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Motor-Mediated Microtubule Self-Organization in Dilute and Semi-Dilute Filament Solutions

Published online by Cambridge University Press:  09 June 2010

S. Swaminathan
Affiliation:
Department of Engineering Sciences & Applied Mathematics Northwestern University, Evanston, IL 60208-3125 USA Materials Science Division, Argonne National Laboratory, Argonne, IL, 60439
F. Ziebert
Affiliation:
Materials Science Division, Argonne National Laboratory, Argonne, IL, 60439 Laboratoire de Physico-Chimie Théorique - UMR CNRS 7083, ESPCI, 10 rue Vauquelin, F-75231 Paris, France
I. S. Aranson
Affiliation:
Department of Engineering Sciences & Applied Mathematics Northwestern University, Evanston, IL 60208-3125 USA Materials Science Division, Argonne National Laboratory, Argonne, IL, 60439
D. Karpeev*
Affiliation:
Mathematics & Computer Science Division, Argonne National Laboratory, Argonne, IL, 60439
*
* Corresponding author. E-mail: s-swaminathan@northwestern.edu
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Abstract

We study molecular motor-induced microtubule self-organization in dilute and semi-dilute filament solutions. In the dilute case, we use a probabilistic model of microtubule interaction via molecular motors to investigate microtubule bundle dynamics. Microtubules are modeled as polar rods interacting through fully inelastic, binary collisions. Our model indicates that initially disordered systems of interacting rods exhibit an orientational instability resulting in spontaneous ordering. We study the existence and dynamic interaction of microtubule bundles analytically and numerically. Our results reveal a long term attraction and coalescing of bundles indicating a clear coarsening in the system; microtubule bundles concentrate into fewer orientations on a slow logarithmic time scale. In semi-dilute filament solutions, multiple motors can bind a filament to several others and, for a critical motor density, induce a transition to an ordered phase with a nonzero mean orientation. Motors attach to a pair of filaments and walk along the pair bringing them into closer alignment. We develop a spatially homogenous, mean-field theory that explicitly accounts for a force-dependent detachment rate of motors, which in turn affects the mean and the fluctuations of the net force acting on a filament. We show that the transition to the oriented state can be both continuous and discontinuous when the force-dependent detachment of motors is important.

