Retromer-dependent neurotransmitter receptor trafficking to synapses is altered by the Parkinson's disease VPS35 mutation p.D620N

Human Molecular Genetics

Volumn 24, Issue 6, 2015, Pages 1691-1703

  Munsie, L N ^a   Milnerwood, A J ^a,b   Seibler, P ^c   Beccano Kelly, D A ^a   Tatarnikov, I ^a   Khinda, J ^a   Volta, M ^a   Kadgien, C ^a   Cao, L P ^a   Tapia, L ^a   Klein, C ^c   Farrer, M J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF LÜBECK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 1; NEUROTRANSMITTER RECEPTOR; PHOSPHOTRANSFERASE; SORTILIN; UNCLASSIFIED DRUG; VPS26 PROTEIN; VPS29 PROTEIN; VPS35 PROTEIN; GLUTAMATE RECEPTOR; VESICULAR TRANSPORT PROTEIN; VPS35 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN CELL CULTURE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; MALE; MOLECULAR DYNAMICS; MOUSE; NERVE CELL CULTURE; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SUBUNIT; SITE DIRECTED MUTAGENESIS; SURFACE PROPERTY; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; DENDRITIC SPINE; GENETICS; METABOLISM; MISSENSE MUTATION; NERVE CELL; PARKINSON DISEASE; PROTEIN TRANSPORT;

MURINAE;

ANIMALS; DENDRITIC SPINES; HUMANS; MICE; MUTATION, MISSENSE; NEURONS; PARKINSON DISEASE; PROTEIN TRANSPORT; RECEPTORS, GLUTAMATE; SYNAPSES; VESICULAR TRANSPORT PROTEINS;

EID: 84935038727     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu582     Document Type: Article

References (51)

