Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1995 Apr;68(4):1231–1245. doi: 10.1016/S0006-3495(95)80299-7

Dynamic and elastic properties of F-actin: a normal-modes analysis.

D ben-Avraham 1, M M Tirion 1
PMCID: PMC1282021  PMID: 7787015

Abstract

We examine the dynamic, elastic, and mechanical consequences of the proposed atomic models of F-actin, using a normal mode analysis. This initial analysis is done in vacuo and assumes that all monomers are rigid and equivalent. Our computation proceeds from the atomic level and, relying on a single fitting parameter, reproduces various experimental results, including persistence lengths, elastic moduli, and contact energies. The computations reveal modes of motion characteristic to all polymers, such as longitudinal pressure waves, torsional waves, and bending, as well as motions unique to F-actin. Motions typical to actin include a "groove-swinging" motion of the two long-pitch helices, as well as an axial slipping motion of the two strands. We prepare snapshots of thermally activated filaments and quantify the accumulation of azimuthal angular "disorder," variations in cross-over lengths, and various other fluctuations. We find that the orientation of a small number of select residues has a surprisingly large effect on the filament flexibility and elasticity characteristics.

Full text

PDF
1231

Selected References

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

  1. Bremer A., Millonig R. C., Sütterlin R., Engel A., Pollard T. D., Aebi U. The structural basis for the intrinsic disorder of the actin filament: the "lateral slipping" model. J Cell Biol. 1991 Nov;115(3):689–703. doi: 10.1083/jcb.115.3.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chen X., Cook R. K., Rubenstein P. A. Yeast actin with a mutation in the "hydrophobic plug" between subdomains 3 and 4 (L266D) displays a cold-sensitive polymerization defect. J Cell Biol. 1993 Dec;123(5):1185–1195. doi: 10.1083/jcb.123.5.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Diamond R. On the use of normal modes in thermal parameter refinement: theory and application to the bovine pancreatic trypsin inhibitor. Acta Crystallogr A. 1990 Jun 1;46(Pt 6):425–435. doi: 10.1107/s0108767390002082. [DOI] [PubMed] [Google Scholar]
  4. Doolittle R. F. Stein and Moore Award address. Reconstructing history with amino acid sequences. Protein Sci. 1992 Feb;1(2):191–200. doi: 10.1002/pro.5560010201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Egelman E. H. An algorithm for straightening images of curved filamentous structures. Ultramicroscopy. 1986;19(4):367–373. doi: 10.1016/0304-3991(86)90096-3. [DOI] [PubMed] [Google Scholar]
  6. Egelman E. H., DeRosier D. J. Image analysis shows that variations in actin crossover spacings are random, not compensatory. Biophys J. 1992 Nov;63(5):1299–1305. doi: 10.1016/S0006-3495(92)81716-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Egelman E. H., Francis N., DeRosier D. J. F-actin is a helix with a random variable twist. Nature. 1982 Jul 8;298(5870):131–135. doi: 10.1038/298131a0. [DOI] [PubMed] [Google Scholar]
  8. Erickson H. P. Co-operativity in protein-protein association. The structure and stability of the actin filament. J Mol Biol. 1989 Apr 5;206(3):465–474. doi: 10.1016/0022-2836(89)90494-4. [DOI] [PubMed] [Google Scholar]
  9. Faure P., Micu A., Pérahia D., Doucet J., Smith J. C., Benoit J. P. Correlated intramolecular motions and diffuse X-ray scattering in lysozyme. Nat Struct Biol. 1994 Feb;1(2):124–128. doi: 10.1038/nsb0294-124. [DOI] [PubMed] [Google Scholar]
  10. Goldman Y. E., Huxley A. F. Actin compliance: are you pulling my chain? Biophys J. 1994 Dec;67(6):2131–2133. doi: 10.1016/S0006-3495(94)80700-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hatta I., Sugi H., Tamura Y. Stiffness changes in frog skeletal muscle during contraction recorded using ultrasonic waves. J Physiol. 1988 Sep;403:193–209. doi: 10.1113/jphysiol.1988.sp017245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Holmes K. C., Popp D., Gebhard W., Kabsch W. Atomic model of the actin filament. Nature. 1990 Sep 6;347(6288):44–49. doi: 10.1038/347044a0. [DOI] [PubMed] [Google Scholar]
