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Myosin-Va and dynamic actin oppose microtubules to drive long-range organelle transport

HUME, ALISTAIR; 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.

Authors

ALISTAIR HUME

Richard D. Evans

Christopher Robinson

Deborah A. Briggs

David J. Tooth

Jose S. Ramalho

Marta Cantero

Lluis Montoliu

Shyamal Patel

Elena V. Sviderskaya

Alistair N. Hume



Abstract

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]. © 2014 The Authors.

Journal Article Type Article
Publication Date Aug 4, 2014
Journal Current Biology
Print ISSN 0960-9822
Electronic ISSN 1879-0445
Publisher Elsevier (Cell Press)
Peer Reviewed Peer Reviewed
Volume 24
Issue 15
Pages 1743-1750
APA6 Citation Evans, R. D., Robinson, C., Briggs, D. A., Tooth, D. J., Ramalho, J. S., Cantero, M., …Hume, A. N. (2014). Myosin-Va and dynamic actin oppose microtubules to drive long-range organelle transport. Current Biology, 24(15), 1743-1750. https://doi.org/10.1016/j.cub.2014.06.019
DOI https://doi.org/10.1016/j.cub.2014.06.019
PMID 25065759
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