The Intracellular Domain of Sortilin Interacts with Amyloid Precursor Protein and Regulates Its Lysosomal and Lipid Raft Trafficking

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Yang, Miao ^a,b   Virassamy, Balaji ^b   Vijayaraj, Swarna Lekha ^b   Lim, Yoon ^a   Saadipour, Khalil ^b   Wang, Yan Jiang ^c   Han, Yan Chuang ^a   Zhong, Jin Hua ^a   Morales, Carlos R ^d   Zhou, Xin Fu ^a,b  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; SORTILIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN TISSUE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CONTROLLED STUDY; FRACTIONATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; LIPID RAFT; LYSOSOME; MOUSE; NONHUMAN; PEPTIDE MAPPING; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REGULATORY MECHANISM; SUCROSE GRADIENT FRACTIONATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BINDING SITES; CEREBRAL CORTEX; ENDOSOMES; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HUMANS; LYSOSOMES; MEMBRANE MICRODOMAINS; MICE; MOLECULAR SEQUENCE DATA; NEURONS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFECTION;

EID: 84877948076     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063049     Document Type: Article

References (46)

1. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, et al. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
2. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, et al. (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155: 853-862.
3. Thinakaran G, Koo EH, (2008) Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283: 29615-29619.
4. De Strooper B, Annaert W, (2000) Proteolytic processing and cell biological functions of the amyloid precursor protein. J Cell Sci 113 (Pt 11): 1857-1870.
5. Caporaso GL, Takei K, Gandy SE, Matteoli M, Mundigl O, et al. (1994) Morphologic and biochemical analysis of the intracellular trafficking of the Alzheimer beta/A4 amyloid precursor protein. J Neurosci 14: 3122-3138.
6. Lorenzen A, Samosh J, Vandewark K, Anborgh PH, Seah C, et al. (2010) Rapid and direct transport of cell surface APP to the lysosome defines a novel selective pathway. Mol Brain 3: 11.
7. Small SA, Gandy S, (2006) Sorting through the cell biology of Alzheimer's disease: intracellular pathways to pathogenesis. Neuron 52: 15-31.
8. Skovronsky DM, Moore DB, Milla ME, Doms RW, Lee VM, (2000) Protein kinase C-dependent alpha-secretase competes with beta-secretase for cleavage of amyloid-beta precursor protein in the trans-golgi network. J Biol Chem 275: 2568-2575.
9. Her LS, Goldstein LS, (2008) Enhanced sensitivity of striatal neurons to axonal transport defects induced by mutant huntingtin. J Neurosci 28: 13662-13672.
10. Kamal A, Stokin GB, Yang Z, Xia CH, Goldstein LS, (2000) Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28: 449-459.
11. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, et al. (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307: 1282-1288.
12. Nielsen MS, Madsen P, Christensen EI, Nykjaer A, Gliemann J, et al. (2001) The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J 20: 2180-2190.
13. Willnow TE, Petersen CM, Nykjaer A, (2008) VPS10P-domain receptors- regulators of neuronal viability and function. Nat Rev Neurosci 9: 899-909.
14. Westergaard UB, Sorensen ES, Hermey G, Nielsen MS, Nykjaer A, et al. (2004) Functional organization of the sortilin Vps10p domain. J Biol Chem 279: 50221-50229.
15. Petersen CM, Nielsen MS, Nykjaer A, Jacobsen L, Tommerup N, et al. (1997) Molecular identification of a novel candidate sorting receptor purified from human brain by receptor-associated protein affinity chromatography. J Biol Chem 272: 3599-3605.
16. Nielsen MS, Gustafsen C, Madsen P, Nyengaard JR, Hermey G, et al. (2007) Sorting by the cytoplasmic domain of the amyloid precursor protein binding receptor SorLA. Mol Cell Biol 27: 6842-6851.
17. Hampe W, Rezgaoui M, Hermans-Borgmeyer I, Schaller HC, (2001) The genes for the human VPS10 domain-containing receptors are large and contain many small exons. Hum Genet 108: 529-536.
18. Mazella J, (2001) Sortilin/neurotensin receptor-3: a new tool to investigate neurotensin signaling and cellular trafficking? Cell Signal 13: 1-6.
19. Dodson SE, Gearing M, Lippa CF, Montine TJ, Levey AI, et al. (2006) LR11/SorLA expression is reduced in sporadic Alzheimer disease but not in familial Alzheimer disease. J Neuropathol Exp Neurol 65: 866-872.
20. Finan GM, Okada H, Kim TW, (2011) BACE1 retrograde trafficking is uniquely regulated by the cytoplasmic domain of sortilin. J Biol Chem 286: 12602-12616.
