Artículo

Este artículo es de Acceso Abierto y puede ser descargado en su versión final desde nuestro repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The organization of the cytoplasm is regulated by molecular motors, which transport organelles and other cargoes along cytoskeleton tracks. In this work, we use single particle tracking to study the in vivo regulation of the transport driven by myosin-V along actin filaments in Xenopus laevis melanophores. Melanophores have pigment organelles or melanosomes, which, in response to hormones, disperse in the cytoplasm or aggregate in the perinuclear region. We followed the motion of melanosomes in cells treated to depolymerize microtubules during aggregation and dispersion, focusing the analysis on the dynamics of these organelles in a time window not explored before to our knowledge. These data could not be explained by previous models that only consider active transport. We proposed a transport-diffusion model in which melanosomes may detach from actin tracks and reattach to nearby filaments to resume the active motion after a given time of diffusion. This model predicts that organelles spend -70% and 10% of the total time in active transport during dispersion and aggregation, respectively. Our results suggest that the transport along actin filaments and the switching from actin to microtubule networks are regulated by changes in the diffusion time between periods of active motion driven by myosin-V. © 2009 by the Biophysical Society.

Registro:

Documento: Artículo
Título:Anomalous dynamics of melanosomes driven by myosin-V in Xenopus laevis melanophores
Autor:Brunstein, M.; Bruno, L.; Desposito, M.; Levi, V.
Filiación:Laboratoire de Photonique et de Nanostructures (Centre National de la Recherche Scientifique), Marcoussis, France
Departamento de Física, Facultad de Ciencias Exactas Y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas Y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:actin; molecular motor; myosin V; actin filament; active transport; animal cell; article; cell organelle; controlled study; diffusion; melanophore; melanosome; microtubule assembly; nonhuman; prediction; transport diffusion model; Xenopus laevis; Xenopus laevis
Año:2009
Volumen:97
Número:6
Página de inicio:1548
Página de fin:1557
DOI: http://dx.doi.org/10.1016/j.bpj.2009.06.048
Título revista:Biophysical Journal
Título revista abreviado:Biophys. J.
ISSN:00063495
CODEN:BIOJA
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00063495_v97_n6_p1548_Brunstein.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00063495_v97_n6_p1548_Brunstein

Referencias:

  • Mallik, R., Gross, S.P., Molecular motors: Strategies to get along (2004) Curr. Biol., 14, pp. R971-R982
  • Vale, R.D., The molecular motor toolbox for intracellular transport (2003) Cell., 112, pp. 467-480
  • Langford, G.M., Myosin-V, a versatile motor for short-range vesicle transport (2002) Traffic., 3, pp. 859-865
  • Atkinson, S.J., Doberstein, S.K., Pollard, T.D., Moving off the beaten track (1992) Curr. Biol., 2, pp. 326-328
  • Visscher, K., Schnltzer, M.J., Block, S.M., Single kinesin molecules studied with a molecular force clamp (1999) Nature, 400 (6740), pp. 184-189. , DOI 10.1038/22146
  • Yildiz, A., Forkey, J.N., McKinney, S.A., Ha, T., Goldman, Y.E., Selvin, P.R., Myosin V walks hand-over-hand: Single fluorophore imaging with 1.5-nm localization (2003) Science, 300 (5628), pp. 2061-2065. , DOI 10.1126/science.1084398
  • Levi, V., Gelfand, V.I., Serpinskaya, A.S., Gratton, E., Melanosomes transported by myosin-V in Xenopus melanophores perform slow 35 nm steps (2006) Biophys. J., 90, pp. L7-L9
  • Gross, S.P., Welte, M.A., Block, S.M., Wieschaus, E.F., Dynein-mediated cargo transport in vivo. a switch controls travel distance (2000) J. Cell Biol., 148, pp. 945-956
  • Nascimento, A.A., Roland, J.T., Gelfand, V.I., Pigment cells: A model for the study of organelle transport (2003) Annu. Rev. Cell Dev. Biol., 19, pp. 469-491
  • Levi, V., Serpinskaya, A.S., Gratton, E., Gelfand, V., Organelle transport along microtubules in Xenopus melanophores: Evidence for cooperation between multiple motors (2006) Biophys. J., 90, pp. 318-327
  • Rozdzial, M.M., Haimo, L.T., Bidirectional pigment granule movements of melanophores are regulated by protein phosphorylation and dephosphorylation (1986) Cell., 47, pp. 1061-1070
  • Sammak, P.J., Adams, S.R., Harootunian, A.T., Schliwa, M., Tsien, R.Y., Intracellular cyclic AMP, not calcium, determines the direction of vesicle movement in melanophores: Direct measurement by fluorescence ratio imaging (1992) J. Cell Biol., 117, pp. 57-72
  • Tuma, M.C., Zill, A., Le Bot, N., Vernos, I., Gelfand, V., Heterotrimeric kinesin II is the microtubulemotor protein responsible for pigment dispersion in Xenopus melanophores (1998) J. Cell Biol., 143, pp. 1547-1558
  • Rogers, S.L., Karcher, R.L., Roland, J.T., Minin, A.A., Steffen, W., Regulation of melanosome movement in the cell cycle by reversible association with myosin V (1999) J. Cell Biol., 146, pp. 1265-1276
  • Nilsson, H., Wallin, M., Evidence for several roles of dynein in pigment transport in melanophores (1997) Cell Motil. Cytoskeleton., 38, pp. 397-409
  • Gross, S.P., Tuma, M.C., Deacon, S.W., Serpinskaya, A.S., Reilein, A.R., Interactions and regulation of molecular motors in Xenopus melanophores (2002) J. Cell Biol., 156, pp. 855-865
  • Bruno, L., Echarte, M.M., Levi, V., Exchange of microtubule molecular motors during melanosome transport in Xenopus laevis melanophores is triggered by collisions with intracellular obstacles (2008) Cell Biochem. Biophys., 52, pp. 191-201
  • Rogers, S.L., Gelfand, V.I., Myosin cooperates with microtubule motors during organelle transport in melanophores (1998) Curr. Biol., 8, pp. 161-164
  • Snider, J., Lin, F., Zahedi, N., Rodionov, V., Yu, C.C., Intracellular actin-based transport: How far you go depends on how often you switch (2004) Proc. Natl. Acad. Sci. USA., 101, pp. 13204-13209
  • Rogers, S.L., Tint, I.S., Fanapour, P.C., Gelfand, V.I., Regulated bidirectional motility of melanophore pigment granules along microtubules in vitro (1997) Proc. Natl. Acad. Sci. USA., 94, pp. 3720-3725
  • Gittes, F., Mickey, B., Nettleton, J., Howard, J., Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape (1993) Journal of Cell Biology, 120 (4), pp. 923-934. , DOI 10.1083/jcb.120.4.923
  • Pampaloni, F., Lattanzi, G., Jonas, A., Surrey, T., Frey, E., Thermal fluctuations of grafted microtubules provide evidence of a length-dependent persistence length (2006) Proc. Natl. Acad. Sci. USA., 103, pp. 10248-10253
  • Brangwynne, C.P., MacKintosh, F.C., Weitz, D.A., Force fluctuations and polymerization dynamics of intracellular microtubules (2007) Proc. Natl. Acad. Sci. USA., 104, pp. 16128-16133
  • Gross, S.P., Welte, M.A., Block, S.M., Wieschaus, E.F., Coordination of opposite-polarity microtubule motors (2002) J. Cell Biol., 156, pp. 715-724
  • Dieterich, P., Klages, R., Preuss, R., Schwab, A., Anomalous dynamics of cell migration (2008) Proc. Natl. Acad. Sci. USA., 105, pp. 459-463
  • Saxton, M.J., Jacobson, K., Single-particle tracking: Applications to membrane dynamics (1997) Annu. Rev. Biophys. Biomol. Struct., 26, pp. 373-399
  • Caspi, A., Granek, R., Elbaum, M., Diffusion and directed motion in cellular transport (2002) Phys. Rev. e Stat. Nonlin. Soft Matter Phys., 66, p. 011916
  • Caspi, A., Granek, R., Elbaum, M., Enhanced diffusion in active intracellular transport (2000) Phys. Rev. Lett., 85, pp. 5655-5658
  • Raupach, C., Paranhos Zitterbart, D., Mierke, C., Metzner, C., Muller, F.A., Stress fluctuations and motion of cytoskeletal-bound markers (2007) Phys. Rev. e Stat. Nonlin. Soft Matter Phys., 76, p. 011918
  • Martin, D.S., Forstner, M.B., Kas, J.A., Apparent subdiffusion inherent to single particle tracking (2002) Biophys. J., 83, pp. 2109-2117
  • Ali, M.Y., Krementsova, E.B., Kennedy, G.G., Mahaffy, R., Pollard, T.D., Myosin Va maneuvers through actin intersections and diffuses along microtubules (2007) Proc. Natl. Acad. Sci. USA., 104, pp. 4332-4336
  • Tseng, Y., Kole, T.P., Wirtz, D., Micromechanical mapping of live cells by multiple-particle-tracking microrheology (2002) Biophysical Journal, 83 (6), pp. 3162-3176
  • Baker, J.E., Krementsova, E.B., Kennedy, G.G., Armstrong, A., Trybus, K.M., Myosin V processivity: Multiple kinetic pathways for head-to-head coordination (2004) Proc. Natl. Acad. Sci. USA., 101, pp. 5542-5546
  • Jeney, S., Stelzer, E.H., Grubmuller, H., Florin, E.L., Mechanical properties of single motor molecules studied by three-dimensional thermal force probing in optical tweezers (2004) ChemPhysChem., 5, pp. 1150-1158
  • Veigel, C., Wang, F., Bartoo, M.L., Sellers, J.R., Molloy, J.E., The gated gait of the processive molecular motor, myosin V (2002) Nat. Cell Biol., 4, pp. 59-65
  • Cappello, G., Pierobon, P., Symonds, C., Busoni, L., Gebhardt, J.C., Myosin V stepping mechanism (2007) Proc. Natl. Acad. Sci. USA., 104, pp. 15328-15333
  • Goldman, R.D., Grin, B., Mendez, M.G., Kuczmarski, E.R., Intermediate filaments: Versatile building blocks of cell structure (2008) Curr. Opin. Cell Biol., 20, pp. 28-34
  • Kural, C., Serpinskaya, A.S., Chou, Y., Goldman, R.D., Gelfand, V.I., Tracking melanosomes inside a cell to study molecular motors and their interaction (2007) Proc. Natl. Acad. Sci. USA., 104, pp. 5378-5382
  • Lu, H., Krementsova, E.B., Trybus, K.M., Regulation of myosin V processivity by calcium at the single molecule level (2006) J. Biol. Chem., 281, pp. 31987-31994
  • Rodionov, V., Yi, J., Kashina, A., Oladipo, A., Gross, S.P., Switching between microtubule- And actin-based transport systems in melanophores is controlled by cAMP levels (2003) Curr. Biol., 13, pp. 1837-1847
  • Slepchenko, B.M., Semenova, I., Zaliapin, I., Rodionov, V., Switching of membrane organelles between cytoskeletal transport systems is determined by regulation of the microtubule-based transport (2007) J. Cell Biol., 179, pp. 635-641
  • Scott, D.W., On optimal and data-based histograms (1979) Biometrika, 3, pp. 605-610

