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Models for the length distributions of actin filaments: I. Simple polymerization and fragmentation

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Abstract

We studied mathematical models for the length distributions of actin filaments under the effects of polymerization/depolymerization, and fragmentation. In this paper, we emphasize the effects of these two processes acting alone. In this case, simple discrete and continuous models can be derived and solved explicitly (in several special cases), making the problem interesting from a modeling and pedagogical point of view. In a companion paper (Ermentrout and Edelstein-Keshet, 1998, Bull. Math. Biol. 60, 477–503) we investigate what happens when the processes act together, with particular attention to fragmentation by gelsolin, and with a greater level of biological detail.

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References

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

    Article  Google Scholar 

  • Alberts, B., D. Bray, J. Lewis, M. Raff, K. Roberts and J. D. Watson (1989). Molecular Biology of the Cell, 2nd edn, New York: Garland.

    Google Scholar 

  • Bonder, E. M., D. J. Fishkind and M. S. Mooseker (1983). Direct measurement of critical concentrations and assembly rate constants at the two ends of an actin filament. Cell 34, 491–501.

    Article  Google Scholar 

  • Brenner, S. L. and E. D. Korn (1983). On the mechanism of actin monomer-polymer subunit exchange at steady state. J. Biol. Chem. 258, 5013–5020.

    Google Scholar 

  • Cano, M. L., L. Cassimeris, M. Fechheimer and S. H. Zigmond (1992). Mechanisms responsible for F-actin stabilization after lysis of polymorphonuclear leukocytes. J. Cell Biol. 116, 1123–1134.

    Article  Google Scholar 

  • Cano, M. L., D. A. Lauffenburger and S. H. Zigmond (1991). Kinetic analysis of F-actin depolymerization in polymorphonuclear leukocyte lysates indicates that chemoattractant stimulation increases actin filament number without altering the filament length distribution. J. Cell. Biol. 115, 677–687.

    Article  Google Scholar 

  • Coluccio, L. M. and L. G. Tilney (1983). Under physiological conditions actin disassembles slowly from the nonpreferred end of an actin filament. J. Cell Biol. 97, 1629–1634.

    Article  Google Scholar 

  • Cooper, J. A. (1991). The role of actin polymerization in cell motility. Ann. Rev. Physiol. 53, 585–605.

    Article  Google Scholar 

  • Coppin, C. M. and P. Leavis (1992). Quantitation of liquid-crystaline ordering in F-actin solutions. Biophys. J. 63, 794–807.

    Google Scholar 

  • Doi, M. and S. F. Edwards (1986). The Theory of Polymer Dynamics, Oxford: Clarendon Press.

    Google Scholar 

  • Edelstein-Keshet, L. (1988). Mathematical Models in Biology, New York: McGraw-Hill.

    MATH  Google Scholar 

  • Edelstein-Keshet, L. and G. B. Ermentrout (1998). Spatially explicit models for actin filament polymerization, (in press).

  • Ermentrout, G. B. and L. Edelstein-Keshet (1998). Models for the Length distribution of actin filaments: II. Polymerization and Fragmentation by Gelsolin acting together. Bull. Math. Biol. 60, 477–503.

    Article  MATH  Google Scholar 

  • Fesce, R., F. Benfenati, P. Greengard and F. Valtorta (1992). Effects of the neuronal phosphoprotein synaptin I on actin polymerization: I. Analytic interpretation of kinetic curves. J. Biol. Chem. 267, 11289–11299.

    Google Scholar 

  • Fiedler, M. (1986). Special Matrices and Their Applications in Numerical Mathematics, Boston: Martinus Hijhoff.

    MATH  Google Scholar 

  • Frieden, C. (1983). Polymerization of actin: mechanism of the Mg2+-induced process at pH 8 and 20 °C. Proc. Natl. Acad. Sci. USA 80, 6513–6517.

    Article  Google Scholar 

  • Furukawa, R., R. Kundra and M. Fechheimer (1993). Formation of liquid crystals from actin filaments. Biochemistry 32, 12346–12352.

