The retromer complex-endosomal protein recycling and beyond

Journal of Cell Science

Volumn 125, Issue 20, 2012, Pages 4693-4702

  Seaman, Matthew N J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Endosome; Recycling; Retromer; Sorting; WASH complex

Indexed keywords

ACTIN; DIMER;

ALZHEIMER DISEASE; CELL POLARITY; ENDOSOME; GOLGI COMPLEX; MICROTUBULE; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN TARGETING; RETROMER COMPLEX; SIGNAL TRANSDUCTION; SPASTIC PARAPLEGIA;

CELL MEMBRANE; ENDOSOMES; GOLGI APPARATUS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROFILAMENT PROTEINS; MULTIPROTEIN COMPLEXES; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; TRANS-GOLGI NETWORK; VESICULAR TRANSPORT PROTEINS;

EUKARYOTA;

EID: 84872183810     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.103440     Document Type: Note

References (115)

1. Andersen, O. M., Reiche, J., Schmidt, V., Gotthardt, M., Spoelgen, R., Behlke, J., von Arnim, C. A., Breiderhoff, T., Jansen, P., Wu, X. et al. (2005). Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc. Natl. Acad. Sci. USA 102, 13461-13466.
2. Andersen, O. M., Schmidt, V., Spoelgen, R., Gliemann, J., Behlke, J., Galatis, D., McKinstry, W. J., Parker, M. W., Masters, C. L., Hyman, B. T. et al. (2006).Molecular dissection of the interaction between amyloid precursor protein and its neuronal trafficking receptor SorLA/LR11. Biochemistry 45, 2618-2628.
3. 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.
4. Attar, N. and Cullen, P. J. (2010). The retromer complex. Adv. Enzyme Regul. 50, 216-236.
5. Belenkaya, T. Y., Wu, Y., Tang, X., Zhou, B., Cheng, L., Sharma, Y. V., Yan, D., Selva, E. M. and Lin, X. (2008). The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev. Cell 14, 120-131.
6. 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.
7. 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.
8. Borner, G. H., Antrobus, R., Hirst, J., Bhumbra, G. S., Kozik, P., Jackson, L. P., Sahlender, D. A. and Robinson, M. S. (2012). Multivariate proteomic profiling identifies novel accessory proteins of coated vesicles. J. Cell Biol. 197, 141-160.
9. Braun, V., Wong, A., Landekic, M., Hong, W. J., Grinstein, S. and Brumell, J. H. (2010). Sorting nexin 3 (SNX3) is a component of a tubular endosomal network induced by Salmonella and involved in maturation of the Salmonella-containing vacuole. Cell. Microbiol. 12, 1352-1367.
10. Bryant, D. M., Kerr, M. C., Hammond, L. A., Joseph, S. R., Mostov, K. E., Teasdale, R. D. and Stow, J. L. (2007). EGF induces macropinocytosis and SNX1- modulated recycling of E-cadherin. J. Cell Sci. 120, 1818-1828.
11. Bugarcic, A., Zhe, Y., Kerr, M. C., Griffin, J., Collins, B. M. and Teasdale, R. D. (2011). Vps26A and Vps26B subunits define distinct retromer complexes. Traffic 12, 1759-1773.
12. Bujny, M. V., Popoff, V., Johannes, L. and Cullen, P. J. (2007). The retromer component sorting nexin-1 is required for efficient retrograde transport of Shiga toxin from early endosome to the trans Golgi network. J. Cell Sci. 120, 2010-2021.
13. Burda, P., Padilla, S. M., Sarkar, S. and Emr, S. D. (2002). Retromer function in endosome-to-Golgi retrograde transport is regulated by the yeast Vps34 PtdIns 3- kinase. J. Cell Sci. 115, 3889-3900.
14. 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.
15. Caplan, S., Naslavsky, N., Hartnell, L. M., Lodge, R., Polishchuk, R. S., Donaldson, J. G. and Bonifacino, J. S. (2002). A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J. 21, 2557-2567.
16. 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 highcurvature membranes and 3-phosphoinositides. Curr. Biol. 14, 1791-1800.
17. 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.