Type
Research Article
Copyright
© EDP Sciences, 2010

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References

Aranson, I. S., Tsimring, L. S.. Pattern formation of microtubules and motors: Inelastic interaction of polar rods . Phys Rev E, 71 (2005), No. 5, 050901.CrossRefGoogle ScholarPubMed
Aranson, I. S., Tsimring, L. S.. Theory of self-assembly of microtubules and motors . Phys Rev E, 74 (2006), No. 3, 031915.Google ScholarPubMed
Aranson, I. S., Tsimring, L. S., Vinokur, V. M.. Continuum theory of axial segregation in a long rotating drum . Phys Rev E, 60 (1999), No. 2, 1975-1987.CrossRefGoogle Scholar
Aranson, I. S., Volfson, D., Tsimring, L. S.. Swirling motion in a system of vibrated elongated particles . Phys Rev E, 75 (2007), No. 5, 051301.CrossRefGoogle Scholar
Ben-Naim, E., Krapivsky, P. L.. Alignment of rods and partition of integers . Phys Rev E, 73 (2006), No. 3, 031109.CrossRefGoogle ScholarPubMed
Campas, O., Kafri, Y., Zeldovich, K. B., Casademunt, J., Joanny, J. F.. Collective dynamics of interacting molecular motors . Phys Rev Lett, 97 (2006), No. 3, 038101.CrossRefGoogle ScholarPubMed
Coppin, C. M., Finer, T., Spudich, J. A., Vale, R. D.. Measurement of the isometric force exerted by a single kinesin molecule . Biophys. J., 68 (1995), 242s244s.Google ScholarPubMed
Coppin, C. M., Pierce, D. W., Hsu, L., Vale, R. D.. The load dependence of kinesin’s mechanical cycle . Proc. Natl. Acad. Sci., 94 (1997), No. 16, 85398544.CrossRefGoogle ScholarPubMed
P. G. de Gennes, J. Prost. The Physics of Liquid Crystals. Clarendon Press, Oxford, 1993.
M. Doi, S. F. Edwards, The Theory of Polymer Dynamics, Clarendon Press, Oxford, 1986.
Fiedor, S. J., Ottino, J. M.. Dynamics of axial segregation and coarsening of dry granular materials and slurries in circular and square tubes . Phys Rev Lett, 91 (2003), No. 24, 244301.CrossRefGoogle ScholarPubMed
Finger, T., Voigt, A., Stadler, J., Niessen, H. G., Naji, L., Stannarius, R.. Coarsening of axial segregation patterns of slurries in a horizontally rotating drum . Phys Rev E, 74 (2006), No. 3, 031312.CrossRefGoogle Scholar
Gilbert, T. L.. A phenomenological theory of damping in ferromagnetic materials , IEEE Trans. Magn, 40 (2004), No. 6, 34433449.CrossRefGoogle Scholar
Grill, S. W., Kruse, K., Jülicher, F.. Theory of mitotic spindle oscillations . Phys Rev Lett, 94 (2005), No. 10, 108104.CrossRefGoogle ScholarPubMed
J. Howard. Mechanics of Motor Proteins and the Cytoskeleton, Springer, New York, 2001.
Humphrey, D., Duggan, C., Saha, D., Smith, D., Käs, J.. Active fluidization of polymer networks through molecular motors . Nature (London), 416 (2002), No. 6879, 413416.CrossRefGoogle ScholarPubMed
Kapitein, L. C., Peterman, E. J. G., Kwok, B. H., Kim, J. H., Kapoor, T. M., Schmidt, C. F.. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks . Letters to Nature, 435 (2005), No. 7038, 114118.CrossRefGoogle ScholarPubMed
Karpeev, D., Aranson, I. S., Tsimring, L. S., Kaper, H. G.. Interactions of Semiflexible Filaments and Molecular Motors , Phys Rev E, 76 (2007), No. 5, 051905.CrossRefGoogle ScholarPubMed
Klumpp, S., Lipowski, R.. Cooperative cargo transport by several molecular motors . Proc. Natl. Acad. Sci., 102 (2005), No. 48, 1728417289.CrossRefGoogle ScholarPubMed
Kruse, K., Joanny, J. F., Jülicher, F., Prost, J., Sekimoto, K.. Asters, vortices, and rotating spirals in active gels of polar filaments . Phys Rev Lett, 92 (2004), No.7, 078101.1078101.4. CrossRefGoogle ScholarPubMed
Kruse, K., Jülicher, F.. Self-organization and mechanical properties of active filament bundles . Phys Rev E, 67 (2004), No. 5 051913.1051913.16. Google ScholarPubMed
Landau, L. D., Lifshitz, E. M., On the theory of the dispersion of magnetic permeability in ferromagnetic bodies . Phys. Z. Sovietunion, 8 (1935), 153169. Google Scholar
