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Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation

Korolchuk, Viktor I., Schütz, Martin M., Gómez-Llorente, Carolina, Rocha, João, Lansu, Nico R., Collins, Stephanie M., Wairkar, Yogesh P., Robinson, Iain M., O'Kane, Cahir J.·2007·Journal of Cell Science

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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Research works printed but not linked: 67

  1. 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
  2. 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
  3. 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.
  4. 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
  5. 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
  6. Burridge, K. and Wennerberg, K. (2004). Rho and Rac take center stage. Cell116, 167-179. · DOI
  7. 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
  8. 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
  9. Conner, S. D. and Schmid, S. L. (2003). Regulated portals of entry into the cell. Nature422, 37-44. · DOI
  10. 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
  11. 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
  12. 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
  13. 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
  14. Eaton, B. A. and Davis, G. W. (2005). LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron47, 695-708. · DOI
  15. Entchev, E. V., Schwabedissen, A. and González-Gaitán, M. (2000). Gradient formation of the TGF-β homolog Dpp. Cell103, 981-991. · DOI
  16. Evans, C. J., Hartenstein, V. and Banerjee, U. (2003). Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev. Cell5, 673-690. · DOI
  17. 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
  18. 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
  19. 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
  20. González-Gaitán, M. and Jäckle, H. (1997). Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell88, 767-776. · DOI
  21. Gruenberg, J. and Stenmark, H. (2004). The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol.5, 317-323. · DOI
  22. 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
  23. 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
  24. Jékely, G. and Rørth, P. (2003). Hrs mediates downregulation of multiple signalling receptors in Drosophila.EMBO Rep.4, 1163-1168. · DOI
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. Kurada, P. and White, K. (1999). Epidermal growth factor receptor: its role in Drosophila eye differentiation and cell survival. Apoptosis4, 239-243. · DOI
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. Marqués, G. (2005). Morphogens and synaptogenesis in Drosophila.J. Neurobiol.64, 417-434. · DOI
  40. 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
  41. 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
  42. Minakhina, S. and Steward, R. (2006). Melanotic mutants in Drosophila: pathways and phenotypes. Genetics174, 253-263. · DOI
  43. 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
  44. 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
  45. 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
  46. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res.29, e45. · DOI · Paper page
  47. 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
  48. Prasad, B. C. and Clark, S. G. (2006). Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans.Development133, 1757-1766. · DOI
  49. Qiu, P., Pan, P. C. and Govind, S. (1998). A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development125, 1909-1920. · DOI
  50. Raiborg, C., Rusten, T. E. and Stenmark, H. (2003). Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol.15, 446-455. · DOI
  51. 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
  52. Roos, J. and Kelly, R. B. (1999). The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol.9, 1411-1414. · DOI
  53. 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
  54. 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
  55. 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
  56. Seaman, M. N. J. (2005). Recycle your receptors with retromer. Trends Cell Biol.15, 68-75. · DOI · Paper page
  57. 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
  58. 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
  59. 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
  60. 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
  61. 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
  62. 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
  63. 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
  64. 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
  65. 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
  66. 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
  67. 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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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
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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