Late compartments of amyloid precursor protein transport in SY5Y cells are involved in β-amyloid secretion

Journal of Neuroscience

Volumn 17, Issue 20, 1997, Pages 7714-7724

  Peraus, Gisela C ^a   Masters, Colin L ^b   Beyreuther, Konrad ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Alzheimer's disease; APP processing; Chimeric proteins; Endosomal lysosomal compartment; Transport; amyloid

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CHIMERIC PROTEIN;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELL SURFACE; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PLAQUE FORMING CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN TRANSPORT;

EID: 0030820822     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-20-07714.1997     Document Type: Article

References (44)

1. Busciglio J, Gabuzda DH, Matsudaira P, Yankner BA (1993) Generation of beta-amyloid in the secretory pathway in neuronal and nonneuronal cells. Proc Natl Acad Sci USA 90:2092-2096.
2. Caporaso GL, Gandy SE, Buxbaum JD, Greengard P (1992) Chloroquine inhibits intracellular degradation but not secretion of Alzheimer beta/A4 amyloid precursor protein. Proc Natl Acad Sci USA 89:2252-2256.
3. Chen JW, Murphy TL, Willingham MC, Pastan I, August JT (1985) Identification of two lysosomal membrane glycoproteins. J Cell Biol 101:85-95.
4. Cole GM, Huynh TV, Saitoh T (1989) Evidence for lysosomal processing of amyloid beta-protein precursor in cultured cells. Neurochem Res 14:933-939.
5. Cosson P, Letourneur F (1994) Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263:1629-1631.
6. Dyrks T, Dyrks E, Monning U, Urmoneit B, Turner J, Beyreuther K (1993) Generation of beta A4 from the amyloid protein precursor and fragments thereof. FEBS Lett 335:89-93.
7. Esch FS, Keim PS, Beattie EC, Blacher RW, Culwell AR, Oltersdorf T, McClure D, Ward PJ (1990) Cleavage of amyloid β peptide during constitutive processing of its precursor. Science 248:1122-1124.
8. Evan GI, Lewis GK, Ramsay G, Bishop JM (1985) Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol 5:3610-3616.
9. Glenner GG, Wong CW (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885-890.
10. Golde TE, Estus S, Younkin LH, Selkoe DJ, Younkin SG (1992) Processing of the amyloid protein precursor to potentially amyloidogenic derivatives. Science 255:728-730.
11. Görlich D, Rapoport TA (1993) Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 75:615-630.
12. Guarnieri FG, Arterburn LM, Penno MB, Cha Y, August JT (1993) The motif Tyr-X-X-hydrophobic residue mediates lysosomal membrane targeting of lysosome-associated membrane protein 1. J Biol Chem 268:1941-1946.
13. Haass C, Selkoe DJ (1993) Cellular processing of beta-amyloid precursor protein and the genesis of amyloid beta-peptide. Cell 75:1039-1042.
14. Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ (1992a) Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357:500-503.
15. Haass C, Schlossmacher MG, Hung AY, Vigo-Pelfrey C, Mellon A, Ostaszewski BL, Lieberburg I, Koo EH, Schenk D, Teplow DB, Selkoe DJ (1992b) Amyloid beta-peptide is produced by cultured cells during normal metabolism. Nature 359:322-325.
16. Haass C, Hung AY, Schlossmacher MG, Oltersdorf T, Teplow DB, Selkoe DJ (1993) β-Amyloid peptide and a 3 kDa fragment are derived by distinct cellular mechanisms. J Biol Chem 268:3021-3024.
17. Hilbich C, Monning U, Grund C, Masters CL, Beyreuther K (1993) Amyloid-like properties of peptides flanking the epitope of amyloid precursor protein-specific monoclonal antibody 22C11. J Biol Chem 268:26571-26577.
18. Höning S, Griffith J, Geuze HJ, Hunziker W (1996) The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgi-derived clathrin-coated vesicles. EMBO J 15:5230-5239.
19. Ida N, Hartmann T, Pantel J, Schröder J, Zerfass R, Förstl H, Sandbrink R, Masters CL, Beyreuther K (1996) Analysis of heterogenous beta-A4 peptides in human cerebrospinal fluid and blood by newly developed sensitive Western blot assay. J Biol Chem 271:22908-22914.
20. Johnson KF, Kornfeld S (1992) A His-Leu-Leu sequence near the carboxyl terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function. J Biol Chem 267:17110-17115.
21. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, Multhaup G, Beyreuther K, Mueller-Hill B (1987) The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325:733-736.
