Cargo trafficking in Alzheimer’s disease: the possible role of retromer

Neurological Sciences

Volumn 37, Issue 1, 2016, Pages 17-22

  Sadigh Eteghad, Saeed ^a   Askari Nejad, Mohammad Sadegh ^a   Mahmoudi, Javad ^a   Majdi, Alireza ^a  

^a TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Alzheimer s disease; APP processing; Cargo trafficking; Retromer; Synaptic plasticity; Wnt signaling

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; DIMER; PROTEIN SERINE THREONINE KINASE VPS10; PROTEIN SERINE THREONINE KINASE VPS15; RETROMER; UNCLASSIFIED DRUG; WNT PROTEIN; AMYLOID PROTEIN;

ALZHEIMER DISEASE; CHEMICAL STRUCTURE; DISEASE COURSE; ENDOPLASMIC RETICULUM; ENDOSOME; HUMAN; LYSOSOME; NERVE CELL PLASTICITY; NEUROTOXICITY; NONHUMAN; PROTEIN LOCALIZATION; REVIEW; WNT SIGNALING PATHWAY; ANIMAL; METABOLISM; PHYSIOLOGY;

ALZHEIMER DISEASE; AMYLOIDOGENIC PROTEINS; ANIMALS; HUMANS; NEURONAL PLASTICITY; WNT SIGNALING PATHWAY;

EID: 84955713505     PISSN: 15901874     EISSN: 15903478     Source Type: Journal    
DOI: 10.1007/s10072-015-2399-3     Document Type: Review

References (75)

