Mutation in VPS35 associated with Parkinson's disease impairs WASH complex association and inhibits autophagy

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zavodszky, Eszter ^a   Seaman, Matthew N J ^a   Moreau, Kevin ^a   Jimenez Sanchez, Maria ^a   Breusegem, Sophia Y ^a   Harbour, Michael E ^a   Rubinsztein, David C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATG 9A PROTEIN; FKBP 15 PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN; UNCLASSIFIED DRUG; VPS 35 PROTEIN; WASH COMPLEX; ATG9A PROTEIN, HUMAN; MEMBRANE PROTEIN; VESICULAR TRANSPORT PROTEIN; VPS35 PROTEIN, HUMAN; WASF1 PROTEIN, HUMAN; WISKOTT ALDRICH SYNDROME PROTEIN;

INHIBITION; MUTATION; NERVOUS SYSTEM DISORDER; PHOSPHATE; PROTEIN;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL SPREADING; CELL SURFACE; CONTROLLED STUDY; ENDOSOME; GENE MUTATION; IMMUNOPRECIPITATION; NONHUMAN; PARKINSON DISEASE; PHENOTYPE; PROTEIN DEPLETION; RNA INTERFERENCE; TRANSIENT EXPRESSION; TRANSIENT TRANSFECTION; GENETICS; GOLGI COMPLEX; HELA CELL LINE; HUMAN; METABOLISM; PROTEIN TRANSPORT; TUMOR CELL LINE;

AUTOPHAGY; CELL LINE, TUMOR; ENDOSOMES; GOLGI APPARATUS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; PARKINSON DISEASE; PROTEIN TRANSPORT; VESICULAR TRANSPORT PROTEINS; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 84900460616     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4828     Document Type: Article

References (63)

