The β-amyloid domain is essential for axonal sorting of amyloid precursor protein

EMBO Journal

Volumn 15, Issue 19, 1996, Pages 5218-5229

  Tienari, Pentti J ^a,b   De Strooper, Bart ^a,c   Ikonen, Elina ^a   Simons, Mikael ^a,b   Weidemann, Andreas ^b   Czech, Christian ^b   Hartmann, Tobias ^b   Ida, Nobuo ^b   Multhaup, Gerd ^b   Masters, Colin L ^d   Van Leuven, Fred ^c   Beyreuther, Konrad ^b   Dotti, Carlos G ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c CENTER FOR HUMAN GENETICS   (Belgium)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Alzheimer's disease; Amyloid; Axonal transport; Cellular polarity; Sorting signals

Indexed keywords

3 [(3 CHOLAMIDOPROPYL)DIMETHYLAMMONIO] 1 PROPANESULFONIC ACID; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; DETERGENT; HEMAGGLUTININ; MUTANT PROTEIN; SIGNAL PEPTIDE; TUNICAMYCIN;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DELETION MUTANT; EMBRYO; EXON; FEMALE; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN TARGETING; RAT; SEMLIKI FOREST ALPHAVIRUS; SOLUBILITY;

ALPHAVIRUS; ANIMALIA; SEMLIKI FOREST VIRUS;

EID: 10144263284     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00907.x     Document Type: Article

References (54)

