Artículo

De Rossi, M.C.; Wetzler, D.E.; Benseñor, L.; De Rossi, M.E.; Sued, M.; Rodríguez, D.; Gelfand, V.; Bruno, L.; Levi, V. "Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells" (2017) Biochimica et Biophysica Acta - General Subjects. 1861(12):3178-3189
El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Background Intracellular transport requires molecular motors that step along cytoskeletal filaments actively dragging cargoes through the crowded cytoplasm. Here, we explore the interplay of the opposed polarity motors kinesin-1 and cytoplasmic dynein during peroxisome transport along microtubules in Drosophila S2 cells. Methods We used single particle tracking with nanometer accuracy and millisecond time resolution to extract quantitative information on the bidirectional motion of organelles. The transport performance was studied in cells expressing a slow chimeric plus-end directed motor or the kinesin heavy chain. We also analyzed the influence of peroxisomes membrane fluidity in methyl-β-ciclodextrin treated cells. The experimental data was also confronted with numerical simulations of two well-established tug of war scenarios. Results and conclusions The velocity distributions of retrograde and anterograde peroxisomes showed a multimodal pattern suggesting that multiple motor teams drive transport in either direction. The chimeric motors interfered with the performance of anterograde transport and also reduced the speed of the slowest retrograde team. In addition, increasing the fluidity of peroxisomes membrane decreased the speed of the slowest anterograde and retrograde teams. General significance Our results support the existence of a crosstalk between opposed-polarity motor teams. Moreover, the slowest teams seem to mechanically communicate with each other through the membrane to trigger transport. © 2017 Elsevier B.V.

Registro:

Documento: Artículo
Título:Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
Autor:De Rossi, M.C.; Wetzler, D.E.; Benseñor, L.; De Rossi, M.E.; Sued, M.; Rodríguez, D.; Gelfand, V.; Bruno, L.; Levi, V.
Filiación:Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Química Biológica, Laboratorio de Dinámica Intracelular, Buenos Aires, Argentina
CONICET-Universidad de Buenos Aires, Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales (IQUIBICEN), Buenos Aires, Argentina
Fundación Instituto Leloir, CONICET, Buenos Aires, Argentina
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales y Ciclo Básico Común, Buenos Aires, Argentina
CONICET-Universidad de Buenos Aires, Instituto de Astronomía y Física del Espacio (IAFE), Buenos Aires, Argentina
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Instituto de Cálculo, Buenos Aires, Argentina
Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, United States
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Física, Buenos Aires, Argentina
CONICET-Universidad de Buenos Aires, Instituto de Física de Buenos Aires (IFIBA), Buenos Aires, Argentina
Palabras clave:Drosophila S2 cells; Intracellular transport; Molecular motors; Single particle tracking; dynein adenosine triphosphatase; kinesin 1; methyl beta cyclodextrin; beta cyclodextrin derivative; methyl-beta-cyclodextrin; Article; cell membrane fluidity; cell motion; cell tracking; cell transport; cellular distribution; chemical procedures; chemical reaction; controlled study; Drosophila melanogaster; measurement accuracy; mechanical coupling; microtubule; millisecond time resolution; nonhuman; peroxisome; priority journal; simulation; single particle tracking; velocity; animal; cell culture; Drosophila; membrane fluidity; metabolism; microtubule; peroxisome; physiology; transport at the cellular level; Animals; beta-Cyclodextrins; Biological Transport; Cells, Cultured; Drosophila; Membrane Fluidity; Microtubules; Peroxisomes
Año:2017
Volumen:1861
Número:12
Página de inicio:3178
Página de fin:3189
DOI: http://dx.doi.org/10.1016/j.bbagen.2017.09.009
Título revista:Biochimica et Biophysica Acta - General Subjects
Título revista abreviado:Biochim. Biophys. Acta Gen. Subj.
