The phosphoinositide-associated protein Rush hour regulates endosomal trafficking in Drosophila

Molecular Biology of the Cell

Volumn 23, Issue 3, 2012, Pages 433-447

  Gailite, Ieva ^a   Egger Adam, Diane ^a   Wodarz, Andreas ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CELL PROTEIN; EARLY ENDOSOME ANTIGEN 1; GDP DISSOCIATION INHIBITOR PROTEIN; HOMOTYPIC FUSION AND VACUOLE PROTEIN SORTING COMPLEX; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PROTEIN; PROTEIN CARNATION; PROTEIN FAB1P; PROTEIN HRS; PROTEIN RAB5; PROTEIN RUSH HOUR; PROTEIN VAC1P; PROTEIN YOTB; RAB PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; FEMALE; GENE INTERACTION; GENE MUTATION; GENE OVEREXPRESSION; HOMOZYGOTE; LYSOSOME; MEMBRANE FUSION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; ENDOCYTOSIS; ENDOSOMES; LYSOSOMES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; VESICULAR TRANSPORT PROTEINS;

DIANTHUS CARYOPHYLLUS;

EID: 84856458812     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-02-0154     Document Type: Article

References (64)

1. Akbar MA, Ray S, Kramer H (2009). The SM protein Car/Vps33A regulates SNARE-mediated trafficking to lysosomes and lysosome-related organelles. Mol Biol Cell 20, 1705-1714.
2. Bachmann A, Knust E (2008). The use of P-element transposons to generate transgenic flies. Methods Mol Biol 420, 61-77.
3. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M (1992). The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70, 715-728.
4. Bucci C, Thompsen P, Nicoziani P, McCarthy J, van Deurs B (2000). Rab7: a key to lysosome biogenesis. Mol Biol Cell 11, 467-468.
5. Busso D, Delagoutte-Busso B, Moras D (2005). Construction of a set Gateway-based destination vectors for high-throughput cloning and expression screening in Escherichia coli. Anal Biochem 343, 313-321. (Pubitemid 41074046)
6. Cavalli V, Vilbois F, Corti M, Marcote MJ, Tamura K, Karin M, Arkinstall S, Gruenberg J (2001). The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol Cell 7, 421-432. (Pubitemid 32206509)
7. Chen W, Li N, Chen T, Han Y, Li C, Wang Y, He W, Zhang L, Wan T, Cao X (2005). The lysosome-associated apoptosis-inducing protein containing the pleckstrin homology (PH) and FYVE domains (LAPF), representative of a novel family of PH and FYVE domain-containing proteins, induces caspase-independent apoptosis via the lysosomal-mitochondrial pathway. J Biol Chem 280, 40985-40995. (Pubitemid 41780594)
8. Chen X et al. (2002). Gene expression patterns in human liver cancers. Mol Biol Cell 13, 1929-1939. (Pubitemid 34651483)
9. Chotard L, Mishra AK, Sylvain MA, Tuck S, Lambright DG, Rocheleau CE (2010). TBC-2 regulates RAB-5/RAB-7-mediated endosomal trafficking in Caenorhabditis elegans. Mol Biol Cell 21, 2285-2296.
10. Chou TB, Perrimon N (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679.
11. Currie RA, Walker KS, Gray A, Deak M, Casamayor A, Downes CP, Cohen P, Alessi DR, Lucocq J (1999). Role of phosphatidylinositol 3,4,5-trisphosphate in regulating the activity and localization of 3-phosphoinositide-dependent protein kinase-1. Biochem J 337, 575-583.
12. Dowler S, Currie RA, Campbell DG, Deak M, Kular G, Downes CP, Alessi DR (2000). Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem J 351, 19-31.
13. Entchev EV, Schwabedissen A, Gonzalez-Gaitan M (2000). Gradient formation of the TGF-&βετα; homolog Dpp. Cell 103, 981-991.
14. Feng Y, Press B, Wandinger-Ness A (1995). Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 131, 1435-1452. (Pubitemid 26001749)
15. Gaullier JM, Ronning E, Gillooly DJ, Stenmark H (2000). Interaction of the EEA1 FYVE finger with phosphatidylinositol 3-phosphate and early endosomes. Role of conserved residues. J Biol Chem 275, 24595-24600. (Pubitemid 30626557)
16. Gillooly DJ, Simonsen A, Stenmark H (2001). Cellular functions of phosphatidylinositol 3-phosphate and FYVE domain proteins. Biochem J 355, 249-258. (Pubitemid 32397782)
17. Gorvel JP, Chavrier P, Zerial M, Gruenberg J (1991). rab5 controls early endosome fusion in vitro. Cell 64, 915-925. (Pubitemid 121001179)
