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Abstract:

Molecular motors play relevant roles on the regulation of mitochondria size and shape, essential properties for the cell homeostasis. In this work, we tracked single rod-shaped mitochondria with nanometer precision to explore the performance of microtubule motor teams during processive anterograde and retrograde transport. We analyzed simultaneously the organelle size and verified that mitochondria retracted during retrograde transport with their leading tip moving slower in comparison with the rear tip. In contrast, mitochondria preserved their size during anterograde runs indicating a different performance of plus-end directed teams. These results were interpreted considering the different performance of dynein and kinesin teams and provide valuable information on the collective action of motors during mitochondria transport. © 2018 The Author(s).

Registro:

Documento: Artículo
Título:Retraction of rod-like mitochondria during microtubule-dependent transport
Autor:De Rossi, M.C.; Levi, V.; Bruno, L.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IQUIBICEN-CONICET, Ciudad Universitaria, Ciudad de Buenos Aires, CP1428, Argentina
Departamento de Física, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IFIBA-CONICET, Ciudad Universitaria, Ciudad de Buenos Aires, CP1428, Argentina
Palabras clave:dynein adenosine triphosphatase; enhanced green fluorescent protein; kinesin; dynein adenosine triphosphatase; kinesin; animal cell; Article; cell organelle; cell size; cell transport; confocal microscopy; homeostasis; immortalized cell line; intracellular transport; melanophore; microtubule; mitochondrion; molecular imaging; nonhuman; Xenopus laevis; animal; genetics; metabolism; microtubule; mitochondrion; organelle shape; single cell analysis; Animals; Dyneins; Homeostasis; Kinesin; Microtubules; Mitochondria; Organelle Shape; Single-Cell Analysis; Xenopus laevis
Año:2018
Volumen:38
Número:3
DOI: http://dx.doi.org/10.1042/BSR20180208
Título revista:Bioscience Reports
Título revista abreviado:Biosci. Rep.
ISSN:01448463
CODEN:BRPTD
CAS:dynein adenosine triphosphatase; Dyneins; Kinesin
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01448463_v38_n3_p_DeRossi

Referencias:

