Abstract:
Intracellular transport of large cargoes, such as organelles, vesicles, or large proteins, is a complex dynamical process that involves the interplay of adenosine triphosphate-consuming molecular motors, cytoskeleton filaments, and the viscoelastic cytoplasm. In this work we investigate the motion of pigment organelles (melanosomes) driven by myosin-V motors in Xenopus laevis melanocytes using a high-spatio-temporal resolution tracking technique. By analyzing the obtained trajectories, we show that the melanosomes mean-square displacement undergoes a transition from a subdiffusive to a superdiffusive behavior. A stochastic theoretical model, which explicitly considers the collective action of the molecular motors, is introduced to generalize the interpretation of our data. Starting from a generalized Langevin equation, we derive an analytical expression for the mean square displacement, which also takes into account the experimental noise. By fitting theoretical expressions to experimental data we were able to discriminate the exponents that characterize the passive and active contributions to the dynamics and to estimate the "global" motor forces correctly. Then, our model gives a quantitative description of active transport in living cells with a reduced number of parameters. © 2009 The American Physical Society.
Registro:
Documento: |
Artículo
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Título: | Transition to superdiffusive behavior in intracellular actin-based transport mediated by molecular motors |
Autor: | Bruno, L.; Levi, V.; Brunstein, M.; Despósito, M.A. |
Filiación: | Departamento de Física, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428 Buenos Aires, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428 Buenos Aires, Argentina Laboratoire de Photonique et Nanoestructure, Route de Nozay, 91460 Marcoussis, France
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Palabras clave: | Active transport; Analytical expressions; Collective action; Cytoskeleton filaments; Dynamical process; Experimental data; Generalized Langevin equation; Intracellular transport; Living cell; Mean-square displacement; Molecular motors; Quantitative description; Spatio-temporal resolution; Theoretical expression; Theoretical models; Tracking techniques; Xenopus laevis; Adenosinetriphosphate; Cytology; Equations of motion; Linear motors; Stochastic models; Motors |
Año: | 2009
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Volumen: | 80
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Número: | 1
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DOI: |
http://dx.doi.org/10.1103/PhysRevE.80.011912 |
Título revista: | Physical Review E - Statistical, Nonlinear, and Soft Matter Physics
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Título revista abreviado: | Phys. Rev. E Stat. Nonlinear Soft Matter Phys.
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ISSN: | 15393755
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CODEN: | PLEEE
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Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_15393755_v80_n1_p_Bruno |
Referencias:
- Mallik, R., Gross, S.P., (2004) Curr. Biol., 14, p. 971. , 10.1016/j.cub.2004.10.046;
- Vale, R.D., (2003) Cell, 112, p. 467. , 10.1016/S0092-8674(03)00111-9
