Whacked and Rab35 polarize dynein-motor-complex-dependent seamless tube growth

Nature Cell Biology

Volumn 14, Issue 4, 2012, Pages 386-393

  Schottenfeld Roames, Jodi ^a   Ghabrial, Amin S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; PROTEIN RAB35; REGULATOR PROTEIN; UNCLASSIFIED DRUG; WHACKED PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL COMPONENT; CELL NUCLEUS; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; INTRACELLULAR TRANSPORT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEAMLESS TUBE; SEQUENCE ANALYSIS;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; DYNEINS; RAB GTP-BINDING PROTEINS; TRACHEA;

EID: 84859430314     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2454     Document Type: Article

References (43)

1. Samakovlis, C. et al. Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122, 1395-1407 (1996). (Pubitemid 26159630)
2. Ribeiro, C., Neumann, M. & Affolter, M. Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr. Biol. 14, 2197-2207 (2004). (Pubitemid 40033356)
3. Buechner, M. Tubes and the single C. elegans excretory cell. Trends Cell Biol. 12, 479-484 (2002). (Pubitemid 35346519)
4. Bar, T., Guldner, F. H. & Wolff, J. R. ̀Seamless' endothelial cells of blood capillaries. Cell Tissue Res. 235, 99-106 (1984). (Pubitemid 14222900)
5. Lubarsky, B. & Krasnow, M. A. Tube morphogenesis: making and shaping biological tubes. Cell 112, 19-28 (2003). (Pubitemid 36106415)
6. Uv, A., Cantera, R. & Samakovlis, C. Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. Trends Cell Biol. 13, 301-309 (2003). (Pubitemid 36638797)
7. Gervais, L. & Casanova, J. In vivo coupling of cell elongation and lumen formation in a single cell. Curr. Biol. 20, 359-366 (2010).
8. Brodu, V., Baffet, A. D., Le Droguen, P. M., Casanova, J. & Guichet, A. A developmentally regulated two-step process generates a noncentrosomal microtubule network in Drosophila tracheal cells. Dev. Cell 18, 790-801 (2010).
9. Sutherland, D., Samakovlis, C. & Krasnow, M. A. branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87, 1091-1101 (1996). (Pubitemid 26427992)
10. Ribeiro, C., Ebner, A. & Affolter, M. In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis. Dev. Cell 2, 677-683 (2002). (Pubitemid 34538147)
11. Jarecki, J., Johnson, E. & Krasnow, M. A. Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF. Cell 99, 211-220 (1999). (Pubitemid 29491787)
12. Berry, K. L., Bulow, H. E., Hall, D. H. & Hobert, O. A. C. elegans CLIC-like protein required for intracellular tube formation and maintenance. Science 302, 2134-2137 (2003). (Pubitemid 38017948)
13. Ulmasov, B., Bruno, J., Gordon, N., Hartnett, M. E. & Edwards, J. C. Chloride intracellular channel protein-4 functions in angiogenesis by supporting acidification of vacuoles along the intracellular tubulogenic pathway. Am. J. Pathol. 174, 1084-1096 (2009).
14. Grawe, F., Wodarz, A., Lee, B., Knust, E. & Skaer, H. The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions. Development 122, 951-959 (1996). (Pubitemid 26095999)
15. Wodarz, A., Hinz, U., Engelbert, M. & Knust, E. Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67-76 (1995).
16. Waterman-Storer, C. M. et al. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc. Natl Acad. Sci. USA 94, 12180-12185 (1997 (Pubitemid 27467863)
17. Ghabrial, A. S., Levi, B. P. & Krasnow, M. A. A systematic screen for tube morphogenesis and branching genes in the Drosophila tracheal system. PLoS Genet. 7, e1002087 (2011).
18. Levi, B. P., Ghabrial, A. S. & Krasnow, M. A. Drosophila talin and integrin genes are required for maintenance of tracheal terminal branches and luminal organization. Development 133, 2383-2393 (2006). (Pubitemid 44044559)
19. Albert, S. & Gallwitz, D. Two new members of a family of Ypt/Rab GTPase activating proteins. Promiscuity of substrate recognition. J. Biol. Chem. 274, 33186-33189 (1999). (Pubitemid 129511611)