1. Sadigh-Eteghad S, Majdi A, Farhoudi M, Talebi M, Mahmoudi J (2014) Different patterns of brain activation in normal aging and Alzheimer’s disease from cognitional sight: meta analysis using activation likelihood estimation. J Neurol Sci 343(1–2):159–166. doi:10.1016/j.jns.2014.05.066
2. Brookmeyer R, Johnson E, Ziegler-Graham K, Arrighi HM (2007) Forecasting the global burden of Alzheimer’s disease. Alzheimers Dement 3(3):186–191. doi:10.1016/j.jalz.2007.04.381
3. Muhammad A, Flores I, Zhang H, Yu R, Staniszewski A, Planel E, Herman M, Ho L, Kreber R, Honig LS (2008) Retromer deficiency observed in Alzheimer’s disease causes hippocampal dysfunction, neurodegeneration, and Aβ accumulation. Proc Natl Acad Sci 105(20):7327–7332
4. Bonifacino JS, Hurley JH (2008) Retromer. Curr Opin Cell Biol 20(4):427–436
5. Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165(1):123–133
6. Sullivan CP, Jay AG, Stack EC, Pakaluk M, Wadlinger E, Fine RE, Wells JM, Morin PJ (2011) Retromer disruption promotes amyloidogenic APP processing. Neurobiol Dis 43(2):338–345
7. Sadigh-Eteghad S, Sabermarouf B, Majdi A, Talebi M, Farhoudi M, Mahmoudi J (2015) Amyloid-beta: a crucial factor in Alzheimer’s disease. Med Princ Pract 24(1):1–10. doi:10.1159/000369101
8. Jarrett JT, Lansbury PT Jr (1993) Seeding “one-dimensional crystallization” of amyloid: a pathogenic mechanism in Alzheimer’s disease and scrapie? Cell 73(6):1055–1058
9. Pastorino L, Sun A, Lu P-J, Zhou XZ, Balastik M, Finn G, Wulf G, Lim J, Li S-H, Li X (2006) The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-β production. Nature 440(7083):528–534
10. Wilhelmus M, Otte-Höller I, Wesseling P, De Waal R, Boelens W, Verbeek M (2006) Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer’s disease brains. Neuropathol Appl Neurobiol 32(2):119–130
11. Eaton S (2008) Retromer retrieves wntless. Dev Cell 14(1):4–6
12. Willert K, Nusse R (2012) Wnt proteins. Cold Spring Harb Perspect Biol 4(9):a007864
13. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469(7330):415–418
14. Cerpa W, Godoy JA, Alfaro I, Farías GG, Metcalfe MJ, Fuentealba R, Bonansco C, Inestrosa NC (2008) Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J Biol Chem 283(9):5918–5927
15. Fjorback AW, Seaman M, Gustafsen C, Mehmedbasic A, Gokool S, Wu C, Militz D, Schmidt V, Madsen P, Nyengaard JR (2012) Retromer binds the FANSHY sorting motif in SorLA to regulate amyloid precursor protein sorting and processing. J Neurosci 32(4):1467–1480
16. Small SA, Petsko GA (2015) Retromer in Alzheimer disease, Parkinson disease and other neurological disorders. Nat Rev Neurosci 16:126–132
17. Seaman MN (2005) Recycle your receptors with retromer. Trends Cell Biol 15(2):68–75
18. Norwood SJ, Shaw DJ, Cowieson NP, Owen DJ, Teasdale RD, Collins BM (2011) Assembly and solution structure of the core retromer protein complex. Traffic 12(1):56–71
19. Wassmer T, Attar N, Bujny MV, Oakley J, Traer CJ, Cullen PJ (2007) A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J Cell Sci 120(1):45–54
20. Rojas R, Kametaka S, Haft CR, Bonifacino JS (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(3):1112–1124
21. Collins BM (2008) The structure and function of the retromer protein complex. Traffic 9(11):1811–1822
22. Small SA, Gandy S (2006) Sorting through the cell biology of Alzheimer’s disease: intracellular pathways to pathogenesis. Neuron 52(1):15–31
23. Wen L, Tang F-L, Hong Y, Luo S-W, Wang C-L, He W, Shen C, Jung J-U, Xiong F, D-h Lee (2011) VPS35 haploinsufficiency increases Alzheimer’s disease neuropathology. J Cell Biol 195(5):765–779
24. Small SA, Kent K, Pierce A, Leung C, Kang MS, Okada H, Honig L, Vonsattel JP, Kim TW (2005) Model-guided microarray implicates the retromer complex in Alzheimer’s disease. Ann Neurol 58(6):909–919
25. Munsie L, Milnerwood A, Seibler P, Beccano-Kelly D, Tatarnikov I, Khinda J, Volta M, Kadgien C, Cao L, Tapia L (2015) Retromer-dependent neurotransmitter receptor trafficking to synapses is altered by the Parkinson’s disease VPS35 mutation p. D620N. Hum Mol Genet 24(6):1691–1703
26. Selkoe DJ (2002) Alzheimer’s disease is a synaptic failure. Science 298(5594):789–791
27. Seaman MN (2012) The retromer complex—endosomal protein recycling and beyond. J Cell Sci 125(20):4693–4702
28. Priller C, Bauer T, Mitteregger G, Krebs B, Kretzschmar HA, Herms J (2006) Synapse formation and function is modulated by the amyloid precursor protein. J Neurosci 26(27):7212–7221