18. Cereghino, J. L., Marcusson, E. G. and Emr, S. D. (1995). The cytoplasmic tail domain of the vacuolar protein sorting receptor Vps10p and a subset of VPS gene products regulate receptor stability, function, and localization. Mol. Biol. Cell 6, 1089-1102.
19. Chen, D., Xiao, H., Zhang, K., Wang, B., Gao, Z., Jian, Y., Qi, X., Sun, J., Miao, L. and Yang, C. (2010). Retromer is required for apoptotic cell clearance by phagocytic receptor recycling. Science 327, 1261-1264.
20. Chia, P. Z., Gasnereau, I., Lieu, Z. Z. and Gleeson, P. A. (2011). Rab9-dependent retrograde transport and endosomal sorting of the endopeptidase furin. J. Cell Sci. 124, 2401-2413.
21. Chin, L. S., Raynor, M. C., Wei, X., Chen, H. Q. and Li, L. (2001). Hrs interacts with sorting nexin 1 and regulates degradation of epidermal growth factor receptor. J. Biol. Chem. 276, 7069-7078.
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.
23. Cozier, G. E., Carlton, J., McGregor, A. H., Gleeson, P. A., Teasdale, R. D., Mellor, H. and Cullen, P. J. (2002). The phox homology (PX) domain-dependent, 3- phosphoinositide-mediated association of sorting nexin-1 with an early sorting endosomal compartment is required for its ability to regulate epidermal growth factor receptor degradation. J. Biol. Chem. 277, 48730-48736.
24. Cullen, P. J. and Korswagen, H. C. (2012). Sorting nexins provide diversity for retromer-dependent trafficking events. Nat. Cell Biol. 14, 29-37.
25. Daumke, O., Lundmark, R., Vallis, Y., Martens, S., Butler, P. J. and McMahon, H. T. (2007). Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449, 923-927.
26. 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.
27. Eaton, S. (2008). Retromer retrieves wntless. Dev. Cell 14, 4-6. Esk, C., Chen, C. Y., Johannes, L. and Brodsky, F. M. (2010). The clathrin heavy chain isoform CHC22 functions in a novel endosomal sorting step. J. Cell Biol. 188, 131-144.
28. Esk, C., Chen, C. Y., Johannes, L. and Brodsky, F. M. (2010). The clathrin heavy chain isoform CHC22 functions in a novel endosomal sorting step. J. Cell Biol. 188, 131-144.
29. Feinstein, T. N., Wehbi, V. L., Ardura, J. A., Wheeler, D. S., Ferrandon, S., Gardella, T. J. and Vilardaga, J. P. (2011). Retromer terminates the generation of cAMP by internalized PTH receptors. Nat. Chem. Biol. 7, 278-284.
30. Fjorback, A. W., Seaman, M., Gustafsen, C., Mehmedbasic, A., Gokool, S., Wu, C., Militz, D., Schmidt, V., Madsen, P., Nyengaard, J. R. et al. (2012). Retromer binds the FANSHY sorting motif in SorLA to regulate amyloid precursor protein sorting and processing. J. Neurosci. 32, 1467-1480.
31. Franch-Marro, X., Wendler, F., Guidato, S., Griffith, J., Baena-Lopez, A., Itasaki, N., Maurice, M. M. and Vincent, J. P. (2008). Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat. Cell Biol. 10, 170-177.
32. Girard, M., Poupon, V., Blondeau, F. and McPherson, P. S. (2005). The DnaJdomain protein RME-8 functions in endosomal trafficking. J. Biol. Chem. 280, 40135-40143.
33. Gokool, S., Tattersall, D. and Seaman, M. N. (2007). EHD1 interacts with retromer to stabilize SNX1 tubules and facilitate endosome-to-Golgi retrieval. Traffic 8, 1873-1886.
34. Gomez, T. S. and Billadeau, D. D. (2009). A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17, 699-711.
35. Gutierrez, M. G., Munafó, D. B., Berón, W. and Colombo, M. I. (2004). Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci. 117, 2687-2697.
36. Harbour, M. E. and Seaman, M. N. J. (2011). Evolutionary variations of VPS29, and their implications for the heteropentameric model of retromer. Commun. Integr. Biol. 4, 619-622.