18. Grosshans BL, Ortiz D, Novick P (2006). Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci USA 103, 11821-11827. (Pubitemid 44215770)
19. Hickey CM, Wickner W (2010). HOPS initiates vacuole docking by tethering membranes before trans-SNARE complex assembly. Mol Biol Cell 21, 2297-2305.
20. Januschke J, Nicolas E, Compagnon J, Formstecher E, Goud B, Guichet A (2007). Rab6 and the secretory pathway affect oocyte polarity in Drosophila. Development 134, 3419-3425. (Pubitemid 350028361)
21. Kim Y, Ikeda W, Nakanishi H, Tanaka Y, Takekuni K, Itoh S, Monden M, Takai Y (2002). Association of frabin with specific actin and membrane structures. Genes Cells 7, 413-420. (Pubitemid 34450048)
22. Kinchen JM, Ravichandran KS (2010). Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464, 778-782.
23. Kutateladze TG ((2006). Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain. Biochim Biophys Acta 1761, 868-877.
24. Li C, Liu Q, Li N, Chen W, Wang L, Wang Y, Yu Y, Cao X (2008). EAPF/Phafin-2, a novel endoplasmic reticulum-associated protein, facilitates TNF-&αλπηα;-triggered cellular apoptosis through endoplasmic reticulum-mitochondrial apoptotic pathway. J Mol Med 86, 471-484.
25. Lin WJ, Yang CY, Lin YC, Tsai MC, Yang CW, Tung CY, Ho PY, Kao FJ, Lin CH (2010). Phafin2 modulates the structure and function of endosomes by a Rab5-dependent mechanism. Biochem Biophys Res Commun 391, 1043-1048.
26. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269. (Pubitemid 34161145)
27. Lu H, Bilder D (2005). Endocytic control of epithelial polarity and proliferation in Drosophila. Nat Cell Biol 7, 1232-1239.
28. Markgraf DF, Ahnert F, Arlt H, Mari M, Peplowska K, Epp N, Griffith J, Reggiori F, Ungermann C (2009). The CORVET subunit Vps8 cooperates with the Rab5 homolog Vps21 to induce clustering of late endosomal compartments. Mol Biol Cell 20, 5276-5289.
29. Melnick MB, Noll E, Perrimon N (1993). The Drosophila stubarista phenotype is associated with a dosage effect of the putative ribosome-associated protein D-p40 on spineless. Genetics 135, 553-564. (Pubitemid 23307606)
30. Morrison HA, Dionne H, Rusten TE, Brech A, Fisher WW, Pfeiffer BD, Celniker SE, Stenmark H, Bilder D (2008). Regulation of early endosomal entry by the Drosophila tumor suppressors Rabenosyn and Vps45. Mol Biol Cell 19, 4167-4176.
31. Mullock BM, Bright NA, Fearon CW, Gray SR, Luzio JP (1998). Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. J Cell Biol 140, 591-601. (Pubitemid 28134062)
32. Nagano M, Hoshino D, Sakamoto T, Kawasaki N, Koshikawa N, Seiki M (2010). ZF21 protein regulates cell adhesion and motility. J Biol Chem 285, 21013-21022.
33. Nordmann M, Cabrera M, Perz A, Brocker C, Ostrowicz C, Engelbrecht-Vandre S, Ungermann C (2010). The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol 20, 1654-1659.
34. Ostrowicz CW, Brocker C, Ahnert F, Nordmann M, Lachmann J, Peplowska K, Perz A, Auffarth K, Engelbrecht-Vandre S, Ungermann C (2010). Defined subunit arrangement and rab interactions are required for functionality of the HOPS tethering complex. Traffic 11, 1334-1346.
35. Parks AL et al. (2004). Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36, 288-292. (Pubitemid 38282755)
36. Peplowska K, Markgraf DF, Ostrowicz CW, Bange G, Ungermann C (2007). The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev Cell 12, 739-750. (Pubitemid 46667746)
37. Pieren M, Schmidt A, Mayer A (2010). The SM protein Vps33 and the t-SNARE H(abc) domain promote fusion pore opening. Nat Struct Mol Biol 17, 710-717.
38. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010). Identification of the switch in early-to-late endosome transition. Cell 141, 497-508.
39. Queenan AM, Ghabrial A, Schupbach T (1997). Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development 124, 3871-3880. (Pubitemid 27482984)
40. Ricard CS et al. (2001). Drosophila rab GDI mutants disrupt development but have normal Rab membrane extraction. Genesis 31, 17-29. (Pubitemid 32927795)