ISSN:03044165
CODEN:BBGSB
CAS:dynein adenosine triphosphatase; beta-Cyclodextrins; methyl-beta-cyclodextrin
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03044165_v1861_n12_p3178_DeRossi

Referencias:

  • Hancock, W.O., Bidirectional cargo transport: moving beyond tug of war (2014) Nat. Rev. Mol. Cell Biol., 15, pp. 615-628
  • Welte, M.A., Bidirectional transport along microtubules (2004) Curr. Biol., 14, pp. R525-537
  • Hirokawa, N., Noda, Y., Tanaka, Y., Niwa, S., Kinesin superfamily motor proteins and intracellular transport (2009) Nat. Rev. Mol. Cell Biol., 10, pp. 682-696
  • De Vos, K.J., Grierson, A.J., Ackerley, S., Miller, C.C., Role of axonal transport in neurodegenerative diseases (2008) Annu. Rev. Neurosci., 31, pp. 151-173
  • Chevalier-Larsen, E., Holzbaur, E.L., Axonal transport and neurodegenerative disease (2006) Biochim. Biophys. Acta, 1762, pp. 1094-1108
  • Bilsland, L.G., Sahai, E., Kelly, G., Golding, M., Greensmith, L., Schiavo, G., Deficits in axonal transport precede ALS symptoms in vivo (2010) Proc. Natl. Acad. Sci. U. S. A., 107, pp. 20523-20528
  • Morfini, G.A., You, Y.M., Pollema, S.L., Kaminska, A., Liu, K., Yoshioka, K., Bjorkblom, B., Brady, S.T., Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin (2009) Nat. Neurosci., 12, pp. 864-871
  • Strom, A.L., Gal, J., Shi, P., Kasarskis, E.J., Hayward, L.J., Zhu, H., Retrograde axonal transport and motor neuron disease (2008) J. Neurochem., 106, pp. 495-505
  • Perlson, E., Jeong, G.B., Ross, J.L., Dixit, R., Wallace, K.E., Kalb, R.G., Holzbaur, E.L., A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration (2009) J. Neurosci., 29, pp. 9903-9917
  • Belyy, V., Schlager, M.A., Foster, H., Reimer, A.E., Carter, A.P., Yildiz, A., The mammalian dynein-dynactin complex is a strong opponent to kinesin in a tug-of-war competition (2016) Nat. Cell Biol., 18, pp. 1018-1024
  • Yildiz, A., Tomishige, M., Vale, R.D., Selvin, P.R., Kinesin walks hand-over-hand (2004) Science, 303, pp. 676-678
  • Mallik, R., Carter, B.C., Lex, S.A., King, S.J., Gross, S.P., Cytoplasmic dynein functions as a gear in response to load (2004) Nature, 427, pp. 649-652
  • Reck-Peterson, S.L., Yildiz, A., Carter, A.P., Gennerich, A., Zhang, N., Vale, R.D., Single-molecule analysis of dynein processivity and stepping behavior (2006) Cell, 126, pp. 335-348
  • Muller, M.J., Klumpp, S., Lipowsky, R., Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors (2008) Proc. Natl. Acad. Sci. U. S. A., 105, pp. 4609-4614
  • 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
  • McLaughlin, R.T., Diehl, M.R., Kolomeisky, A.B., Collective dynamics of processive cytoskeletal motors (2016) Soft Matter, 12, pp. 14-21
  • Blasius, T.L., Cai, D., Jih, G.T., Toret, C.P., Verhey, K.J., Two binding partners cooperate to activate the molecular motor kinesin-1 (2007) J. Cell Biol., 176, pp. 11-17
  • Fu, M.M., Holzbaur, E.L., Integrated regulation of motor-driven organelle transport by scaffolding proteins (2014) Trends Cell Biol., 24, pp. 564-574
  • Blehm, B.H., Selvin, P.R., Single-molecule fluorescence and in vivo optical traps: how multiple dyneins and kinesins interact (2014) Chem. Rev., 114, pp. 3335-3352
  • Ally, S., Larson, A.G., Barlan, K., Rice, S.E., Gelfand, V.I., Opposite-polarity motors activate one another to trigger cargo transport in live cells (2009) J. Cell Biol., 187, pp. 1071-1082
  • Kural, C., Kim, H., Syed, S., Goshima, G., Gelfand, V.I., Selvin, P.R., Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? (2005) Science, 308, pp. 1469-1472
