Artículo

De Rossi, M.C.; Bruno, L.; Wolosiuk, A.; Despósito, M.A.; Levi, V. "When size does matter: Organelle size influences the properties of transport mediated by molecular motors" (2013) Biochimica et Biophysica Acta - General Subjects. 1830(11):5095-5103
La versión final de este artículo es de uso interno. El editor solo permite incluir en el repositorio el artículo en su versión post-print. Por favor, si usted la posee enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Background Organelle transport is driven by the action of molecular motors. In this work, we studied the dynamics of organelles of different sizes with the aim of understanding the complex relation between organelle motion and microenvironment. Methods We used single particle tracking to obtain trajectories of melanosomes (pigmented organelles in Xenopus laevis melanophores). In response to certain hormones, melanosomes disperse in the cytoplasm or aggregate in the perinuclear region by the combined action of microtubule and actin motors. Results and conclusions Melanosome trajectories followed an anomalous diffusion model in which the anomalous diffusion exponent (α) provided information regarding the trajectories' topography and thus of the processes causing it. During aggregation, the directionality of big organelles was higher than that of small organelles and did not depend on the presence of either actin or intermediate filaments (IF). Depolymerization of IF significantly reduced α values of small organelles during aggregation but slightly affect their directionality during dispersion. General significance Our results could be interpreted considering that the number of copies of active motors increases with organelle size. Transport of big organelles was not influenced by actin or IF during aggregation showing that these organelles are moved processively by the collective action of dynein motors. Also, we found that intermediate filaments enhance the directionality of small organelles suggesting that this network keeps organelles close to the tracks allowing their efficient reattachment. The higher directionality of small organelles during dispersion could be explained considering the better performance of kinesin-2 vs. dynein at the single molecule level. © 2013 Elsevier B.V.

Registro:

Documento: Artículo
Título:When size does matter: Organelle size influences the properties of transport mediated by molecular motors
Autor:De Rossi, M.C.; Bruno, L.; Wolosiuk, A.; Despósito, M.A.; Levi, V.
Filiación:Departamento de Química Biológica, IQUIBICEN-CONICET, Ciudad Universitaria, CP 1428 Ciudad de Buenos Aires, Argentina
Departamento de Física, Facultad de Ciencias Exactas y Naturales, Ciudad Universitaria, CP 1428 Ciudad de Buenos Aires, Argentina
Gerencia de Quimica - Centro Atomico Constituyentes - Comision Nacional de Energia Atomica, Av. Gral. Paz 1499, 1650 San-Martín, Buenos Aires, Argentina
Palabras clave:Intracellular transport; Molecular motors; Organelle trafficking; Single particle tracking; Xenopus laevis melanophores-; actin; molecular motor; animal cell; article; cell aggregation; cell tracking; cell transport; controlled study; depolymerization; diffusion; dispersion; intermediate filament; melanosome; nonhuman; organelle size; priority journal; Xenopus laevis; anomalous diffusion exponent; DLS; dynamic light scattering; FE-SEM; field emission-scanning electron microscopy; IF; intermediate filaments; Intracellular transport; mean square displacement; Molecular motors; MSD; optical radius; OR; Organelle trafficking; Single particle tracking; Xenopus laevis melanophores; α; Actins; Animals; Biological Transport; Cells, Cultured; Cellular Microenvironment; Diffusion; Dyneins; Intermediate Filaments; Melanophores; Melanosomes; Microtubules; Molecular Motor Proteins; Organelle Size; Organelles; Structure-Activity Relationship; Xenopus laevis
Año:2013
Volumen:1830
Número:11
Página de inicio:5095
Página de fin:5103
DOI: http://dx.doi.org/10.1016/j.bbagen.2013.06.043
Título revista:Biochimica et Biophysica Acta - General Subjects
Título revista abreviado:Biochim. Biophys. Acta Gen. Subj.
ISSN:03044165
CODEN:BBGSB
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03044165_v1830_n11_p5095_DeRossi

Referencias:

  • Ishii, Y., Yanagida, T., Single molecule measurments and molecular motors (2003) Molecular Motors, , M. Schliwa, Wiley-VCH Munchen
  • 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
  • Brunstein, M., Bruno, L., Desposito, M., Levi, V., Anomalous dynamics of melanosomes driven by myosin-V in Xenopus laevis melanophores (2009) Biophys. J., 97, pp. 1548-1557
  • 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
  • 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. 7-L9
  • Mallik, R., Gross, S.P., Molecular motors: Strategies to get along (2004) Curr. Biol., 14, pp. 971-R982
  • Vale, R.D., The molecular motor toolbox for intracellular transport (2003) Cell, 112 (4), pp. 467-480. , DOI 10.1016/S0092-8674(03)00111-9
  • Kulic, I.M., Brown, A.E.X., Kim, H., Kural, C., Blehm, B., Selvin, P.R., Nelson, P.C., Gelfand, V., The role of microtubule movement in bidirectional organelle transport (2008) Proc. Natl. Acad. Sci. U. S. A., 105, pp. 10011-10016
  • Semenova, I., Buralov, A., Berardone, N., Zaliapin, I., Slepchenko, B., Svittkina, T., Kashina, A., Rodionov, V., Actin dynamics is essential for myosin-based transport of membrane organelles (2008) Curr. Biol., 18, pp. 1581-1586
  • Kural, C., Serpinskaya, A.S., Chou, Y.-H., Goldman, R.D., Gelfand, V.I., Selvin, P.R., Tracking melanosomes inside a cell to study molecular motors and their interaction (2007) Proceedings of the National Academy of Sciences of the United States of America, 104 (13), pp. 5378-5382. , DOI 10.1073/pnas.0700145104
  • Chang, L., Barlan, K., Chou, Y.H., Grin, B., Lakonishok, M., Serpinskaya, A.S., Shumaker, D.K., Goldman, R.D., The dynamic properties of intermediate filaments during organelle transport (2009) J. Cell Sci., 122, pp. 2914-2923
  • Nekrasova, O.E., Mendez, M.G., Chernoivanenko, I.S., Tyurin-Kuzmin, P.A., Kuczmarski, E.R., Gelfand, V.I., Goldman, R.D., Minin, A.A., Vimentin intermediate filaments modulate the motility of mitochondria (2011) Mol. Biol. Cell, 22, pp. 2282-2289
  • Potokar, M., Kreft, M., Li, L., Andersson, J.D., Pangrsic, T., Chowdhury, H.H., Pekny, M., Zorec, R., Cytoskeleton and vesicle mobility in astrocytes (2007) Traffic, 8 (1), pp. 12-20. , DOI 10.1111/j.1600-0854.2006.00509.x
  • Nascimento, A.A., Roland, J.T., Gelfand, V.I., Pigment Cells: A Model for the Study of Organelle Transport (2003) Annual Review of Cell and Developmental Biology, 19, pp. 469-491. , DOI 10.1146/annurev.cellbio.19.111401.092937
  • 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
  • Nilsson, H., Wallin, M., Evidence for several roles of dynein in pigment transport in melanophores (1997) Cell Motility and the Cytoskeleton, 38 (4), pp. 397-409. , DOI 10.1002/(SICI)1097-0169(1997)38:4<397::AID-CM9>3.0.CO;2-0
  • Tuma, M.C., Zill, A., Le Bot, N., Vernos, I., Gelfand, V., Heterotrimeric kinesin II is the microtubule motor protein responsible for pigment dispersion in Xenopus melanophores (1998) Journal of Cell Biology, 143 (6), pp. 1547-1558. , DOI 10.1083/jcb.143.6.1547
  • Rogers, S.L., Karcher, R.L., Roland, J.T., Minin, A.A., Gelfand, S.W.V.I., Regulation of melanosome movement in the cell cycle by reversible association with myosin v (1999) J. Cell Sci., 146, pp. 1265-1276
  • 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. U. S. A., 94, pp. 3720-3725
  • Gross, S.P., Carolina Tuma, M., Deacon, S.W., Serpinskaya, A.S., Reilein, A.R., Gelfand, V.I., Interactions and regulation of molecular motors in Xenopus melanophores (2002) Journal of Cell Biology, 156 (5), pp. 855-865. , DOI 10.1083/jcb.200105055
  • Rogers, S.L., Tint, I.S., Gelfand, V.I., In vitro motility assay for melanophore pigment organelles (1998) Methods in Enzymology, 298, pp. 361-372. , DOI 10.1016/S0076-6879(98)98032-6
  • Turkevich, J., Cooper Stevenson, P., Hillier, J., A study of the nucleation and growth processes in the synthesis of colloidal gold (1951) Discuss. Faraday Soc., 11, pp. 55-75
  • Dodes Traian, M.M., Gonzalez Flecha, F.L., Levi, V., Imaging lipid lateral organization in membranes with C-laurdan in a confocal microscope (2012) J. Lipid Res., 53, pp. 609-616
  • Saxton, M.J., Jacobson, K., Single-particle tracking: Applications to membrane dynamics (1997) Annual Review of Biophysics and Biomolecular Structure, 26, pp. 373-399. , DOI 10.1146/annurev.biophys.26.1.373
