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Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation
Abstract
To identify novel proteins required for receptor-mediated endocytosis, we have developed an RNAi-based screening method in Drosophila S2 cells, based on uptake of a scavenger receptor ligand. Some known endocytic proteins are essential for endocytosis in this assay, including clathrin and α-adaptin; however, other proteins important for synaptic vesicle endocytosis are not required. In a small screen for novel endocytic proteins, we identified the Drosophila homologue of Vps35, a component of the retromer complex, involved in endosome-to-Golgi trafficking. Loss of Vps35 inhibits scavenger receptor ligand endocytosis, and causes mislocalisation of a number of receptors and endocytic proteins. Vps35 has tumour suppressor properties because its loss leads to overproliferation of blood cells in larvae. Its loss also causes signalling defects at the neuromuscular junction, including upregulation of TGFβ/BMP signalling and excessive formation of synaptic terminals. Vps35 negatively regulates actin polymerisation, and genetic interactions suggest that some of the endocytic and signalling defects of vps35 mutants are due to this function.
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Flies lacking Vps35 have NMJ synaptic overgrowth and satellite boutons.
“flies lacking Vps35, the retromer component that interacts with the WASH complex, have NMJ synaptic overgrowth and satellite boutons.”
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Kirchhausen, T. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.699 · Cited by 560
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Research works printed but not linked: 67
- Abrams, J. M., Lux, A., Steller, H. and Krieger, M. (1992). Macrophages in Drosophila embryos and L2 cells exhibit scavenger receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA89, 10375-10379. · DOI
- Arighi, C. N., Harmell, L. M., Aguilar, R. C., Haft, C. R. and Bonifacino, J. S. (2004). Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol.165, 123-133. · DOI · Paper page
- Bettencourt-Dias, M., Sinka, R., Frenz, L. and Glover, D. (2005). RNAi in Drosophila cell cultures. In Gene Silencing by RNA Interference: Technology and Application (ed. M. Sohail), pp. 147-166. Boca Raton: CRC Press.
- Blondeau, F., Ritter, B., Allaire, P. D., Wasiak, S., Girard, M., Hussain, N. K., Angers, A., Legendre-Guillemin, V., Roy, L., Boismenu, D. et al. (2004). Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. USA101, 3833-3838. · DOI
- Borner, G. H., Harbour, M., Hester, S., Lilley, K. S. and Robinson, M. S. (2006). Comparative proteomics of clathrin-coated vesicles. J. Cell Biol.175, 571-578. · DOI
- Burridge, K. and Wennerberg, K. (2004). Rho and Rac take center stage. Cell116, 167-179. · DOI
- Chang, H. C., Newmer, S. L., Hull, M. J., Ebersold, M., Schmid, S. L. and Mellman, I. (2002). Hsc70 is required for endocytosis and clathrin function in Drosophila.J. Cell Biol.159, 477-487. · DOI
- Chang, H. C., Hull, M. and Mellman, I. (2004). The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila.J. Cell Biol.164, 1055-1064. · DOI
- Conner, S. D. and Schmid, S. L. (2003). Regulated portals of entry into the cell. Nature422, 37-44. · DOI
- Coudreuse, D. Y., Roel, G., Betist, M. C., Destree, O. and Korswagen, H. C. (2006). Wnt gradient formation requires retromer function in Wnt-producing cells. Science312, 921-924. · DOI
- Dickman, D. K., Lu, Z., Meinertzhagen, I. A. and Schwarz, T. L. (2006). Altered synaptic development and active zone spacing in endocytosis mutants. Curr. Biol.16, 591-598. · DOI
- Duchek. P., Somogyi, K., Jekely, G., Beccari, S. and Rørth, P. (2001). Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell107, 17-26. · DOI
- Dudu, V., Bittig, T., Entchev, E., Kicheva, A., Jülicher, F. and González-Gaitán, M. (2006). Postsynaptic Mad signaling at the Drosophila neuromuscular junction. Curr. Biol.16, 625-635. · DOI
- Eaton, B. A. and Davis, G. W. (2005). LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron47, 695-708. · DOI
- Entchev, E. V., Schwabedissen, A. and González-Gaitán, M. (2000). Gradient formation of the TGF-β homolog Dpp. Cell103, 981-991. · DOI
- Evans, C. J., Hartenstein, V. and Banerjee, U. (2003). Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev. Cell5, 673-690. · DOI
- Franc, N. C., Heitzler, P., Ezekowitz, R. A. and White, K. (1999). Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila.Science284, 1991-1994. · DOI