1. Allinquant, B., Moya, K., Bouillot, C. and Prochiantz, A. (1994) Amyloid precursor protein in cortical neurons: coexistence of two pools differently distributed in axons and dendrites and association with cytoskeleton. J. Neurosci., 14, 6842-6854.
2. Aoreti, B. and Mostov, K. (1994) Polarized sorting of polymeric immunoglobulin receptor in the exocytic and endocytic pathways is controlled by the same amino acids. EMBO J., 13, 2297-2304.
3. Caporaso, G.L., Takei, K., Gandy, S.E., Matteoli, M., Mundigl, O., Greengard, P. and de Camilli, P. (1994) Morphological and biochemical analysis of the intracellular trafficking of the Alzheimer's β/A4 amyloid precursor protein. J. Neurosci., 14, 3122-3138.
4. Citron, M., Teplow, D.B. and Selkoe, D.J. (1995) Generation of amyloid β protein from its precursor is sequence specific. Neuron, 14, 661-670.
5. Craig, A.M. and Banker, G. (1994) Neuronal polarity. Annu. Rev. Neurosci., 17, 267-310.
6. De Hoop, M., von Poser, C., Lange, C. Ikonen, E., Hunziker, W. and Dotti, C.G. (1995) Intracellular routing of wild-type and mutated polymeric immunoglobulin receptor in hippocampal neurons in culture. J. Cell Biol., 130, 1447-1459.
7. De Strooper, B. Craessaerts, K., Dewachter, I., Moechars, D., Greenberg, B., Van Leuven, F. and Van Den Berghe, H. (1995a) Basolateral secretion of amyloid precursor protein in Madin-Darby canine kidney cells is disturbed by alterations of intracellular pH and by introducing a mutation associated with familial Alzheimer's disease. J. Biol. Chem., 270, 4058-4065.
8. De Strooper, B., Craessaerts, K., Van Leuven, F. and Van Den Berghe, H. (1995b) Exchanging the extracellular domain of amyloid precursor protein for horseradish peroxidase does not interfere with alpha-secretase cleavage of the beta-amyloid region, but randomizes secretion in Madin-Darby canine kidney cells. J Biol. Chem., 270, 30310-30314.
9. De Strooper, B., Simons, M. Multhaup, G., Van Leuven, F., Beyreuther, K. and Dotti, C.G. (1995c) Production of intracellular amyloid-containing fragments in hippocampal neurons expressing human amyloid precursor protein and protection against amyloidogenesis by subtle amino acid substitutions in the rodent sequence. EMBO J., 14, 4932-4938.
10. Deng, W.P. and Nickoloff, J.A. (1992) Site-directed mutagenesis of virtually any plasmid eliminating a unique site. Annu. Biochem., 200, 81-88.
11. Dotti, C.G. and Simons, K. (1990) Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell, 62, 63-72.
12. Dotti, C.G., Parton, R.G. and Simons, K. (1991) Polarised sorting of glypiated proteins in hippocampal neurons. Nature, 349, 158-161.
13. Dotti, C.G., Kartenbeck, J. and Simons, K. (1992) Polarized delivery of the glycoproteins of Vesicular Stomatitits, Fowl Plague, and Semliki Forest viruses in hippocampal neurons in culture: a light and electron microscopy study. Brain Res., 610, 141-147.
14. Dyrks, T., Weidemann, A., Multhaup, G., Salbaum, J.M., Lemaire, H.G., Kang, J., Muller-Hill, B., Masters, C.L. and Beyreuther, K. (1988) Identification, transmembrane orientation and biogenesis of the amyloid A4 precursor of Alzheimer's disease. EMBO J., 7, 949-957.
15. Dyrks, T., Dyrks, E., Monning, U., Urmoneit, B., Turner, J. and Beyreuther, K. (1993) Generation of beta A4 from the amyloid protein precursor and fragments thereof. FEBS Lett., 335, 89-93.
16. Evan, G., Lewis, G.K., Ramsay, G. and Bishop, J.M. (1985) Isolation of monoclonal antibodies specific for c-myc proto-oncogene product. Mol. Cell. Biol., 5, 3610-3616.
17. Ferreira, A., Caceres, A. and Kosik, K. (1993) Intraneuronal compartments of amyloid precursor protein. J. Neurosci., 13, 3112-3123.
18. Fiedler, K. and Simons, K. (1995) The role of N-glycans in the secretory pathway. Cell, 81, 309-312.
19. Fiedler, K., Kobayashi, T., Kurzhalia, T.V. and Simons, K. (1993) Glycosphingolipid-enriched, detergent-insoluble complexes in protein sorting in epithelial cells. Biochemistry, 32, 6365-6373.
20. Glenner, G.C. and Wong, C.W. (1984) Alzheimer's disease: initial report of the purification and characterisation of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun., 120, 885-890.
21. Goate, A. et al. (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature, 349, 704-706.
22. Goslin, K. and Banker, G.A. (1991) Rat hippocampal neurons in low density culture. In Banker, G.A. and Goslin, K. (eds). Culturing Nerve Cells. MIT Press, Cambridge, MA, pp. 251-281.
23. Haass, C. and Selkoe, D.J. (1993) Cellular processing of β-amyloid precursor protein and the genesis of amyloid β-peptide. Cell, 75, 1039-1042.
24. Haass, C. Koo, E.H., Teplow, D. and Selkoe, D.J. (1995) Polarised secretion of β-amyloid precursor protein and β-amyloid peptide in MDCK cells. J. Cell Biol., 128, 537-547.
25. Hansson, H.A., Holmgren, J. and Svennerholm, L. (1977) Ultrastructural localization of cell membrane GM1 ganglioside by cholera toxin. Proc. Natl Acad. Sci. USA, 74, 3782-3786.
26. Higuchi, R. (1990) Recombinant PCR. In Innis, M.A., Gelfand, D.H., Sninsky, J.J. and White, T.J. (eds), PCR Protocols, A Guide to Methods and Applications. Academic Press, London, UK, pp. 177-183.
27. Ikonen, E., Parton, R.G., Hunziker, W., Simons, K. and Dotti, C.G. (1993) Transcytosis of the polymeric immunoglobulin receptor in cultured hippocampal neurons. Curr. Biol., 3, 635-644.
