Recruitment of the endosomal WASH complex is mediated by the extended 'tail' of Fam21 binding to the retromer protein Vps35

Biochemical Journal

Volumn 442, Issue 1, 2012, Pages 209-220

  Harbour, Michael E ^a   Breusegem, Sophia Y ^a   Seaman, Matthew N J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Endosome; FK506 binding protein 15 (FKBP15); Retromer; Sorting; Tubule; Wiskott Aldrich syndrome homologue (WASH) complex

Indexed keywords

BINDING PROTEIN; FK506 BINDING PROTEIN 15; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 35; WISKOTT ALDRICH SYNDROME PROTEIN;

ARTICLE; CELL FRACTIONATION; CELL MIGRATION; CELL MOTION; CELL SHAPE; CELL SPREADING; CELL SURFACE; CONTROLLED STUDY; ENDOSOME; HUMAN; HUMAN CELL; IN VIVO CULTURE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING;

ENDOSOMES; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; PROTEIN TRANSPORT; PROTEINS; VESICULAR TRANSPORT PROTEINS; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 84856281728     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111761     Document Type: Article

References (45)

1. Jovic, M., Sharma, M., Rahajeng, J. and Caplan, S. (2010) The early endosome: a busy sorting station for proteins at the crossroads. Histol. Histopathol. 25, 99-112
2. Balasubramanian, N., Scott, D. W., Castle, J. D., Casanova, J. E. and Schwartz, M. A. (2007) Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nat. Cell Biol. 9, 1381-1391 (Pubitemid 350201751)
3. Jovíc, M., Naslavsky, N., Rapaport, D., Horowitz, M. and Caplan, S. (2007) EHD1 regulates β1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J. Cell Sci. 120, 802-814 (Pubitemid 46523482)
4. Veale, K. J., Offenhäuser, C., Lei, N., Stanley, A. C., Stow, J. L. and Murray, R. Z. (2011) VAMP3 regulates podosome organisation in macrophages and together with Stx4/SNAP23 mediates adhesion, cell spreading and persistent migration. Exp. Cell Res. 317, 1817-1829
5. Rosenbaum, A. I. and Maxfield, F. R. (2011) Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J. Neurochem. 116, 789-795
6. Salinas, S., Proukakis, C., Crosby, A. and Warner, T. T. (2008) Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms. Lancet Neurol. 7, 1127-1138
7. Blackstone, C., O'Kane, C. J. and Reid, E. (2011) Hereditary spastic paraplegias: membrane traffic and the motor pathway. Nat. Rev. Neurosci. 12, 31-42
8. Burd, C. G. (2011) Physiology and pathology of endosome-to-Golgi retrograde sorting. Traffic 12, 948-955
9. Toei, M., Saum, R. and Forgac, M. (2010) Regulation and isoform function of the V-ATPases. Biochemistry 49, 4715-4723
10. +-ATPase in vesicular trafficking: targeting, regulation and function. Curr. Opin. Cell Biol. 20, 415-426
11. Arighi, C. N., Hartnell, 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 (Pubitemid 38649182)
12. Seaman, M. N. (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122
13. Canuel, M., Lefrancois, S., Zeng, J. and Morales, C. R. (2008) AP-1 and retromer play opposite roles in the trafficking of sortilin between the Golgi apparatus and the lysosomes. Biochem. Biophys. Res. Commun. 366, 724-730
14. Nielsen, M. S., Gustafsen, C., Madsen, P., Nyengaard, J. R., Hermey, G., Bakke, O., Mari, M., Schu, P., Pohlmann, R., Dennes, A. and Petersen, C. M. (2007) Sorting by the cytoplasmic domain of the amyloid precursor protein binding receptor SorLA. Mol. Cell Biol. 27, 6842-6851 (Pubitemid 47483634)