1. 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.
2. Steinberg, F., Gallon, M., Winfield, M., Thomas, E.C., Bell, A.J., Heesom, K.J., Tavare, 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.
3. Hu, F., Padukkavidana, T., Vaegter, C.B., Brady, O.A., Zheng, Y., Mackenzie, I.R., Feldman, H.H., Nykjaer, A. and Strittmatter, S.M. (2010) Sortilin-mediated endocytosis determines levels of the frontotemporal dementia protein, progranulin. Neuron, 68, 654-667.
4. Vardarajan, B.N., Bruesegem, S.Y., Harbour, M.E., Inzelberg, R., Friedland, R., St George-Hyslop, P., Seaman, M.N. and Farrer, L.A. (2012) Identification of Alzheimer disease-associated variants in genes that regulate retromer function. Neurobiol. Aging, 33, 2231.e2215-2231. e2230.
5. 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.
6. Vilarino-Guell, 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.
7. Struhal, W., Presslauer, S., Spielberger, S., Zimprich, A., Auff, E., Bruecke, T., Poewe, W. and Ransmayr, G. and Austrian VPS-35 Investigators Team (2014) VPS35 Parkinson's disease phenotype resembles the sporadic disease. J. Neural Transm., 121, 755-759.
8. Bhalla, A., Vetanovetz, C.P., Morel, E., Chamoun, Z., Di Paolo, G. and Small, S.A. (2012) The location and trafficking routes of the neuronal retromer and its role in amyloid precursor protein transport. Neurobiol. Dis., 47, 126-134.
9. Choy, R.W., Park, M., Temkin, P., Herring, B.E., Marley, A., Nicoll, R.A. and von Zastrow, M. (2014) Retromer mediates a discrete route of local membrane delivery to dendrites. Neuron, 82, 55-62.
10. 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.
11. Wang, C.L., Tang, F.L., Peng, Y., Shen, C.Y., Mei, L. and Xiong, W.C. (2012) VPS35 regulates developing mouse hippocampal neuronal morphogenesis by promoting retrograde trafficking of BACE1. Biol. Open, 1, 1248-1257.
12. Temkin, P., Lauffer, B., Jager, 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.
13. Korolchuk, V.I., Schutz, M.M., Gomez-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.
14. Zhang, D., Isack, N.R., Glodowski, D.R., Liu, J., Chen, C.C., Xu, X.Z., Grant, B.D. and Rongo, C. (2012) RAB-6.2 and the retromer regulate glutamate receptor recycling through a retrograde pathway. J. Cell Biol., 196, 85-101.
15. Bi, F., Li, F., Huang, C. and Zhou, H. (2013) Pathogenic mutation in VPS35 impairs its protection against MPP(+) cytotoxicity. Int. J. Biol. Sci., 9, 149-155.
16. 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.
17. Collins, B.M. (2008) The structure and function of the retromer protein complex. Traffic, 9, 1811-1822.
18. Caron, N.S., Munsie, L.N., Keillor, J.W. and Truant, R. (2012) Using FLIM-FRET to measure conformational changes of transglutaminase type 2 in live cells. PLoS ONE, 7, e44159.
19. Kaufman, A.M., Milnerwood, A.J., Sepers, M.D., Coquinco, A., She, K., Wang, L., Lee, H., Craig, A.M., Cynader, M. and Raymond, L.A. (2012) Opposing roles of synaptic and extrasynaptic NMDA receptor signaling in cocultured striatal and cortical neurons. J. Neurosci., 32, 3992-4003.
20. Milnerwood, A.J., Kaufman, A.M., Sepers, M.D., Gladding, C.M., Zhang, L., Wang, L., Fan, J., Coquinco, A., Qiao, J.Y., Lee, H. et al. (2012) Mitigation of augmented extrasynaptic NMDAR signaling and apoptosis in cortico-striatal co-cultures fromHuntington's disease mice. Neurobiol. Dis., 48, 40-51.
21. Freeman, C., Seaman, M.N. and Reid, E. (2013) The hereditary spastic paraplegia protein strumpellin: characterisation in neurons and of the effect of disease mutations onWASH complex assembly and function. Biochim. Biophys. Acta, 1832, 160-173.
22. Bonifacino, J.S. and Hurley, J.H. (2008) Retromer. Curr. Opin. Cell Biol., 20, 427-436.
23. 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. (2013) The Vps35 D620N mutation linked to Parkinson's disease disrupts the cargo sorting function of retromer. Traffic, 15, 230-244.
24. Hussain, N.K., Diering, G.H., Sole, J., Anggono, V. and Huganir, R.L. (2014) Sorting Nexin 27 regulates basal and activity-dependent trafficking of AMPARs. Proc. Natl Acad. Sci. USA, 111, 11840-11845.
25. Kopec, C.D., Li, B., Wei, W., Boehm, J. and Malinow, R. (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci., 26, 2000-2009.
26. Makino, H. and Malinow, R. (2009) AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron, 64, 381-390.
27. Kumar, K.R., Weissbach, A., Heldmann, M., Kasten, M., Tunc, S., Sue, C.M., Svetel, M., Kostic, V.S., Segura-Aguilar, J., Ramirez, A. et al. (2012) Frequency of the D620N mutation in VPS35 in Parkinson disease. Arch. Neurol., 69, 1360-1364.
