Hook is an adapter that coordinates kinesin-3 and dynein cargo attachment on early endosomes

Journal of Cell Biology

Volumn 204, Issue 6, 2014, Pages 989-1007

  Bielska, Ewa ^a   Schuster, Martin ^a   Roger, Yvonne ^a   Berepiki, Adokiye ^a,b   Soanes, Darren M ^a   Talbot, Nicholas J ^a   Steinberg, Gero ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; HOK1 PROTEIN; HOOK3 PROTEIN; KINESIN; KINESIN 3; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL MOTILITY; CELL STRUCTURE; ENDOSOME; LOSS OF FUNCTION MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; USTILAGO MAYDIS;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; DYNEINS; ENDOSOMES; FUNGAL PROTEINS; KINESIN; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; USTILAGO;

EID: 84896271300     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201309022     Document Type: Article

References (83)

1. Aichinger, C., K. Hansson, H. Eichhorn, F. Lessing, G. Mannhaupt, W. Mewes, and R. Kahmann. 2003. Identification of plant-regulated genes in Ustilago maydis by enhancer-trapping mutagenesis. Mol. Genet. Genomics. 270:303-314. http://dx.doi.org/10.1007/s00438-003-0926-z
2. Akhmanova, A., and J.A. Hammer III. 2010. Linking molecular motors to membrane cargo. Curr. Opin. Cell Biol. 22:479-487. http://dx.doi.org/ 10.1016/j.ceb.2010.04.008
3. Baron Gaillard, C.L., E. Pallesi-Pocachard, D. Massey-Harroche, F. Richard, J.P. Arsanto, J.P. Chauvin, P. Lecine, H. Krämer, J.P. Borg, and A. Le Bivic. 2011. Hook2 is involved in the morphogenesis of the primary cilium. Mol. Biol. Cell. 22:4549-4562. http://dx.doi.org/10.1091/ mbc.E11-05-0405
4. Beakes, G.W., S.L. Glockling, and S. Sekimoto. 2012. The evolutionary phylogeny of the oomycete "fungi". Protoplasma. 249:3-19. http://dx.doi .org/10.1007/s00709-011-0269-2
5. Beeg, J., S. Klumpp, R. Dimova, R.S. Gracià, E. Unger, and R. Lipowsky. 2008. Transport of beads by several kinesin motors. Biophys. J. 94:532-541. http://dx.doi.org/10.1529/biophysj.106.097881
6. Bottin, A., J. Kämper, and R. Kahmann. 1996. Isolation of a carbon sourceregulated gene from Ustilago maydis. Mol. Gen. Genet. 253:342-352.
7. Brachmann, A., G. Weinzierl, J. Kämper, and R. Kahmann. 2001. Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol. Microbiol. 42:1047-1063. http://dx.doi.org/10.1046/j.1365-2958.2001. 02699.x
8. Brady, S.T. 1985. A novel brain ATPase with properties expected for the fast axonal transport motor. Nature. 317:73-75. http://dx.doi.org/10.1038/ 317073a0
9. Caviston, J.P., and E.L. Holzbaur. 2009. Huntingtin as an essential integrator of intracellular vesicular trafficking. Trends Cell Biol. 19:147-155. http:// dx.doi.org/10.1016/j.tcb.2009.01.005
10. Colin, E., D. Zala, G. Liot, H. Rangone, M. Borrell-Pagès, X.J. Li, F. Saudou, and S. Humbert. 2008. Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J. 27:2124-2134. http://dx.doi.org/10.1038/emboj.2008.133
11. Dagdas, Y.F., K. Yoshino, G. Dagdas, L.S. Ryder, E. Bielska, G. Steinberg, and N.J. Talbot. 2012. Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science. 336:1590-1595. http://dx.doi.org/10 .1126/science.1222934
12. Davidse, L.C., and W. Flach. 1977. Differential binding of methyl benzimidazol-2-yl carbamate to fungal tubulin as a mechanism of resistance to this antimitotic agent in mutant strains of Aspergillus nidulans. J. Cell Biol. 72:174-193. http://dx.doi.org/10.1083/jcb.72.1.174
