Retromer: Structure, function, and roles in mammalian disease

European Journal of Cell Biology

Volumn 94, Issue 11, 2015, Pages 513-521

  Trousdale, Christopher ^a   Kim, Kyoungtae ^a  

^a MISSOURI STATE UNIVERSITY   (United States)

Author keywords

Cargo; Retrograde; Retromer; Trafficking; Yeast

Indexed keywords

PROTEIN; RETROMER; UNCLASSIFIED DRUG; SACCHAROMYCES CEREVISIAE PROTEIN; VESICULAR TRANSPORT PROTEIN;

ALZHEIMER DISEASE; ARTICLE; BACTERIUM; DIABETES MELLITUS; ENDOSOME; MAMMALIAN DISEASE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; VIRUS; ANIMAL; CHEMISTRY; DEGENERATIVE DISEASE; GENETICS; HUMAN; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; DIABETES MELLITUS; HUMANS; NEURODEGENERATIVE DISEASES; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 84952631386     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2015.07.002     Document Type: Review

References (82)

1. Arighi C.N., Hartnell L.M., Aguilar R.C., Haft C.R., Bonifacino J.S. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 2004, 165:123-133.
2. Arlt H., Auffarth K., Kurre R., Lisse D., Piehler J., Ungermann C. Spatiotemporal dynamics of membrane remodeling and fusion proteins during endocytic transport. Mol. Biol. Cell 2015, 26:1357-1370.
3. Belenkaya T.Y., Wu Y., Tang X., Zhou B., Cheng L., Sharma Y.V., Yan D., Selva E.M., Lin X. The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev. Cell 2008, 14:120-131.
4. Blot G., Janvier K., Le Panse S., Benarous R., Berlioz-Torrent C. Targeting of the human immunodeficiency virus type 1 envelope to the trans-Golgi network through binding to TIP47 is required for env incorporation into virions and infectivity. J. Virol. 2003, 77:6931-6945.
5. Bonifacino J.S., Hurley J.H. Retromer. Curr. Opin. Cell Biol. 2008, 20:427-436.
6. Bryan A., Youngster I., McAdam A.J. Shiga toxin producing Escherichia coli. Clin. Lab. Med. 2015, 35:247-272.
7. Bugarcic A., Zhe Y., Kerr M.C., Griffin J., Collins B.M., Teasdale R.D. Vps26A and Vps26B subunits define distinct retromer complexes. Traffic 2011, 12:1759-1773.
8. Bujny M.V., Popoff V., Johannes L., Cullen P.J. 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. 2007, 120:2010-2021.
9. Burd C., Cullen P.J. Retromer: a master conductor of endosome sorting. Cold Spring Harb. Perspect. Biol. 2014, 6.
10. Chi R.J., Liu J., West M., Wang J., Odorizzi G., Burd C.G. Fission of SNX-BAR-coated endosomal retrograde transport carriers is promoted by the dynamin-related protein Vps1. J. Cell Biol. 2014, 204:793-806.
11. Choy R.W.-Y., Cheng Z., Schekman R. Amyloid precursor protein (APP) traffics from the cell surface via endosomes for amyloid β (Aβ) production in the trans-Golgi network. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E2077-E2082.
12. Choy R.W.-Y., Park M., Temkin P., Herring B.E., Marley A., Nicoll R.A., von Zastrow M. Retromer mediates a discrete route of local membrane delivery to dendrites. Neuron 2014, 82:55-62.
13. Conibear E., Stevens T.H. Multiple sorting pathways between the late Golgi and the vacuole in yeast. Biochim. Biophys. Acta 1998, 1404:211-230.
14. Coudreuse D.Y.M., Roël G., Betist M.C., Destrée O., Korswagen H.C. Wnt gradient formation requires retromer function in Wnt-producing cells. Science 2006, 312:921-924.
15. de Groot R.E.A., Farin H.F., Macůrková M., van Es J.H., Clevers H.C., Korswagen H.C. Retromer dependent recycling of the Wnt secretion factor Wls is dispensable for stem cell maintenance in the mammalian intestinal epithelium. PLoS ONE 2013, 8:e76971.
16. Deng H., Gao K., Jankovic J. The VPS35 gene and Parkinson's disease. Mov. Disord. 2013, 28:569-575.
17. Edgar A.J., Polak J.M. Human homologues of yeast vacuolar protein sorting 29 and 35. Biochem. Biophys. Res. Commun. 2000, 277:622-630.
18. Farias G.G., Gershlick D.C., Bonifacino J.S. Going forward with retromer. Dev. Cell 2014, 29:3-4.
19. Feyder S., De Craene J.-O., Bär S., Bertazzi D.L., Friant S. Membrane trafficking in the yeast Saccharomyces cerevisiae model. Int. J. Mol. Sci. 2015, 16:1509-1525.