37. Harbour, M. E., Breusegem, S. Y. A., Antrobus, R., Freeman, C., Reid, E. and Seaman, M. N. J. (2010). The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 123, 3703-3717.
38. Harbour, M. E., Breusegem, S. Y. and Seaman, M. N. J. (2012). Recruitment of the endosomal WASH complex is mediated by the extended 'tail' of Fam21 binding to the retromer protein Vps35. Biochem. J. 442, 209-220.
39. 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.
40. Hong, Z., Yang, Y., Zhang, C., Niu, Y., Li, K., Zhao, X. and Liu, J. J. (2009). The retromer component SNX6 interacts with dynactin p150(Glued) and mediates endosome-to-TGN transport. Cell Res. 19, 1334-1349.
41. Horazdovsky, B. F., Davies, B., Seaman, M. N. J., McLauglin, S. A., Yoon, S.-K. and Emr, S. D. (1997). A sorting nexin-1 homologue, Vps5p, forms a complex with Vps17p and is required for recycling the vacuolar protein-sorting receptor. Mol. Biol. Cell 8, 1529-1541.
42. Huang, C. Y., Lu, T. Y., Bair, C. H., Chang, Y. S., Jwo, J. K. and Chang, W. (2008). A novel cellular protein, VPEF, facilitates vaccinia virus penetration into HeLa cells through fluid phase endocytosis. J. Virol. 82, 7988-7999.
43. Jäger, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Saftig, P. and Eskelinen, E. L. (2004). Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117, 4837-4848.
44. 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. USA 107, 10442-10447.
45. Jia, D., Gomez, T. S., Billadeau, D. D. and Rosen, M. K. (2012). Multiple repeat elements within the FAM21 tail link the WASH actin regulatory complex to the retromer. Mol. Biol. Cell. 23, 2352-2361.
46. 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. Traffic 6, 991-1001.
47. Kingston, D., Chang, H., Ensser, A., Lee, H. R., Lee, J., Lee, S. H., Jung, J. U. and Cho, N. H. (2011). Inhibition of retromer activity by herpesvirus saimiri tip leads to CD4 downregulation and efficient T cell transformation. J. Virol. 85, 10627-10638.
48. Koumandou, V. L., Klute, M. J., Herman, E. K., Nunez-Miguel, R., Dacks, J. B. and Field, M. C. (2011). Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J. Cell Sci. 124, 1496-1509.
49. Kurten, R. C., Eddington, A. D., Chowdhury, P., Smith, R. D., Davidson, A. D. and Shank, B. B. (2001). Self-assembly and binding of a sorting nexin to sorting endosomes. J. Cell Sci. 114, 1743-1756.
50. Lane, R. F., Raines, S. M., Steele, J. W., Ehrlich, M. E., Lah, J. A., Small, S. A., Tanzi, R. E., Attie, A. D. and Gandy, S. (2010). Diabetes-associated SorCS1 regulates Alzheimer's amyloid-beta metabolism: evidence for involvement of SorL1 and the retromer complex. J. Neurosci. 30, 13110-13115.
51. Lee, J. J., Radice, G., Perkins, C. P. and Costantini, F. (1992). Identification and characterization of a novel, evolutionarily conserved gene disrupted by the murine H beta 58 embryonic lethal transgene insertion. Development 115, 277-288.
52. Lieu, Z. Z. and Gleeson, P. A. (2010). Identification of different itineraries and retromer components for endosome-to-Golgi transport of TGN38 and Shiga toxin. Eur. J. Cell Biol. 89, 379-393.
53. Lu, N., Shen, Q., Mahoney, T. R., Liu, X. and Zhou, Z. (2011). Three sorting nexins drive the degradation of apoptotic cells in response to PtdIns(3)P signaling. Mol. Biol. Cell 22, 354-374.
54. Lumb, J. H., Leung, K. F., Dubois, K. N. and Field, M. C. (2011). Rab28 function in trypanosomes: interactions with retromer and ESCRT pathways. J. Cell Sci. 124, 3771-3783.
55. Mamo, A., Jules, F., Dumaresq-Doiron, K., Costantino, S. and Lefrancois, S. (2012). The role of ceroid lipofuscinosis neuronal protein 5 (CLN5) in endosomal sorting. Mol. Cell. Biol. 32, 1855-1866.