13. Deacon, S.W., A. Nascimento, A.S. Serpinskaya, and V.I. Gelfand. 2005. Regulation of bidirectional melanosome transport by organelle bound MAP kinase. Curr. Biol. 15:459-463. http://dx.doi.org/10.1016/j.cub.2004.12.074
14. DeGiorgis, J.A., T.A. Petukhova, T.A. Evans, and T.S. Reese. 2008. Kinesin-3 is an organelle motor in the squid giant axon. Traffic. 9:1867-1877. http:// dx.doi.org/10.1111/j.1600-0854.2008.00809.x
15. Derr, N.D., B.S. Goodman, R. Jungmann, A.E. Leschziner, W.M. Shih, and S.L. Reck-Peterson. 2012. Tug-of-war in motor protein ensembles revealed with a programmable DNA origami scaffold. Science. 338:662-665. http://dx.doi.org/10.1126/science.1226734
16. Engelender, S., A.H. Sharp, V. Colomer, M.K. Tokito, A. Lanahan, P. Worley, E.L. Holzbaur, and C.A. Ross. 1997. Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum. Mol. Genet. 6:2205-2212. http://dx.doi.org/10.1093/hmg/6.13.2205
17. Fischer-Parton, S., R.M. Parton, P.C. Hickey, J. Dijksterhuis, H.A. Atkinson, and N.D. Read. 2000. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J. Microsc. 198:246-259. http://dx.doi.org/10.1046/j.1365-2818.2000.00708.x
18. Fridolfsson, H.N., N. Ly, M. Meyerzon, and D.A. Starr. 2010. UNC-83 coordinates kinesin-1 and dynein activities at the nuclear envelope during nuclear migration. Dev. Biol. 338:237-250. http://dx.doi.org/10.1016/j .ydbio.2009.12.004
19. Fu, M.M., and E.L. Holzbaur. 2013. JIP1 regulates the directionality of APP axonal transport by coordinating kinesin and dynein motors. J. Cell Biol. 202:495-508. http://dx.doi.org/10.1083/jcb.201302078
20. Fuchs, U., I. Manns, and G. Steinberg. 2005. Microtubules are dispensable for the initial pathogenic development but required for long-distance hyphal growth in the corn smut fungus Ustilago maydis. Mol. Biol. Cell. 16:2746-2758. http://dx.doi.org/10.1091/mbc.E05-03-0176
21. Fuchs, U., G. Hause, I. Schuchardt, and G. Steinberg. 2006. Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell. 18:2066-2081. http://dx.doi.org/10.1105/tpc.105.039388
22. Ge, X., C.L. Frank, F. Calderon de Anda, and L.H. Tsai. 2010. Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron. 65:191-203. http://dx.doi.org/10.1016/j .neuron.2010.01.011
23. Gross, S.P. 2004. Hither and yon: a review of bi-directional microtubule-based transport. Phys. Biol. 1:R1-R11. http://dx.doi.org/10.1088/1478-3967/ 1/2/R01
24. Hammond, J.W., D. Cai, T.L. Blasius, Z. Li, Y. Jiang, G.T. Jih, E. Meyhofer, and K.J. Verhey. 2009. Mammalian Kinesin-3 motors are dimeric in vivo and move by processive motility upon release of autoinhibition. PLoS Biol. 7:e72. http://dx.doi.org/10.1371/journal.pbio.1000072
25. Hendricks, A.G., E. Perlson, J.L. Ross, H.W. Schroeder III, M. Tokito, and E.L. Holzbaur. 2010. Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr. Biol. 20:697-702. http://dx.doi.org/ 10.1016/j.cub.2010.02.058
26. Higuchi, Y., P. Ashwin, Y. Roger, and G. Steinberg. 2014. Early endosome motility spatially organizes polysome distribution. J. Cell Biol. 204:343-357. http://dx.doi.org/10.1083/jcb.201307164
27. Hirokawa, N., S. Niwa, and Y. Tanaka. 2010. Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron. 68:610-638. http://dx.doi.org/10.1016/j.neuron.2010.09.039
28. Hoepfner, S., F. Severin, A. Cabezas, B. Habermann, A. Runge, D. Gillooly, H. Stenmark, and M. Zerial. 2005. Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell. 121:437-450. http://dx.doi.org/10.1016/j.cell.2005.02.017
29. Hoffman, C.S., and F. Winston. 1987. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene. 57:267-272. http://dx.doi.org/10.1016/0378-1119 (87)90131-4
