Skip to main content
SpringerLink
Log in

Actin binding proteins that change extent and rate of actin monomer-polymer distribution by different mechanisms

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Actin binding proteins control actin assembly and disassembly by altering the critical concentration and by changing the kinetics of polymerization. All of these control mechanisms in some way or the other make use of the energy of hydrolysis of actin-bound ATP. Capping of barbed filament ends increases the critical concentration as long as ATP hydrolysis maintains a difference in the actin monomer binding constants of the two ends. A further increase in the critical concentration on adding a second cap, tropomodulin, to the other, pointed filament end also requires ATP hydrolysis as described by the model presented here. Changes in the critical concentration are amplified into much larger changes of the monomer pool by actin sequestering proteins, provided their actin binding equilibrium constants fall within a relatively narrow range around the values for the two critical concentrations of actin. Cofilin greatly speeds up treadmilling, which requires ATP hydroysis, by increasing the rate constant of depolymerization. Profilin increases the rate of elongation at the barbed filament end, coupled to a lowering of the critical concentration, only if ATP hydrolysis makes profilin binding to the barbed end independent of its binding constant for actin monomers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Oosawa F, Asakura S: Thermodynamics of the polymerization of proteins, Academic Press New York, 1975

    Google Scholar 

  2. Carlier M-F: Actin: Protein structure and filament dynamics. J Biol Chem 266: 1–4, 1991

    Google Scholar 

  3. Pollard TD, Cooper JA: Actin and actin binding proteins. A critical evaluation of mechanisms and functions. Ann Rev Biochem 55: 987–103, 1986

    Google Scholar 

  4. Wegner A: Treadmilling of actin at physiological salt solutions. J Mol Biol 161: 607–615, 1982

    Google Scholar 

  5. Young CL, Southwick FS, Weber A: Kinetics of the interaction of a 41-kilodalton macrophage capping protein with actin: Promotion of nucleation during prolongation of the lag period. Biochemistry 29: 2232–2240, 1990

    Google Scholar 

  6. Schafer DA, Cooper JA: Control of actin assembly at filament ends. Ann Rev Cell Dev Biol 11: 497–514, 1995

    Google Scholar 

  7. Weber A, Pennise CR, Babcock Gary G, Fowler VM: Tropomodulin caps the pointed ends of actin filaments. J Cell Biol 127: 1627–1635, 1994

    Google Scholar 

  8. Fowler VM: Identification and purification of a novel Mr 43,000 tropomyosin binding protein from human erythrocyte membranes. J Biol Chem 262: 12792–12800, 1987

    Google Scholar 

  9. Fowler VM: Regulation of actin filament length in erythrocytes and muscle. Curr Opin Cell Biol 8: 86–96, 1996

    Google Scholar 

  10. Detmers P, Weber A, Elzinga M, Stephens RE: 7-chloro-4-nitrobenzeno-2-oxa-1,3-diazole actin as a probe for actin polymerization. J Biol Chem 256: 99–105, 1981

    Google Scholar 

  11. Weber A, Nachmias VT, Pennise CR, Pring M, Safer D: Interaction of thymosin β4 with muscle and platelet actin: implications for actin sequestration in resting platelets. Biochemistry 31: 6179–6185, 1992

    Google Scholar 

  12. Goldschmidt-Clemont PJ, Machesky LM, Baldassare JJ, Pollard TD: The actin-binding protein profilin binds to PIP2 and inhibits its hydrolysis by phospholipase C. Science 247: 1575–1578, 1990

    Google Scholar 

  13. Sun HQ, Kwiatkowska K, Yin HL: Actin monomer binding proteins. Curr Opin Cell Biol 7: 102–110, 1995

    Google Scholar 

  14. Moon AL, Janmey PA, Louie KA, Drubin DG: Cofilin is an essential component of the yeast cortical cytoskeleton. J Cell Biol 120: 421–435, 1993

    Google Scholar 

  15. Carlier M-F, Laurent V, Santolini J, Melki R, Didry D, Xia G-X, Hong Y, Chua WK, Pantaloni D: Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: Implication for actin-based motility. J Cell Biol 136: 1307–1322, 1997

    Google Scholar 

  16. Theriot JA, Mitchison TJ: Actin microfilament dynamics in locomoting cells. Nature 352: 126–131, 1991

    Google Scholar 

  17. Zigmond SH: Recent quantitative studies of actin filament turnover during cell locomotion. Cell Motil Cytoskeleton 25: 309–316, 1993

    Google Scholar 

  18. Pollard TD: Actin cytoskeleton. Missing link for intracellular bacterial motility. Curr Biol 5: 837–840, 1995

    Google Scholar 

  19. Rosenblatt J, Agnew BJ, Abe H, Bamburg JR, Mitchison TJ: Xenopos actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails. J Cell Biol 136: 1323–1332, 1997

    Google Scholar 

  20. Agnew BJ, Minamide LS, Bamburg JR: Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J Biol Chem 270: 17582–17587, 1995

    Google Scholar 

  21. Aizawa H, Sutoh K, Yahara I: Overexpression of cofilin stimulates bundling of actin filaments, membrane ruffling, and cell movement in Dictyostelium. J Cell Biol 132: 335–344, 1996

    Google Scholar 

  22. Sohn RH, Goldschmidt-Clemont PJ: At the crossroads of signal transduction and the actin cytoskeleton. Bioassays 16: 465–472, 1994

    Google Scholar 

  23. Pantaloni D, Carlier MF: How profilin promotes actin filament assembly in the presence of thymosin-β4. Cell 75: 1007–1014, 1993

    Google Scholar 

  24. Pring M, Weber A, Bubb MR: Profilin-actin complexes directly elongate actin filaments at the barbed end. Biochemistry 31: 1827–1836, 1992

    Google Scholar 

  25. Tilney LC, Inoue S: Acrosomal reaction of Thione sperm III. The relationship between actin assembly and water influx during extension of the acrosomal process. J Cell Biol 100: 1273–1283, 1985

    Google Scholar 

  26. Tilney LC, Inoue S: Acrosomal reaction of Thione sperm II. The kinetics and possible mechanism of acrosomal process elongation. J Cell Biol 91: 820–827, 1982

    Google Scholar 

  27. Tilney LC, Bonder EM, Coluccio LM, Mooseker MS: Actin from Thyone sperm assembles on only one end of an actin filament: A behaviour regulated by profilin. J Cell Biol 97: 112–124, 1983

    Google Scholar 

  28. Pollard TD, Cooper JA: Quantitative analysis of the effect of Acanthamoeba profilin on actin filament nucleation and elongation. Biochemistry 23: 6631–6641, 1984

    Google Scholar 

  29. Kaiser DA, Sato M, Ebert RF, Pollard TD: Purification and characterization of two isoforms of acantharroeba profilin. J Cell Biol 102: 221–226, 1986

    Google Scholar 

  30. Cooley L, Verheyen E, Ayers K: Chicadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell: 69: 173–184, 1992

    Google Scholar 

  31. Haarer BK, Lillie SH, Adams AEM, Magdolen V, Bandlow W, Brown SS: Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. J Cell Biol 110: 105–114, 1989

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Biophysics, University of Pennsylvania, Philadelphia, PA, USA

    Annemarie Weber

Authors
  1. Annemarie Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weber, A. Actin binding proteins that change extent and rate of actin monomer-polymer distribution by different mechanisms. Mol Cell Biochem 190, 67–74 (1999). https://doi.org/10.1023/A:1006984010267

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006984010267

Search

Navigation