Citas:

---------- APA ----------
Brunstein, M., Bruno, L., Desposito, M. & Levi, V. (2009) . Anomalous dynamics of melanosomes driven by myosin-V in Xenopus laevis melanophores. Biophysical Journal, 97(6), 1548-1557.
http://dx.doi.org/10.1016/j.bpj.2009.06.048
---------- CHICAGO ----------
Brunstein, M., Bruno, L., Desposito, M., Levi, V. "Anomalous dynamics of melanosomes driven by myosin-V in Xenopus laevis melanophores" . Biophysical Journal 97, no. 6 (2009) : 1548-1557.
http://dx.doi.org/10.1016/j.bpj.2009.06.048
---------- MLA ----------
Brunstein, M., Bruno, L., Desposito, M., Levi, V. "Anomalous dynamics of melanosomes driven by myosin-V in Xenopus laevis melanophores" . Biophysical Journal, vol. 97, no. 6, 2009, pp. 1548-1557.
http://dx.doi.org/10.1016/j.bpj.2009.06.048
---------- VANCOUVER ----------
Brunstein, M., Bruno, L., Desposito, M., Levi, V. Anomalous dynamics of melanosomes driven by myosin-V in Xenopus laevis melanophores. Biophys. J. 2009;97(6):1548-1557.
http://dx.doi.org/10.1016/j.bpj.2009.06.048