20. Follett J., Norwood S.J., Hamilton N.A., Mohan M., Kovtun O., Tay S., Zhe Y., Wood S.A., Mellick G.D., Silburn P.A., et al. The Vps35 D620N mutation linked to Parkinson's disease disrupts the cargo sorting function of retromer. Traffic 2014, 15:230-244.
21. Gillooly D.J., Morrow I.C., Lindsay M., Gould R., Bryant N.J., Gaullier J.-M., Parton R.G., Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 2000, 19:4577-4588.
22. Gokool S., Tattersall D., Reddy J.V., Seaman M.N.J. Identification of a conserved motif required for Vps35p/Vps26p interaction and assembly of the retromer complex. Biochem. J. 2007, 408:287-295.
23. Goodarzi M.O., Lehman D.M., Taylor K.D., Guo X., Cui J., Quiñones M.J., Clee S.M., Yandell B.S., Blangero J., Hsueh W.A., et al. SORCS1: a novel human type 2 diabetes susceptibility gene suggested by the mouse. Diabetes 2007, 56:1922-1929.
24. Griffin C.T., Trejo J., Magnuson T. Genetic evidence for a mammalian retromer complex containing sorting nexins 1 and 2. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15173-15177.
25. Groppelli E., Len A.C., Granger L.A., Jolly C. Retromer regulates HIV-1 envelope glycoprotein trafficking and incorporation into virions. PLoS Pathog. 2014, 10:e1004518.
26. Haft C.R., de la Luz Sierra M., Bafford R., Lesniak M.A., Barr V.A., Taylor S.I. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol. Biol. Cell 2000, 11:4105-4116.
27. Harbour M.E., Breusegem S.Y.A., Antrobus R., Freeman C., Reid E., Seaman M.N.J. The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 2010, 123:3703-3717.
28. Harrison M.S., Hung C.-S., Liu T.-t., Christiano R., Walther T.C., Burd C.G. A mechanism for retromer endosomal coat complex assembly with cargo. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:267-272.
29. Hierro A., Rojas A.L., Rojas R., Murthy N., Effantin G., Kajava A.V., Steven A.C., Bonifacino J.S., Hurley J.H. Functional architecture of the retromer cargo-recognition complex. Nature 2007, 449:1063-1067.
30. Horazdovsky B.F., Davies B.A., Seaman M.N., McLaughlin S.A., Yoon S., Emr S.D. A sorting nexin-1 homologue, Vps5p, forms a complex with Vps17p and is required for recycling the vacuolar protein-sorting receptor. Mol. Biol. Cell 1997, 8:1529-1541.
31. Ishiura S. Proteolytic cleavage of the Alzheimer's disease amyloid A4 precursor protein. J. Neurochem. 1991, 56:363-369.
32. Kerr M.C., Bennetts J.S., Simpson F., Thomas E.C., Flegg C., Gleeson P.A., Wicking C., Teasdale R.D. A novel mammalian retromer component, Vps26B. Traffic 2005, 6:991-1001.
33. Kim E., Lee Y., Lee H.-J., Kim J.S., Song B.-S., Huh J.-W., Lee S.-R., Kim S.-U., Kim S.-H., Hong Y., et al. Implication of mouse Vps26b-Vps29-Vps35 retromer complex in sortilin trafficking. Biochem. Biophys. Res. Commun. 2010, 403:167-171.
34. Kingston D., Chang H., Ensser A., Lee H.-R., Lee J., Lee S.-H., Jung J.U., Cho N.-H. Inhibition of retromer activity by herpesvirus saimiri tip leads to CD4 downregulation and efficient T cell transformation. J. Virol. 2011, 85:10627-10638.
35. Kooner J.S., Saleheen D., Sim X., Sehmi J., Zhang W., Frossard P., Been L.F., Chia K.-S., Dimas A.S., Hassanali N., et al. Genome-wide association study in individuals of South Asian ancestry identifies six new type 2 diabetes susceptibility loci. Nat. Genet. 2011, 43:984-989.
36. Lane R.F., Raines S.M., Steele J.W., Ehrlich M.E., Lah J.A., Small S.A., Tanzi R.E., Attie A.D., Gandy S. Diabetes-associated SorCS1 regulates Alzheimer's amyloid-beta metabolism: evidence for involvement of SorL1 and the retromer complex. J. Neurosci. 2010, 30:13110-13115.
37. Liang X., Slifer M., Martin E.R., Schnetz-Boutaud N., Bartlett J., Anderson B., Züchner S., Gwirtsman H., Gilbert J.R., Pericak-Vance M.A., et al. Genomic convergence to identify candidate genes for Alzheimer disease on chromosome 10. Hum. Mutat. 2009, 30:463-471.
38. Lipovsky A., Popa A., Pimienta G., Wyler M., Bhan A., Kuruvilla L., Guie M.-A., Poffenberger A.C., Nelson C.D.S., Atwood W.J., et al. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7452-7457.