29. Kang J, Lemaire H-G, Unterbeck A, Salbaum JM, Masters CL, Grzeschik K-H, Multhaup G, Beyreuther K, Müller-Hill B (1987) The precursor of Alzheimer’s disease amyloid A4 protein resembles a cell-surface receptor. Nature 325:733–736
30. Bhalla A, Vetanovetz CP, Morel E, Chamoun Z, Di Paolo G, Small SA (2012) The location and trafficking routes of the neuronal retromer and its role in amyloid precursor protein transport. Neurobiol Dis 47(1):126–134
31. Wassmer T, Attar N, Harterink M, van Weering JR, Traer CJ, Oakley J, Goud B, Stephens DJ, Verkade P, Korswagen HC (2009) The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev Cell 17(1):110–122
32. Cai H, Wang Y, McCarthy D, Wen H, Borchelt DR, Price DL, Wong PC (2001) BACE1 is the major β-secretase for generation of Aβ peptides by neurons. Nat Neurosci 4(3):233–234
33. Esch FS, Keim PS, Beattie EC, Blacher RW, Culwell AR, Oltersdorf T, McClure D, Ward PJ (1990) Cleavage of amyloid beta peptide during constitutive processing of its precursor. Science 248(4959):1122–1124
34. Vetrivel KS, Thinakaran G (2006) Amyloidogenic processing of β-amyloid precursor protein in intracellular compartments. Neurology 66(1 suppl 1):S69–S73
35. Zheng L, Cedazo-Minguez A, Hallbeck M, Jerhammar F, Marcusson J, Terman A (2012) Intracellular distribution of amyloid beta peptide and its relationship to the lysosomal system. Transl Neurodegener 1(19):10.1186
36. Thinakaran G, Koo EH (2008) Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283(44):29615–29619
37. Choy RW-Y, Cheng Z, Schekman R (2012) 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 109(30):E2077–E2082
38. Hu X, Crick SL, Bu G, Frieden C, Pappu RV, Lee J-M (2009) Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc Natl Acad Sci 106(48):20324–20329
39. Nunan J, Shearman MS, Checler F, Cappai R, Evin G, Beyreuther K, Masters CL, Small DH (2001) The C-terminal fragment of the Alzheimer’s disease amyloid protein precursor is degraded by a proteasome-dependent mechanism distinct from γ-secretase. Eur J Biochem 268(20):5329–5336
40. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297(5580):353–356
41. Okada H, Zhang W, Peterhoff C, Hwang JC, Nixon RA, Ryu SH, Kim T-W (2010) Proteomic identification of sorting nexin 6 as a negative regulator of BACE1-mediated APP processing. FASEB J 24(8):2783–2794
42. Wang C-L, Tang F-L, Peng Y, Shen C-Y, Mei L, Xiong W-C (2012) VPS35 regulates developing mouse hippocampal neuronal morphogenesis by promoting retrograde trafficking of BACE1. Biol Open 1(12):1248–1257
43. Small SA (2008) Retromer sorting: a pathogenic pathway in late-onset Alzheimer disease. Arch Neurol 65(3):323–328
44. Seaman MN (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165(1):111–122
45. Rogaeva E, Meng Y, Lee JH, Gu Y, Kawarai T, Zou F, Katayama T, Baldwin CT, Cheng R, Hasegawa H (2007) The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat Genet 39(2):168–177
46. Schmidt V, Baum K, Lao A, Rateitschak K, Schmitz Y, Teichmann A, Wiesner B, Petersen CM, Nykjaer A, Wolf J (2012) Quantitative modelling of amyloidogenic processing and its influence by SORLA in Alzheimer’s disease. EMBO J 31(1):187–200
47. Andersen OM, Reiche J, Schmidt V, Gotthardt M, Spoelgen R, Behlke J, Von Arnim CA, Breiderhoff T, Jansen P, Wu X (2005) Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc Natl Acad Sci USA 102(38):13461–13466
48. Offe K, Dodson SE, Shoemaker JT, Fritz JJ, Gearing M, Levey AI, Lah JJ (2006) The lipoprotein receptor LR11 regulates amyloid β production and amyloid precursor protein traffic in endosomal compartments. J Neurosci 26(5):1596–1603
49. De Ferrari GV, Inestrosa NC (2000) Wnt signaling function in Alzheimer’s disease. Brain Res Rev 33(1):1–12
50. Bänziger C, Soldini D, Schütt C, Zipperlen P, Hausmann G, Basler K (2006) Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 125(3):509–522
51. Lorenowicz MJ, Korswagen HC (2009) Sailing with the Wnt: charting the Wnt processing and secretion route. Exp Cell Res 315(16):2683–2689
52. Belenkaya TY, Wu Y, Tang X, Zhou B, Cheng L, Sharma YV, Yan D, Selva EM, Lin X (2008) The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell 14(1):120–131
53. Harterink M, Port F, Lorenowicz MJ, McGough IJ, Silhankova M, Betist MC, van Weering JR, van Heesbeen RG, Middelkoop TC, Basler K (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(8):914–923