    Google Scholar 

  • Hartwig, J. H. and D. J. Kwiatkowski (1991). Actin binding proteins. Curr. Opin. Cell Biol. 3, 87–97.

    Article  Google Scholar 

  • Hawkins, M., B. Pope, S. K. Maciver and A. G. Weeds (1993). Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochemistry 32, 9985–9993.

    Article  Google Scholar 

  • Hayden, S. M., P. Miller, A. Brauweiler and J. R. Bamburg (1993). Analysis of the interactions of actin depolymerizing factor with G-and F-actin. Biochemistry 32, 9994–10004.

    Article  Google Scholar 

  • Horn, R. A. and C. R. Johnson (1985). Matrix Analysis, Cambridge: Cambridge University Press.

    MATH  Google Scholar 

  • Houmeida, A., R. Bennes, Y. Benyamin and C. Roustan (1995). Sequences of actin implicated in the poymerization process: a simplified mathematical approach to probe the role of these segments. Biophys. Chem. 56, 201–214.

    Article  Google Scholar 

  • Janmey, P. A., S. Hvidt, J. Kas, D. Lerche, A. Maggs, E. Sackmann, M. Schliwa and T. Stossel (1994). The mechanical properties of actin gels. J. Biol. Chem. 269, 32503–32513.

    Google Scholar 

  • Janmey, P. A. and P. T. Matsudaira (1988). Functional comparison of vilin and gelsolin. J. Biol. Chem. 263, 16738–16743.

    Google Scholar 

  • Janmey, P. A., J. Peetermans, K. S. Zaner, T. P. Stossel and T. Tanaka (1986). Structure and mobility of actin filaments as measured by quasielectric light scattering, viscometry and electron microscopy. J. Biol. Chem. 261, 8357–8362.

    Google Scholar 

  • Kas, J., H. Strey, J. X. Tang, D. Finger, R. Ezzell, E. Sackmann, and P. A. Janmey (1996). F-actin, a model polymer for semiflexible chains in dilute, semidilute, and liquid crystaline solutions. Biophys. J. 70, 609–625.

    Google Scholar 

  • Kawamura, M. and K. Maruyama (1970). Electron microscopic particle length of F-actin polymerized in vitro. J. Biochem 67, 437–457.

    Google Scholar 

  • Kirschner, M. W. (1980). Implications of treadmilling for the stability and polarity of actin and tubulin polymers in vivo. J. Cell Biol. 86, 330–334.

    Article  Google Scholar 

  • Korn, E. D., M. Carlier and D. Pantaloni (1987). Actin polymerization and ATP hydrolysis. Science 238, 638–644.

    Google Scholar 

  • Lauffenburger, D. A. and A. F. Horowitz (1996). Cell migration: a physically integrated molecular process. Cell 84, 359–369.

    Article  Google Scholar 

  • Lumsden, C. J. and P. A. Dufort (1993). Cellular automaton model of the actin cytoskeleton. Cell Motil. Cytoskel. 25, 87–104.

    Article  Google Scholar 

  • Maciver, S. K., H. G. Zot and T. D. Pollard (1991). Characterization of actin filament severing by actophorin from Acanthamoeba castellanii. J. Cell. Biol. 115, 1611–1620.

    Article  Google Scholar 

  • Marchand, J., P. Moreau, A. Paoletti, P. Cossart, M. Carlier and D. Pantaloni (1995). Actin-based movement of Listeria monocytogenes: actin assembly results from the local maintenance of uncapped filament barbed ends at the bacterium surface. J. Cell Biol. 130, 331–343.

    Article  Google Scholar 

  • Mitchison, T. J. and L. Cramer (1996). Actin-based cell motility and cell locomotion. Cell 84, 371–379.

    Article  Google Scholar 

  • Mogilner, A. and G. Oster (1996). Cell motility driven by actin polymerization. Biophys. J. 71, 3030–3045.

