The mammalian dynein–dynactin complex is a strong opponent to kinesin in a tug-of-war competition (original) (raw)
References
Hancock, W. O. Bidirectional cargo transport: moving beyond tug of war. Nat. Rev. Mol. Cell Biol.15, 615–628 (2014). ArticleCAS Google Scholar
Kunwar, A. et al. Mechanical stochastic tug-of-war models cannot explain bidirectional lipid-droplet transport. Proc. Natl Acad. Sci. USA108, 18960–18965 (2011). ArticleCAS Google Scholar
Schlager, M. A., Hoang, H. T., Urnavicius, L., Bullock, S. L. & Carter, A. P. In vitro reconstitution of a highly processive recombinant human dynein complex. EMBO J.33, 1855–1868 (2014). ArticleCAS Google Scholar
McKenney, R. J., Huynh, W., Tanenbaum, M. E., Bhabha, G. & Vale, R. D. Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes. Science345, 337–341 (2014). ArticleCAS Google Scholar
Urnavicius, L. et al. The structure of the dynactin complex and its interaction with dynein. Science347, 1441–1446 (2015). ArticleCAS Google Scholar
Splinter, D. et al. BICD2, dynactin, and LIS1 cooperate in regulating dynein recruitment to cellular structures. Mol. Biol. Cell23, 4226–4241 (2012). ArticleCAS Google Scholar
Roberts, A. J., Kon, T., Knight, P. J., Sutoh, K. & Burgess, S. A. Functions and mechanics of dynein motor proteins. Nat. Rev. Mol. Cell Biol.14, 713–726 (2013). ArticleCAS Google Scholar
Burgess, S. A., Walker, M. L., Sakakibara, H., Knight, P. J. & Oiwa, K. Dynein structure and power stroke. Nature421, 715–718 (2003). ArticleCAS Google Scholar
Torisawa, T. et al. Autoinhibition and cooperative activation mechanisms of cytoplasmic dynein. Nat. Cell Biol.16, 1118–1124 (2014). ArticleCAS Google Scholar
Moughamian, A. J., Osborn, G. E., Lazarus, J. E., Maday, S. & Holzbaur, E. L. F. Ordered recruitment of dynactin to the microtubule plus-end is required for efficient initiation of retrograde axonal transport. J. Neurosci.33, 13190–13203 (2013). ArticleCAS Google Scholar
Wang, Z. & Sheetz, M. P. One-dimensional diffusion on microtubules of particles coated with cytoplasmic dynein and immunoglobulins. Cell Struct. Funct.24, 373–383 (1999). ArticleCAS Google Scholar
Ayloo, S. et al. Dynactin functions as both a dynamic tether and brake during dynein-driven motility. Nat. Commun.5, 4807 (2014). ArticleCAS Google Scholar
McKenney, R. J., Vershinin, M., Kunwar, A., Vallee, R. B. & Gross, S. P. LIS1 and NudE induce a persistent dynein force-producing state. Cell141, 304–314 (2010). ArticleCAS Google Scholar
Rai, A. K., Ramaiya, A. J., Jha, R. & Mallik, R. Molecular adaptations allow dynein to generate large collective forces inside cells. Cell152, 172–182 (2013). ArticleCAS Google Scholar
Mallik, R., Carter, B. C., Lex, S. A., King, S. J. & Gross, S. P. Cytoplasmic dynein functions as a gear in response to load. Nature427, 649–652 (2004). ArticleCAS Google Scholar
Tripathy, S. K. et al. Autoregulatory mechanism for dynactin control of processive and diffusive dynein transport. Nat. Cell Biol.16, 1192–1201 (2014). ArticleCAS Google Scholar
Ori-McKenney, K. M., Xu, J., Gross, S. P. & Vallee, R. B. A cytoplasmic dynein tail mutation impairs motor processivity. Nat. Cell Biol.12, 1228–1234 (2010). ArticleCAS Google Scholar
Visscher, K., Schnitzer, M. J. & Block, S. M. Single kinesin molecules studied with a molecular force clamp. Nature400, 184–189 (1999). ArticleCAS Google Scholar
Rai, A. et al. Dynein clusters into lipid microdomains on phagosomes to drive rapid transport toward lysosomes. Cell164, 722–734 (2016). ArticleCAS Google Scholar