15. Tabuchi, M., Yanatori, I., Kawai, Y. and Kishi, F. (2010) Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J. Cell Sci. 123, 756-766
16. Seaman, M. N. (2005) Recycle your receptors with retromer. Trends Cell Biol. 15, 68-75
17. Collins, BM. (2008) The structure and function of the retromer protein complex. Traffic 9, 1811-1822
18. Rojas, R., van Vlijmen, T., Mardones, G. A., Prabhu, Y., Rojas, A. L., Mohammed, S., Heck, A. J., Raposo, G., van der Sluijs, P. and Bonifacino, J. S. (2008) Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183, 513-526
19. Seaman, M. N., Harbour, M. E., Tattersall, D., Read, E. and Bright, N. (2009) Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5. J. Cell Sci. 122, 2371-2382
20. Nothwehr, S. F., Ha, S. A. and Bruinsma, P. (2000) Sorting of yeast membrane proteins into an endosome-to-Golgi pathway involves direct interaction of their cytosolic domains with Vps35p. J. Cell Biol. 151, 297-310
21. Shi, H., Rojas, R., Bonifacino, J. S. and Hurley, J. H. (2006) The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat. Struct. Mol. Biol. 13, 540-548 (Pubitemid 43848909)
22. Collins, B. M., Norwood, S. J., Kerr, M. C., Mahony, D., Seaman, M. N., Teasdale, R. D. and Owen, D. J. (2008) Structure of Vps26B and mapping of its interaction with the retromer protein complex. Traffic 9, 366-379 (Pubitemid 351188996)
23. Attar, N. and Cullen, P. J. (2010) The retromer complex. Adv. Enzyme Regul. 50, 216-236
24. Carlton, J., Bujny, M., Peter, B. J., Oorschot, V. M., Rutherford, A., Mellor, H., Klumperman, J., McMahon, H. T. and Cullen, P. J. (2004) Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high-curvature membranes and 3-phosphoinositides. Curr. Biol. 14, 1791-1800 (Pubitemid 39408768)
25. Harbour, M. E., Breusegem, S. Y., Antrobus, R., Freeman, C., Reid, E. and Seaman, M. N. (2010) The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 123, 3703-3717
26. Viklund, I. M., Aspenström, P., Meas-Yedid, V., Zhang, B., Kopec, J., Agren, D., Schneider, G., D'Amato, M., Olivo-Marin, J. C., Sansonetti, P., Van Nhieu, G. T. and Pettersson, S. (2009) WAFL, a new protein involved in regulation of early endocytic transport at the intersection of actin and microtubule dynamics. Exp. Cell Res. 15, 1040-1052
27. Nakajima, O., Nakamura, F., Yamashita, N., Tomita, Y., Suto, F., Okada, T., Iwamatsu, A., Kondo, E., Fujisawa, H., Takei, K. and Goshima, Y. (2006) FKBP133: a novel mouse FK506-binding protein homolog alters growth cone morphology. Biochem. Biophys. Res. Commun. 346, 140-149 (Pubitemid 43865978)
28. Gomez, T. S. and Billadeau, D. D. (2009) A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17, 699-711
29. Derivery, E., Sousa, C., Gautier, J. J., Lombard, B., Loew, D. and Gautreau, A. (2009) The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev. Cell 17, 712-723
30. Carnell, M., Zech, T., Calaminus, S. D., Ura, S., Hagedorn, M., Johnston, S. A., May, R. C., Soldati, T., Machesky, L. M. and Insall, R. H. (2011) Actin polymerization driven by WASH causes V-ATPase retrieval and vesicle neutralization before exocytosis. J. Cell Biol. 193, 831-839
31. Jia, D., Gomez, T. S., Metlagel, Z., Umetani, J., Otwinowski, Z., Rosen, M. K. and Billadeau, D. D. (2010) WASH and WAVE actin regulators of the Wiskott-Aldrich syndrome protein (WASP) family are controlled by analogous structurally related complexes. Proc. Natl. Acad. Sci. U.S.A. 107, 10442-10447