28. Seibler, P., Graziotto, J., Jeong, H., Simunovic, F., Klein, C. and Krainc, D. (2011) Mitochondrial Parkin recruitment is impaired in neurons derived from mutant PINK1 induced pluripotent stem cells. J. Neurosci., 31, 5970-5976.
29. Morais, V.A., Haddad, D., Craessaerts, K., De Bock, P.J., Swerts, J., Vilain, S., Aerts, L., Overbergh, L., Grunewald, A., Seibler, P. et al. (2014) PINK1 loss-of-function mutations affect mitochondrial complex I activity via NdufA10 ubiquinone uncoupling. Science, 344, 203-207.
30. MacLeod, D.A., Rhinn, H., Kuwahara, T., Zolin, A., Di Paolo, G., McCabe, 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.
31. Zavodszky, E., Seaman, M.N., 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.
32. Cohen, S. and Greenberg, M.E. (2008) Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu. Rev. Cell Dev. Biol., 24, 183-209.
33. Bredt, D.S. and Nicoll, R.A. (2003) AMPA receptor trafficking at excitatory synapses. Neuron, 40, 361-379.
34. 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.
35. VanWeering, J.R., Sessions, R.B., Traer, C.J., Kloer, D.P., Bhatia, V.K., Stamou, D., Carlsson, S.R., Hurley, J.H. and Cullen, P.J. (2012) Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO, 31, 4466-4480.
36. 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.
37. Seaman, M.N., Gautreau, A. and Billadeau, D.D. (2013) Retromer-mediated endosomal protein sorting: all WASHed up! Trends Cell Biol., 23, 522-528.
38. 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.
39. Small, S.A., Kent, K., Pierce, A., Leung, C., Kang, M.S., Okada, H., Honig, L., Vonsattel, J.P. and Kim, T.W. (2005) Modelguided microarray implicates the retromer complex in Alzheimer's disease. Ann. Neurol., 58, 909-919.
40. Trinh, J. and Farrer, M. (2013) Advances in the genetics of Parkinson disease. Nat. Rev. Neurol., 9, 445-454.
41. Vilarino-Guell, C., Rajput, A., Milnerwood, A.J., Shah, B., Szu-Tu, C., Trinh, J., Yu, I., Encarnacion, M., Munsie, L.N., Tapia, L. et al. (2013) DNAJC13 mutations in Parkinson disease. Hum. Mol. Genet., 23, 1794-1801.
42. Freeman, C.L., Hesketh, G. and Seaman, M.N. (2014) RME-8 coordinates the activity of theWASH complex with the function of the retromer SNX dimer to control endosomal tubulation. J. Cell Sci., 127, 2053-2070.
43. Matta, S., Van Kolen, K., da Cunha, R., van den Bogaart, G., Mandemakers, W., Miskiewicz, K., De Bock, P.J., Morais, V.A., Vilain, S., Haddad, D. et al. (2012) LRRK2 controls an EndoA phosphorylation cycle in synaptic endocytosis. Neuron, 75, 1008-1021.
44. Girard, M., Poupon, V., Blondeau, F. and McPherson, P.S. (2005) The DnaJ-domain protein RME-8 functions in endosomal trafficking. J. Biol. Chem., 280, 40135-40143.
45. Parisiadou, L., Yu, J., Sgobio, C., Xie, C., Liu, G., Sun, L., Gu, X.L., Lin, X., Crowley, N.A., Lovinger, D.M. et al. (2014) LRRK2 regulates synaptogenesis and dopamine receptor activation throughmodulation of PKA activity. Nat. Neurosci., 17, 367-376.
46. Beccano-Kelly, D.A., Kuhlmann, N., Tatarnikov, I., Volta, M., Munsie, L.N., Chou, P., Han, H., Tapia, L., Farrer, M.L. and Milnerwood, A.J. (2014) Synaptic function is modulated by LRRK2 and glutamate release is increased in cortical neurons of G2019S LRRK2 knock-in mice. Front. Cell Neurosci, 8, doi:10.3389/fncel.2014.00301.
47. Tashiro, A. and Yuste, R. (2003) Structure and molecular organization of dendritic spines. Histol. Histopathol., 18, 617-634.
48. Xie, C., Markesbery, W.R. and Lovell, M.A. (2000) Survival of hippocampal and cortical neurons in amixture ofMEM+ and B27-supplemented neurobasal medium. Free Radic. Biol. Med., 28, 665-672.
49. Tapia, L., Milnerwood, A., Guo, A., Mills, F., Yoshida, E., Vasuta, C., Mackenzie, I.R., Raymond, L., Cynader, M., Jia, W. et al. (2011) Progranulin deficiency decreases gross neural connectivity but enhances transmission at individual synapses. J. Neurosci., 31, 11126-11132.
50. Brigidi, G.S., Sun, Y., Beccano-Kelly, D., Pitman, K., Mobasser, M., Borgland, S.L., Milnerwood, A.J. and Bamji, S.X. (2014) Palmitoylation of delta-catenin by DHHC5 mediates activityinduced synapse plasticity. Nat. Neurosci., 17, 522-532.
51. Kriks, S., Shim, J.W., Piao, J., Ganat, Y.M., Wakeman, D.R., Xie, Z., Carrillo-Reid, L., Auyeung, G., Antonacci, C., Buch, A. et al. (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature, 480, 547-551.