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Myosin-Va and Dynamic Actin Oppose Microtubules to Drive Long-Range Organelle Transport

In animal cells, microtubule and actin tracks and their associated motors (dynein, kinesin, and myosin) are thought to regulate long- and short-range transport, respectively [1–8]. Consistent with this, microtubules extend from the perinuclear centrosome to the plasma membrane and allow bidirectiona...

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Autores principales: Evans, Richard D., Robinson, Christopher, Briggs, Deborah A., Tooth, David J., Ramalho, Jose S., Cantero, Marta, Montoliu, Lluis, Patel, Shyamal, Sviderskaya, Elena V., Hume, Alistair N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4131108/
https://www.ncbi.nlm.nih.gov/pubmed/25065759
http://dx.doi.org/10.1016/j.cub.2014.06.019
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author Evans, Richard D.
Robinson, Christopher
Briggs, Deborah A.
Tooth, David J.
Ramalho, Jose S.
Cantero, Marta
Montoliu, Lluis
Patel, Shyamal
Sviderskaya, Elena V.
Hume, Alistair N.
author_facet Evans, Richard D.
Robinson, Christopher
Briggs, Deborah A.
Tooth, David J.
Ramalho, Jose S.
Cantero, Marta
Montoliu, Lluis
Patel, Shyamal
Sviderskaya, Elena V.
Hume, Alistair N.
author_sort Evans, Richard D.
collection PubMed
description In animal cells, microtubule and actin tracks and their associated motors (dynein, kinesin, and myosin) are thought to regulate long- and short-range transport, respectively [1–8]. Consistent with this, microtubules extend from the perinuclear centrosome to the plasma membrane and allow bidirectional cargo transport over long distances (>1 μm). In contrast, actin often comprises a complex network of short randomly oriented filaments, suggesting that myosin motors move cargo short distances. These observations underpin the “highways and local roads” model for transport along microtubule and actin tracks [2]. The “cooperative capture” model exemplifies this view and suggests that melanosome distribution in melanocyte dendrites is maintained by long-range transport on microtubules followed by actin/myosin-Va-dependent tethering [5, 9]. In this study, we used cell normalization technology to quantitatively examine the contribution of microtubules and actin/myosin-Va to organelle distribution in melanocytes. Surprisingly, our results indicate that microtubules are essential for centripetal, but not centrifugal, transport. Instead, we find that microtubules retard a centrifugal transport process that is dependent on myosin-Va and a population of dynamic F-actin. Functional analysis of mutant proteins indicates that myosin-Va works as a transporter dispersing melanosomes along actin tracks whose +/barbed ends are oriented toward the plasma membrane. Overall, our data highlight the role of myosin-Va and actin in transport, and not tethering, and suggest a new model in which organelle distribution is determined by the balance between microtubule-dependent centripetal and myosin-Va/actin-dependent centrifugal transport. These observations appear to be consistent with evidence coming from other systems showing that actin/myosin networks can drive long-distance organelle transport and positioning [10, 11].
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spelling pubmed-41311082014-08-15 Myosin-Va and Dynamic Actin Oppose Microtubules to Drive Long-Range Organelle Transport Evans, Richard D. Robinson, Christopher Briggs, Deborah A. Tooth, David J. Ramalho, Jose S. Cantero, Marta Montoliu, Lluis Patel, Shyamal Sviderskaya, Elena V. Hume, Alistair N. Curr Biol Report In animal cells, microtubule and actin tracks and their associated motors (dynein, kinesin, and myosin) are thought to regulate long- and short-range transport, respectively [1–8]. Consistent with this, microtubules extend from the perinuclear centrosome to the plasma membrane and allow bidirectional cargo transport over long distances (>1 μm). In contrast, actin often comprises a complex network of short randomly oriented filaments, suggesting that myosin motors move cargo short distances. These observations underpin the “highways and local roads” model for transport along microtubule and actin tracks [2]. The “cooperative capture” model exemplifies this view and suggests that melanosome distribution in melanocyte dendrites is maintained by long-range transport on microtubules followed by actin/myosin-Va-dependent tethering [5, 9]. In this study, we used cell normalization technology to quantitatively examine the contribution of microtubules and actin/myosin-Va to organelle distribution in melanocytes. Surprisingly, our results indicate that microtubules are essential for centripetal, but not centrifugal, transport. Instead, we find that microtubules retard a centrifugal transport process that is dependent on myosin-Va and a population of dynamic F-actin. Functional analysis of mutant proteins indicates that myosin-Va works as a transporter dispersing melanosomes along actin tracks whose +/barbed ends are oriented toward the plasma membrane. Overall, our data highlight the role of myosin-Va and actin in transport, and not tethering, and suggest a new model in which organelle distribution is determined by the balance between microtubule-dependent centripetal and myosin-Va/actin-dependent centrifugal transport. These observations appear to be consistent with evidence coming from other systems showing that actin/myosin networks can drive long-distance organelle transport and positioning [10, 11]. Cell Press 2014-08-04 /pmc/articles/PMC4131108/ /pubmed/25065759 http://dx.doi.org/10.1016/j.cub.2014.06.019 Text en © 2014 The Authors http://creativecommons.org/licenses/by/3.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).
spellingShingle Report
Evans, Richard D.
Robinson, Christopher
Briggs, Deborah A.
Tooth, David J.
Ramalho, Jose S.
Cantero, Marta
Montoliu, Lluis
Patel, Shyamal
Sviderskaya, Elena V.
Hume, Alistair N.
Myosin-Va and Dynamic Actin Oppose Microtubules to Drive Long-Range Organelle Transport
title Myosin-Va and Dynamic Actin Oppose Microtubules to Drive Long-Range Organelle Transport
title_full Myosin-Va and Dynamic Actin Oppose Microtubules to Drive Long-Range Organelle Transport
title_fullStr Myosin-Va and Dynamic Actin Oppose Microtubules to Drive Long-Range Organelle Transport
title_full_unstemmed Myosin-Va and Dynamic Actin Oppose Microtubules to Drive Long-Range Organelle Transport
title_short Myosin-Va and Dynamic Actin Oppose Microtubules to Drive Long-Range Organelle Transport
title_sort myosin-va and dynamic actin oppose microtubules to drive long-range organelle transport
topic Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4131108/
https://www.ncbi.nlm.nih.gov/pubmed/25065759
http://dx.doi.org/10.1016/j.cub.2014.06.019
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