30. Holliday, R. 1974. Ustilago maydis. In Handbook of Genetics R.C. King, editor. Plenum Press, New York. 575-595.
31. Jolly, A.L., and V.I. Gelfand. 2011. Bidirectional intracellular transport: utility and mechanism. Biochem. Soc. Trans. 39:1126-1130. http://dx.doi.org/10.1042/BST0391126
32. Jung, M.K., I.B. Wilder, and B.R. Oakley. 1992. Amino acid alterations in the benA (β-tubulin) gene of Aspergillus nidulans that confer benomyl resistance. Cell Motil. Cytoskeleton. 22:170-174. http://dx.doi.org/10.1002/ cm.970220304
33. Kämper, J., R. Kahmann, M. Bölker, L.J. Ma, T. Brefort, B.J. Saville, F. Banuett, J.W. Kronstad, S.E. Gold, O. Müller, et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature. 444:97-101. http://dx.doi.org/10.1038/nature05248
34. Klopfenstein, D.R., M. Tomishige, N. Stuurman, and R.D. Vale. 2002. Role of phosphatidylinositol(4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell. 109:347-358. http://dx.doi.org/ 10.1016/S0092-8674(02)00708-0
35. Klumpp, S., and R. Lipowsky. 2005. Cooperative cargo transport by several molecular motors. Proc. Natl. Acad. Sci. USA. 102:17284-17289. http:// dx.doi.org/10.1073/pnas.0507363102
36. Knop, M., K. Siegers, G. Pereira, W. Zachariae, B. Winsor, K. Nasmyth, and E. Schiebel. 1999. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast. 15(10B):963-972. http://dx.doi.org/10.1002/(SICI)1097-0061(199907)15:10B963:: AID-YEA3993.0.CO;2-W
37. Krämer, H., and M. Phistry. 1996. Mutations in the Drosophila hook gene inhibit endocytosis of the boss transmembrane ligand into multivesicular bodies. J. Cell Biol. 133:1205-1215. http://dx.doi.org/10.1083/jcb.133.6.1205
38. Krämer, H., and M. Phistry. 1999. Genetic analysis of hook, a gene required for endocytic trafficking in Drosophila. Genetics. 151:675-684.
39. Kunwar, A., S.K. Tripathy, J. Xu, M.K. Mattson, P. Anand, R. Sigua, M. Vershinin, R.J. McKenney, C.C. Yu, A. Mogilner, and S.P. Gross. 2011. Mechanical stochastic tug-of-war models cannot explain bidirectional lipid-droplet transport. Proc. Natl. Acad. Sci. USA. 108:18960-18965. http://dx.doi.org/ 10.1073/pnas.1107841108
40. Lenz, J.H., I. Schuchardt, A. Straube, and G. Steinberg. 2006. A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J. 25:2275-2286. http://dx.doi.org/10.1038/sj.emboj.7601119
41. Lesche, R., A. Peetz, F. van der Hoeven, and U. Rüther. 1997. Ft1, a novel gene related to ubiquitin-conjugating enzymes, is deleted in the Fused toes mouse mutation. Mamm. Genome. 8:879-883. http://dx.doi.org/10.1007/ s003359900604
42. Li, H., and R. Durbin. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 25:1754-1760. http://dx.doi .org/10.1093/bioinformatics/btp324
43. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, and R. Durbin; 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/ btp352
44. Li, S.H., C.A. Gutekunst, S.M. Hersch, and X.J. Li. 1998. Interaction of huntingtin-associated protein with dynactin P150Glued. J. Neurosci. 18:1261-1269.