Lee, H. Y., Kardar, M.. Macroscopic equations for pattern formation in mixtures of microtubules and motors . Phys Rev E, 64 (2001), No. 5 056113.1056113.8. Google Scholar
Loi, D., Mossa, S., Cugliandolo, L. F.. Effective temperature of active matter . Phys Rev E, 77 (2008), No. 5, 051111.CrossRefGoogle ScholarPubMed
Liverpool, T. B., Maggs, A. C., Ajdari, A.. Viscoelasticity of solutions of motile polymers . Phys Rev Lett, 86 (2001), No. 18, 41714174.CrossRefGoogle ScholarPubMed
Liverpool, T. B., Marchetti, M. C.. Instabilities of isotropic solutions of active polar filaments . Phys Rev Lett, 90 (2003), No. 13, 138102.CrossRefGoogle ScholarPubMed
H. Lodish, A. Berk, S. L. Zipursky, P. Matsudaira, D. Baltimore J. Darnell. Molecular Cell Biology, W.H. Freeman, New York, 1999.
Mizuno, D., Tardin, C., Schmidt, C. F., MacKintosh, F. C.. Nonequilibrium mechanics of active cytoskeletal networks . Science, 315 (2007), No. 5810, 370373.CrossRefGoogle ScholarPubMed
Nédélec, F., Surrey, T., Maggs, A. C.. Dynamic Concentration of Motors in Microtubule Arrays . Phys Rev Lett, 86 (2001), No. 14, 31923195.CrossRefGoogle ScholarPubMed
Nédélec, F. J., Surrey, T., Maggs, A. C., Leibler, S.. Self-organization of microtubules and motors . Nature (London), 389 (1997), No. 6648, 305308.Google ScholarPubMed
Onsager, L.. Effects of shape on the interaction of colloidal particles . Ann. N.Y. Acad. Sci., 51 (1949), No. 4, 627659.CrossRefGoogle Scholar
Parmeggiani, A., Jülicher, F., Peliti, L., Prost, J.. Detachment of molecular motors under tangential loading . Europhys Lett, 56 (2001), No. 4, 603609.CrossRefGoogle Scholar
H. Risken. The Fokker-Planck Equation, Springer, Berlin (1989).
Simha, R. A., Ramaswamy, S.. Hydrodynamic fluctuations and instabilities in ordered suspensions of self-propelled particles . Phys Rev Lett, 89 (2002), No. 5, 058101.Google Scholar
Smith, D., Ziebert, F., Humphrey, D., Duggan, C., Steinbeck, M., Zimmermann, W., Kas, J.. Molecular motor-induced instabilities and cross-linkers determine biopolymer organization . Biophysical Journal, 93 (2007), No. 12, 44454452.CrossRefGoogle ScholarPubMed
Sokolov, A., Aranson, I. S., O.Kessler, J., Goldstein, R. E.. Concentration dependence of the collective dynamics of swimming bacteria . Phys Rev Lett, 98 (2007), No. 15, 158102.CrossRefGoogle ScholarPubMed
Surrey, T., Nédélec, F., Leibler, S., Karsenti, E.. Physical properties determining self-organization of motors and microtubules . Science, 292 (2001), No. 5519, 11671171.CrossRefGoogle ScholarPubMed
Swaminathan, S., Karpeev, D., Aranson, I. S.. Bundle dynamics of interacting polar rods . Phys Rev E, 77 (2008), No. 6, 066206.CrossRefGoogle ScholarPubMed
Swaminathan, S., Ziebert, F., Karpeev, D., Aranson, I. S.. Motor-mediated alignment of microtubules in semidilute mixtures . Phys Rev E, 79 (2009), No. 3, 036207.CrossRefGoogle ScholarPubMed
Takiguch, K.. Heavy meromyosin induces sliding movements between antiparallel actin filaments . J. Biochem, 109 (1991), No. 4, 520527.CrossRefGoogle Scholar
Urrutia, R., McNiven, M. A., Albanesi, J. P., Murphy, D. B., Kachar, B.. Purified kinesin promotes vesicle motility and induces active sliding between microtubules in vitro . Proc Natl Acad Sci, 88 (1991), No. 15, 67016705.CrossRefGoogle ScholarPubMed
Vale, R. D., Milligan, R .A.. The way things move: Looking under the hood of molecular motor proteins . Science, 288 (2000), No. 5463, 8895.CrossRefGoogle ScholarPubMed
Ziebert, F., Aranson, I. S. Rheological and structural properties of dilute active filament solutions , Phys Rev E, 77 (2008), No. 1, 011918.CrossRefGoogle ScholarPubMed
Ziebert, F., Aranson, I. S., Tsimring, L. S.. Effects of crosslinks on filament-motor organization . New J. Phys., 9 (2007), No. 11, 421.CrossRefGoogle Scholar
Ziebert, F., Vershinin, M., Gross, S. P., Aranson, I. S.. Collective alignment of polar filaments by molecular motors . Eur. Phys. J. E, 28 (2009), No. 4, 401409.CrossRefGoogle ScholarPubMed