review). Here we provide evidence for another effect of adenine nucleotides. We find that actin filaments made from ATP-containing monomers, the ATPase activity of which hydrolyses ATP to ADP following polymerization, are stiff rods, whereas filaments prepared from ADP-monomers are flexible. ATP exchanges with ADP in such filaments and stiffens them. Because both kinds of actin filaments contain mainly ADP, we suggest the alignment of actin monomers in filaments that have bound and hydrolysed ATP traps them conformationally and stores elastic energy. This energy would be available for release by actin-binding proteins that transduce force or sever actin filaments. These data support earlier proposals that actin is not merely a passive cable, but has an active mechanochemical role in cell function4–6.

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References

  1. Straub, F. B. & Feuer, G. Biochim. biophys. Acta 4, 455–470 (1950).

    Article  CAS  Google Scholar 

  2. Asakura, S. Arch. Biochem. Biophys. 92, 140–151 (1961).

    Article  CAS  Google Scholar 

  3. Carlier, M.-F. Int. Rev. Cytol. 115, 139–170 (1989).

    Article  CAS  Google Scholar 

  4. Szent-Gyorgyi, A. & Prior, G. J. molec. Biol. 15, 515–538 (1966).

    Article  CAS  Google Scholar 

  5. Yanagida, T. & Oosawa, F. J. molec. Biol. 126, 507–524 (1978).

    Article  CAS  Google Scholar 

  6. Schutt, C. E., Lindberg, U., Myslik, J. & Strauss, N. J. molec. Biol. 209, 735–746 (1989).

    Article  CAS  Google Scholar 

  7. Neidl, C. & Engel, J. Eur. J. Biochem. 101, 163–169 (1979).

    Article  CAS  Google Scholar 

  8. Yin, H. L. & Stossel, T. P. Nature 281, 583–586 (1979).

    Article  ADS  CAS  Google Scholar 

  9. Janmey, P. A. & Stossel, T. P. J. Muscle Res. Cell Motil. 7, 446–454 (1986).

    Article  CAS  Google Scholar 

  10. Pollard, T. D. J. Cell Biol. 103, 2747–2754 (1986).

    Article  CAS  Google Scholar 

  11. Brenner, S. L. & Korn, E. D. J. biol. Chem. 259, 1441–1446 (1984).

    CAS  PubMed  Google Scholar 

  12. Hozumi, T. J.Biochem. 104, 285–288 (1988).

    Article  CAS  Google Scholar 

  13. Dancker, P. & Fischer, S. Z. Naturforsch. 44c, 698–704 (1989).

    Article  Google Scholar 

  14. Martonosi, A., Gouvea, M. A. & Gergeley, J. J. biol. Chem. 235, 1700 (1960).

    CAS  PubMed  Google Scholar 

  15. Doi, M. & Kuzuu, N. Y. J. Polym. Sci. Polym. Phys. Ed. 18, 409–419 (1980).

    Article  ADS  CAS  Google Scholar 

  16. Janmey, P. A. et al. Biochemistry 27, 8218–8227 (1988).

    Article  CAS  Google Scholar 

  17. Ferry, J. Viscoelastic properties of polymers (John Wiley, New York, 1980).

    Google Scholar 

  18. deGennes, P. G. Macromolecules 9, 587–593 (1976).

    Article  ADS  CAS  Google Scholar 

  19. Ookubo, N., Komatsubara, M., Nakajima, H. & Wada, Y. Biopolymers 15, 929–947 (1976).

    Article  CAS  Google Scholar 

  20. Newman, J. & Carlson, F. D. Biophys. J. 29, 37–48 (1980).

    Article  ADS  CAS  Google Scholar 

  21. Oosawa, F. & Asakura, S. J. molec. Biol. 161, 217–227 (1982).

    Article  Google Scholar 

  22. Janmey, P., Amis, E. & Ferry, J. J. Rheol. 27, 135–153 (1983).

    Article  ADS  Google Scholar 

  23. Fujime, S. & Ishiwata, S. J. molec. Biol. 62, 251–265 (1971).

    Article  CAS  Google Scholar 

  24. Schmidt, C. F., Baermann, M., Isenberg, G. & Sackmann, E. Macromolecules 22, 3638–3649 (1989).

    Article  ADS  CAS  Google Scholar 

  25. Rich, S. A. & Estes, J. E. J. molec. Biol. 104, 777–792 (1976).

    Article  CAS  Google Scholar 

  26. Faulstich, H., Merkler, I., Blackholm, H. & Stournaras, C. Biochemistry 23, 1608–1612 (1984).

    Article  CAS  Google Scholar 

  27. Aebi, U., Millonig, R., Salvo, H. & Engel, A. Ann. NY. Acad. Sci. 483, 100–119 (1986).

    Article  ADS  CAS  Google Scholar 

  28. Egelman, E. H. J. Muscle Res. Cell Motil. 6, 129–151 (1985).

    Article  CAS  Google Scholar 

  29. Erickson, H. J. molec. Biol. 208. 465–474 (1989).

    Article  Google Scholar 

  30. Coue, M. & Korn, E. J. biol. Chem. 261, 3628–3631 (1986).

    CAS  PubMed  Google Scholar 

  31. Coue, M. & Korn, E. D. J. biol. Chem. 260, 15033–15041 (1985).

    CAS  PubMed  Google Scholar 

  32. Ando, T. J. Biochem. 105, 818–822 (1989).

    Article  CAS  Google Scholar 

  33. Pollard, T. J. Cell Biol. 99, 769–777 (1984).

    Article  CAS  Google Scholar 

  34. Kouyama, T. & Mihashi, K. Eur. J. Biochem. 114, 33–38 (1981).

    Article  CAS  Google Scholar 

  35. Heuser, J. J. molec. Biol. 169, 155–195 (1983).

    Article  CAS  Google Scholar 

  36. Greaser, M. & Gergely, J. J. biol. Chem. 246, 4226–4232 (1971).

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Hematology Unit, Massachusetts General Hospital, Department of Medicine, Harvard Medical School, Boston, Massachusetts, 02114, USA

    Paul A. Janmey, Jennifer Lamb, Thomas P. Stossel & John H. Hartwig

  2. Hematology Unit, Massachusetts General Hospital, Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, Massachusetts, 02114, USA

    Paul A. Janmey

  3. Hematology Unit, Massachusetts General Hospital, Department of Anatomy and Cellular Biology, Harvard Medical School, Boston, Massachusetts, 02114, USA

    John H. Hartwig

  4. Department of Chemistry, Ris0 National Laboratory and Roskilde University, DK-4000, Roskilde, Denmark

    Soren Hvidt

  5. Departments of Entomology and Biophysics, University of California, Berkeley, California, 94720, USA

    George F. Oster

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  1. Paul A. Janmey
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  4. Jennifer Lamb
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  5. Thomas P. Stossel
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  6. John H. Hartwig
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Janmey, P., Hvidt, S., Oster, G. et al. Effect of ATP on actin filament stiffness. Nature 347, 95–99 (1990). https://doi.org/10.1038/347095a0

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