21. Ni X, Morales CR, (2006) The lysosomal trafficking of acid sphingomyelinase is mediated by sortilin and mannose 6-phosphate receptor. Traffic 7: 889-902.
22. Yang M, Lim Y, Li X, Zhong JH, Zhou XF, (2011) Precursor of brain-derived neurotrophic factor (proBDNF) forms a complex with Huntingtin-associated protein-1 (HAP1) and sortilin that modulates proBDNF trafficking, degradation, and processing. J Biol Chem 286: 16272-16284.
23. Vetrivel KS, Cheng H, Lin W, Sakurai T, Li T, et al. (2004) Association of gamma-secretase with lipid rafts in post-Golgi and endosome membranes. J Biol Chem 279: 44945-44954.
24. Hung YH, Robb EL, Volitakis I, Ho M, Evin G, et al. (2009) Paradoxical condensation of copper with elevated beta-amyloid in lipid rafts under cellular copper deficiency conditions: implications for Alzheimer disease. J Biol Chem 284: 21899-21907.
25. Waldo GS, Standish BM, Berendzen J, Terwilliger TC, (1999) Rapid protein-folding assay using green fluorescent protein. Nature biotechnology 17: 691-695.
26. Chen WJ, Goldstein JL, Brown MS, (1990) NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 265: 3116-3123.
27. Suzuki T, Nakaya T, (2008) Regulation of amyloid beta-protein precursor by phosphorylation and protein interactions. J Biol Chem 283: 29633-29637.
28. Kaether C, Haass C, (2004) A lipid boundary separates APP and secretases and limits amyloid beta-peptide generation. J Cell Biol 167: 809-812.
29. Rushworth JV, Hooper NM, (2010) Lipid Rafts: Linking Alzheimer's Amyloid-beta Production, Aggregation, and Toxicity at Neuronal Membranes. Int J Alzheimers Dis 2011: 603052.
30. Kwon S, Christian JL, (2011) Sortilin associates with transforming growth factor-beta family proteins to enhance lysosome-mediated degradation. J Biol Chem 286: 21876-21885.
31. Cole GM, Bell L, Truong QB, Saitoh T, (1992) An endosomal-lysosomal pathway for degradation of amyloid precursor protein. Ann N Y Acad Sci 674: 103-117.
32. Ono Y, Kinouchi T, Sorimachi H, Ishiura S, Suzuki K, (1997) Deletion of an endosomal/lysosomal targeting signal promotes the secretion of Alzheimer's disease amyloid precursor protein (APP). J Biochem 121: 585-590.
33. Andersen OM, Schmidt V, Spoelgen R, Gliemann J, Behlke J, et al. (2006) Molecular dissection of the interaction between amyloid precursor protein and its neuronal trafficking receptor SorLA/LR11. Biochemistry 45: 2618-2628.
34. Andersen OM, Reiche J, Schmidt V, Gotthardt M, Spoelgen R, et al. (2005) Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc Natl Acad Sci U S A 102: 13461-13466.
35. Spoelgen R, von Arnim CA, Thomas AV, Peltan ID, Koker M, et al. (2006) Interaction of the cytosolic domains of sorLA/LR11 with the amyloid precursor protein (APP) and beta-secretase beta-site APP-cleaving enzyme. J Neurosci 26: 418-428.
36. Borg JP, Ooi J, Levy E, Margolis B, (1996) The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein. Mol Cell Biol 16: 6229-6241.
37. Burgos PV, Mardones GA, Rojas AL, daSilva LL, Prabhu Y, et al. (2010) Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev Cell 18: 425-436.
38. Ando K, Iijima KI, Elliott JI, Kirino Y, Suzuki T, (2001) Phosphorylation-dependent regulation of the interaction of amyloid precursor protein with Fe65 affects the production of beta-amyloid. J Biol Chem 276: 40353-40361.
39. King GD, Scott Turner R, (2004) Adaptor protein interactions: modulators of amyloid precursor protein metabolism and Alzheimer's disease risk? Exp Neurol 185: 208-219.
40. Verhey KJ, Meyer D, Deehan R, Blenis J, Schnapp BJ, et al. (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 152: 959-970.
41. Li XJ, Li SH, (2005) HAP1 and intracellular trafficking. Trends Pharmacol Sci 26: 1-3.
42. Gauthier LR, Charrin BC, Borrell-Pages M, Dompierre JP, Rangone H, et al. (2004) Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118: 127-138.
43. Lefrancois S, Zeng J, Hassan AJ, Canuel M, Morales CR, (2003) The lysosomal trafficking of sphingolipid activator proteins (SAPs) is mediated by sortilin. EMBO J 22: 6430-6437.
44. Ehehalt R, Keller P, Haass C, Thiele C, Simons K, (2003) Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 160: 113-123.
45. Di Paolo G, Kim TW, (2011) Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat Rev Neurosci 12: 284-296.
46. Xu H, Sweeney D, Wang R, Thinakaran G, Lo AC, et al. (1997) Generation of Alzheimer beta-amyloid protein in the trans-Golgi network in the apparent absence of vesicle formation. Proc Natl Acad Sci U S A 94: 3748-3752.