1. Seaman, M. N. J. The retromer complex-endosomal protein recycling and beyond. J. Cell Sci. 125, 4693-4702 (2012).
2. 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. 165, 123-133 (2004). (Pubitemid 38649182)
3. Seaman, M. N. J. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122 (2004). (Pubitemid 38649181)
4. Harbour, M. E. et al. The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 123, 3703-3717 (2010).
5. Derivery, E. et al. The Arp2/3 Activator WASH controls the fission of endosomes through a large multiprotein complex. Dev. Cell 17, 712-723 (2009).
6. Gomez, T. S. & Billadeau, D. D. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17, 699-711 (2009).
7. Piotrowski, J. T., Gomez, T. S., Schoon, R. A., Mangalam, A. K. & Billadeau, D. D. WASH knockout T cells demonstrate defective receptor trafficking, proliferation, and effector function. Mol. Cell. Biol. 33, 958-973 (2013).
8. Temkin, P. et al. SNX27 mediates retromer tubule entry and endosome-toplasma membrane trafficking of signalling receptors. Nat. Cell Biol. 13, 715-721 (2011).
9. Zech, T. et al. The Arp2/3 activator WASH regulates α5β1- integrin-mediated invasive migration. J. Cell Sci. 124, 3753-3759 (2011).
10. Seaman, M. N. J., Gautreau, A. & Billadeau, D. D. Retromer-mediated endosomal protein sorting: all WASHed up! Trends Cell Biol. 23, 522-528 (2013).
11. Harbour, M. E., Breusegem, S. Y. & Seaman, M. N. J. 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 (2012).
12. Helfer, E. et al. Endosomal recruitment of the WASH complex: active sequences and mutations impairing interaction with the retromer. Biol. Cell 105, 191-207 (2013).
13. Jia, D., Gomez, T. S., Billadeau, D. D. & Rosen, M. K. Multiple repeat elements within the FAM21 tail link the WASH actin regulatory complex to the retromer. Mol. Biol. Cell 23, 2352-2361 (2012).
14. Nakajima, O. et al. FKBP133: a novel mouse FK506-binding protein homolog alters growth cone morphology. Biochem. Biophys. Res. Commun. 346, 140-149 (2006). (Pubitemid 43865978)
15. Freeman, C., Seaman, M. N. J. & Reid, E. The hereditary spastic paraplegia protein strumpellin: characterisation in neurons and of the effect of disease mutations on WASH complex assembly and function. Biochim. Biophys. Acta 1832, 160-173 (2013).
16. Valdmanis, P. N. et al. Mutations in the KIAA0196 gene at the SPG8 locus cause hereditary spastic paraplegia. Am. J. Hum. Genet. 80, 152-161 (2007). (Pubitemid 46047658)
17. Ropers, F. et al. Identification of a novel candidate gene for non-syndromic autosomal recessive intellectual disability: the WASH complex member SWIP. Hum. Mol. Genet. 20, 2585-2590 (2011).
18. Vilariño-Güell, C. et al. VPS35 Mutations in Parkinson Disease. Am. J. Hum. Genet. 89, 162-167 (2011).
19. Zimprich, A. et al. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson Disease. Am. J. Hum. Genet. 89, 168-175 (2011).
20. Kroemer, G., Mariño, G. & Levine, B. Autophagy and the integrated stress response. Mol. Cell 40, 280-293 (2010).
21. Birmingham, C. L., Smith, A. C., Bakowski, M. A., Yoshimori, T. & Brumell, J. H. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J. Biol. Chem. 281, 11374-11383 (2006). (Pubitemid 43855562)
22. Kageyama, S. et al. The LC3 recruitment mechanism is separate from Atg9L1- dependent membrane formation in the autophagic response against Salmonella. Mol. Biol. Cell 22, 2290-2300 (2011).
23. Ravikumar, B., Duden, R. & Rubinsztein, D. C. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 11, 1107-1117 (2002). (Pubitemid 34521091)
24. Ravikumar, B. et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36, 585-595 (2004). (Pubitemid 38715985)
25. Webb, J. L., Ravikumar, B., Atkins, J., Skepper, J. N. & Rubinsztein, D. C. a-Synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 278, 25009-25013 (2003). (Pubitemid 37548663)
26. Lynch-Day, M. A., Mao, K., Wang, K., Zhao, M. & Klionsky, D. J. The role of autophagy in Parkinson's Disease. Cold Spring Harb. Perspect. Med. 2, a009357 (2012).
27. Winslow, A. R. et al. α-Synuclein impairs macroautophagy: implications for Parkinson's disease. J. Cell Biol. 190, 1023-1037 (2010).
28. Dengjel, J. et al. Identification of autophagosome-associated proteins and regulators by quantitative proteomic analysis and genetic screens. Mol. Cell. Proteomics. 11:M111.014035. doi:10.1074/mcp.M111.014035 (2012).
29. Hierro, A. et al. Functional architecture of the retromer cargo-recognition complex. Nature 449, 1063-1067 (2007). (Pubitemid 350014597)
30. 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. 408, 287-295 (2007). (Pubitemid 350206352)
31. Restrepo, R. et al. Structural features of vps35p involved in interaction with other subunits of the retromer complex. Traffic. 8, 1841-1853 (2007). (Pubitemid 350066693)