  • Wayne, R., (2009) Light and Video Microscopy, pp. 35-65. , Elsevier Inc. Amsterdam
  • Levi, V., Gratton, E., Exploring dynamics in living cells by tracking single particles (2007) Cell Biochemistry and Biophysics, 48 (1), pp. 1-15. , DOI 10.1007/s12013-007-0010-0
  • Robert, D., Aubertin, K., Bacri, J.C., Wilhelm, C., Magnetic nanomanipulations inside living cells compared with passive tracking of nanoprobes to get consensus for intracellular mechanics (2012) Phys. Rev. e Stat. Nonlinear Soft Matter Phys., 85, p. 011905
  • Bruno, L., Levi, V., Brunstein, M., Desposito, M.A., Transition to superdiffusive behavior in intracellular actin-based transport mediated by molecular motors (2009) Phys. Rev. e Stat. Nonlinear Soft Matter Phys., 80, p. 011912
  • Salman, H., Gil, Y., Granek, R., Elbaum, M., Microtubules, motor proteins, and anomalous mean squared displacements (2002) Chem. Phys., 284, pp. 389-397
  • Caspi, A., Granek, R., Elbaum, M., Diffusion and directed motion in cellular transport (2002) Phys. Rev. e Stat. Nonlinear Soft Matter Phys., 66, p. 011916
  • Gal, N., Weihs, D., Experimental evidence of strong anomalous diffusion in living cells (2010) Phys. Rev. e Stat. Nonlinear Soft Matter Phys., 81, p. 020903
  • Wilhelm, C., Out-of-equilibrium microrheology inside living cells (2008) Phys. Rev. Lett., 101, p. 028101
  • 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) Journal of Cell Biology, 179 (4), pp. 635-641. , http://www.jcb.org/cgi/reprint/179/4/635, DOI 10.1083/jcb.200705146
  • 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
  • Snezhko, A., Barlan, K., Aranson, I.S., Gelfand, V.I., Statistics of active transport in Xenopus melanophores cells (2010) Biophys. J., 99, pp. 3216-3223
  • Aspengren, S., New insights into melanosome transport in vertebrate pigment cells (2009) Int. J. Cell Mol. Biol., 272, pp. 245-302
  • Langford, G.M., Actin- and microtubule-dependent organelle motors: Interrelationships between the two motility systems (1995) Curr. Opin. Cell Biol., 7, pp. 82-88
  • Beeg, J., Klumpp, S., Dimova, R., Gracia, R.S., Unger, E., Lipowsky, R., Transport of beads by several kinesin motors (2008) Biophys. J., 94, pp. 532-541
  • Muller, M.J., Klumpp, S., Lipowsky, R., Bidirectional transport by molecular motors: Enhanced processivity and response to external forces (2010) Biophys. J., 98, pp. 2610-2618
  • Mallik, R., Petrov, D., Lex, S.A., King, S.J., Gross, S.P., Building complexity: An in vitro study of cytoplasmic dynein with in vivo implications (2005) Current Biology, 15 (23), pp. 2075-2085. , DOI 10.1016/j.cub.2005.10.039, PII S0960982205012790
  • Vershinin, M., Carter, B.C., Razafsky, D.S., King, S.J., Gross, S.P., Multiple-motor based transport and its regulation by Tau (2007) Proceedings of the National Academy of Sciences of the United States of America, 104 (1), pp. 87-92. , DOI 10.1073/pnas.0607919104
  • Schroeder III, H.W., Mitchell, C., Shuman, H., Holzbaur, E.L., Goldman, Y.E., Motor number controls cargo switching at actin-microtubule intersections in vitro (2010) Curr. Biol., 20, pp. 687-696
  • Schroeder III, H.W., Hendricks, A.G., Ikeda, K., Shuman, H., Rodionov, V., Ikebe, M., Goldman, Y.E., Holzbaur, E.L., Force-dependent detachment of kinesin-2 biases track switching at cytoskeletal filament intersections (2012) Biophys. J., 103, pp. 48-58
  • Hendricks, A.G., Perlson, E., Ross, J.L., Schroeder III, H.W., Tokito, M., Holzbaur, E.L., Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport (2010) Curr. Biol., 20, pp. 697-702
  • Soppina, V., Rai, A.K., Ramaiya, A.J., Barak, P., Mallik, R., Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 19381-19386
  • Hendricks, A.G., Holzbaur, E.L., Goldman, Y.E., Force measurements on cargoes in living cells reveal collective dynamics of microtubule motors (2012) Proc. Natl. Acad. Sci. U. S. A., 109, pp. 18447-18452
  • Snider, J., Lin, F., Zahedi, N., Rodionovt, V., Yu, C.C., Gross, S.P., Intracellular actin-based transport: How far you go depends on how often you switch (2004) Proceedings of the National Academy of Sciences of the United States of America, 101 (36), pp. 13204-13209. , DOI 10.1073/pnas.0403092101
  • Muthukrishnan, G., Zhang, Y., Shastry, S., Hancock, W.O., The processivity of kinesin-2 motors suggests diminished front-head gating (2009) Curr. Biol., 19, pp. 442-447

