Drosophila PAT1 is required for Kinesin-1 to transport cargo and to maximize its motility

Development

Volumn 137, Issue 16, 2010, Pages 2763-2772

  Loiseau, Philippe ^a   Davies, Tim ^b   Williams, Lucy S ^a   Mishima, Masanori ^b   Palacios, Isabel M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Drosophila; Kinesin; Oocyte; Trafficking

Indexed keywords

BINDING PROTEIN; CARRIER PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN 1; MESSENGER RNA; PROTEIN OSKAR; PROTEIN PAT1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTERIOR POSTERIOR AXIS; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DROSOPHILA; GERM LINE; HEAVY CHAIN; LIGHT CHAIN; MOLECULAR CLONING; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; KINESIN; PROTEIN BIOSYNTHESIS; RNA, MESSENGER;

EID: 77955732887     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.048108     Document Type: Article

References (48)

1. Adio, S., Jaud, J., Ebbing, B., Rief, M. and Woehlke, G. (2009). Dissection of kinesin's processivity. PLoS ONE 4, e4612.
2. Blasius, T. L., Cai, D., Jih, G. T., Toret, C. P. and Verhey, K. J. (2007). Two binding partners cooperate to activate the molecular motor Kinesin-1. J. Cell Biol. 176, 11-17. (Pubitemid 46041675)
3. Bowman, A. B., Kamal, A., Ritchings, B. W., Philp, A. V., McGrail, M., Gindhart, J. G. and Goldstein, L. S. (2000). Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 103, 583-594.
4. Brendza, K. M., Rose, D. J., Gilbert, S. P. and Saxton, W. M. (1999). Lethal kinesin mutations reveal amino acids important for ATPase activation and structural coupling. J. Biol. Chem. 274, 31506-31514.
5. Brendza, R. P., Serbus, L. R., Duffy, J. B. and Saxton, W. M. (2000a). A function for Kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289, 2120-2122.
6. Brendza, R. P., Sheehan, K. B., Turner, F. R. and Saxton, W. M. (2000b). Clonal tests of conventional kinesin function during cell proliferation and differentiation. Mol. Biol. Cell 11, 1329-1343.
7. Brendza, R. P., Serbus, L. R., Saxton, W. M. and Duffy, J. B. (2002). Posterior localization of dynein and dorsal-ventral axis formation depend on kinesin in Drosophila oocytes. Curr. Biol. 12, 1541-1545.
8. Cai, D., Hoppe, A. D., Swanson, J. A. and Verhey, K. J. (2007a). Kinesin-1 structural organization and conformational changes revealed by FRET stoichiometry in live cells. J. Cell Biol. 176, 51-63. (Pubitemid 46041680)
9. Cai, D., Verhey, K. J. and Meyhofer, E. (2007b). Tracking single Kinesin molecules in the cytoplasm of mammalian cells. Biophys. J. 92, 4137-4144. (Pubitemid 46910529)
10. Chou, T. B. and Perrimon, N. (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679. (Pubitemid 26427915)
11. D1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras. Development 119, 1359-1369.
12. Clark, I., Giniger, E., Ruohola-Baker, H., Jan, L. Y. and Jan, Y. N. (1994). Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr. Biol. 4, 289-300.
13. Coy, D. L., Hancock, W. O., Wagenbach, M. and Howard, J. (1999). Kinesin's tail domain is an inhibitory regulator of the motor domain. Nat. Cell Biol. 1, 288-292. (Pubitemid 129495779)
14. Diefenbach, R. J., Mackay, J. P., Armati, P. J. and Cunningham, A. L. (1998). The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain. Biochemistry 37, 16663-16670.
15. Duncan, J. E. and Warrior, R. (2002). The cytoplasmic Dynein and Kinesin motors have interdependent roles in patterning the Drosophila oocyte. Curr. Biol. 12, 1982-1991.
16. Friedman, D. S. and Vale, R. D. (1999). Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain. Nat. Cell Biol. 1, 293-7.
17. Gauger, A. K. and Goldstein, L. S. (1993). The Drosophila kinesin light chain. Primary structure and interaction with kinesin heavy chain. J. Biol. Chem. 268, 13657-13666. (Pubitemid 23307798)
18. Gindhart, J. G., Jr, Desai, C. J., Beushausen, S., Zinn, K. and Goldstein, L. S. (1998). Kinesin light chains are essential for axonal transport in Drosophila. J. Cell Biol. 141, 443-454. (Pubitemid 28237092)
19. Gindhart, J. G., Chen, J., Faulkner, M., Gandhi, R., Doerner, K., Wisniewski, T. and Nandlestadt, A. (2003). The kinesin-associated protein UNC-76 is required for axonal transport in the Drosophila nervous system. Mol. Biol. Cell 14, 3356-3365. (Pubitemid 37013132)
20. Hackney, D. D., Stock, M. F., Moore, J. and Patterson, R. A. (2003). Modulation of kinesin half-site ADP release and kinetic processivity by a spacer between the head groups. Biochemistry 42, 12011-12018.
21. Hammond, J. W., Griffin, K., Jih, G. T., Stuckey, J. and Verhey, K. J. (2008). Co-operative versus independent transport of different cargoes by Kinesin-1. Traffic 9, 725-741. (Pubitemid 351494303)
22. Helenius, J., Brouhard, G., Kalaidzidis, Y., Diez, S. and Howard, J. (2006). The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. Nature 441, 115-119. (Pubitemid 43827962)