  • Kim, H., Ling, S.C., Rogers, G.C., Kural, C., Selvin, P.R., Rogers, S.L., Gelfand, V.I., Microtubule binding by dynactin is required for microtubule organization but not cargo transport (2007) J. Cell Biol., 176, pp. 641-651
  • Ling, S.C., Fahrner, P.S., Greenough, W.T., Gelfand, V.I., Transport of Drosophila fragile X mental retardation protein-containing ribonucleoprotein granules by kinesin-1 and cytoplasmic dynein (2004) Proc. Natl. Acad. Sci. U. S. A., 101, pp. 17428-17433
  • Aboelkassem, Y., Bonilla, J.A., McCabe, K.J., Campbell, S.G., Contributions of Ca(2 +)-independent thin filament activation to cardiac muscle function (2015) Biophys. J., 109, pp. 2101-2112
  • Verhey, K.J., Lizotte, D.L., Abramson, T., Barenboim, L., Schnapp, B.J., Rapoport, T.A., Light chain-dependent regulation of kinesin's interaction with microtubules (1998) J. Cell Biol., 143, pp. 1053-1066
  • Friedman, D.S., Vale, R.D., Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain (1999) Nat. Cell Biol., 1, pp. 293-297
  • Cai, D., McEwen, D.P., Martens, J.R., Meyhofer, E., Verhey, K.J., Single molecule imaging reveals differences in microtubule track selection between kinesin motors (2009) PLoS Biol., 7
  • 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
  • Kim, H.M., Choo, H.J., Jung, S.Y., Ko, Y.G., Park, W.H., Jeon, S.J., Kim, C.H., Cho, B.R., A two-photon fluorescent probe for lipid raft imaging: C-laurdan (2007) Chembiochem, 8, pp. 553-559
  • 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
  • Kunwar, A., Mogilner, A., Robust transport by multiple motors with nonlinear force-velocity relations and stochastic load sharing (2010) Phys. Biol., 7, p. 16012
  • 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
  • Bouzat, S., Levi, V., Bruno, L., Transport properties of melanosomes along microtubules interpreted by a tug-of-war model with loose mechanical coupling (2012) PLoS One, 7
  • De Rossi, M.C., De Rossi, M.E., Sued, M., Rodriguez, D., Bruno, L., Levi, V., Asymmetries in kinesin-2 and cytoplasmic dynein contributions to melanosome transport (2015) FEBS Lett., 589, pp. 2763-2768
  • Valentine, M.T., Fordyce, P.M., Krzysiak, T.C., Gilbert, S.P., Block, S.M., Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro (2006) Nat. Cell Biol., 8, pp. 470-476
  • Wasserman, L., All of Statistics: A Concise Course in Statistical Inference (2010), Springer-Verlag New York; Render, R.A., Mixture Densities, Maximum Likelihood and the EM Algorithm (1984), 26. , SIAM Review; Schwarz, G., Estimating the dimension of a model (1978) Ann. Stat., 62, pp. 461-464
  • Corder, G.W., Foreman, D.I., Nonparametric Statistics: A Step-by-Step Approach (2014), 2nd Edition; Pallavicini, C., Levi, V., Wetzler, D.E., Angiolini, J.F., Bensenor, L., Desposito, M.A., Bruno, L., Lateral motion and bending of microtubules studied with a new single-filament tracking routine in living cells (2014) Biophys. J., 106, pp. 2625-2635
  • Encalada, S.E., Goldstein, L.S., Biophysical challenges to axonal transport: motor-cargo deficiencies and neurodegeneration (2014) Annu. Rev. Biophys., 43, pp. 141-169
  • Reis, G.F., Yang, G., Szpankowski, L., Weaver, C., Shah, S.B., Robinson, J.T., Hays, T.S., Goldstein, L.S., Molecular motor function in axonal transport in vivo probed by genetic and computational analysis in Drosophila (2012) Mol. Biol. Cell, 23, pp. 1700-1714
  • Encalada, S.E., Szpankowski, L., Xia, C.H., Goldstein, L.S., Stable kinesin and dynein assemblies drive the axonal transport of mammalian prion protein vesicles (2011) Cell, 144, pp. 551-565
  • Xu, J., Shu, Z., King, S.J., Gross, S.P., Tuning multiple motor travel via single motor velocity (2012) Traffic, 13, pp. 1198-1205