56. McCormick, P. J., Dumaresq-Doiron, K., Pluviose, A. S., Pichette, V., Tosato, G. and Lefrancois, S. (2008). Palmitoylation controls recycling in lysosomal sorting and trafficking. Traffic 9, 1984-1997.
57. McGough, I. J. and Cullen, P. J. (2011). Recent advances in retromer biology. Traffic 12, 963-971.
58. Muhammad, A., Flores, I., Zhang, H., Yu, R., Staniszewski, A., Planel, E., Herman, M., Ho, L., Kreber, R., Honig, L. S. et al. (2008). Retromer deficiency observed in Alzheimer's disease causes hippocampal dysfunction, neurodegeneration, and Abeta accumulation. Proc. Natl. Acad. Sci. USA 105, 7327-7332.
59. Mukhopadhyay, A., Pan, X., Lambright, D. G. and Tissenbaum, H. A. (2007). An endocytic pathway as a target of tubby for regulation of fat storage. EMBO Rep. 8, 931-938.
60. Nakada-Tsukui, K., Saito-Nakano, Y., Ali, V. and Nozaki, T. (2005). A retromerlike complex is a novel Rab7 effector that is involved in the transport of the virulence factor cysteine protease in the enteric protozoan parasite Entamoeba histolytica. Mol. Biol. Cell 16, 5294-5303.
61. Naslavsky, N., McKenzie, J., Altan-Bonnet, N., Sheff, D. and Caplan, S. (2009). EHD3 regulates early-endosome-to-Golgi transport and preserves Golgi morphology. J. Cell Sci. 122, 389-400.
62. Nielsen, M. S., Gustafsen, C., Madsen, P., Nyengaard, J. R., Hermey, G., Bakke, O., Mari, M., Schu, P., Pohlmann, R., Dennes, A. et al. (2007). Sorting by the cytoplasmic domain of the amyloid precursor protein binding receptor SorLA. Mol. Cell. Biol. 27, 6842-6851.
63. Nisar, S., Kelly, E., Cullen, P. J. and Mundell, S. J. (2010). Regulation of P2Y1 receptor traffic by sorting Nexin 1 is retromer independent. Traffic 11, 508-519.
64. Nothwehr, S. F. and Hindes, A. E. (1997). The yeast VPS5/GRD2 gene encodes a sorting nexin-1-like protein required for localizing membrane proteins to the late Golgi. J. Cell Sci. 110, 1063-1072.
65. 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.
66. Orvedahl, A., Sumpter, R., Jr, Xiao, G., Ng, A., Zou, Z., Tang, Y., Narimatsu, M., Gilpin, C., Sun, Q., Roth, M. et al. (2011). Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 480, 113-117.
67. Pan, C. L., Baum, P. D., Gu, M., Jorgensen, E. M., Clark, S. G. and Garriga, G. (2008). C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/ Wntless. Dev. Cell 14, 132-139.
68. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J., Evans, P. R. and McMahon, H. T. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499.
69. Pocha, S. M., Wassmer, T., Niehage, C., Hoflack, B. and Knust, E. (2011). Retromer controls epithelial cell polarity by trafficking the apical determinant Crumbs. Curr. Biol. 21, 1111-1117.
70. Popoff, V., Mardones, G. A., Tenza, D., Rojas, R., Lamaze, C., Bonifacino, J. S., Raposo, G. and Johannes, L. (2007). The retromer complex and clathrin define an early endosomal retrograde exit site. J. Cell Sci. 120, 2022-2031.
71. Popoff, V., Mardones, G. A., Bai, S. K., Chambon, V., Tenza, D., Burgos, P. V., Shi, A., Benaroch, P., Urbé, S., Lamaze, C. et al. (2009). Analysis of articulation between clathrin and retromer in retrograde sorting on early endosomes. Traffic 10, 1868-1880.
72. Popovic, D., Akutsu, M., Novak, I., Harper, W., Behrends, C. and Dikic, I. (2012). Rab GAPs in Autophagy: regulation of endocytic and autophagy pathways by direct binding to human ATG8 modifiers. Mol. Cell. Biol. 32, 1733-1744.
73. Port, F., Kuster, M., Herr, P., Furger, E., Bänziger, C., Hausmann, G. and Basler, K. (2008). Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat. Cell Biol. 10, 178-185.
74. Prosser, D. C., Tran, D., Schooley, A., Wendland, B. and Ngsee, J. K. (2010). A novel, retromer-independent role for sorting nexins 1 and 2 in RhoG-dependent membrane remodeling. Traffic 11, 1347-1362.