23. Hisanaga, S., Murofushi, H., Okuhara, K., Sato, R., Masuda, Y., Sakai, H. and Hirokawa, N. (1989). The molecular structure of adrenal medulla kinesin. Cell Motil. Cytoskeleton 12, 264-272. (Pubitemid 19128532)
24. Hoepfner, S., Severin, F., Cabezas, A., Habermann, B., Runge, A., Gillooly, D., Stenmark, H. and Zerial, M. (2005). Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121, 437-450. (Pubitemid 40692303)
25. Hurd, D. D., Stern, M. and Saxton, W. M. (1996). Mutation of the axonal transport motor kinesin enhances paralytic and suppresses Shaker in Drosophila. Genetics 142, 195-204.
26. Hutterer, A., Glotzer, M. and Mishima, M. (2009). Clustering of centralspindlin is essential for its accumulation to the central spindle and the midbody. Curr. Biol. 19, 2043-2049.
27. Januschke, J., Gervais, L., Dass, S., Kaltschmidt, J. A., Lopez-Schier, H., Johnston, D. S., Brand, A. H., Roth, S. and Guichet, A. (2002). Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation. Curr. Biol. 12, 1971-1981. (Pubitemid 35450920)
28. Kuan, Y. H., Gruebl, T., Soba, P., Eggert, S., Nesic, I., Back, S., Kirsch, J., Beyreuther, K. and Kins, S. (2006). PAT1a modulates intracellular transport and processing of amyloid precursor protein (APP), APLP1, and APLP2. J. Biol. Chem. 281, 40114-40123. (Pubitemid 46041816)
29. Littleton, J. T., Bellen, H. J. and Perin, M. S. (1993). Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development 118, 1077-1088.
30. Markussen, F. H., Michon, A. M., Breitwieser, W. and Ephrussi, A. (1995). Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly. Development 121, 3723-3732.
31. McGrail, M. and Hays, T. S. (1997). The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124, 2409-2419. (Pubitemid 27309740)
32. Micklem, D. R., Dasgupta, R., Elliott, H., Gergely, F., Davidson, C., Brand, A., Gonzalez-Reyes, A. and St Johnston, D. (1997). The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila. Curr. Biol. 7, 468-478. (Pubitemid 27308970)
33. Munro, T. P., Kwon, S., Schnapp, B. J. and St Johnston, D. (2006). A repeated IMP-binding motif controls oskar mRNA translation and anchoring independently of Drosophila melanogaster IMP. J. Cell Biol. 172, 577-588. (Pubitemid 43243878)
34. Nielsen, E., Severin, F., Backer, J. M., Hyman, A. A. and Zerial, M. (1999). Rab5 regulates motility of early endosomes on microtubules. Nat. Cell Biol. 1, 376-382. (Pubitemid 129493581)
35. Okada, Y. and Hirokawa, N. (1999). A processive single-headed motor: kinesin superfamily protein KIF1A. Science 283, 1152-1157. (Pubitemid 129504116)
36. Palacios, I. M. and St Johnston, D. (2002). Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 129, 5473-5485.
37. Rice, S. E. and Gelfand, V. I. (2006). Paradigm lost: milton connects kinesin heavy chain to miro on mitochondria. J. Cell Biol. 173, 459-461.
38. Serbus, L. R., Cha, B. J., Theurkauf, W. E. and Saxton, W. M. (2005). Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132, 3743-3752.
39. St Johnston, D., Beuchle, D. and Nusslein-Volhard, C. (1991). Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51-63. (Pubitemid 121001346)
40. Sung, H. H., Telley, I. A., Papadaki, P., Ephrussi, A., Surrey, T. and Rorth, P. (2008). Drosophila ensconsin promotes productive recruitment of Kinesin-1 to microtubules. Dev. Cell 15, 866-876. (Pubitemid 352770218)
41. van Eeden, F. J., Palacios, I. M., Petronczki, M., Weston, M. J. and St Johnston, D. (2001). Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole. J. Cell Biol. 154, 511-523. (Pubitemid 34286158)
42. Verhey, K. J., Lizotte, D. L., Abramson, T., Barenboim, L., Schnapp, B. J. and Rapoport, T. A. (1998). Light chain-dependent regulation of Kinesin's interaction with microtubules. J. Cell Biol. 143, 1053-1066.
43. Verhey, K. J., Meyer, D., Deehan, R., Blenis, J., Schnapp, B. J., Rapoport, T. A. and Margolis, B. (2001). Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152, 959-970. (Pubitemid 34286072)
44. 2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 136, 163-174.
45. Yildiz, A., Tomishige, M., Gennerich, A. and Vale, R. D. (2008). Intramolecular strain coordinates kinesin stepping behavior along microtubules. Cell 134, 1030-1041.
46. Zheng, P., Eastman, J., Vande Pol, S. and Pimplikar, S. W. (1998). PAT1, a microtubule-interacting protein, recognizes the basolateral sorting signal of amyloid precursor protein. Proc. Natl. Acad. Sci. USA 95, 14745-14750.
47. Zimyanin, V., Lowe, N. and St Johnston, D. (2007). An oskar-dependent positive feedback loop maintains the polarity of the Drosophila oocyte. Curr. Biol. 17, 353-359. (Pubitemid 46241888)
48. Zimyanin, V. L., Belaya, K., Pecreaux, J., Gilchrist, M. J., Clark, A., Davis, I. and St Johnston, D. (2008). In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134, 843-853.