Hendricks, A. G. et al. Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr. Biol.20, 697–702 (2010). ArticleCAS Google Scholar
Thirumurugan, K., Sakamoto, T., Hammer, J. A. III, Sellers, J. R. & Knight, P. J. The cargo-binding domain regulates structure and activity of myosin 5. Nature442, 212–215 (2006). ArticleCAS Google Scholar
Kaan, H. Y. K., Hackney, D. D. & Kozielski, F. The structure of the kinesin-1 motor-tail complex reveals the mechanism of autoinhibition. Science333, 883–885 (2011). ArticleCAS Google Scholar
King, S. J. & Schroer, T. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol.2, 20–24 (2000). ArticleCAS Google Scholar
Chowdhury, S., Ketcham, S. A., Schroer, T. A. & Lander, G. C. Structural organization of the dynein–dynactin complex bound to microtubules. Nat. Struct. Mol. Biol.22, 345–347 (2015). ArticleCAS Google Scholar
Nicholas, M. P. et al. Control of cytoplasmic dynein force production and processivity by its C-terminal domain. Nat. Commun.6, 6206 (2015). ArticleCAS Google Scholar
DeWitt, M. A., Chang, A. Y., Combs, P. A. & Yildiz, A. Cytoplasmic dynein moves through uncoordinated stepping of the AAA + ring domains. Science335, 221–225 (2012). ArticleCAS Google Scholar
Cleary, F. B. et al. Tension on the linker gates the ATP-dependent release of dynein from microtubules. Nat. Commun.5, 4587 (2014). ArticleCAS Google Scholar
Belyy, V., Hendel, N. L., Chien, A. & Yildiz, A. Cytoplasmic dynein transports cargos via load-sharing between the heads. Nat. Commun.5, 5544 (2014). ArticleCAS Google Scholar
Gennerich, A., Carter, A. P., Reck-Peterson, S. L. & Vale, R. D. Force-induced bidirectional stepping of cytoplasmic dynein. Cell131, 952–965 (2007). ArticleCAS Google Scholar
Svoboda, K. & Block, S. M. Force and velocity measured for single kinesin molecules. Cell77, 773–784 (1994). ArticleCAS Google Scholar
Derr, N. D. et al. Tug-of-war in motor protein ensembles revealed with a programmable DNA origami scaffold. Science338, 662–665 (2012). ArticleCAS Google Scholar
Diehl, M. R., Zhang, K., Lee, H. J. & Tirrell, D. A. Engineering cooperativity in biomotor-protein assemblies. Science311, 1468–1471 (2006). ArticleCAS Google Scholar
Fu, M. M. & Holzbaur, E. L. F. JIP1 regulates the directionality of APP axonal transport by coordinating kinesin and dynein motors. J. Cell Biol.202, 495–508 (2013). ArticleCAS Google Scholar
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. Proc. Natl Acad. Sci. USA106, 19381–19386 (2009). ArticleCAS Google Scholar
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. Biophys. J.103, 492–500 (2012). ArticleCAS Google Scholar
Shubeita, G. T. et al. Consequences of motor copy number on the intracellular transport of kinesin-1-driven lipid droplets. Cell135, 1098–1107 (2008). ArticleCAS Google Scholar
Fu, M. & Holzbaur, E. L. F. Integrated regulation of motor-driven organelle transport by scaffolding proteins. Trends Cell Biol.24, 564–574 (2014). ArticleCAS Google Scholar
Klumpp, S. & Lipowsky, R. Cooperative cargo transport by several molecular motors. Proc. Natl Acad. Sci. USA102, 17284–17289 (2005). ArticleCAS Google Scholar
Reck-Peterson, S. L. et al. Single-molecule analysis of dynein processivity and stepping behavior. Cell126, 335–348 (2006). ArticleCAS Google Scholar
Castoldi, M. & Popov, A. V. Purification of brain tubulin through two cycles of polymerization–depolymerization in a high-molarity buffer. Protein Expr. Purif.32, 83–88 (2003). ArticleCAS Google Scholar