Citas:

---------- APA ----------
De Rossi, M.C., Bruno, L., Wolosiuk, A., Despósito, M.A. & Levi, V. (2013) . When size does matter: Organelle size influences the properties of transport mediated by molecular motors. Biochimica et Biophysica Acta - General Subjects, 1830(11), 5095-5103.
http://dx.doi.org/10.1016/j.bbagen.2013.06.043
---------- CHICAGO ----------
De Rossi, M.C., Bruno, L., Wolosiuk, A., Despósito, M.A., Levi, V. "When size does matter: Organelle size influences the properties of transport mediated by molecular motors" . Biochimica et Biophysica Acta - General Subjects 1830, no. 11 (2013) : 5095-5103.
http://dx.doi.org/10.1016/j.bbagen.2013.06.043
---------- MLA ----------
De Rossi, M.C., Bruno, L., Wolosiuk, A., Despósito, M.A., Levi, V. "When size does matter: Organelle size influences the properties of transport mediated by molecular motors" . Biochimica et Biophysica Acta - General Subjects, vol. 1830, no. 11, 2013, pp. 5095-5103.
http://dx.doi.org/10.1016/j.bbagen.2013.06.043
---------- VANCOUVER ----------
De Rossi, M.C., Bruno, L., Wolosiuk, A., Despósito, M.A., Levi, V. When size does matter: Organelle size influences the properties of transport mediated by molecular motors. Biochim. Biophys. Acta Gen. Subj. 2013;1830(11):5095-5103.
http://dx.doi.org/10.1016/j.bbagen.2013.06.043