Microtubule binding by dynactin is required for microtubule organization but not cargo transport

Journal of Cell Biology

Volumn 176, Issue 5, 2007, Pages 641-651

  Kim, Hwajin ^a   Ling, Shuo Chien ^a   Rogers, Gregory C ^b   Kural, Comert ^c   Selvin, Paul R ^c,d   Rogers, Stephen L ^b   Gelfand, Vladimir I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHALASIN D; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL DIVISION; CELL MOTILITY; CELL ORGANELLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; MICROTUBULE ORGANIZING CENTER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BIOLOGICAL TRANSPORT; CELL LINE; DROSOPHILA MELANOGASTER; DYNEIN ATPASE; KINESIN; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULE-ORGANIZING CENTER; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PEROXISOMES; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; SEQUENCE DELETION;

DROSOPHILA MELANOGASTER;

EID: 33847343375     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200608128     Document Type: Article

References (59)

1. Akhmanova, A., and C.C. Hoogenraad. 2005. Microtubule plus-end-tracking proteins: mechanisms and functions. Curr. Opin. Cell Biol. 17:47-54.
2. Askham, J.M., K.T. Vaughan, H.V. Goodson, and E.E. Morrison. 2002. Evidence that an interaction between EB1 and p150(Glued) is required for the formation and maintenance of a radial microtubule array anchored at the centrosome. Mol. Biol. Cell. 13:3627-3645.
3. Blangy, A., L. Arnaud, and E.A. Nigg. 1997. Phosphorylation by p34cdc2 protein kinase regulates binding of the kinesin-related motor HsEg5 to the dynactin subunit p150. J. Biol. Chem. 272:19418-19424.
4. Buffin, E., C. Lefebvre, J. Huang, M.E. Gagou, and R.E. Karess. 2005. Recruitment of Mad2 to the kinetochore requires the Rod/Zw10 complex. Curr. Biol. 15:856-861.
5. Burkhardt, J.K., C.J. Echeverri, T. Nilsson, and R.B. Vallee. 1997. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139:469-484.
6. Campbell, R.E., O. Tour, A.E. Palmer, P.A. Steinbach, G.S. Baird, D.A. Zacharias, and R.Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA. 99:7877-7882.
7. Culver-Hanlon, T.L., S.A. Lex, A.D. Stephens, N.J. Quintyne, and S.J. King. 2006. A microtubule-binding domain in dynactin increases dynein processivity by skating along microtubules. Nat. Cell Biol. 8:264-270.
8. Deacon, S.W., A.S. Serpinskaya, P.S. Vaughan, M. Lopez Fanarraga, I. Vernos, K.T. Vaughan, and V.I. Gelfand. 2003. Dynactin is required for bidirectional organelle transport. J. Cell Biol. 160:297-301.
9. Duncan, J.E., and R. Warrior. 2002. The cytoplasmic dynein and kinesin motors have interdependent roles in patterning the Drosophila oocyte. Curr. Biol. 12:1982-1991.
10. Echeverri, C.J., B.M. Paschal, K.T. Vaughan, and R.B. Vallee. 1996. 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.
11. Fukuda, M., T.S. Kuroda, and K. Mikoshiba. 2002. Slac2-a/melanophilin, the missing link between Rab27 and myosin Va: implications of a tripartite protein complex for melanosome transport. J. Biol. Chem. 277:12432-12436.
12. Gill, S.R., T.A. Schroer, I. Szilak, E.R. Steuer, M.P. Sheetz, and D.W. Cleveland. 1991. Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115:1639-1650.
13. Goldstein, L.S., and S. Gunawardena. 2000. Flying through the Drosophila cytoskeletal genome. J. Cell Biol. 150:F63-F68.
14. Goshima, G., and R.D. Vale. 2003. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol. 162:1003-1016.
15. Gross, S.P., M.A. Welte, S.M. Block, and E.F. Wieschaus. 2002. Coordination of opposite-polarity microtubule motors. J. Cell Biol. 156:715-724.