22. Kim KS, Miller DL, Sapienza VJ, Chen C-MJ, Bai C, Grundke-Iqbal I, Currie JR, Wisniewski HM (1988) Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid peptide. Neurosci Res Commun 2:121-130.
23. Klumperman J, Hille A, Veenendaal T, Oorschot V, Stoorvogel W, von Figura K, Geuze HJ (1993) Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J Cell Biol 121:997-1010.
24. Koo EH, Squazzo SL (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem 269:17386-17389.
25. Koo EH, Squazzo SL, Selkoe DJ, Koo CH (1996) Trafficking of cell-surface amyloid beta-protein precursor. 1. Secretion, endocytosis, and recycling as detected by labeled monoclonal antibody. J Cell Sci 109:991-998.
26. Kornfeld S (1992) Structure and function of the mannose 6-phosphate; insulin-like growth factor II receptors. Annu Rev Biochem 61:307-330.
27. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA 82:4245-4249.
28. Meresse S, Hoflack B (1993) Phosphorylation of the cation-independent mannose 6-phosphate receptor is closely associated with its exit from the trans-Golgi network. J Cell Biol 120:67-75.
29. Pohlmann R, Nagel G, Schmidt B, Stein M, Lorkowski G, Krentler C, Cully J, Meyer HE, Grzeschik KH, Mersmann G, Hasilik A, von Figura K (1987) Cloning of a cDNA encoding the human cation-dependent mannose 6-phosphate-specific receptor. Proc Natl Acad Sci USA 84:5575-5579.
30. Ponnambalam S, Rabouille C, Luzio JP, Nilsson T, Warren G (1994) The TGN38 glycoprotein contains two non-overlapping signals that mediate localization to the trans-Golgi network. J Cell Biol 125:253-268.
31. Ponnambalam S, Girotti M, Yaspo M-L, Owen CW, Perry ACF, Suganuma T, Nilsson T, Fried M, Banting G, Warren G (1996) Primate homologues of rat TGN38: primary structure, expression and functional implications. J Cell Sci 109:675-685.
32. Reaves B, Horn M, Banting G (1993) TGN38/41 recycles between the cell surface and the TGN: brefeldin A affects its rate of return to the TGN. Mol Biol Cell 4:93-105.
33. Rohrer J, Schweizer A, Johnson KF, Kornfeld S (1995) A determinant in the cytoplasmic tail of the cation-dependent mannose 6-phosphate receptor prevents trafficking to lysosomes. J Cell Biol 130:1297-1306.
34. Ross RA, Spengler BA, Biedler JL (1983) Coordinate morphological and biochemical interconversion of human neuroblastoma cells. J Natl Cancer Inst 71:741-747.
35. Sambamurti K, Shioi J, Anderson JP, Pappolla MA, Robakis NK (1992) Evidence for intracellular cleavage of the Alzheimer's amyloid precursor in PC12 cells. J Neurosci Res 33:319-329.
36. Schagger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368-379.
37. Shoji M, Golde TE, Ghiso J, Cheung TT, Estus S, Shaffer LM, Cai XD, McKay DM, Tintner R, Frangione B, Younkin SG (1992) Production of the Alzheimer amyloid beta protein by normal proteolytic processing. Science 258:126-129.
38. Siman R, Mistretta S, Durkin JT, Savage MJ, Loh T, Trusko S, Scott RW (1993) Processing of the beta-amyloid precursor. Multiple proteases generate and degrade potentially amyloidogenic fragments. J Biol Chem 268:16602-16609.
39. Simons M, Ikonen E, Tienari PJ, Cidarregui A, Monning U, Beyreuther K, Dotti CG (1995) Intracellular routing of human amyloid protein precursor: axonal delivery followed by transport to the dendrites. J Neurosci Res 41:121-128.
40. Simons M, De Strooper B, Multhaup G, Tienari PJ, Dotti CG, Beyreuther K (1996) Amyloidogenic processing of the human amyloid precursor protein in primary cultures of rat hippocampal neurons. J Neurosci 16:899-908.
41. Sisodia SS (1992) Beta-amyloid precursor protein cleavage by a membrane-bound protease. Proc Natl Acad Sci USA 89:6075-6079.
42. Usami M, Yamao-Harigaya W, Maruyama K (1993) The triplet of lysine residues (Lys724-Lys725-Lys726) of Alzheimer's amyloid precursor protein plays an important role in membrane anchorage and processing. J Neurochem 61:239-246.
43. Weidemann A, Konig G, Bunke D, Fischer P, Salbaum JM, Masters CL, Beyreuther K (1989) Identification, biogenesis, and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell 57:115-126.
44. Yamazaki T, Koo EH, Selkoe DJ (1996) Trafficking of cell-surface amyloid beta-protein precursor. 2. Endocytosis, recycling, and lysosomal targeting detected by immunolocalization. J Cell Sci 109:999-1008.