54. Maurice MM, Korswagen HC (2014) Wnt Signaling in development and disease: molecular mechanisms and biological functions. In: Hoppler SP, Moon RT (eds) Wnt Signal Production, Secretion, and Diffusion. Wiley, New York, pp 3–14
55. Franch-Marro X, Wendler F, Guidato S, Griffith J, Baena-Lopez A, Itasaki N, Maurice MM, Vincent J-P (2008) Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol 10(2):170–177
56. Jackson GR, Wiedau-Pazos M, Sang T-K, Wagle N, Brown CA, Massachi S, Geschwind DH (2002) Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34(4):509–519
57. Clevers H, Nusse R (2012) Wnt/beta-catenin signaling and disease. Cell 149(6):1192–1205. doi:10.1016/j.cell.2012.05.012
58. Boonen RA, van Tijn P, Zivkovic D (2009) Wnt signaling in Alzheimer’s disease: up or down, that is the question. Ageing Res Rev 8(2):71–82
59. Li HL, Wang HH, Liu SJ, Deng YQ, Zhang YJ, Tian Q, Wang XC, Chen XQ, Yang Y, Zhang JY, Wang Q, Xu H, Liao FF, Wang JZ (2007) Phosphorylation of tau antagonizes apoptosis by stabilizing beta-catenin, a mechanism involved in Alzheimer’s neurodegeneration. Proc Natl Acad Sci USA 104(9):3591–3596. doi:10.1073/pnas.0609303104
60. Caricasole A, Copani A, Caruso A, Caraci F, Iacovelli L, Sortino MA, Terstappen GC, Nicoletti F (2003) The Wnt pathway, cell-cycle activation and β-amyloid: novel therapeutic strategies in Alzheimer’s disease? Trends Pharmacol Sci 24(5):233–238
61. Almeida CG, Tampellini D, Takahashi RH, Greengard P, Lin MT, Snyder EM, Gouras GK (2005) Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol Dis 20(2):187–198. doi:10.1016/j.nbd.2005.02.008
62. Choy RW-Y, Park M, Temkin P, Herring BE, Marley A, Nicoll RA, von Zastrow M (2014) Retromer mediates a discrete route of local membrane delivery to dendrites. Neuron 82(1):55–62
63. Zhang D, Isack NR, Glodowski DR, Liu J, Chen CC-H, Xu XS, Grant BD, Rongo C (2012) RAB-6.2 and the retromer regulate glutamate receptor recycling through a retrograde pathway. J Cell Biol 196(1):85–101
64. Munsie L, Milnerwood A, Seibler P, Beccano-Kelly D, Tatarnikov I, Khinda J, Volta M, Kadgien C, Cao L, Tapia L (2014) Retromer-dependent neurotransmitter receptor trafficking to synapses is altered by the Parkinson’s disease VPS35 mutation p. D620N. Hum Mol Genet:ddu582
65. Nakanishi S (1994) Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron 13(5):1031–1037
66. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25(1):103–126
67. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, Lambert MP, Velasco PT, Bigio EH, Finch CE (2004) Synaptic targeting by Alzheimer’s-related amyloid β oligomers. J Neurosci 24(45):10191–10200
68. Lane RF, St George-Hyslop P, Hempstead BL, Small SA, Strittmatter SM, Gandy S (2012) Vps10 family proteins and the retromer complex in aging-related neurodegeneration and diabetes. J Neurosci 32(41):14080–14086
69. Chen Y, Durakoglugil MS, Xian X, Herz J (2010) ApoE4 reduces glutamate receptor function and synaptic plasticity by selectively impairing ApoE receptor recycling. Proc Natl Acad Sci 107(26):12011–12016
70. Weeber EJ, Beffert U, Jones C, Christian JM, Förster E, Sweatt JD, Herz J (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 277(42):39944–39952
71. Vardarajan BN, Bruesegem SY, Harbour ME, Inzelberg R, Friedland R, St George-Hyslop P, Seaman MN, Farrer LA (2012) Identification of Alzheimer disease-associated variants in genes that regulate retromer function. Neurobiol Aging 33(9):2231 e2215–2231 e2230. doi:10.1016/j.neurobiolaging.2012.04.020
72. Lucin KM, O’Brien CE, Bieri G, Czirr E, Mosher KI, Abbey RJ, Mastroeni DF, Rogers J, Spencer B, Masliah E, Wyss-Coray T (2013) Microglial beclin 1 regulates retromer trafficking and phagocytosis and is impaired in Alzheimer’s disease. Neuron 79(5):873–886. doi:10.1016/j.neuron.2013.06.046
73. Muhammad A, Flores I, Zhang H, Yu R, Staniszewski A, Planel E, Herman M, Ho L, Kreber R, Honig LS, Ganetzky B, Duff K, Arancio O, Small SA (2008) Retromer deficiency observed in Alzheimer’s disease causes hippocampal dysfunction, neurodegeneration, and Abeta accumulation. Proc Natl Acad Sci USA 105(20):7327–7332. doi:10.1073/pnas.0802545105
74. Small SA, Petsko GA (2015) Retromer in Alzheimer disease, Parkinson disease and other neurological disorders. Nat Rev Neurosci 16(3):126–132. doi:10.1038/nrn3896
75. Mecozzi VJ, Berman DE, Simoes S, Vetanovetz C, Awal MR, Patel VM, Schneider RT, Petsko GA, Ringe D, Small SA (2014) Pharmacological chaperones stabilize retromer to limit APP processing. Nat Chem Biol 10(6):443–449. doi:10.1038/nchembio.1508