  • Hancock, W.O., Bidirectional cargo transport: Moving beyond tug of war (2014) Nat. Rev. Mol. Cell Biol., 15, pp. 615-628. , https://doi.org/10.1038/nrm3853
  • Welte, M.A., Bidirectional transport along microtubules (2004) Curr. Biol., 14, pp. R525-R537. , https://doi.org/10.1016/j.cub.2004.06.045
  • 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. , https://doi.org/10.1038/ncb3393
  • 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. , https://doi.org/10.1038/nature02293
  • Schnitzer, M.J., Visscher, K., Block, S.M., Force production by single kinesin motors (2000) Nat. Cell Biol., 2, pp. 718-723. , https://doi.org/10.1038/35036345
  • Jamison, D.K., Driver, J.W., Rogers, A.R., Constantinou, P.E., Diehl, M.R., Two kinesins transport cargo primarily via the action of one motor: Implications for intracellular transport (2010) Biophys. J., 99, pp. 2967-2977. , https://doi.org/10.1016/j.bpj.2010.08.025
  • 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. , https://doi.org/10.1038/embor.2008.169
  • De Rossi, M.C., Wetzler, D.E., Bensenor, L., De Rossi, M.E., Sued, M., Rodriguez, D., Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells (2017) Biochim. Biophys. Acta, 1861, pp. 3178-3189. , https://doi.org/10.1016/j.bbagen.2017.09.009
  • 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-E3995. , https://doi.org/10.1073/pnas.1406535111
  • 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. , https://doi.org/10.1016/j.cell.2015.12.054
  • 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. , https://doi.org/10.1073/pnas.0706825105
  • 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. , https://doi.org/10.1073/pnas.0906524106
  • McLaughlin, R.T., Diehl, M.R., Kolomeisky, A.B., Collective dynamics of processive cytoskeletal motors (2016) Soft Matter, 12, pp. 14-21. , https://doi.org/10.1039/C5SM01609F
  • 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. , https://doi.org/10.1083/jcb.200605099
  • Fu, M.M., Holzbaur, E.L., Integrated regulation of motor-driven organelle transport by scaffolding proteins (2014) Trends Cell Biol, 24, pp. 564-574. , https://doi.org/10.1016/j.tcb.2014.05.002
  • 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. , https://doi.org/10.1021/cr4005555
  • 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. , https://doi.org/10.1016/j.cell.2012.11.044
  • Chan, D.C., Mitochondria: Dynamic organelles in disease, aging, and development (2006) Cell, 125, pp. 1241-1252. , https://doi.org/10.1016/j.cell.2006.06.010
  • Roger, A.J., Munoz-Gomez, S.A., Kamikawa, R., The origin and diversification of mitochondria (2017) Curr. Biol., 27, pp. R1177-R1192. , https://doi.org/10.1016/j.cub.2017.09.015
  • Youle, R.J., van der Bliek, A.M., Mitochondrial fission, fusion, and stress (2012) Science, 337, pp. 1062-1065. , https://doi.org/10.1126/science.1219855
  • Hoppins, S., The regulation of mitochondrial dynamics (2014) Curr. Opin. Cell Biol., 29, pp. 46-52. , https://doi.org/10.1016/j.ceb.2014.03.005
  • Benard, G., Karbowski, M., Mitochondrial fusion and division: Regulation and role in cell viability (2009) Semin. Cell Dev. Biol., 20, pp. 365-374. , https://doi.org/10.1016/j.semcdb.2008.12.012
  • Liu, X., Weaver, D., Shirihai, O., Hajnoczky, G., Mitochondrial ‘kiss-and-run’: Interplay between mitochondrial motility and fusion-fission dynamics (2009) EMBO J, 28, pp. 3074-3089. , https://doi.org/10.1038/emboj.2009.255
  • Woods, L.C., Berbusse, G.W., Naylor, K., Microtubules are essential for mitochondrial dynamics-fission, fusion, and motility-in Dictyostelium discoideum (2016) Front. Cell Dev. Biol., 4, p. 19. , https://doi.org/10.3389/fcell.2016.00019
  • Varadi, A., Johnson-Cadwell, L.I., Cirulli, V., Yoon, Y., Allan, V.J., Rutter, G.A., Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1 (2004) J. Cell Sci., 117, pp. 4389-4400. , https://doi.org/10.1242/jcs.01299
  • Iworima, D.G., Pasqualotto, B.A., Rintoul, G.L., Kif5 regulates mitochondrial movement, morphology, function and neuronal survival (2016) Mol. Cell. Neurosci., 72, pp. 22-33. , https://doi.org/10.1016/j.mcn.2015.12.014