45. Linstedt, A.D. 2004. Positioning the Golgi apparatus. Cell. 118:271-272. http:// dx.doi.org/10.1016/j.cell.2004.07.015
46. Maldonado-Báez, L., N.B. Cole, H. Krämer, and J.G. Donaldson. 2013. Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1. J. Cell Biol. 201:233-247. http://dx.doi.org/10.1083/jcb .201208172
47. Malone, C.J., L. Misner, N. Le Bot, M.C. Tsai, J.M. Campbell, J. Ahringer, and J.G. White. 2003. The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell. 115:825-836. http://dx.doi.org/10.1016/S0092-8674(03)00985-1
48. McGuire, J.R., J. Rong, S.H. Li, and X.J. Li. 2006. Interaction of Huntingtinassociated protein-1 with kinesin light chain: implications in intracellular trafficking in neurons. J. Biol. Chem. 281:3552-3559. http://dx.doi .org/10.1074/jbc.M509806200
49. Miki, H., M. Setou, K. Kaneshiro, and N. Hirokawa. 2001. All kinesin superfamily protein, KIF, genes in mouse and human. Proc. Natl. Acad. Sci. USA. 98:7004-7011. http://dx.doi.org/10.1073/pnas.111145398
50. Mitchell, D.J., K.R. Blasier, E.D. Jeffery, M.W. Ross, A.K. Pullikuth, D. Suo, J. Park, W.R. Smiley, K.W. Lo, J. Shabanowitz, et al. 2012. Trk activation of the ERK1/2 kinase pathway stimulates intermediate chain phosphorylation and recruits cytoplasmic dynein to signaling endosomes for retrograde axonal transport. J. Neurosci. 32:15495-15510. http://dx.doi .org/10.1523/JNEUROSCI.5599-11.2012
51. Müller, M.J., S. Klumpp, and R. Lipowsky. 2008. Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc. Natl. Acad. Sci. USA. 105:4609-4614. http://dx.doi.org/ 10.1073/pnas.0706825105
52. Niwa, S., Y. Tanaka, and N. Hirokawa. 2008. KIF1Bβ-and KIF1A-mediated axonal transport of presynaptic regulator Rab3 occurs in a GTP-dependent manner through DENN/MADD. Nat. Cell Biol. 10:1269-1279. http:// dx.doi.org/10.1038/ncb1785
53. Raymond, C.K., T.A. Pownder, and S.L. Sexson. 1999. General method for plasmid construction using homologous recombination. Biotechniques. 26:134-141.
54. Reis, G.F., G. Yang, L. Szpankowski, C. Weaver, S.B. Shah, J.T. Robinson, T.S. Hays, G. Danuser, and L.S. Goldstein. 2012. Molecular motor function in axonal transport in vivo probed by genetic and computational analysis in Drosophila. Mol. Biol. Cell. 23:1700-1714. http://dx.doi.org/10.1091/ mbc.E11-11-0938
55. Schuster, M., S. Kilaru, P. Ashwin, C. Lin, N.J. Severs, and G. Steinberg. 2011a. Controlled and stochastic retention concentrates dynein at microtubule ends to keep endosomes on track. EMBO J. 30:652-664. http://dx.doi .org/10.1038/emboj.2010.360
56. Schuster, M., S. Kilaru, G. Fink, J. Collemare, Y. Roger, and G. Steinberg. 2011b. Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array. Mol. Biol. Cell. 22:3645-3657. http://dx.doi.org/10.1091/mbc.E11-03-0217
57. Schuster, M., R. Lipowsky, M.A. Assmann, P. Lenz, and G. Steinberg. 2011c. Transient binding of dynein controls bidirectional long-range motility of early endosomes. Proc. Natl. Acad. Sci. USA. 108:3618-3623. http:// dx.doi.org/10.1073/pnas.1015839108
58. Schuster, M., S. Treitschke, S. Kilaru, J. Molloy, N.J. Harmer, and G. Steinberg. 2012. Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J. 31:214-227. http://dx.doi .org/10.1038/emboj.2011.361
59. Soppina, V., A.K. Rai, A.J. Ramaiya, P. Barak, and R. Mallik. 2009. Tugof-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. Proc. Natl. Acad. Sci. USA. 106:19381-19386. http://dx.doi.org/10.1073/pnas.0906524106
60. Spellig, T., A. Bottin, and R. Kahmann. 1996. Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252:503-509.
61. Splinter, D., M.E. Tanenbaum, A. Lindqvist, D. Jaarsma, A. Flotho, K.L. Yu, I. Grigoriev, D. Engelsma, E.D. Haasdijk, N. Keijzer, et al. 2010. Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol. 8:e1000350. http://dx.doi.org/10.1371/journal.pbio.1000350
62. Steenkamp, E.T., J. Wright, and S.L. Baldauf. 2006. The protistan origins of animals and fungi. Mol. Biol. Evol. 23:93-106. http://dx.doi.org/10 .1093/molbev/msj011
63. Steinberg, G., and J. Perez-Martin. 2008. Ustilago maydis, a new fungal model system for cell biology. Trends Cell Biol. 18:61-67. http://dx.doi .org/10.1016/j.tcb.2007.11.008
64. Steinberg, G., M. Schliwa, C. Lehmler, M. Bölker, R. Kahmann, and J.R. McIntosh. 1998. Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. J. Cell Sci. 111:2235-2246.