32. Hernandez-Valladares, M., Kim, T., Kannan, B., Tung, A., Aguda, A. H., Larsson, M., Cooper, J. A. and Robinson, R. C. (2010) Structural characterization of a capping protein interaction motif defines a family of actin filament regulators. Nat. Struct. Mol. Biol. 17, 497-503
33. Tiwari, R. K., Kusari, J. and Sen, G. C. (1987) Functional equivalents of interferon-mediated signals needed for induction of an mRNA can be generated by double-stranded RNA and growth factors. EMBO J. 6, 3373-3378
34. Strochlic, T. I., Setty, T. G., Sitaram, A. and Burd, C. G. (2007) Grd19/Snx3p functions as a cargo-specific adapter for retromer-dependent endocytic recycling. J. Cell Biol. 177, 115-125 (Pubitemid 46588406)
35. Harterink, M., Port, F., Lorenowicz, M. J., McGough, I. J., Silhankova, M., Betist, M. C., van Weering, J. R., van Heesbeen, R. G., Middelkoop, T. C., Basler, K. et al. (2011) A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat. Cell Biol. 13, 914-923
36. Hierro, A., Rojas, A. L., Rojas, R., Murthy, N., Effantin, G., Kajava, A. V., Steven, A. C., Bonifacino, J. S. and Hurley, J. H. (2007) Functional architecture of the retromer cargo-recognition complex. Nature 449, 1063-1067 (Pubitemid 350014597)
37. Korolchuk, V. I., Schütz, M. M., Gómez-Llorente, C., Rocha, J., Lansu, N. R., Collins, S. M., Wairkar, Y. P., Robinson, I. M. and O'Kane, C. J. (2007) Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation. J. Cell Sci. 120, 4367-4376
38. Chapman, R. E. and Munro, S. (1994) Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO J. 13, 2305-2312 (Pubitemid 24157605)
39. Fritz-Laylin, L. K., Prochnik, S. E., Ginger, M. L., Dacks, J. B., Carpenter, M. L., Field, M. C., Kuo, A., Paredez, A., Chapman, J., Pham, J. et al. (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631-642
40. Formstecher, E., Aresta, S., Collura, V., Hamburger, A., Meil, A., Trehin, A., Reverdy, C., Betin, V., Maire, S., Brun, C. et al. (2005) Protein interaction mapping: a Drosophila case study. Genome Res. 15, 376-384 (Pubitemid 40467779)
41. Damer, C. K., Bayeva, M., Kim, P. S., Ho, L. K., Eberhardt, E. S., Socec, C. I., Lee, J. S., Bruce, E. A., Goldman-Yassen, A. E. and Naliboff, L. C. (2007) Copine A is required for cytokinesis, contractile vacuole function, and development in Dictyostelium. Eukaryot. Cell 6, 430-442 (Pubitemid 46492331)
42. Tomsig, J. L., Snyder, S. L. and Creutz, C. E. (2003) Identification of targets for calcium signaling through the copine family of proteins. Characterization of a coiled-coil copine-binding motif. J. Biol. Chem. 278, 10048-10054 (Pubitemid 36800259)
43. Voineagu, I., Huang, L., Winden, K., Lazaro, M., Haan, E., Nelson, J., McGaughran, J., Nguyen, L. S., Friend, K., Hackett, A. et al. (2011) CCDC22: a novel candidate gene for syndromic X-linked intellectual disability. Mol. Psychiatry, doi:10.1038/mp.2011.95
44. Temkin, P., Lauffer, B., Jäger, S., Cimermancic, P., Krogan, N. J. and von Zastrow, M. (2011) SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat. Cell Biol. 13, 715-721
45. Gokool, S., Tattersall, D., Reddy, J. V. and Seaman, M. N. (2007) Identification of a conserved motif required for Vps35p/Vps26p interaction and assembly of the retromer complex. Biochem. J. 408, 287-295 (Pubitemid 350206352)