41. Richardson SC, Winistorfer SC, Poupon V, Luzio JP, Piper RC (2004). Mammalian late vacuole protein sorting orthologues participate in early endosomal fusion and interact with the cytoskeleton. Mol Biol Cell 15, 1197-1210. (Pubitemid 38316227)
42. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005). Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749. (Pubitemid 41242638)
43. Rosenfeld JL, Moore RH, Zimmer KP, Alpizar-Foster E, Dai W, Zarka MN, Knoll BJ (2001). Lysosome proteins are redistributed during expression of a GTP-hydrolysis-defective rab5a. J Cell Sci 114, 4499-4508. (Pubitemid 34082870)
44. Rubino M, Miaczynska M, Lippe R, Zerial M (2000). Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J Biol Chem 275, 3745-3748. (Pubitemid 30094593)
45. Sevrioukov EA, He JP, Moghrabi N, Sunio A, Kramer H (1999). A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila. Mol Cell 4, 479-486. (Pubitemid 29531128)
46. Sisson JC, Field C, Ventura R, Royou A, Sullivan W (2000). Lava lamp, a novel peripheral Golgi protein, is required for Drosophila melanogaster cellularization. J Cell Biol 151, 905-918.
47. Sriram V, Krishnan KS, Mayor S (2003). deep-orange and carnation define distinct stages in late endosomal biogenesis in Drosophila melanogaster. J Cell Biol 161, 593-607. (Pubitemid 36578583)
48. Sun W, Yan Q, Vida TA, Bean AJ (2003). Hrs regulates early endosome fusion by inhibiting formation of an endosomal SNARE complex. J Cell Biol 162, 125-137. (Pubitemid 36859540)
49. Tanaka T, Nakamura A (2008). The endocytic pathway acts downstream of Oskar in Drosophila germ plasm assembly. Development 135, 1107-1117. (Pubitemid 351578139)
50. Torres VA, Mielgo A, Barila D, Anderson DH, Stupack D (2008). Caspase 8 promotes peripheral localization and activation of Rab5. J Biol Chem 283, 36280-36289.
51. Ullrich O, Stenmark H, Alexandrov K, Huber LA, Kaibuchi K, Sasaki T, Takai Y, Zerial M (1993). Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins. J Biol Chem 268, 18143-18150. (Pubitemid 23260335)
52. van Meer G, Voelker DR, Feigenson GW (2008). Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9, 112-124. (Pubitemid 351158912)
53. Vanlandingham PA, Ceresa BP (2009). Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J Biol Chem 284, 12110-12124.
54. 1 and p130. J Biol Chem 277, 27412-27422.
55. Visser Smit GD, Place TL, Cole SL, Clausen KA, Vemuganti S, Zhang G, Koland JG, Lill NL (2009). Cbl controls EGFR fate by regulating early endosome fusion. Sci Signal 2, ra86.
56. Vitelli R, Santillo M, Lattero D, Chiariello M, Bifulco M, Bruni CB, Bucci C (1997). Role of the small GTPase Rab7 in the late endocytic pathway. J Biol Chem 272, 4391-4397. (Pubitemid 27078515)
57. Wegner CS, Malerod L, Pedersen NM, Progida C, Bakke O, Stenmark H, Brech A (2010). Ultrastructural characterization of giant endosomes induced by GTPase-deficient Rab5. Histochem Cell Biol 133, 41-55.
58. Weisz A, Basile W, Scafoglio C, Altucci L, Bresciani F, Facchiano A, Sismondi P, Cicatiello L, De Bortoli M (2004). Molecular identification of ER&αλπηα;-positive breast cancer cells by the expression profile of an intrinsic set of estrogen regulated genes. J Cell Physiol 200, 440-450. (Pubitemid 39006936)
59. Wodarz A (2008). Extraction and immunoblotting of proteins from embryos. In: Drosophila: Methods and Protocols, Vol. 420, ed. C. Dahmann, Totowa, NJ: Humana, 335-345.
60. Wucherpfennig T, Wilsch-Brauninger M, Gonzalez-Gaitan M (2003). Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J Cell Biol 161, 609-624. (Pubitemid 36578584)
61. Wurmser AE, Sato TK, Emr SD (2000). New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J Cell Biol 151, 551-562.
62. 1 alter the ligand binding, phospholipase activity, and interaction with the plasma membrane. J Biol Chem 273, 417-424.
63. Yan Y, Denef N, Schupbach T (2009). The vacuolar proton pump, V-ATPase, is required for notch signaling and endosomal trafficking in Drosophila. Dev Cell 17, 387-402.
64. Zerial M, McBride H (2001). Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2, 107-117. (Pubitemid 33674039)