- Girard, M., Poupon, V., Blondeau, F. and McPherson, P. S. (2005a). The DnaJ-domain protein RME-8 functions in endosomal trafficking. J. Biol. Chem.280, 40135-40143. · DOI
- Girard, M., Allaire, P. D., McPherson, P. S. and Blondeau, F. (2005b). Non-stoichiometric relationship between clathrin heavy and light chains revealed by quantitative comparative proteomics of clathrin-coated vesicles from brain and liver. Mol. Cell. Proteomics4, 1145-1154. · DOI
- González-Gaitán, M. and Jäckle, H. (1997). Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell88, 767-776. · DOI
- Gruenberg, J. and Stenmark, H. (2004). The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol.5, 317-323. · DOI
- Guha, A., Sriram, V., Krishnan, K. S. and Mayor, S. (2003). Shibire mutations reveal distinct dynamin-independent and -dependent endocytic pathways in primary cultures of Drosophila hemocytes. J. Cell Sci.116, 3373-3386. · DOI
- Hashimoto, C., Gerttula, S. and Anderson, K. V. (1991). Plasma membrane localization of the Toll protein in the syncytial Drosophila embryo: importance of transmembrane signaling for dorsal-ventral pattern formation. Development111, 1021-1028. · DOI
- Jékely, G. and Rørth, P. (2003). Hrs mediates downregulation of multiple signalling receptors in Drosophila.EMBO Rep.4, 1163-1168. · DOI
- Jou, T. S., Leung, S. M., Fung, L. M., Ruiz, W. G., Nelson, W. J. and Apodaca, G. (2000). Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol. Biol. Cell11, 287-304. · DOI
- Kaksonen, M., Toret, C. P. and Drubin, D. G. (2006). Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol.7, 404-414. · DOI · Paper page
- Kerr, M. C., Bennetts, J. S., Simpson, F., Thomas, E. C., Flegg, C., Gleeson, P. A., Wicking, C. and Teasdale, R. D. (2005). A novel mammalian retromer component, Vps26B. Traffic6, 991-1001. · DOI · Paper page
- Koh, T. W., Verstreken, P. and Bellen, H. J. (2004). Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron43, 193-205. · DOI
- Koh, T.-W., Korolchuk, V. I., Wairkar, Y. P., Jiao, W., Evergren, E., Pan, H., Zhou, Y., Venken, K. J. T., Shupliakov, O., Robinson, et al. (2007). Eps15 and Dap160 control synaptic vesicle retrieval and synapse development. J. Cell Biol.178, 309-322. · DOI
- Kozak, M. (1984). Point mutations close to the AUG initiator codon affect the efficiency of translation of rat preproinsulin in vivo. Nature308, 241-246. · DOI
- Kubota, K., Keith, F. J. and Gay, N. J. (1993). Relocalization of Drosophila dorsal protein can be induced by a rise in cytoplasmic calcium concentration and the expression of constitutively active but not wild-type Toll receptors. Biochem. J.296, 497-503. · DOI
- Kurada, P. and White, K. (1999). Epidermal growth factor receptor: its role in Drosophila eye differentiation and cell survival. Apoptosis4, 239-243. · DOI
- Kuromi, H. and Kidokoro, Y. (2002). Selective replenishment of two vesicle pools depends on the source of Ca2+ at the Drosophila synapse. Neuron35, 333-343. · DOI
- Lamaze, C., Chuang, T. H., Terlecky, L. J., Bokoch, G. M. and Schmid, S. L. (1996). Regulation of receptor-mediated endocytosis by Rho and Rac. Nature382, 177-179. · DOI
- Lamaze, C., Fujimoto, L. M., Yin, H. L. and Schmid, S. L. (1997). The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem.272, 20332-20335. · DOI
- Liang, Y. Y., Lin, X., Liang, M., Brunicardi, F. C., ten Dijke, P., Chen, Z., Choi, K. W. and Feng, X. H. (2003). dSmurf selectively degrades decapentaplegic-activated MAD, and its overexpression disrupts imaginal disc development. J. Biol. Chem.278, 26307-26310. · DOI
- 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. Development118, 1077-1088. · DOI
- Marcoux, N. and Vuori, K. (2005). EGF receptor activity is essential for adhesion-induced stress fiber formation and cofilin phosphorylation. Cell. Signal.17, 1449-1455. · DOI
- Marqués, G. (2005). Morphogens and synaptogenesis in Drosophila.J. Neurobiol.64, 417-434. · DOI
- McCabe, B. D., Marqués, G., Haghighi, A. P., Fetter, R. D., Crotty, M. L., Haerry, T. E., Goodman, C. S. and O'Connor, M. B. (2003). The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron39, 241-254. · DOI
- McCabe, B. D., Hom, S., Aberle, H., Fetter, R. D., Marques, G., Haerry, T. E., Wan, H., O'Connor, M. B., Goodman, C. S. and Haghighi, A. P. (2004). Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron41, 891-905. · DOI
- Minakhina, S. and Steward, R. (2006). Melanotic mutants in Drosophila: pathways and phenotypes. Genetics174, 253-263. · DOI
- Packard, M., Koo, E. S., Gorczyca, M., Sharpe, J., Cumberledge, S. and Budnik, V. (2002). The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell111, 319-330. · DOI
