Autoregulatory mechanism for dynactin control of processive and diffusive dynein transport

Nature Cell Biology

Volumn 16, Issue 12, 2014, Pages 1192-1201

  Tripathy, Suvranta K ^a   Weil, Sarah J ^b,c   Chen, Chen ^b,c   Anand, Preetha ^a   Vallee, Richard B ^b   Gross, Steven P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Department of Medicine   (United States)

^c Columbia University New York ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CC1A PROTEIN; CC1B PROTEIN; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; P150 GLUED PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; MICROTUBULE ASSOCIATED PROTEIN; PEPTIDE FRAGMENT; PROTEIN BINDING; RECOMBINANT PROTEIN;

ALLOSTERISM; ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; AUTOREGULATION; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MICROTUBULE; PROTEIN TERTIARY STRUCTURE; RAT; SF9 CELL LINE; SPODOPTERA;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; DYNEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RECOMBINANT PROTEINS; SF9 CELLS; SPODOPTERA;

EID: 84926032408     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3063     Document Type: Article

References (57)

1. Vallee, R. B., McKenney, R. J. &Ori-McKenney, K. M. Multiple modes of cytoplasmic dynein regulation. Nat. Cell Biol. 14, 224-230 (2012).
2. McKenney, R. J., Vershinin, M., Kunwar, A., Vallee, R. B. &Gross, S. P. LIS1 and NudE induce a persistent dynein force-producing state. Cell 141, 304-314 (2010).
3. Huang, J., Roberts, A. J., Leschziner, A. E. &Reck-Peterson, S. L. Lis1 acts as a Clutch between the ATPase and microtubule-binding domains of the dynein motor. Cell 150, 975-986 (2012).
4. Schroer, T. A. Dynactin. Annu. Rev. Cell Dev. Biol. 20, 759-779 (2004).
5. Echeverri, C. J., Paschal, B. M., Vaughan, K. T. &Vallee, R. B. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J. Cell Biol. 132, 617-633 (1996).
6. Holleran, E. A., Tokito, M. K., Karki, S. &Holzbaur, E. L. Centractin (ARP1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles. J. Cell Biol. 135, 1815-1829 (1996).
7. King, S. J. &Schroer, T. A. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol. 2, 20-24 (2000).
8. Culver-Hanlon, T. L., Lex, S. A., Stephens, A. D., Quintyne, N. J. &King, S. J. A microtubule-binding domain in dynactin increases dynein processivity by skating along microtubules. Nat. Cell Biol. 8, 264-270 (2006).
9. Kardon, J. R., Reck-Peterson, S. L. &Vale, R. D. Regulation of the processivity and intracellular localization of Saccharomyces cerevisiae dynein by dynactin. Proc. Natl Acad. Sci. USA 106, 5669-5674 (2009).
10. Holzbaur, E. L. F. et al. Homology of a 150K cytoplasmic dynein-Associated polypeptide with the Drosophila gene Glued. Nature 351, 579-583 (1991).
11. Vaughan, K. T. &Vallee, R. B. Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. J. Cell Biol. 131, 1507-1516 (1995).
12. Waterman-Storer, C. M., Karki, S. &Holzbaur, E. L. The p150Glued component of the dynactin complex binds to both microtubules and the actin-related protein centractin (Arp-1). Proc. Natl Acad. Sci. USA 92, 1634-1638 (1995).
13. Vaughan, P. S., Miura, P., Henderson, M., Byrne, B. &Vaughan, K. T. A role for regulated binding of p150(Glued) to microtubule plus ends in organelle transport. J. Cell Biol. 158, 305-319 (2002).
14. Watson, P. &Stephens, D. J. Microtubule plus-end loading of p150Glued is mediated by EB1 and CLIP-170 but is not required for intracellular membrane traffic in mammalian cells. J. Cell Sci. 119, 2758-2767 (2006).
15. Dixit, R., Levy, J. R., Tokito, M., Ligon, L. A. &Holzbaur, E. L. F. Regulation of dynactin through the differential expression of p150(Glued) isoforms. J. Biol. Chem. 283, 33611-33619 (2008).
16. Kim, H. et al. Microtubule binding by dynactin is required for microtubule organization but not cargo transport. J. Cell Biol. 176, 641-651 (2007).
17. Moughamian, A. J. &Holzbaur, E. L. Dynactin is required for transport initiation from the distal axon. Neuron 74, 331-343 (2012).
18. Lloyd, T. E. et al. The p150(Glued) CAP-Gly domain regulates initiation of retrograde transport at synaptic termini. Neuron 74, 344-360 (2012).
19. Gross, S. P., Welte, M. A., Block, S. M. &Wieschaus, E. F. Coordination of oppositepolarity microtubule motors. J. Cell Biol. 156, 715-724 (2002).
20. Haghnia, M. et al. Dynactin is required for coordinated bidirectional motility, but not for dynein membrane attachment. Mol. Biol. Cell 18, 2081-2089 (2007).
21. McKenney, R. J., Weil, S. J., Scherer, J. &Vallee, R. B. Mutually exclusive cytoplasmic dynein regulation by NudE-Lis1 and dynactin. J. Biol. Chem. 286, 39615-39622 (2011).
22. Siglin, A. E. et al. Dynein and dynactin leverage their bivalent character to form a high-Affinity interaction. PLoS ONE 8, e59453 (2013).
23. Lau, S. Y., Taneja, A. K. &Hodges, R. S. Synthesis of a model protein of defined secondary and quaternary structure. Effect of chain length on the stabilization and formation of two-stranded alpha-helical coiled-coils. J. Biol. Chem. 259, 13253-13261 (1984).