- Gross, S.P., Welte, M.A., Block, S.M., Wieschaus, E.F., (2000) J. Cell Biol., 148, p. 945. , 10.1083/jcb.148.5.945
- Levi, V., Serpinskaya, A.S., Gratton, E., Gelfand, V.I., (2006) Biophys. J., 90, p. 318. , 10.1529/biophysj.105.067843
- Bruno, L., Echarte, M.M., Levi, V., (2008) Cell Biochem. Biophys., 52, p. 191. , 10.1007/s12013-008-9034-3
- Gross, S.P., Tuma, M.C., Deacon, S.W., Serpinskaya, A.S., Reilein, A.R., Gelfand, V.I., (2002) J. Cell Biol., 156, p. 855. , 10.1083/jcb.200105055
- Langford, G.M., (2002) Traffic, 3, p. 859
- Atkinson, S.J., Doberstein, S.K., Pollard, T.D., (1992) Curr. Biol., 2, p. 326. , 10.1016/0960-9822(92)90896-I
- Mizuno, D., Tardin, C., Schmidt, C.F., MacKintosh, F.C., (2007) Science, 315, p. 370. , 10.1126/science.1134404
- Bursac, P., Lenormand, G., Fabry, B., Oliver, M., Weitz, D.A., Viasnoff, V., Butler, J.P., Fredberg, J.J., (2005) Nature Mater., 4, p. 557. , 10.1038/nmat1404
- Snider, J., Lin, F., Zahedi, N., Rodionov, V., Yu, C.C., Gross, S.P., (2004) Proc. Natl. Acad. Sci. U.S.A., 101, p. 13204. , 10.1073/pnas.0403092101
- Waigh, T.A., (2005) Rep. Prog. Phys., 68, p. 685. , See 10.1088/0034-4885/68/3/R04
- Lau, A.W.C., Hoffmann, B.D., Davies, A., Crocker, J.C., Lubensky, T.C., (2003) Phys. Rev. Lett., 91, p. 198101. , 10.1103/PhysRevLett.91.198101
- Wilhelm, C., (2008) Phys. Rev. Lett., 101, p. 028101. , 10.1103/PhysRevLett.101.028101
- Brunstein, M., Bruno, L., Despósito, M.A., Levi, V., ; Gallet, F., Arcizet, D., Bohec, P., Richert, A., arXiv:0901.3087; Metzner, C., Raupach, C., Paranhos Zitterbart, D., Fabry, B., (2007) Phys. Rev. e, 76, p. 021925. , 10.1103/PhysRevE.76.021925
- Kulic, I.M., Brown, A.E.X., Kim, H., Kural, C., Blehm, B., Selvin, P.R., Nelson, P.C., Gelfand, V.I., (2008) Proc. Natl. Acad. Sci. U.S.A., 105, p. 10011. , 10.1073/pnas.0800031105
- Salman, H., Gil, Y., Granek, R., Elbaum, M., (2002) Chem. Phys., 284, p. 389. , 10.1016/S0301-0104(02)00669-9
- Lenormand, G., Chopin, J., Bursac, P., Fredberg, J.J., Butler, J.P., (2007) Biochem. Biophys. Res. Commun., 360, p. 797. , 10.1016/j.bbrc.2007.05.228
- Trepat, X., Lenormand, G., Fredberg, J.J., (2008) Soft Matter, 4, p. 1750. , 10.1039/b804866e
- Tseng, Y., Kole, T.P., Wirtz, D., (2002) Biophys. J., 83, p. 3162. , 10.1016/S0006-3495(02)75319-8
- Weiss, M., Elsner, M., Kartberg, F., Nilssony, T., (2004) Biophys. J., 87, p. 3518. , 10.1529/biophysj.104.044263
- Saxton, M.J., (2004) Biophys. J., 86, pp. 369A
- Saxton, M.J., (2007) Biophys. J., 92, p. 1178. , 10.1529/biophysj.106.092619
- Banks, D.S., Fradin, C., (2005) Biophys. J., 89, p. 2960. , 10.1529/biophysj.104.051078
- Martin, D.S., Forstner, M.B., Käs, J.A., (2002) Biophys. J., 83, p. 2109. , 10.1016/S0006-3495(02)73971-4
- Shubeita, G.T., Tran, S.L., Xu, J., Vershinin, M., Cermelli, S., Cotton, S.L., Welte, M.A., Gross, S.P., (2008) Cell, 135, p. 1098. , 10.1016/j.cell.2008.10.021
- Shtridelman, Y., Cahyuti, T., Townsend, B., Dewitt, D., MacOsko, J.C., (2008) Cell Biochem. Biophys., 52, p. 19. , 10.1007/s12013-008-9021-8
- Nascimento, A.A., Roland, J.T., Gelfand, V.I., (2003) Annu. Rev. Cell Dev. Biol., 19, p. 469. , 10.1146/annurev.cellbio.19.111401.092937
- Levi, V., Gelfand, V.I., Serpinskaya, A.S., Gratton, E., (2006) Biophys. J., 90, p. 07. , 10.1529/biophysj.105.075556