16. Hayashi, I., A. Wilde, T.K. Mal, and M. Ikura. 2005. Structural basis for the activation of microtubule assembly by the EB1 and p150Glued complex. Mol. Cell. 19:449-460.
17. Holleran, E.A., S. Karki, and E.L. Holzbaur. 1998. The role of the dynactin complex in intracellular motility. Int. Rev. Cytol. 182:69-109.
18. Januschke, J., L. Gervais, S. Dass, J.A. Kaltschmidt, H. Lopez-Schier, D. St Johnston, A.H. Brand, S. Roth, and A. Guichet. 2002. Polar transport in the Drosophila oocyte requires dynein and kinesin I cooperation. Curr. Biol. 12:1971-1981.
19. Kamal, A., and L.S. Goldstein. 2002. Principles of cargo attachment to cytoplasmic motor proteins. Curr. Opin. Cell Biol. 14:63-68.
20. Karcher, R.L., S.W. Deacon, and V.I. Gelfand. 2002. Motor-cargo interactions: the key to transport specificity. Trends Cell Biol. 12:21-27.
21. Karki, S., and E.L. Holzbaur. 1995. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270:28806-28811.
22. Karki, S., and E.L. Holzbaur. 1999. Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr. Opin. Cell Biol. 11:45-53.
23. King, S.J., and T.A. Schroer. 2000. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol. 2:20-24.
24. King, S.J., C.L. Brown, K.C. Maier, N.J. Quintyne, and T.A. Schroer. 2003. Analysis of the dynein-dynactin interaction in vitro and in vivo. Mol. Biol. Cell. 14:5089-5097.
25. Kobayashi, T., K. Shiroguchi, M. Edamatsu, and Y.Y. Toyoshima. 2006. Microtubule-binding properties of dynactin p150 expedient for dynein motility. Biochem. Biophys. Res. Commun. 340:23-28.
26. Kural, C., H. Kim, S. Syed, G. Goshima, V.I. Gelfand, and P.R. Selvin. 2005. Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science. 308:1469-1472.
27. Lansbergen, G., Y. Komarova, M. Modesti, C. Wyman, C.C. Hoogenraad, H.V. Goodson, R.P. Lemaitre, D.N. Drechsel, E. van Munster, T.W. Gadella Jr., et al. 2004. Conformational changes in CLIP-170 regulate its binding to microtubules and dynactin localization. J. Cell Biol. 166:1003-1014.
28. Levy, J.R., C.J. Sumner, J.P. Caviston, M.K. Tokito, S. Ranganathan, L.A. Ligon, K.E. Wallace, B.H. Lamonte, G.G. Harmison, I. Puls, et al. 2006. A motor neuron disease-associated mutation in p150Glued perturbs dynactin function and induces protein aggregation. J. Cell Biol. 172:733-745.
29. Ligon, L.A., S.S. Shelly, M. Tokito, and E.L. Holzbaur. 2003. The microtubule plus-end proteins EB1 and dynactin have differential effects on microtubule polymerization. Mol. Biol. Cell. 14:1405-1417.
30. Ligon, L.A., M. Tokito, J.M. Finklestein, F.E. Grossman, and E.L. Holzbaur. 2004. A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity. J. Biol. Chem. 279:19201-19208.
31. Ling, S.C., P.S. Fahrner, W.T. Greenough, and V.I. Gelfand. 2004. Transport of Drosophila fragile X mental retardation protein-containing ribonucleoprotein granules by kinesin-1 and cytoplasmic dynein. Proc. Natl. Acad. Sci. USA. 101:17428-17433.
32. Mallik, R., and S.P. Gross. 2004. Molecular motors: strategies to get along. Curr. Biol. 14:R971-R982.
33. Martin, M., S.J. Iyadurai, A. Gassman, J.G. Gindhart Jr., T.S. Hays, and W.M. Saxton. 1999. Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol. Biol. Cell. 10:3717-3728.
34. Mimori-Kiyosue, Y., and S. Tsukita. 2003. "Search-and-capture" of microtubules through plus-end-binding proteins (+TIPs). J. Biochem. (Tokyo). 134:321-326.
35. Morales-Mulia, S., and J.M. Scholey. 2005. Spindle pole organization in Drosophila S2 cells by dynein, abnormal spindle protein (Asp), and KLP10A. Mol. Biol. Cell. 16:3176-3186.
36. Puls, I., C. Jonnakuty, B.H. LaMonte, E.L. Holzbaur, M. Tokito, E. Mann, M.K. Floeter, K. Bidus, D. Drayna, S.J. Oh, et al. 2003. Mutant dynactin in motor neuron disease. Nat. Genet. 33:455-456.