24. Ross, J. L., Wallace, K., Shuman, H., Goldman, Y. E. &Holzbaur, E. L. F. Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat. Cell Biol. 8, 562-570 (2006).
25. Mallik, R., Carter, B. C., Lex, S. A., King, S. J. &Gross, S. P. Cytoplasmic dynein functions as a gear in response to load. Nature 427, 649-652 (2004).
26. Wang, Z., Khan, S. &Sheetz, M. P. Single cytoplasmic dynein molecule movements: characterization and comparison with kinesin. Biophys. J. 69, 2011-2023 (1995).
27. Tokito, M. K., Howland, D. S., Lee, V. M. &Holzbaur, E. L. Functionally distinct isoforms of dynactin are expressed in human neurons. Mol. Biol. Cell 7, 1167-1180 (1996).
28. Quintyne, N. J. et al. Dynactin is required for microtubule anchoring at centrosomes. J. Cell Biol. 147, 321-334 (1999).
29. Morgan, J. L., Song, Y. &Barbar, E. Structural dynamics and multiregion interactions in dynein-dynactin recognition. J. Biol. Chem. 286, 39349-39359 (2011).
30. 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).
31. DeWitt, M. A., Chang, A. Y., Combs, P. A. &Yildiz, A. Cytoplasmic dynein moves through uncoordinated stepping of the AAAC ring domains. Science 335, 221-225 (2012).
32. Qiu, W. et al. Dynein achieves processive motion using both stochastic and coordinated stepping. Nat. Struct. Mol. Biol. 19, 193-200 (2012).
33. Weisbrich, A. et al. Structure-function relationship of CAP-Gly domains. Nat. Struct. Mol. Biol. 14, 959-967 (2007).
34. Rao, L. et al. The yeast dynein Dyn2-Pac11 complex is a dynein dimerization/processivity factor: structural and single-molecule characterization. Mol. Biol. Cell 24, 2362-2377 (2013).
35. Ananthanarayanan, V. et al. Dynein motion switches from diffusive to directed upon cortical anchoring. Cell 153, 1526-1536 (2013).
36. Tang, X., Germain, B. S. &Lee, W-L. A novel patch assembly domain in Num1 mediates dynein anchoring at the cortex during spindle positioning. J. Cell Biol. 196, 743-756 (2012).
37. Scherer, J, Yi, J. &Vallee, R. B. PKA-dependent dynein cargo switching from lysosomes to adenovirus: a novel form of host-virus competition. J. Cell Biol. 205, 163-177 (2014).
38. 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).
39. McKenney, R. J., Huynh, W., Tanenbaum, M. E., Bhabha, G. &Vale, R. D. Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes. Science 345, 337-341 (2014).
40. Paschal, B. M. et al. Characterization of a 50-kDa polypeptide in cytoplasmic dynein preparations reveals a complex with p150GLUED and a novel actin. J. Biol. Chem. 268, 15318-15323 (1993).
41. Yi, J. Y. et al. High-resolution imaging reveals indirect coordination of opposite motors and a role for LIS1 in high-load axonal transport. J. Cell Biol. 195, 193-201 (2011).
42. Bremner, K. H. et al. Adenovirus transport via direct interaction of cytoplasmic dynein with the viral capsid hexon subunit. Cell Host Microbe 6, 523-535 (2009).
43. Sigua, R., Tripathy, S., Anand, P. &Gross, S. P. Isolation and purification of kinesin from Drosophila embryos. J. Vis. Exp. (2012).
44. Paschal, B. M., Shpetner, H. S. &Vallee, R. B. Purification of brain cytoplasmic dynein and characterization of its in vitro properties. Methods Enzymol. 196, 181-191 (1991).
45. Mikami, A. et al. Molecular structure of cytoplasmic dynein 2 and its distribution in neuronal and ciliated cells. J. Cell Sci. 115, 4801-4808 (2002).
46. Bohm, K. J., Stracke, R. &Unger, E. Speeding up kinesin-driven microtubule gliding in vitro by variation of cofactor composition and physicochemical parameters. Cell Biol. Int. 24, 335-341 (2000).
47. Kelly, S. M., Jess, T. J. &Price, N. C. How to study proteins by circular dichroism. Biochim. Biophys. Acta 1751, 119-139 (2005).
48. Kunwar, A. et al. Mechanical stochastic tug-of-war models cannot explain bidirectional lipid-droplet transport. Proc. Natl Acad. Sci. USA 108, 18960-18965 (2011).
49. Svoboda, K. &Block, S. M. Force and velocity measured for single kinesin molecules. Cell 77, 773-784 (1994).
50. Vershinin, M., Carter, B. C., Razafsky, D. S., King, S. J. &Gross, S. P. Multiplemotor based transport and its regulation by Tau. Proc. Natl Acad. Sci. USA 104, 87-92 (2007).
51. 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. Curr. Biol. 15, 2075-2085 (2005).
52. Lang, M. J., Asbury, C. L., Shaevitz, J. W. &Block, S. M. An automated twodimensional optical force clamp for single molecule studies. Biophys. J. 83, 491-501 (2002).
53. Kerssemakers, J. W. et al. Assembly dynamics of microtubules at molecular resolution. Nature 442, 709-712 (2006).
54. Carter, B. C., Vershinin, M. &Gross, S. P. A comparison of step-detection methods: how well can you do? Biophys. J. 94, 306-319 (2008).
55. Pearson, C. G. et al. Measuring nanometer scale gradients in spindle microtubule dynamics using model convolution microscopy. Mol. Biol. Cell 17, 4069-4079 (2006).
56. Carter, N. J. &Cross, R. A. Mechanics of the kinesin step. Nature 435, 308-312 (2005).
57. Carter, B. C., Shubeita, G. T. &Gross, S. P. Tracking single particles: a user-friendly quantitative evaluation. Phys. Biol. 2, 60-72 (2005).