    Google Scholar 

  • Moon, A. and D. G. Drubin (1995). The ADF/cofilin proteins: stimulus-responsive modulators of actin dynamics. Mol. Biol. Cell 6, 1423–1431.

    Google Scholar 

  • Oosawa, F. and M. Kasai (1962). A theory of linear and helical aggregations of macromolecules. J. Mol. Biol. 4, 10–21.

    Article  Google Scholar 

  • Oster, G. F. (1994). Biophysics of Cell Motility, Lecture Notes, Berkeley, University of California.

    Google Scholar 

  • Podolski, J. L. and T. L. Steck (1990). Length distributions of F-actin in Dictyostelium discoideum. J. Biol. Chem. 265, 1312–1318.

    Google Scholar 

  • Pollard, T. D. (1986). Rate constants for the reactions of ATP-and ADP-actin with the ends of actin filaments. J. Cell Biol. 103, 2747–2754.

    Article  Google Scholar 

  • Pollard, T. D. and M. S. Mooseker (1981). Direct measurement of actin polymerization rate constants by electron microscopy of actin filaments nucleated by isolated microvillus cores. J. Cell Biol. 88, 654–659.

    Article  Google Scholar 

  • Redmond, T. and S. H. Zigmond (1993). Distribution of F-actin elongation sites in lysed polymorphonuclear leukocytes parallels the distribution of endogenous F-actin. Cell Motil. Cytoskel. 26, 1–18.

    Article  Google Scholar 

  • Sechi, A., J. Wehland and J. V. Small (1996). Actin filament organization in isolated comet tails of Listeria monocytogenes: The molecular basis of cell locomotion. 13th Harden Discussion Meeting, Wye College, England.

    Google Scholar 

  • Selve, N. and A. Wegner (1986). Rate of treadmilling of actin filaments in vitro. J. Mol. Biol. 187, 627–631.

    Article  Google Scholar 

  • Sun, H. Q., K. Kwiatkowska and H. L. Yin (1996). Beta-thymosins are not simple actin monomer buffering proteins. Insights from overexpression studies. J. Biol. Chem. 271, 9223–9230.

    Article  Google Scholar 

  • Suzuki, A., T. Maeda and T. Ito (1991). Formation of liquid crystalline phase of actin filament solutions and its dependence on filament length as studied by optical birefringence. Biophys J. 59, 25–30.

    Google Scholar 

  • Theriot, J. A. (1994). Actin filament dynamics in cell motility, in Actin:Biophysics, Biochemistry, and Cell Biology, J. E. Estes and P. J. Higgins (Eds), New York: Plenum Press, pp. 133–145.

    Google Scholar 

  • Tobacman, L. S. and E. D. Korn (1983). The kinetics of actin nucleation and polymerization, J. Biol. Chem. 258, 3207–3214.

    Google Scholar 

  • Wachsstock, D. H., W. H. Schwarz and T. D. Pollard (1993). Affinity of α-actinin for actin determines the structure and mechanical properties of actin filament gels. Biophys. J. 65, 205–214.

    Google Scholar 

  • Wachsstock, D. H., W. H. Schwarz and T. D. Pollard (1994). Cross-linker dynamics determine the mechanical properties of actin gels. Biophys. J. 66, 801–809.

    Google Scholar 

  • Wegner, A. and J. Engel (1975). Kinetics of cooperative association of actin to actin filaments. Biophys. Chem. 3, 215–225.

    Article  Google Scholar 

  • Zaner, K. S. (1995). Physics of actin networks. I. Rheology of semi-dilute F-actin. Biophys. J. 68, 1019–1026.

    Article  Google Scholar 

  • Zigmond, S. H. (1993). Recent quantitative studies of actin filament turnover during cell locomotion. Cell Motil. Cytoskel. 25, 309–316.

    Article  Google Scholar 

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Edelstein-Keshet, L., Ermentrout, G.B. Models for the length distributions of actin filaments: I. Simple polymerization and fragmentation. Bull. Math. Biol. 60, 449–475 (1998). https://doi.org/10.1006/bulm.1997.0011

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