39. Marcusson E.G., Horazdovsky B.F., Cereghino J.L., Gharakhanian E., Emr S.D. The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 1994, 77:579-586.
40. McDermott H., Kim K. Molecular dynamics at the endocytic portal and regulations of endocytic and recycling traffics. Eur. J. Cell Biol. 2015.
41. McGough I.J., Cullen P.J. Recent advances in retromer biology. Traffic 2011, 12:963-971.
42. McGough I.J., Steinberg F., Jia D., Barbuti P.A., McMillan K.J., Heesom K.J., Whone A.L., Caldwell M.A., Billadeau D.D., Rosen M.K., et al. Retromer binding to FAM21 and the WASH complex is perturbed by the Parkinson disease-linked VPS35(D620N) mutation. Curr. Biol. 2014, 24:1670-1676.
43. Muhammad A., Flores I., Zhang H., Yu R., Staniszewski A., Planel E., Herman M., Ho L., Kreber R., Honig L.S., et al. Retromer deficiency observed in Alzheimer's disease causes hippocampal dysfunction, neurodegeneration, and Abeta accumulation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7327-7332.
44. Munn A.L. The yeast endocytic membrane transport system. Microsc. Res. Tech. 2000, 51:547-562.
45. Nielsen M.S., Gustafsen C., Madsen P., Nyengaard J.R., Hermey G., Bakke O., Mari M., Schu P., Pohlmann R., Dennes A., et al. Sorting by the cytoplasmic domain of the amyloid precursor protein binding receptor SorLA. Mol. Cell. Biol. 2007, 27:6842-6851.
46. Norwood S.J., Shaw D.J., Cowieson N.P., Owen D.J., Teasdale R.D., Collins B.M. Assembly and solution structure of the core retromer protein complex. Traffic 2011, 12:56-71.
47. Nothwehr S.F., Bruinsma P., Strawn L.A. Distinct domains within Vps35p mediate the retrieval of two different cargo proteins from the yeast prevacuolar/endosomal compartment. Mol. Biol. Cell 1999, 10:875-890.
48. Nothwehr S.F., Ha S.A., Bruinsma P. Sorting of yeast membrane proteins into an endosome-to-Golgi pathway involves direct interaction of their cytosolic domains with Vps35p. J. Cell Biol. 2000, 151:297-310.
49. Paterson A.D., Waggott D., Boright A.P., Hosseini S.M., Shen E., Sylvestre M.-P., Wong I., Bharaj B., Cleary P.A., Lachin J.M., et al. A genome-wide association study identifies a novel major locus for glycemic control in type 1 diabetes, as measured by both A1C and glucose. Diabetes 2010, 59:539-549.
50. Popa A., Zhang W., Harrison M.S., Goodner K., Kazakov T., Goodwin E.C., Lipovsky A., Burd C.G., DiMaio D. Direct binding of retromer to human papillomavirus type 16 minor capsid protein L2 mediates endosome exit during viral infection. PLoS Pathog. 2015, 11:e1004699.
51. 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. Analysis of articulation between clathrin and retromer in retrograde sorting on early endosomes. Traffic 2009, 10:1868-1880.
52. Popoff V., Mardones G.A., Tenza D., Rojas R., Lamaze C., Bonifacino J.S., Raposo G., Johannes L. The retromer complex and clathrin define an early endosomal retrograde exit site. J. Cell Sci. 2007, 120:2022-2031.
53. Priller C., Bauer T., Mitteregger G., Krebs B., Kretzschmar H.A., Herms J. Synapse formation and function is modulated by the amyloid precursor protein. J. Neurosci. 2006, 26:7212-7221.
54. Priya A., Kalaidzidis I.V., Kalaidzidis Y., Lambright D., Datta S. Molecular insights into Rab7-mediated endosomal recruitment of core retromer: deciphering the role of Vps26 and Vps35. Traffic 2015, 16:68-84.
55. Reddy J.V., Seaman M.N. Vps26p, a component of retromer, directs the interactions of Vps35p in endosome-to-Golgi retrieval. Mol. Biol. Cell 2001, 12:3242-3256.
56. Rojas R., van Vlijmen T., Mardones G.A., Prabhu Y., Rojas A.L., Mohammed S., Heck A.J.R., Raposo G., van der Sluijs P., Bonifacino J.S. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 2008, 183:513-526.
57. Sapp M.J. HPV virions hitchhike a ride on retromer complexes. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7116-7117.
58. Schelhaas M., Shah B., Holzer M., Blattmann P., Kühling L., Day P.M., Schiller J.T., Helenius A. Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS Pathog. 2012, 8:e1002657.