32. Zhao, X. et al. Dominant-negative behavior of mammalian Vps35 in yeast requires a conserved PRLYL motif involved in retromer assembly. Traffic. 8, 1829-1840 (2007). (Pubitemid 350066692)
33. Collins, B. M., Skinner, C. F., Watson, P. J., Seaman, M. N. J. & Owen, D. J. Vps29 has a phosphoesterase fold that acts as a protein interaction scaffold for retromer assembly. Nat. Struct. Mol. Biol. 12, 594-602 (2005). (Pubitemid 40980809)
34. Jia, D. et al. 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 (2010).
35. Steinberg, F. et al. 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 (2013).
36. Jahreiss, L., Menzies, F. M. & Rubinsztein, D. C. The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic. 9, 574-587 (2008). (Pubitemid 351351616)
37. Yamamoto, A. et al. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct. Funct. 23, 33-42 (1998). (Pubitemid 28223394)
38. Popovic, D. & Dikic, I. TBC1D5 and the AP2 complex regulate ATG9 trafficking and initiation of autophagy. EMBO Rep. 15, 392-401 (2014).
39. Zavodszky, E., Vicinanza, M. & Rubinsztein, D. C. Biology and trafficking of ATG9 and ATG16L1, two proteins that regulate autophagosome formation. FEBS Lett. 587, 1988-1996 (2013).
40. Takahashi, Y. et al. Bif-1 regulates Atg9 trafficking by mediating the fission of Golgi membranes during autophagy. Autophagy 7, 61-73 (2011).
41. Orsi, A. et al. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol. Biol. Cell 23, 1860-1873 (2012).
42. Saitoh, T. et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl Acad Sci. 106, 20842-20846 (2009).
43. Puri, C., Renna, M., Bento, C. F., Moreau, K. & Rubinsztein, D. C. Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154, 1285-1299 (2013).
44. Ravikumar, B., Berger, Z., Vacher, C., O'Kane, C. J. & Rubinsztein, D. C. Rapamycin pre-treatment protects against apoptosis. Hum. Mol. Genet. 15, 1209-1216 (2006).
45. +cytotoxicity. Int. J. Biol. Sci. 9, 149-155 (2013).
46. Puri, C. et al. Overexpression of myosin VI in prostate cancer cells enhances PSA and VEGF secretion, but has no effect on endocytosis. Oncogene 29, 188-200 (2010).
47. Tang, H.-W. et al. Atg1-mediated myosin II activation regulates autophagosome formation during starvation-induced autophagy. EMBO J. 30, 636-651 (2011).
48. Webber, J. L. & Tooze, S. A. Coordinated regulation of autophagy by p38a MAPK through mAtg9 and p38IP. EMBO J. 29, 27-40 (2010).
49. Young, A. R. J. et al. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 119, 3888-3900 (2006). (Pubitemid 44614440)
50. Follett, J. et al. The Vps35 D620N mutation linked to Parkinson's disease disrupts the cargo sorting function of retromer. Traffic. 15, 230-244 (2014).
51. MacLeod, D. A. et al. RAB7L1 Interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's Disease Risk. Neuron 77, 425-439 (2013).
52. Pan, Y. F., Viklund, I.-M., Tsai, H. H., Pettersson, S. & Maruyama, I. N. The ulcerative colitis marker protein WAFL interacts with accessory proteins in endocytosis. Int. J. Biol. Sci. 6, 163-171 (2010).
53. Viklund, I.-M. et al. WAFL, a new protein involved in regulation of early endocytic transport at the intersection of actin and microtubule dynamics. Exp. Cell Res. 315, 1040-1052 (2009).
54. Vilariño-Güell, C. et al. DNAJC13 mutations in Parkinson disease. Hum. Mol. Genet. 23, 1794-1801 (2013).
55. Freeman, C. L., Hesketh, G. & Seaman, M. N. J. RME-8 coordinates the WASH complex with the retromer SNX-BAR dimer to control endosomal tubulation. J. Cell Sci. (2014) (in press).
56. Gokool, S., Tattersall, D. & Seaman, M. N. J. EHD1 interacts with retromer to stabilize SNX1 tubules and facilitate endosome-to-Golgi retrieval. Traffic. 8, 1873-1886 (2007). (Pubitemid 350066695)
57. Narain, Y., Wyttenbach, A., Rankin, J., Furlong, R. A. & Rubinsztein, D. C. A molecular investigation of true dominance in Huntington's disease. J. Med. Genet. 36, 739-746 (1999). (Pubitemid 29462317)
58. Furlong, R. A., Narain, Y., Rankin, J., Wyttenbach, A. & Rubinsztein, D. C. Alpha-synuclein overexpression promotes aggregation of mutant huntingtin. Biochem. J. 346(Pt 3): 577-581 (2000). (Pubitemid 30171015)
59. Kabeya, Y. et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728 (2000).
60. Kimura, S., Noda, T. & Yoshimori, T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452-460 (2007). (Pubitemid 47293726)
61. Vonderheit, A. & Helenius, A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol. 3, e233 (2005).
62. Reddy, J. V. & Seaman, M. N. Vps26p, a component of retromer, directs the interactions of Vps35p in endosome-to-Golgi retrieval. Mol. Biol. Cell 12, 3242-3256 (2001). (Pubitemid 33062976)
63. 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. 122, 2371-2382 (2009).