The retromer complex in development and disease

Development (Cambridge)

Volumn 142, Issue 14, 2015, Pages 2392-2396

  Wang, Shiuan ^a   Bellen, Hugo J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Alzheimer s disease; Endocytic recycling; Epithelial apical polarity; Heme formation; Parkinson s disease; Photoreceptor degeneration; Retromer; Wingless Wnt signaling

Indexed keywords

CELL MEMBRANE PROTEIN; RETROMER COMPLEX PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; MULTIPROTEIN COMPLEX; VESICULAR TRANSPORT PROTEIN; VPS26A PROTEIN, HUMAN; VPS29 PROTEIN, HUMAN; VPS35 PROTEIN, HUMAN; WNT PROTEIN;

ALZHEIMER DISEASE; ARTICLE; CELL MEMBRANE; CELL POLARITY; COMPLEX FORMATION; DISEASE COURSE; DROSOPHILA; ENDOSOME; HEME SYNTHESIS; MAMMAL CELL; NONHUMAN; PARKINSON DISEASE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TRANS GOLGI NETWORK; TRANSPORT VESICLE; WNT SIGNALING PATHWAY; ANIMAL; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; ANIMALS; CELL MEMBRANE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOSOMES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MULTIPROTEIN COMPLEXES; NEURONS; PARKINSON DISEASE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANS-GOLGI NETWORK; VESICULAR TRANSPORT PROTEINS; WNT PROTEINS;

EID: 84937877476     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.123737     Document Type: Article

References (54)