59. Schwarz D.G., Griffin C.T., Schneider E.A., Yee D., Magnuson T. Genetic analysis of sorting nexins 1 and 2 reveals a redundant and essential function in mice. Mol. Biol. Cell 2002, 13:3588-3600.
60. Seaman M.N., Marcusson E.G., Cereghino J.L., Emr S.D. 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. 1997, 137:79-92.
61. Seaman M.N., McCaffery J.M., Emr S.D. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 1998, 142:665-681.
62. Seaman M.N.J. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 2004, 165:111-122.
63. Seaman M.N.J. Recycle your receptors with retromer. Trends Cell Biol. 2005, 15:68-75.
64. Seaman M.N.J. Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J. Cell Sci. 2007, 120:2378-2389.
65. Seaman M.N.J. The retromer complex - endosomal protein recycling and beyond. J. Cell Sci. 2012, 125:4693-4702.
66. Seaman M.N.J., Harbour M.E., Tattersall D., Read E., Bright N. 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. 2009, 122:2371-2382.
67. Seaman M.N.J., Williams H.P. Identification of the functional domains of yeast sorting nexins Vps5p and Vps17p. Mol. Biol. Cell 2002, 13:2826-2840.
68. Shaw J.D., Cummings K.B., Huyer G., Michaelis S., Wendland B. Yeast as a model system for studying endocytosis. Exp. Cell Res. 2001, 271:1-9.
69. Shi H., Rojas R., Bonifacino J.S., Hurley J.H. The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat. Struct. Mol. Biol. 2006, 13:540-548.
70. Small S.A., Kent K., Pierce A., Leung C., Kang M.S., Okada H., Honig L., Vonsattel J.-P., Kim T.-W. Model-guided microarray implicates the retromer complex in Alzheimer's disease. Ann. Neurol. 2005, 58:909-919.
71. Small S.A., Petsko G.A. Retromer in Alzheimer disease, Parkinson disease and other neurological disorders. Nat. Rev. Neurosci. 2015, 16:126-132.
72. Song X., Xu W., Zhang A., Huang G., Liang X., Virbasius J.V., Czech M.P., Zhou G.W. Phox homology domains specifically bind phosphatidylinositol phosphates. Biochemistry 2001, 40:8940-8944.
73. Sullivan C.P., Jay A.G., Stack E.C., Pakaluk M., Wadlinger E., Fine R.E., Wells J.M., Morin P.J. Retromer disruption promotes amyloidogenic APP processing. Neurobiol. Dis. 2011, 43:338-345.
74. Swarbrick J.D., Shaw D.J., Chhabra S., Ghai R., Valkov E., Norwood S.J., Seaman M.N.J., Collins B.M. VPS29 is not an active metallo-phosphatase but is a rigid scaffold required for retromer interaction with accessory proteins. PLoS ONE 2011, 6:e20420.
75. Tabuchi M., Yanatori I., Kawai Y., Kishi F. Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J. Cell Sci. 2010, 123:756-766.
76. Temkin P., Lauffer B., Jäger S., Cimermancic P., Krogan N.J., von Zastrow M. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat. Cell Biol. 2011, 13:715-721.
77. van Weering J.R.T., Verkade P., Cullen P.J. SNX-BAR-mediated endosome tubulation is co-ordinated with endosome maturation. Traffic 2012, 13:94-107.
78. Vieira S.I., Rebelo S., Esselmann H., Wiltfang J., Lah J., Lane R., Small S.A., Gandy S., da Cruz E., Silva E.F., da Cruz E., Silva O.A. Retrieval of the Alzheimer's amyloid precursor protein from the endosome to the TGN is S655 phosphorylation state-dependent and retromer-mediated. Mol. Neurodegener. 2010, 5:40.
79. Wang C.-L., Tang F.-L., Peng Y., Shen C.-Y., Mei L., Xiong W.-C. VPS35 regulates developing mouse hippocampal neuronal morphogenesis by promoting retrograde trafficking of BACE1. Biol. Open 2012, 1:1248-1257.
80. Wang D., Guo M., Liang Z., Fan J., Zhu Z., Zang J., Zhu Z., Li X., Teng M., Niu L., et al. Crystal structure of human vacuolar protein sorting protein 29 reveals a phosphodiesterase/nuclease-like fold and two protein-protein interaction sites. J. Biol. Chem. 2005, 280:22962-22967.
81. Wendland B., Emr S.D., Riezman H. Protein traffic in the yeast endocytic and vacuolar protein sorting pathways. Curr. Opin. Cell Biol. 1998, 10:513-522.
82. Zavodszky E., Seaman M.N.J., Moreau K., Jimenez-Sanchez M., Breusegem S.Y., Harbour M.E., Rubinsztein D.C. Mutation in VPS35 associated with Parkinson's disease impairs WASH complex association and inhibits autophagy. Nat. Commun. 2014, 5:3828.