  • 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) Curr. Biol., 15, pp. 2075-2085
  • Vershinin, M., Carter, B.C., Razafsky, D.S., King, S.J., Gross, S.P., Multiple-motor based transport and its regulation by Tau (2007) Proc. Natl. Acad. Sci. U. S. A., 104, pp. 87-92
  • McKenney, R.J., Huynh, W., Tanenbaum, M.E., Bhabha, G., Vale, R.D., Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes (2014) Science, 345, pp. 337-341
  • Kashina, A.S., Baskin, R.J., Cole, D.G., Wedaman, K.P., Saxton, W.M., Scholey, J.M., A bipolar kinesin (1996) Nature, 379, pp. 270-272
  • Kapitein, L.C., Peterman, E.J., Kwok, B.H., Kim, J.H., Kapoor, T.M., Schmidt, C.F., The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks (2005) Nature, 435, pp. 114-118
  • Krzysiak, T.C., Wendt, T., Sproul, L.R., Tittmann, P., Gross, H., Gilbert, S.P., Hoenger, A., A structural model for monastrol inhibition of dimeric kinesin Eg5 (2006) EMBO J., 25, pp. 2263-2273
  • Valentine, M.T., Gilbert, S.P., To step or not to step? How biochemistry and mechanics influence processivity in Kinesin and Eg5 (2007) Curr. Opin. Cell Biol., 19, pp. 75-81
  • Chen, G.Y., Mickolajczyk, K.J., Hancock, W.O., The kinesin-5 chemomechanical cycle is dominated by a two-heads-bound state (2016) J. Biol. Chem., 291, pp. 20283-20294
  • Hackney, D.D., Highly processive microtubule-stimulated ATP hydrolysis by dimeric kinesin head domains (1995) Nature, 377, pp. 448-450
  • Campas, O., Leduc, C., Bassereau, P., Casademunt, J., Joanny, J.F., Prost, J., Coordination of Kinesin motors pulling on fluid membranes (2008) Biophys. J., 94, pp. 5009-5017
  • Cai, D., Verhey, K.J., Meyhofer, E., Tracking single kinesin molecules in the cytoplasm of mammalian cells (2007) Biophys. J., 92, pp. 4137-4144
  • Cai, D., Hoppe, A.D., Swanson, J.A., Verhey, K.J., Kinesin-1 structural organization and conformational changes revealed by FRET stoichiometry in live cells (2007) J. Cell Biol., 176, pp. 51-63
  • Bieling, P., Telley, I.A., Piehler, J., Surrey, T., Processive kinesins require loose mechanical coupling for efficient collective motility (2008) EMBO Rep., 9, pp. 1121-1127
  • Müller, M.J.I., Lipowsky, R., Motility states of molecular motors engaged in a stochastic tug-of-war (2008) J. Stat. Phys., 133, p. 1059
  • Efremov, A.K., Radhakrishnan, A., Tsao, D.S., Bookwalter, C.S., Trybus, K.M., Diehl, M.R., Delineating cooperative responses of processive motors in living cells (2014) Proc. Natl. Acad. Sci. U. S. A., 111, pp. E334-343
  • Rai, A.K., Rai, A., Ramaiya, A.J., Jha, R., Mallik, R., Molecular adaptations allow dynein to generate large collective forces inside cells (2013) Cell, 152, pp. 172-182
  • McKenney, R.J., Vershinin, M., Kunwar, A., Vallee, R.B., Gross, S.P., LIS1 and NudE induce a persistent dynein force-producing state (2010) Cell, 141, pp. 304-314
  • Sanderson, J.M., Resolving the kinetics of lipid, protein and peptide diffusion in membranes (2012) Mol. Membr. Biol., 29, pp. 118-143
  • Nelson, S.R., Trybus, K.M., Warshaw, D.M., Motor coupling through lipid membranes enhances transport velocities for ensembles of myosin Va (2014) Proc. Natl. Acad. Sci. U. S. A., 111, pp. E3986-3995
  • Erickson, R.P., Jia, Z., Gross, S.P., Yu, C.C., How molecular motors are arranged on a cargo is important for vesicular transport (2011) PLoS Comput. Biol., 7
  • Kunwar, A., Vershinin, M., Xu, J., Gross, S.P., Stepping, strain gating, and an unexpected force-velocity curve for multiple-motor-based transport (2008) Curr. Biol., 18, pp. 1173-1183
  • Coppin, C.M., Pierce, D.W., Hsu, L., Vale, R.D., The load dependence of kinesin's mechanical cycle (1997) Proc. Natl. Acad. Sci. U. S. A., 94, pp. 8539-8544