1. Alloway, P. G., Howard, L. and Dolph, P. J. (2000). The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 28, 129-138.
2. Alzheimer, A. A., Stelzmann, R. A., Schnitzlein, H. N. and Murtagh, F. R. (1995). An English translation of Alzheimer’s 1907 paper, “Uber eine eigenartige Erkankung der Hirnrinde”. Clin. Anat. 8, 429-431.
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. Bänziger, C., Soldini, D., Schütt, C., Zipperlen, P., Hausmann, G. and Basler, K. (2006). Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell., 125, 509-522.
5. Bartscherer, K., Pelte, N., Ingelfinger, D. and Boutros, M. (2006). Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 125, 523-533.
6. 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.
7. Bendor, J. T., Logan, T. P. and Edwards, R. H. (2013). The function of α-synuclein. Neuron 79, 1044-1066.
8. Burd, C. and Cullen, P. J. (2014). Retromer: a master conductor of endosome sorting. Cold Spring Harb. Perspect. Biol. 6, a016774.
9. Chen, C., Garcia-Santos, D., Ishikawa, Y., Seguin, A., Li, L., Fegan, K. H., Hildick-Smith, G. J., Shah, D. I., Cooney, J. D., Chen, W. et al. (2013). Snx3 regulates recycling of the transferrin receptor and iron assimilation. Cell Metab. 17, 343-352.
10. Chinchore, Y., Mitra, A. and Dolph, P. J. (2009). Accumulation of rhodopsin in late endosomes triggers photoreceptor cell degeneration. PLoS Genet. 5, e1000377.
11. Coudreuse, D. Y. M., Roë L G., Betist, M. C., Destrée, O. and Korswagen, H. C. (2006). Wnt gradient formation requires retromer function in Wnt-producing cells. Science 312, 921-924.
12. De Domenico, I., McVey Ward, D. and Kaplan, J. (2008). Regulation of iron acquisition and storage: consequences for iron-linked disorders. Nat. Rev. Mol. Cell Biol. 9, 72-81.
13. de Vreede, G., Schoenfeld, J. D., Windler, S. L., Morrison, H., Lu, H. and Bilder, D. (2014). The Scribble module regulates retromer-dependent endocytic trafficking during epithelial polarization. Development 141, 2796-2802.
14. Dell’Angelica, E. C. (2009). AP-3-dependent trafficking and disease: the first decade. Curr. Opin. Cell Biol. 21, 552-559.
15. 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.
16. Freeman, C. L., Hesketh, G. and Seaman, M. N. J. (2014). RME-8 coordinates the activity of the WASH complex with the function of the retromer SNX dimer to control endosomal tubulation. J. Cell Sci. 127, 2053-2070.
17. Gallon, M. and Cullen, P. J. (2015). Retromer and sorting nexins in endosomal sorting. Biochem. Soc. Trans. 43, 33-47.
18. Gomez, T. S. and Billadeau, D. D. (2009). A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17, 699-711.
19. Haft, C. R., de la Luz Sierra, M., Bafford, R., Lesniak, M. A., Barr, V. A. and Taylor, S. I. (2000). Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol. Biol. Cell 11, 4105-4116.
20. Hao, Y.-H., Doyle, J. M., Ramanathan, S., Gomez, T. S., Jia, D., Xu, M., Chen, Z. J., Billadeau, D. D., Rosen, M. K. and Potts, P. R. (2013). Regulation of WASH-dependent actin polymerization and protein trafficking by ubiquitination. Cell 152, 1051-1064.
21. Harterink, M., Port, F., Lorenowicz, M. J., McGough, I. J., Silhankova, M., Betist, M. C., van Weering, J. R. T., van Heesbeen, R. G. H. P., 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.
22. Linhart, R., Wong, S. A., Cao, J., Tran, M., Huynh, A., Ardrey, C., Park, J. M., Hsu, C., Taha, S., Peterson, R. et al. (2014). Vacuolar protein sorting 35 (Vps35) rescues locomotor deficits and shortened lifespan in Drosophila expressing a Parkinson’s disease mutant of Leucine-rich repeat kinase 2 (LRRK2). Mol. Neurodegener. 9, 23.
23. Macleod, D. A., Rhinn, H., Kuwahara, T., Zolin, A., Di Paolo, G., MacCabe, B. D., Marder, K. S., Honig, L. S., Clark, L. N., Small, S. A. et al. (2013). RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson’s disease risk. Neuron 77, 425-439.
24. 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. (2014). Retromer binding to FAM21 and theWASH complex is perturbed by the Parkinson disease-linked VPS35(D620N) mutation. Curr. Biol. 24, 1670-1676.
25. Miura, E., Hasegawa, T., Konno, M., Suzuki, M., Sugeno, N., Fujikake, N., Geisler, S., Tabuchi, M., Oshima, R., Kikuchi, A. et al. (2014). VPS35 dysfunction impairs lysosomal degradation of alpha-synuclein and exacerbates neurotoxicity in a Drosophila model of Parkinson’s disease. Neurobiol. Dis. 71, 1-13.
26. 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.
27. Niu, Y., Zhang, C., Sun, Z., Hong, Z., Li, K., Sun, D., Yang, Y., Tian, C., Gong, W. and Liu, J.-J. (2013). PtdIns(4)P regulates retromer–motor interaction to facilitate dynein–cargo dissociation at the trans-Golgi network. Nat. Cell Biol. 15, 417-429.
28. Perez-Victoria, F.-J., Mardones, G. A. and Bonifacino, J. S. (2008). Requirement of the human GARP complex for mannose 6-phosphate-receptor-dependent sorting of cathepsin D to lysosomes. Mol. Biol. Cell 19, 2350-2362.
29. 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.
30. Popoff, V., Mardones, G. A., Bai, S. K., Chambon, V., Tenza, D., Burgos, P. V., Shi, A., Benaroch, P., Urbe, S., Lamaze, C. et al. (2009). Analysis of articulation between clathrin and retromer in retrograde sorting on early endosomes. Traffic 28, 3290-3302.
31. Port, F. and Basler, K. (2010). Wnt trafficking: new insights into Wnt maturation, secretion and spreading. Traffic 11, 1265-1271.
32. 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.
33. 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. and Bonifacino, J. S. (2008). Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183, 513-526.
34. Seaman, M. N. J. (2004). Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122.
35. Seaman, M. N. and Williams, H. P. (2002). Identification of the functional domains of yeast sorting nexins Vps5p and Vps17p. Mol. Biol. Cell 13, 2826-2840.
36. 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.
37. 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.
38. 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.
39. Small, S. A. and Gandy, S. (2006). Sorting through the cell biology of Alzheimer’s disease: intracellular pathways to pathogenesis. Neuron 52, 15-31.
40. 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.
41. Steinberg, F., Gallon, M., Winfield, M., Thomas, E. C., Bell, A. J., Heesom, K. J., Tavaré, J. M. and Cullen, P. J. (2013). A global analysis of SNX27–retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat. Cell Biol. 15, 461-471.
42. Temkin, P., Lauffer, B., Jäger, S., Cimermancic, P., Krogan, N. J. and von Zastrow, M. (2011). SNX27 mediates retromer tubule entry and endosome-toplasma membrane trafficking of signalling receptors. Nat. Cell Biol. 13, 717-723.
43. Tepass, U. (2012). The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Ann. Rev. Cell Dev. Biol. 28, 655-685.
44. Tsika, E., Glauser, L., Moser, R., Fiser, A., Daniel, G., Sheerin, U.-M., Lees, A., Troncoso, J. C., Lewis, P. A., Bandopadhyay, R. et al. (2014). Parkinson’s disease-linked mutations in VPS35 induce dopaminergic neurodegeneration. Hum. Mol. Genet. 23, 4621-4638.
45. 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.
46. Wang, T. and Montell, C. (2007). Phototransduction and retinal degeneration in Drosophila. Pflügers Arch. 454, 821-847.
47. Wang, S., Tan, K. L., Agosto, M. A., Xiong, B., Yamamoto, S., Sandoval, H., Jaiswal, M., Bayat, V., Zhang, K., Charng, W.-L. et al. (2014). The retromer complex is required for rhodopsin recycling and its loss leads to photoreceptor degeneration. PLoS Biol. 12, e1001847.
48. Wassmer, T., Attar, N., Harterink, M., van Weering, J. R. T., 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.
49. 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.
50. Vardarajan, B. N., Bruesegem, S. Y., Harbour, M. E., St George-Hyslop, P., Seaman, M. N. J. and Farrer, L. A. (2012). Identification of Alzheimer diseaseassociated variants in genes that regulate retromer function. Neurobiol. Aging 33, 2231.e15-2231.e30.
51. Yang, P.-T., Lorenowicz, M. J., Silhankova, M., Coudreuse, D. Y. M., 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.
52. Zavodszky, E., Seaman, M. N. J., Moreau, K., Jimenez-Sanchez, M., Breusegem, S. Y., Harbour, M. E. and Rubinsztein, D. C. (2014). Mutation in VPS35 associated with Parkinson’s disease impairs WASH complex association and inhibits autophagy. Nat. Commun. 5, 3828.
53. Zhou, B., Wu, Y. and Lin, X. (2011). Retromer regulates apical–basal polarity through recycling crumbs. Dev. Biol. 360, 87-95.
54. Zimprich, A., Benet-Pagès, 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 lateonset Parkinson disease. Am. J. Hum. Genet. 89, 168-175.