75. Puthenveedu, M. A., Lauffer, B., Temkin, P., Vistein, R., Carlton, P., Thorn, K., Taunton, J., Weiner, O. D., Parton, R. G. and von Zastrow, M. (2010). Sequencedependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143, 761-773.
76. Radice, G., Lee, J. J. and Costantini, F. (1991). H beta 58, an insertional mutation affecting early postimplantation development of the mouse embryo. Development 111, 801-811.
77. Rapaport, D., Auerbach, W., Naslavsky, N., Pasmanik-Chor, M., Galperin, E., Fein, A., Caplan, S., Joyner, A. L. and Horowitz, M. (2006). Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic 7, 52-60.
78. Rojas, R., Kametaka, S., Haft, C. R. and Bonifacino, J. S. (2007). Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol. Cell. Biol. 27, 1112-1124.
79. 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.
80. Ropers, F., Derivery, E., Hu, H., Garshasbi, M., Karbasiyan, M., Herold, M., Nürnberg, G., Ullmann, R., Gautreau, A., Sperling, K. et al. (2011). Identification of a novel candidate gene for non-syndromic autosomal recessive intellectual disability: the WASH complex member SWIP. Hum. Mol. Genet. 20, 2585-2590.
81. Ruck, A., Attonito, J., Garces, K. T., Núnez, L., Palmisano, N. J., Rubel, Z., Bai, Z., Nguyen, K. C., Sun, L., Grant, B. D. et al. (2011). The Atg6/Vps30/Beclin 1 ortholog BEC-1 mediates endocytic retrograde transport in addition to autophagy in C. elegans. Autophagy 7, 386-400.
82. Schwarz, D. G., Griffin, C. T., Schneider, E. A., Yee, D. and Magnuson, T. (2002). Genetic analysis of sorting nexins 1 and 2 reveals a redundant and essential function in mice. Mol. Biol. Cell 13, 3588-3600.
83. Seaman, M. N. J. (2004). Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122.
84. Seaman, M. N. J. (2007). Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J. Cell Sci. 120, 2378-2389.
85. Seaman, M. N. J., Marcusson, E. G., Cereghino, J.-L. and Emr, S. D. (1997). Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J. Cell Biol. 137, 79-92.
86. Seaman, M. N. J., 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.
87. Seaman, M. N. J., 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.
88. 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.
89. Shi, A., Sun, L., Banerjee, R., Tobin, M., Zhang, Y. and Grant, B. D. (2009). Regulation of endosomal clathrin and retromer-mediated endosome to Golgi retrograde transport by the J-domain protein RME-8. EMBO J. 28, 3290-3302.
90. Silhankova, M., Port, F., Harterink, M., Basler, K. and Korswagen, H. C. (2010). Wnt signalling requires MTM-6 and MTM-9 myotubularin lipid-phosphatase function in Wnt-producing cells. EMBO J. 29, 4094-4105.
91. Skånland, S. S., Wälchli, S., Brech, A. and Sandvig, K. (2009). SNX4 in complex with clathrin and dynein: implications for endosome movement. PLoS ONE 4, e5935.
92. Small, S. A., Kent, K., Pierce, A., Leung, C., Kang, M. S., Okada, H., Honig, L., Vonsattel, J. P. and Kim, T. W. (2005). Model-guided microarray implicates the retromer complex in Alzheimer's disease. Ann. Neurol. 58, 909-919.
93. Stack, J. H., Herman, P. K., Schu, P. V. and Emr, S. D. (1993). A membraneassociated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J. 12, 2195-2204.
94. 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.
95. Swarbrick, J. D., Shaw, D. J., Chhabra, S., Ghai, R., Valkov, E., Norwood, S. J., Seaman, M. N. J. and Collins, B. M. (2011). VPS29 is not an active metallophosphatase but is a rigid scaffold required for retromer interaction with accessory proteins. PLoS ONE 6, e20420.
96. 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.