  • Bruno, L., Salierno, M., Wetzler, D.E., Desposito, M.A., Levi, V., Mechanical properties of organelles driven by microtubule-dependent molecular motors in living cells (2011) PLoS One, 6
  • 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
  • Schnitzer, M.J., Visscher, K., Block, S.M., Force production by single kinesin motors (2000) Nat. Cell Biol., 2, pp. 718-723
  • Leduc, C., Campas, O., Zeldovich, K.B., Roux, A., Jolimaitre, P., Bourel-Bonnet, L., Goud, B., Prost, J., Cooperative extraction of membrane nanotubes by molecular motors (2004) Proc. Natl. Acad. Sci. U. S. A., 101, pp. 17096-17101
  • Mallik, R., Rai, A.K., Barak, P., Rai, A., Kunwar, A., Teamwork in microtubule motors (2013) Trends Cell Biol., 23, pp. 575-582
  • Rai, A., Pathak, D., Thakur, S., Singh, S., Dubey, A.K., Mallik, R., Dynein clusters into lipid microdomains on phagosomes to drive rapid transport toward lysosomes (2016) Cell, 164, pp. 722-734
  • Zidovetzki, R., Levitan, I., Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies (2007) Biochim. Biophys. Acta, 1768, pp. 1311-1324
  • Akhmanova, A., Hammer, J.A., 3rd, Linking molecular motors to membrane cargo (2010) Curr. Opin. Cell Biol., 22, pp. 479-487
  • 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
  • Dixit, R., Ross, J.L., Goldman, Y.E., Holzbaur, E.L., Differential regulation of dynein and kinesin motor proteins by tau (2008) Science, 319, pp. 1086-1089
  • Wang, B., Kuo, J., Granick, S., Bursts of active transport in living cells (2013) Phys. Rev. Lett., 111, p. 208102
  • Ligon, L.A., Tokito, M., Finklestein, J.M., Grossman, F.E., Holzbaur, E.L., A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity (2004) J. Biol. Chem., 279, pp. 19201-19208
  • Arpag, G., Shastry, S., Hancock, W.O., Tuzel, E., Transport by populations of fast and slow kinesins uncovers novel family-dependent motor characteristics important for in vivo function (2014) Biophys. J., 107, pp. 1896-1904
  • Reddy, B.J., Mattson, M., Wynne, C.L., Vadpey, O., Durra, A., Chapman, D., Vallee, R.B., Gross, S.P., Load-induced enhancement of dynein force production by LIS1-NudE in vivo and in vitro (2016) Nat. Commun., 7, p. 12259
  • Leidel, C., Longoria, R.A., Gutierrez, F.M., Shubeita, G.T., Measuring molecular motor forces in vivo: implications for tug-of-war models of bidirectional transport (2012) Biophys. J., 103, pp. 492-500

Citas:

---------- APA ----------
De Rossi, M.C., Wetzler, D.E., Benseñor, L., De Rossi, M.E., Sued, M., Rodríguez, D., Gelfand, V.,..., Levi, V. (2017) . Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells. Biochimica et Biophysica Acta - General Subjects, 1861(12), 3178-3189.
http://dx.doi.org/10.1016/j.bbagen.2017.09.009
---------- CHICAGO ----------
De Rossi, M.C., Wetzler, D.E., Benseñor, L., De Rossi, M.E., Sued, M., Rodríguez, D., et al. "Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells" . Biochimica et Biophysica Acta - General Subjects 1861, no. 12 (2017) : 3178-3189.
http://dx.doi.org/10.1016/j.bbagen.2017.09.009
---------- MLA ----------
De Rossi, M.C., Wetzler, D.E., Benseñor, L., De Rossi, M.E., Sued, M., Rodríguez, D., et al. "Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells" . Biochimica et Biophysica Acta - General Subjects, vol. 1861, no. 12, 2017, pp. 3178-3189.
http://dx.doi.org/10.1016/j.bbagen.2017.09.009
---------- VANCOUVER ----------
De Rossi, M.C., Wetzler, D.E., Benseñor, L., De Rossi, M.E., Sued, M., Rodríguez, D., et al. Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells. Biochim. Biophys. Acta Gen. Subj. 2017;1861(12):3178-3189.
http://dx.doi.org/10.1016/j.bbagen.2017.09.009