37. Quintyne, N.J., and T.A. Schroer. 2002. Distinct cell cycle-dependent roles for dynactin and dynein at centrosomes. J. Cell Biol. 159:245-254.
38. Quintyne, N.J., S.R. Gill, D.M. Eckley, C.L. Crego, D.A. Compton, and T.A. Schroer. 1999. Dynactin is required for microtubule anchoring at centrosomes. J. Cell Biol. 147:321-334.
39. Quintyne, N.J., J.E. Reing, D.R. Hoffelder, S.M. Gollin, and W.S. Saunders. 2005. Spindle multipolarity is prevented by centrosomal clustering. Science. 307:127-129.
40. Reilein, A., and W.J. Nelson. 2005. APC is a component of an organizing template for cortical microtubule networks. Nat. Cell Biol. 7:463-473.
41. Robinson, J.T., E.J. Wojcik, M.A. Sanders, M. McGrail, and T.S. Hays. 1999. Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila. J. Cell Biol. 146:597-608.
42. Schliwa, M., and G. Woehlke. 2003. Molecular motors. Nature. 422:759-765.
43. Schroer, T.A. 2004. Dynactin. Annu. Rev. Cell Dev. Biol. 20:759-779.
44. Schroer, T.A., and M.P. Sheetz. 1991. Two activators of microtubule-based vesicle transport. J. Cell Biol. 115:1309-1318.
45. Sharp, D.J., H.M. Brown, M. Kwon, G.C. Rogers, G. Holland, and J.M. Scholey. 2000a. Functional coordination of three mitotic motors in Drosophila embryos. Mol. Biol. Cell. 11:241-253.
46. Sharp, D.J., G.C. Rogers, and J.M. Scholey. 2000b. Cytoplasmic dynein is required for poleward chromosome movement during mitosis in Drosophila embryos. Nat. Cell Biol. 2:922-930.
47. Tokito, M.K., D.S. Howland, V.M. Lee, and E.L. Holzbaur. 1996. Functionally distinct isoforms of dynactin are expressed in human neurons. Mol. Biol. Cell. 7:1167-1180.
48. Vale, R.D. 2003. The molecular motor toolbox for intracellular transport. Cell. 112:467-480.
49. Vaughan, K.T. 2005a. Microtubule plus ends, motors, and traffic of Golgi membranes. Biochim. Biophys. Acta. 1744:316-324.
50. Vaughan, K.T. 2005b. TIP maker and TIP marker; EB1 as a master controller of microtubule plus ends. J. Cell Biol. 171:197-200.
51. Vaughan, K.T., and R.B. Vallee. 1995. Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. J. Cell Biol. 131:1507-1516.
52. Vaughan, K.T., S.H. Tynan, N.E. Faulkner, C.J. Echeverri, and R.B. Vallee. 1999. Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends. J. Cell Sci. 112:1437-1447.
53. Vaughan, P.S., P. Miura, M. Henderson, B. Byrne, and K.T. Vaughan. 2002. A role for regulated binding of p150(Glued) to microtubule plus ends in organelle transport. J. Cell Biol. 158:305-319.
54. Waterman-Storer, C.M., S. Karki, and E.L. Holzbaur. 1995. 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.
55. Waterman-Storer, C.M., S.B. Karki, S.A. Kuznetsov, J.S. Tabb, D.G. Weiss, G.M. Langford, and E.L. Holzbaur. 1997. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc. Natl. Acad. Sci. USA. 94:12180-12185.
56. Watson, P., and D.J. Stephens. 2006. Microtubule plus-end loading of p150(Glued) is mediated by EB1 and CLIP-170 but is not required for intracellular membrane traffic in mammalian cells. J. Cell Sci. 119:2758-2767.
57. Wojcik, E., R. Basto, M. Serr, F. Scaerou, R. Karess, and T. Hays. 2001. Kinetochore dynein: its dynamics and role in the transport of the Rough deal checkpoint protein. Nat. Cell Biol. 3:1001-1007.
58. Wu, X.S., K. Rao, H. Zhang, F. Wang, J.R. Sellers, L.E. Matesic, N.G. Copeland, N.A. Jenkins, and J.A. Hammer III. 2002. Identification of an organelle receptor for myosin-Va. Nat. Cell Biol. 4:271-278.
59. Yildiz, A., and P.R. Selvin. 2005. Fluorescence imaging with one nanometer accuracy: application to molecular motors. Acc. Chem. Res. 38:574-582.