97. Teasdale, R. D. and Collins, B. M. (2012). Insights into the PX (phox-homology) domain and SNX (sorting nexin) protein families: structures, functions and roles in disease. Biochem. J. 441, 39-59.
98. 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.
99. Valdmanis, P. N., Meijer, I. A., Reynolds, A., Lei, A., MacLeod, P., Schlesinger, D., Zatz, M., Reid, E., Dion, P. A., Drapeau, P. et al. (2007). Mutations in the KIAA0196 gene at the SPG8 locus cause hereditary spastic paraplegia. Am. J. Hum. Genet. 80, 152-161.
100. van Weering, J. R., Verkade, P. and Cullen, P. J. (2012). SNX-BAR-mediated endosome tubulation is co-ordinated with endosome maturation. Traffic 13, 94-107.
101. Vardarajan, B., Bruesegem, S., Harbour, M., St George-Hyslop, P., Seaman, M. N. J. and Farrer, L. A. (2012). Identification of Alzheimer disease associated variants in genes that regulate retromer function. Neurobiol. Aging. 33, 2231.e15-e30.
102. Vergés, 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.
103. Vilariño-Güell, C., Wider, C., Ross, O. A., Dachsel, J. C., Kachergus, J. M., Lincoln, S. J., Soto-Ortolaza, A. I., Cobb, S. A., Wilhoite, G. J., Bacon, J. A. et al. (2011). VPS35 mutations in Parkinson disease. Am. J. Hum. Genet. 89, 162-167.
104. Wang, J. T., Kerr, M. C., Karunaratne, S., Jeanes, A., Yap, A. S. and Teasdale, R. D. (2010). The SNX-PX-BAR family in macropinocytosis: the regulation of macropinosome formation by SNX-PX-BAR proteins. PLoS ONE 5, e13763.
105. Wassmer, T., Attar, N., Bujny, M. V., Oakley, J., Traer, C. J. and Cullen, P. J. (2007). A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J. Cell Sci. 120, 45-54.
106. Wassmer, T., Attar, N., Harterink, M., van Weering, J. R., Traer, C. J., Oakley, J., Goud, B., Stephens, D. J., Verkade, P., Korswagen, H. C. et al. (2009). The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev. Cell 17, 110-122.
107. Wen, L., Tang, F. L., Hong, Y., Luo, S. W., Wang, C. L., He, W., Shen, C., Jung, J. U., Xiong, F., Lee, D. H. et al. (2011). VPS35 haploinsufficiency increases Alzheimer's disease neuropathology. J. Cell Biol. 195, 765-779.
108. Yang, P. T., Lorenowicz, M. J., Silhankova, M., Coudreuse, D. Y., Betist, M. C. and Korswagen, H. C. (2008). Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells. Dev. Cell 14, 140-147.
109. Young, A. R., Chan, E. Y., Hu, X. W., Köchl, R., Crawshaw, S. G., High, S., Hailey, D. W., Lippincott-Schwartz, J. and Tooze, S. A. (2006). Starvation and ULK1- dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 119, 3888-3900.
110. Yu, J. W. and Lemmon, M. A. (2001). All phox homology (PX) domains from Saccharomyces cerevisiae specifically recognize phosphatidylinositol 3-phosphate. J. Biol. Chem. 276, 44179-44184.
111. Zech, T., Calaminus, S. D., Caswell, P., Spence, H. J., Carnell, M., Insall, R. H., Norman, J. and Machesky, L. M. (2011). The Arp2/3 activator WASH regulates a5b1-integrin-mediated invasive migration. J. Cell Sci. 124, 3753-3759.
112. Zhang, P., Wu, Y., Belenkaya, T. Y. and Lin, X. (2011). SNX3 controls Wingless/Wnt secretion through regulating retromer-dependent recycling of Wntless. Cell Res. 21, 1677-1690.
113. Zhang, J., Reiling, C., Reinecke, J. B., Prislan, I., Marky, L. A., Sorgen, P. L., Naslavsky, N. and Caplan, S. (2012). Rabankyrin-5 interacts with EHD1 and Vps26 to regulate endocytic trafficking and retromer function. Traffic 13, 745-757.
114. Zhou, B., Wu, Y. and Lin, X. (2011). Retromer regulates apical-basal polarity through recycling Crumbs. Dev. Biol. 360, 87-95.
115. Zimprich, A., Benet-Page's, A., Struhal, W., Graf, E., Eck, S. H., Offman, M. N., Haubenberger, D., Spielberger, S., Schulte, E. C., Lichtner, P. et al. (2011). A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am. J. Hum. Genet. 89, 168-175.