  • Anesti, V., Scorrano, L., The relationship between mitochondrial shape and function and the cytoskeleton (2006) Biochim. Biophys. Acta, 1757, pp. 692-699. , https://doi.org/10.1016/j.bbabio.2006.04.013
  • Frederick, R.L., Shaw, J.M., Moving mitochondria: Establishing distribution of an essential organelle (2007) Traffic, 8, pp. 1668-1675. , https://doi.org/10.1111/j.1600-0854.2007.00644.x
  • Nangaku, M., Sato-Yoshitake, R., Okada, Y., Noda, Y., Takemura, R., Yamazaki, H., KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria (1994) Cell, 79, pp. 1209-1220. , https://doi.org/10.1016/0092-8674(94)90012-4
  • Tanaka, Y., Kanai, Y., Okada, Y., Nonaka, S., Takeda, S., Harada, A., Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria (1998) Cell, 93, pp. 1147-1158. , https://doi.org/10.1016/S0092-8674(00)81459-2
  • 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) Biochim. Biophys. Acta, 1830, pp. 5095-5103. , https://doi.org/10.1016/j.bbagen.2013.06.043
  • 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. , https://doi.org/10.1529/biophysj.105.067843
  • Olesen, O.F., Kawabata-Fukui, H., Yoshizato, K., Noro, N., Molecular cloning of XTP, a tau-like microtubule-associated protein from Xenopus laevis tadpoles (2002) Gene, 283, pp. 299-309. , https://doi.org/10.1016/S0378-1119(01)00869-1
  • 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. , https://doi.org/10.1073/pnas.94.8.3720
  • Gross, S.P., Tuma, M.C., Deacon, S.W., Serpinskaya, A.S., Reilein, A.R., Gelfand, V.I., Interactions and regulation of molecular motors in Xenopus melanophores (2002) J. Cell Biol., 156, pp. 855-865. , https://doi.org/10.1083/jcb.200105055
  • Pallavicini, C., Levi, V., Wetzler, D.E., Angiolini, J.F., Bensenor, L., Desposito, M.A., Lateral Motion and bending of microtubules studied with a new single-filament tracking routine in living cells (2014) Biophys. J., 106, pp. 2625-2635. , https://doi.org/10.1016/j.bpj.2014.04.046
  • 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. , https://doi.org/10.1371/journal.pone.0018332
  • Agresti, A., (2006) An Introduction to Categorical Data Analysis, , John Wiley & Sons, Inc
  • McCarron, J.G., Wilson, C., Sandison, M.E., Olson, M.L., Girkin, J.M., Saunter, C., From structure to function: Mitochondrial morphology, motion and shaping in vascular smooth muscle (2013) J. Vasc. Res., 50, pp. 357-371. , https://doi.org/10.1159/000353883
  • Driver, J.W., Jamison, D.K., Uppulury, K., Rogers, A.R., Kolomeisky, A.B., Diehl, M.R., Productive cooperation among processive motors depends inversely on their mechanochemical efficiency (2011) Biophys. J., 101, pp. 386-395. , https://doi.org/10.1016/j.bpj.2011.05.067
  • Takshak, A., Kunwar, A., Importance of anisotropy in detachment rates for force production and cargo transport by a team of motor proteins (2016) Protein Sci, 25, pp. 1075-1079. , https://doi.org/10.1002/pro.2905
  • Nunnari, J., Suomalainen, A., Mitochondria: In sickness and in health (2012) Cell, 148, pp. 1145-1159. , https://doi.org/10.1016/j.cell.2012.02.035
  • 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. , https://doi.org/10.1016/j.bpj.2012.06.038
  • Goychuk, I., Kharchenko, V.O., Metzler, R., How molecular motors work in the crowded environment of living cells: Coexistence and efficiency of normal and anomalous transport (2014) PLoS ONE, 9. , https://doi.org/10.1371/journal.pone.0091700

Citas:

---------- APA ----------
De Rossi, M.C., Levi, V. & Bruno, L. (2018) . Retraction of rod-like mitochondria during microtubule-dependent transport. Bioscience Reports, 38(3).
http://dx.doi.org/10.1042/BSR20180208
---------- CHICAGO ----------
De Rossi, M.C., Levi, V., Bruno, L. "Retraction of rod-like mitochondria during microtubule-dependent transport" . Bioscience Reports 38, no. 3 (2018).
http://dx.doi.org/10.1042/BSR20180208
---------- MLA ----------
De Rossi, M.C., Levi, V., Bruno, L. "Retraction of rod-like mitochondria during microtubule-dependent transport" . Bioscience Reports, vol. 38, no. 3, 2018.
http://dx.doi.org/10.1042/BSR20180208
---------- VANCOUVER ----------
De Rossi, M.C., Levi, V., Bruno, L. Retraction of rod-like mitochondria during microtubule-dependent transport. Biosci. Rep. 2018;38(3).
http://dx.doi.org/10.1042/BSR20180208