- Rozdzial, M.M., Haimo, L.T., (1986) Cell, 47, p. 1061. , 10.1016/0092-8674(86)90821-4;
- Sammak, P.J., Adams, S.R., Harootunian, A.T., Schliwa, M., Tsien, R.Y., (1992) J. Cell Biol., 117, p. 57. , 10.1083/jcb.117.1.57
- Dietrich, C., Yang, B., Fujiwara, T., Kusumi, A., Jacobson, K., (2002) Biophys. J., 82, p. 274. , 10.1016/S0006-3495(02)75393-9
- Bursac, P., Fabry, B., Trepat, X., Lenormand, G., Butler, J.P., Wang, N., Fredberg, J.J., An, S.S., (2007) Biochem. Biophys. Res. Commun., 355, p. 324. , 10.1016/j.bbrc.2007.01.191
- Bruno, L., Despósito, M.A., arXiv:0904.2133; Zwanzig, R., (2001) Nonequilibrium Statistical Mechanics, , Oxford University Press, New York
- Wang, K.G., (1992) Phys. Rev. A, 45, p. 833. , 10.1103/PhysRevA.45.833;
- Lutz, E., (2001) Europhys. Lett., 54, p. 293. , 10.1209/epl/i2001-00240-x;
- Viñales, A.D., Despósito, M.A., (2006) Phys. Rev. e, 73, p. 016111. , 10.1103/PhysRevE.73.016111
- Rogers, S.L., Tint, I.S., Fanapour, P.C., Gelfand, V.I., (1997) Proc. Natl. Acad. Sci. U.S.A., 94, p. 3720. , 10.1073/pnas.94.8.3720
- Sharma, S., Wagh, S., Govindarajan, R., (2002) Pigment Cell Res., 15, p. 127. , 10.1034/j.1600-0749.2002.1o076.x
- Yamada, S., Wirtz, D., Kuo, S.C., (2000) Biophys. J., 78, p. 1736. , 10.1016/S0006-3495(00)76725-7
- Dieterich, P., Klages, R., Preuss, R., Schwab, A., (2008) Proc. Natl. Acad. Sci. U.S.A., 105, p. 459. , 10.1073/pnas.0707603105
- Raupach, C., Zitterbart, D.P., Mierke, C.T., Metzner, C., Muller, F.A., Fabry, B., (2007) Phys. Rev. e, 76, p. 011918. , 10.1103/PhysRevE.76.011918
- Cappello, G., Pierobon, P., Symonds, C., Busoni, L., Christof, J., Gebhardt, M., Rief, M., Prost, J., (2007) Proc. Natl. Acad. Sci. U.S.A., 104, p. 15328. , 10.1073/pnas.0706653104;
- Clemen, A.E.M., Vilfan, M., Jaud, J., Zhang, J., Bärmann, M., Rief, M., (2005) Biophys. J., 88, p. 4402. , 10.1529/biophysj.104.053504
- Rogers, S.L., Karcher, R.L., Roland, J.T., Minin, A.A., Steffen, W., Gelfand, V.I., (1999) J. Cell Biol., 146, p. 1265
Citas:
---------- APA ----------
Bruno, L., Levi, V., Brunstein, M. & Despósito, M.A.
(2009)
. Transition to superdiffusive behavior in intracellular actin-based transport mediated by molecular motors. Physical Review E - Statistical, Nonlinear, and Soft Matter Physics, 80(1).
http://dx.doi.org/10.1103/PhysRevE.80.011912---------- CHICAGO ----------
Bruno, L., Levi, V., Brunstein, M., Despósito, M.A.
"Transition to superdiffusive behavior in intracellular actin-based transport mediated by molecular motors"
. Physical Review E - Statistical, Nonlinear, and Soft Matter Physics 80, no. 1
(2009).
http://dx.doi.org/10.1103/PhysRevE.80.011912---------- MLA ----------
Bruno, L., Levi, V., Brunstein, M., Despósito, M.A.
"Transition to superdiffusive behavior in intracellular actin-based transport mediated by molecular motors"
. Physical Review E - Statistical, Nonlinear, and Soft Matter Physics, vol. 80, no. 1, 2009.
http://dx.doi.org/10.1103/PhysRevE.80.011912---------- VANCOUVER ----------
Bruno, L., Levi, V., Brunstein, M., Despósito, M.A. Transition to superdiffusive behavior in intracellular actin-based transport mediated by molecular motors. Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 2009;80(1).
http://dx.doi.org/10.1103/PhysRevE.80.011912