28. Kang, J., Lemaire, H.G., Unterbeck, A., Salbaum, J.M., Masters, C.L., Grzeschik, K.H., Multhaup, G., Beyreuther, K. and Muller-Hill, B. (1987) The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature, 325, 733-736.
29. Koo, E.H., Sisodia, S.S., Archer, D.A., Martin, L.J., Weidemann, A., Beyreuther, K., Masters, C.L. and Price, D.L. (1990) Precursor of amyloid precursor protein in Alzheimer's disease undergoes fast anterograde axonal transport. Proc. Natl Acad. Sci. USA, 87, 1561-1565.
30. Kurzchalia, T.V., Dupree, P., Parton, R.G., Kellner, R., Virta, H., Lehnen, M. and Simons, K. (1992) VIP21, a 21 kDa membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J. Cell Biol., 118, 1003-1014.
31. Levy, E., Carman, M.D., Fernandez-Madrid, I.J., Power, M.D., Lieberburg, I., van Duinen, S.G., Bots, G.T.A.M., Luyendijk, W. and Frangione, B. (1990) Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral amyloidosis, Dutch type. Science, 248, 1124-1126.
32. Liljeström, P. and Garoff, H. (1991) A new generation of animal cell expression vectors based on the Semliki Forest Virus Replicon. Biotechnology, 9, 1356-1361.
33. Masters, C.L., Multhaup, G., Simms, G., Pottgiesser, J., Martins, R.N. and Beyreuther, K. (1985) Amyloid core protein in Alzheimer's disease and Down's syndrome. Proc. Natl Acad. Sci. USA, 82, 4245-4249.
34. Matlin, K.S. and Simons, K. (1983) Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell, 34, 233-234.
35. Matter, K. and Mellman, I. (1994) Mechanisms of cell polarity: sorting and transport in epithelial cells. Curr. Opin. Cell Biol., 6, 545-554.
36. Matter, K., Whitney, J.A., Yamamoto, E.M. and Mellman, I. (1993) Common signals control LDL receptor sorting in endosomes and the Golgi complex of MDCK cells. Cell, 74, 1053-1064.
37. Mullan, M., Crawford, F., Axelman, K., Houlden, H., Lilius, L., Winnblad, B. and Lannfelt, L. (1992) A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of β-amyloid. Nature Genet., 1, 345-347.
38. Olkkonen, V.M., Liljeström, P., Garoff, H., Simons, K. and Dotti, C.G. (1993) Expression of heterologous proteins in cultured rat hippocampal neurons using Semliki forest virus vector. J. Neurosci. Res., 35, 445-451.
39. Parton, R.G. (1994) Ultrastructural localization of gangliosides: GM1 is concentrated in caveolae. J. Histochem. Cytochem., 42, 155-166.
40. Pietrini, G., Suh, Y.J., Edelmann, L., Rudnick, G. and Caplan, M.J. (1994) The axonal γ-aminobutyric acid transporter GAT-1 is sorted to the apical membranes of polarized epithelial cells. J. Biol. Chem., 269, 4668-4674.
41. Rodriguez-Boulan, E. and Powell, S.K. (1992) Polarity of epithelial and neuronal cells. Annu. Rev. Cell Biol., 8, 395-427.
42. Sandbrink, R., Masters, C.L. and Beyreuther, K. (1994) βA4 amyloid protein precursor mRNA isoforms without exon 15 are ubiquitously expressed in rat tissues including brain, but not in neurons. J. Biol. Chem., 269, 1510-1517.
43. Scheiffele, P., Peränen, J. and Simons, K. (1995) N-Glycans as apical sorting signals in epithelial cells. Nature, 387, 96-98.
44. Schubert, W., Prior, R., Weidemann, A., Lemaire, H.G., Masters, C.L. and Beyreuther, K. (1991) Localization of Alzheimer's βA4 amyloid presursor protein at central and peripheral synaptic sites. Brain Res., 563, 184-194.
45. Simons, K. and Zerial, M. (1993) Rab proteins and the road maps for intracellular transport. Neuron, 11, 789-799.
46. Simons, M., Ikonen, E., Tienari, P.J., Cid-Arregui, A., Mönnong, U., Beyreuther, K. and Dotti, C.G. (1995) Intracellular routing of human amyloid protein precursor: axonal delivery followed by transport to the dendrites. J. Neurosci. Res., 41, 121-128.
47. Simons, M., De Strooper, B., Multhaup, G., Tienari, P.J., Dotti, C.G. and Beyreuther, K. (1996) Amyloidogenic processing of the human amyloid precursor protein in primary cultures of rat hippocampal neurons. J. Neurosci., 16, 899-908.
48. Sisodia, S.S. (1992) Beta-amyloid precursor protein cleavage by a membrane-bound protease. Proc. Natl Acad. Sci. USA, 89, 6075-6079.
49. Wandinger-Ness, A., Bennett, M.K., Antony, C. and Simons, K. (1990) Distinct transport vesicles mediate the delivery of plama membrane proteins to the apical and basolateral domains of MDCK cells. J. Cell Biol., 111, 987-1000.
50. Weidemanri, A., Konig, G., Bunke, D., Fischer, P., Masters, C.L. and Beyreuther, K. (1989) Identification, biogenesis and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell. 57, 115-126.
51. Wertkin, A.M., Turner, R.S., Pleasure, S.J., Golde, S.G., Trojanowski, J.Q. and Lee, V.M.Y. (1993) Human neurons derived from a teratocarcinoma cell line express solely the 695-amino acid amyloid precursor and produce intracellular β-amyloid or A4 peptides. Proc. Natl Acad. Sci. USA, 90, 9513-9517.
52. Yamazaki, T., Selkoe, D.J. and Koo, E.H. (1995) Trafficking of cell surface β-amyloid precursor protein: retrograde and transcytotic transport in cultured neurons. J. Cell Biol., 129, 431-442.
53. Yanagisawa, K., Odaka, A., Suzuki, N. and Ihara, Y. (1995) GM1 ganglioside-bound amyloid β-protein (Aβ): a possible form of preamyloid in Alzheimer's disease. Nature Med., 1, 1062-1066.
54. Ying, Y.-S., Anderson, R.G.W. and Rothberg, K.G. (1992) Each caveola contains multiple glycosyl-phosphtidylinositol anchored membrane proteins. Cold Spring Harbor Symp. Quant. Biol., 57, 593-602.