- Parnas, D., Haghighi, A. P., Fetter, R. D., Kim, S. W. and Goodman, C. S. (2001). Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron32, 415-424. · DOI
- Pelkmans, L., Fava, E., Grabner, H., Hannus, M., Habermann, B., Krausz, E. and Zerial, M. (2005). Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature436, 78-86. · DOI
- Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res.29, e45. · DOI · Paper page
- Praefcke, G. J., Ford, M. G., Schmid, E. M., Olesen, L. E., Gallop, J. L., Peak-Chew, S. Y., Vallis, Y., Babu, M. M., Mills, I. G. and McMahon, H. T. (2004). Evolving nature of the AP2 alpha-appendage hub during clathrin-coated vesicle endocytosis. EMBO J.23, 4371-4383. · DOI · Paper page
- Prasad, B. C. and Clark, S. G. (2006). Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans.Development133, 1757-1766. · DOI
- Qiu, P., Pan, P. C. and Govind, S. (1998). A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development125, 1909-1920. · DOI
- Raiborg, C., Rusten, T. E. and Stenmark, H. (2003). Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol.15, 446-455. · DOI
- Roos, J. and Kelly, R. B. (1998). Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J. Biol. Chem.273, 19108-19119. · DOI
- Roos, J. and Kelly, R. B. (1999). The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol.9, 1411-1414. · DOI
- Rosin, D., Schejter, E., Volk, T. and Shilo, B. Z. (2004). Apical accumulation of the Drosophila PDGF/VEGF receptor ligands provides a mechanism for triggering localized actin polymerization. Development131, 1939-1948. · DOI
- Ryder, E., Blows, F., Ashburner, M., Bautista-Llacer, R., Coulson, D., Drummond, J., Webster, J., Gubb, D., Gunton, N., Johnson, G. et al. (2004). The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster.Genetics167, 797-813. · DOI
- Seaman, M. N. J. (2004). Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol.165, 111-122. · DOI · Paper page
- Seaman, M. N. J. (2005). Recycle your receptors with retromer. Trends Cell Biol.15, 68-75. · DOI · Paper page
- Seaman, M. N., McCaffery, J. M. and Emr, S. D. (1998). A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol.142, 665-681. · DOI · Paper page
- Sweeney, S. T. and Davis, G. W. (2002). Unrestricted synaptic growth in spinster – a late endosomal protein implicated in TGF-beta-mediated synaptic growth regulation. Neuron36, 403-416. · DOI
- Verges, M., Luton, F., Gruber, C., Tiemann, F., Reinders, L. G., Huang, L., Burlingame, A. L., Haft, C. R. and Mostov, K. E. (2004). The mammalian retromer regulates transcytosis of the polymeric immunoglobulin receptor. Nat. Cell Biol.6, 763-769. · DOI
- Verstreken, P., Kjaerulff, O., Lloyd, T. E., Atkinson, R., Zhou, Y., Meinertzhagen, I. A. and Bellen, H. J. (2002). Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell109, 101-112. · DOI
- Verstreken, P., Koh, T. W., Schulze, K. L., Zhai, R. G., Hiesinger, P. R., Zhou, Y., Mehta, S. Q., Cao, Y., Roos, J. and Bellen, H. J. (2003). Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron40, 733-748. · DOI
- Wang, X., Shaw, W. R., Tsang, H. T., Reid, E. and O'Kane, C. J. (2007). Drosophila spichthyin inhibits BMP signaling and regulates synaptic growth and axonal microtubules. Nat. Neurosci.10, 177-185. · DOI
- Williams, M. J., Wiklund, M. L., Wikman, S. and Hultmark, D. (2006). Rac1 signalling in the Drosophila larval cellular immune response. J. Cell Sci.119, 2015-2024. · DOI
- Wucherpfennig, T., Wilsch-Brauninger, M. and González-Gaitán, M. (2003). Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol.161, 609-624. · DOI
- Yoshida, H., Kwon, E., Hirose, F., Otsuki, K., Yamada. M. and Yamaguchi, M. (2004). DREF is required for EGFR signalling during Drosophila wing vein development. Genes Cells9, 935-944. · DOI
- Zettervall, C. J., Anderl, I., Williams, M. J., Palmer, R., Kurucz, E., Ando, I. and Hultmark, D. (2004). A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA101, 14192-14197. · DOI
- Zhang, B., Koh, Y. H., Beckstead, R. B., Budnik, V., Ganetzky, B. and Bellen, H. J. (1998). Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron21, 1465-1475. · DOI · Paper page
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Metadata
- Authors
- Korolchuk, V. I., Schütz, M. M., Gómez-Llorente, C., Rocha, J., Lansu, N. R., Collins, S. M., Wairkar, Y. P., Robinson, I. M., & O'Kane, C. J.
- Affiliations
- Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 2007-12-15
- Volume
- 120
- Issue
- 24
- Pages
- 4367-4376
- ISSN
- 1477-9137
- 0021-9533
- Cited by
- 86
- References
- 1
- Language
- en
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