65. Steinberg, G., M. Schuster, U. Theisen, S. Kilaru, A. Forge, and M. Martin-Urdiroz. 2012. Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport. J. Cell Biol. 198:343-355. http://dx.doi.org/10.1083/jcb.201201087
66. Sunio, A., A.B. Metcalf, and H. Krämer. 1999. Genetic dissection of endocytic trafficking in Drosophila using a horseradish peroxidase-bride of sevenless chimera: hook is required for normal maturation of multivesicular endosomes. Mol. Biol. Cell. 10:847-859. http://dx.doi.org/10 .1091/mbc.10.4.847
67. Szebenyi, G., B. Hall, R. Yu, A.I. Hashim, and H. Krämer. 2007. Hook2 localizes to the centrosome, binds directly to centriolin/CEP110 and contributes to centrosomal function. Traffic. 8:32-46. http://dx.doi.org/10.1111/j.1600-0854.2006.00511.x
68. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121
69. Tang, X., M.S. Halleck, R.A. Schlegel, and P. Williamson. 1996. A subfamily of P-type ATPases with aminophospholipid transporting activity. Science. 272:1495-1497. http://dx.doi.org/10.1126/science.272.5267.1495
70. Theisen, U., A. Straube, and G. Steinberg. 2008. Dynamic rearrangement of nucleoporins during fungal "open" mitosis. Mol. Biol. Cell. 19:1230-1240. http://dx.doi.org/10.1091/mbc.E07-02-0130
71. Vale, R.D. 2003. The molecular motor toolbox for intracellular transport. Cell. 112:467-480. http://dx.doi.org/10.1016/S0092-8674(03)00111-9
72. Vale, R.D., T.S. Reese, and M.P. Sheetz. 1985. Identification of a novel forcegenerating protein, kinesin, involved in microtubule-based motility. Cell. 42:39-50. http://dx.doi.org/10.1016/S0092-8674(85)80099-4
73. Vallee, R.B., J.C. Williams, D. Varma, and L.E. Barnhart. 2004. Dynein: An ancient motor protein involved in multiple modes of transport. J. Neurobiol. 58:189-200. http://dx.doi.org/10.1002/neu.10314
74. van Spronsen, M., M. Mikhaylova, J. Lipka, M.A. Schlager, D.J. van den Heuvel, M. Kuijpers, P.S. Wulf, N. Keijzer, J. Demmers, L.C. Kapitein, et al. 2013. TRAK/Milton motor-adaptor proteins steer mitochondrial trafficking to axons and dendrites. Neuron. 77:485-502. http://dx.doi .org/10.1016/j.neuron.2012.11.027
75. Vida, T.A., and S.D. Emr. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128:779-792. http://dx.doi.org/10.1083/jcb.128.5.779
76. Walenta, J.H., A.J. Didier, X. Liu, and H. Krämer. 2001. The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 152:923-934. http://dx.doi.org/10.1083/jcb.152.5.923
77. Wedlich-Söldner, R., M. Bölker, R. Kahmann, and G. Steinberg. 2000. A putative endosomal t-SNARE links exo-and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J. 19:1974-1986. http://dx.doi .org/10.1093/emboj/19.9.1974
78. Wedlich-Söldner, R., I. Schulz, A. Straube, and G. Steinberg. 2002a. Dynein supports motility of endoplasmic reticulum in the fungus Ustilago maydis. Mol. Biol. Cell. 13:965-977. http://dx.doi.org/10.1091/mbc.01-10-0475
79. Wedlich-Söldner, R., A. Straube, M.W. Friedrich, and G. Steinberg. 2002b. A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis. EMBO J. 21:2946-2957. http://dx.doi .org/10.1093/emboj/cdf296
80. Welte, M.A. 2004. Bidirectional transport along microtubules. Curr. Biol. 14:R525-R537. http://dx.doi.org/10.1016/j.cub.2004.06.045
81. Winston, F., C. Dollard, and S.L. Ricupero-Hovasse. 1995. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast. 11:53-55. http://dx.doi.org/10.1002/yea.320110107
82. Xu, L., M.E. Sowa, J. Chen, X. Li, S.P. Gygi, and J.W. Harper. 2008. An FTS/ Hook/p107(FHIP) complex interacts with and promotes endosomal clustering by the homotypic vacuolar protein sorting complex. Mol. Biol. Cell. 19:5059-5071. http://dx.doi.org/10.1091/mbc.E08-05-0473
83. Zhang, J., X. Yao, L. Fischer, J.F. Abenza, M.A. Peñalva, and X. Xiang. 2011. The p25 subunit of the dynactin complex is required for dynein-early endosome interaction. J. Cell Biol. 193:1245-1255. http://dx.doi.org/ 10.1083/jcb.201011022