20. Albert, S., Will, E. & Gallwitz, D. Identification of the catalytic domains and their functionally critical arginine residues of two yeast GTPase-activating proteins specific for Ypt/Rab transport GTPases. EMBO J. 18, 5216-5225 (1999). (Pubitemid 29465572)
21. Strom, M., Vollmer, P., Tan, T. J. & Gallwitz, D. A yeast GTPase-activating protein that interacts specifically with a member of the Ypt/Rab family. Nature 361, 736-739 (1993). (Pubitemid 23070483)
22. Zhang, J. et al. Thirty-one avors of Drosophila rab proteins. Genetics 176, 1307-1322 (2007). (Pubitemid 46961123)
23. Hsu, C. et al. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J. Cell Biol. 189, 223-232 (2010).
24. Pan, F. et al. Feedback inhibition of calcineurin and Ras by a dual inhibitory protein Carabin. Nature 445, 433-436 (2007). (Pubitemid 46160911)
25. Itoh, T. & Fukuda, M. Identification of EPI64 as a GTPase-activating protein specific for Rab27A. J. Biol. Chem. 281, 31823-31831 (2006). (Pubitemid 46041447)
26. Ishibashi, K., Kanno, E., Itoh, T. & Fukuda, M. Identification and characterization of a novel Tre-2/Bub2/Cdc16 (TBC) protein that possesses Rab3A-GAP activity. Genes Cells 14, 41-52 (2009).
27. Chevallier, J. et al. Rab35 regulates neurite outgrowth and cell shape. FEBS Lett. 583, 1096-1101 (2009).
28. Chua, C. E., Lim, Y. S. & Tang, B. L. Rab35 a vesicular trafic-regulating small GTPase with actin modulating roles. FEBS Lett. 584, 1-6 (2010).
29. Echard, A. Membrane trafic and polarization of lipid domains during cytokinesis. Biochem. Soc. Trans. 36, 395-399 (2008). (Pubitemid 351839341)
30. Gao, Y. et al. Recycling of the Ca2C-activated KC channel, KCa2.3, is dependent upon RME-1, Rab35/EPI64C, and an N-terminal domain. J. Biol. Chem. 285, 17938-17953 (2010).
31. Kouranti, I., Sachse, M., Arouche, N., Goud, B. & Echard, A. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr. Biol. 16, 1719-1725 (2006). (Pubitemid 44691778)
32. Patino-Lopez, G. et al. Rab35 and its GAP EPI64C in T cells regulate receptor recycling and immunological synapse formation. J. Biol. Chem. 283, 18323-18330 (2008).
33. Sato, M. et al. Regulation of endocytic recycling by C. elegans Rab35 and its regulator RME-4, a coated-pit protein. EMBO J. 27, 1183-1196 (2008). (Pubitemid 351574749)
34. Shim, J. et al. Rab35 mediates transport of Cdc42 and Rac1 to the plasma membrane during phagocytosis. Mol. Cell Biol. 30, 1421-1433 (2010).
35. Uytterhoeven, V., Kuenen, S., Kasprowicz, J., Miskiewicz, K. & Verstreken, P. Loss of skywalker reveals synaptic endosomes as sorting stations for synaptic vesicle proteins. Cell 145, 117-132 (2011).
36. Zhang, J., Fonovic, M., Suyama, K., Bogyo, M. & Scott, M. P. Rab35 controls actin bundling by recruiting fascin as an effector protein. Science 325, 1250-1254 (2009).
37. Lee, S. & Kolodziej, P. A. The plakin Short Stop and the RhoA GTPase are required for E-cadherin-dependent apical surface remodeling during tracheal tube fusion. Development 129, 1509-1520 (2002). (Pubitemid 34874171)
38. Lee, T., Hacohen, N., Krasnow, M. & Montell, D. J. Regulated Breathless receptor tyrosine kinase activity required to pattern cell migration and branching in the Drosophila tracheal system. Genes Dev. 10, 2912-2921 (1996). (Pubitemid 26394251)
39. Pfeffer, S. Filling the Rab GAP. Nat. Cell Biol. 7, 856-857 (2005). (Pubitemid 41486284)
40. Fuchs, E. et al. Specific Rab GTPase-activating proteins dëne the Shiga toxin and epidermal growth factor uptake pathways. J. Cell Biol. 177, 1133-1143 (2007). (Pubitemid 46955715)
41. Huang, J., Zhou, W., Dong, W., Watson, A. M. & Hong, Y. Directed, eficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc. Natl Acad. Sci. USA 106, 8284-8289 (2009).
42. Rubin, G. M. & Spradling, A. C. Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353 (1982). (Pubitemid 12037603)
43. Bellen, H. J. et al. The BDGP gene disruption project: single transposon insertions associated with 40 of Drosophila genes. Genetics 167, 761-781 (2004). (Pubitemid 38931863)