  13. Huxley H. E., Stewart A., Sosa H., Irving T. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J. 1994 Dec;67(6):2411–2421. doi: 10.1016/S0006-3495(94)80728-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kabsch W., Mannherz H. G., Suck D., Pai E. F., Holmes K. C. Atomic structure of the actin:DNase I complex. Nature. 1990 Sep 6;347(6288):37–44. doi: 10.1038/347037a0. [DOI] [PubMed] [Google Scholar]
  15. Kidera A., Go N. Normal mode refinement: crystallographic refinement of protein dynamic structure. I. Theory and test by simulated diffraction data. J Mol Biol. 1992 May 20;225(2):457–475. doi: 10.1016/0022-2836(92)90932-a. [DOI] [PubMed] [Google Scholar]
  16. Kojima H., Ishijima A., Yanagida T. Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12962–12966. doi: 10.1073/pnas.91.26.12962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Levitt M., Sander C., Stern P. S. Protein normal-mode dynamics: trypsin inhibitor, crambin, ribonuclease and lysozyme. J Mol Biol. 1985 Feb 5;181(3):423–447. doi: 10.1016/0022-2836(85)90230-x. [DOI] [PubMed] [Google Scholar]
  18. Lorenz M., Popp D., Holmes K. C. Refinement of the F-actin model against X-ray fiber diffraction data by the use of a directed mutation algorithm. J Mol Biol. 1993 Dec 5;234(3):826–836. doi: 10.1006/jmbi.1993.1628. [DOI] [PubMed] [Google Scholar]
  19. McLaughlin P. J., Gooch J. T., Mannherz H. G., Weeds A. G. Structure of gelsolin segment 1-actin complex and the mechanism of filament severing. Nature. 1993 Aug 19;364(6439):685–692. doi: 10.1038/364685a0. [DOI] [PubMed] [Google Scholar]
  20. Miki M., Kouyama T. Domain motion in actin observed by fluorescence resonance energy transfer. Biochemistry. 1994 Aug 23;33(33):10171–10177. doi: 10.1021/bi00199a045. [DOI] [PubMed] [Google Scholar]
  21. Orlova A., Egelman E. H. A conformational change in the actin subunit can change the flexibility of the actin filament. J Mol Biol. 1993 Jul 20;232(2):334–341. doi: 10.1006/jmbi.1993.1393. [DOI] [PubMed] [Google Scholar]
  22. Orlova A., Egelman E. H. Structural basis for the destabilization of F-actin by phosphate release following ATP hydrolysis. J Mol Biol. 1992 Oct 20;227(4):1043–1053. doi: 10.1016/0022-2836(92)90520-t. [DOI] [PubMed] [Google Scholar]
  23. Schutt C. E., Myslik J. C., Rozycki M. D., Goonesekere N. C., Lindberg U. The structure of crystalline profilin-beta-actin. Nature. 1993 Oct 28;365(6449):810–816. doi: 10.1038/365810a0. [DOI] [PubMed] [Google Scholar]
  24. Sosa H., Popp D., Ouyang G., Huxley H. E. Ultrastructure of skeletal muscle fibers studied by a plunge quick freezing method: myofilament lengths. Biophys J. 1994 Jul;67(1):283–292. doi: 10.1016/S0006-3495(94)80479-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Thomas D. D., Seidel J. C., Gergely J. Rotational dynamics of spin-labeled F-actin in the sub-millisecond time range. J Mol Biol. 1979 Aug 15;132(3):257–273. doi: 10.1016/0022-2836(79)90259-6. [DOI] [PubMed] [Google Scholar]
  26. Tirion M. M., ben-Avraham D., Lorenz M., Holmes K. C. Normal modes as refinement parameters for the F-actin model. Biophys J. 1995 Jan;68(1):5–12. doi: 10.1016/S0006-3495(95)80156-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tirion M. M., ben-Avraham D. Normal mode analysis of G-actin. J Mol Biol. 1993 Mar 5;230(1):186–195. doi: 10.1006/jmbi.1993.1135. [DOI] [PubMed] [Google Scholar]
  28. Wakabayashi K., Sugimoto Y., Tanaka H., Ueno Y., Takezawa Y., Amemiya Y. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J. 1994 Dec;67(6):2422–2435. doi: 10.1016/S0006-3495(94)80729-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yanagida T., Nakase M., Nishiyama K., Oosawa F. Direct observation of motion of single F-actin filaments in the presence of myosin. Nature. 1984 Jan 5;307(5946):58–60. doi: 10.1038/307058a0. [DOI] [PubMed] [Google Scholar]
  30. Yanagida T., Oosawa F. Polarized fluorescence from epsilon-ADP incorporated into F-actin in a myosin-free single fiber: conformation of F-actin and changes induced in it by heavy meromyosin. J Mol Biol. 1978 Dec 15;126(3):507–524. doi: 10.1016/0022-2836(78)90056-6. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES