Intracellular accumulation of detergent-soluble amyloidogenic Aβ fragment of Alzheimer's disease precursor protein in the hippocampus of aged transgenic mice

Journal of Neurochemistry

Volumn 72, Issue 6, 1999, Pages 2479-2487

  Li, Qiao Xin ^a   Maynard, Christa ^a   Cappai, Roberto ^a   McLean, Catriona A ^a   Cherny, Robert A ^a   Lynch, Toni ^a   Culvenor, Janetta G ^a   Trevaskis, Jim ^a   Tanner, Jane E ^a   Bailey, Karen A ^a,d   Czech, Christian ^e   Bush, Ashley I ^b   Beyreuther, Konrad ^f   Masters, Colin L ^a,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e SANOFI   (France)

^f NONE

Author keywords

Alzheimer's disease; Amyloid protein; Amyloid precursor protein; C100; Processing; Transgenic mouse

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; COMPLEMENTARY DNA; MONOCLONAL ANTIBODY;

AGING; ALZHEIMER DISEASE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DEGENERATIVE DISEASE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

AGING; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DETERGENTS; HIPPOCAMPUS; HUMANS; KINETICS; MICE; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; SOLUBILITY;

EID: 0033051445     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0722479.x     Document Type: Article

References (52)

1. Cai X., Golde T. E., and Younkin S. G. (1993) Release of excess amyloid β protein from a mutant amyloid β protein precursor. Science 259, 514-516.
2. Citron M., Oltersdorf T., Haass C., McConlogue L., Hung A. Y., Seubert P., Vigo-Pelfrey C., Lieberburg I., and Selkoe D. J. (1992) Mutation of the β-amyloid precursor protein in familial Alzheimer's disease increases β-protein production. Nature 360, 672-674.
3. Citron M., Diehl T. S., Gordon G., Biere A. L., Seubert P., and Selkoe D. J. (1996) Evidence that the 42- and 40-amino acid forms of amyloid β protein are generated from the β-amyloid precursor protein by different protease activities. Proc. Natl. Acad. Sci. USA 93, 13170-13175.
4. Conn K. J., Papastoitsis G., Meckelein B., and Abraham C. R. (1994) Identification of full length β-amyloid precursor protein in human neuronal and non-neuronal cell culture supernatant: a possible source for the generation of Aβ. Amyloid Int. J. Exp. Clin. Invest. 1, 232-239.
5. Dyrks T., Dyrks E., Masters C., and Beyreuther K. (1992) Membrane inserted APP fragments containing the βA4 sequence of Alzheimer's disease do not aggregate. FEBS Lett. 309, 20-24.
6. Dyrks T., Dyrks E., Mönning U., Urmoneit B., Turner J., and Beyreuther K. (1993) Generation of βA4 from the amyloid protein precursor and fragments thereof. FEBS Lett. 335, 89-93.
7. Engel I. and Hedrick S. M. (1988) Site-directed mutations in the VDJ junctional region of a T cell receptor β chain cause changes in antigenic peptide recognition. Cell 54, 473-484.
8. Esch F. S., Keim P. S., Beattie E. C., Blacher R. W., Culwell A. R., Oltersdorf T., McClure D., and Ward P. J. (1990) Cleavage of amyloid β peptide during constitutive processing of its precursor. Science 248, 1122-1124.
9. Estus S., Golde T. E., Kunishita T., Blades D., Lowery D., Eisen M., Usiak M., Qu X., Tabira T., Greenberg B. D., and Younkin S. G. (1992) Potentially amyloidogenic, carboxyl-terminal derivatives of the amyloid protein precursor. Science 255, 726-728.
10. Evin G., Beyreuther K., and Masters C. L. (1994) Alzheimer's disease amyloid precursor protein (AβPP): proteolytic processing, secretases and βA4 amyloid production. Amyloid Int. J. Exp. Clin. Invest. 1, 263-280.
11. Fukuchi K., Sopher B., Furlong C. E., Smith A. C., Dang N., and Martin G. M. (1993) Selective neurotoxicity of COOH-terminal fragments of the beta-amyloid precursor protein. Neurosci. Lett. 154, 145-148.
12. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., Gillespie F., Guido T., Hagopian S., Johnson-Wood K., Khan K., Lee M., Leibowitz E., McConlogue S., Montoya-Zavala M., Mucke L., Paganini L., Penniman E., Power M., Schenk D., Seubert P., Snyder B., Soriano F., Tan H., Vitale J., Wadsworth S., Wolozin B., and Zhao J. (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373, 523-527.
13. Gandy S. E., Bhasin R., Ramabhadran T. V., Koo E. H., Price D. L., Goldgaber D., and Greengard P. (1992) Alzheimer β/A4-amyloid precursor protein: evidence for putative amyloidogenic fragment. J. Neurochem. 58, 383-386.
14. Gardella J. E., Gorgone G. A., Newman P., Frangione B., and Gorevic P. D. (1992) Characterization of Alzheimer amyloid precursor protein transcripts in platelets and megakarocytes. Neurosci. Lett. 138, 229-232.
15. Ghiso J., Gardella J. E., Liem L., Gorevic P. D., and Frangione B. (1994) Characterization of a novel processing pathway for Alzheimer's amyloid β precursor protein. Neurosci. Lett. 171, 213-216.
16. Glenner G. G. and Wong C. W. (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120, 885-890.
17. Golde T. E., Estus S., Usiak M., Younkin L. H., and Younkin S. G. (1990) Expression of β amyloid protein precursor mRNAs: recognition of a novel alternatively spliced form and quantitation in Alzheimer's disease using PCR. Neuron 4, 253-267.
18. Hardy J. (1997) Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci. 20, 154-159.
19. Hilbich C., Kisters-Woike B., Reed J., Masters C. L., and Beyreuther K. (1991) Aggregation and secondary structure of synthetic amyloid βA4 peptides of Alzheimer's disease. J. Mol. Biol. 218, 149-163.
20. Hogan B., Costantini F., and Lacy E. (1986) Manipulating the Mouse Embryo. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
21. Hsiao K., Borchelt D. R., Olson K., Johannsdottir R., Kitt C., Yunis W., Xu S., Eckman C., Younkin S., Price D., Iadecola C., Clark H. B., and Carlson G. (1995) Age related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron 15, 1203-1218.
22. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F. S., and Cole G. (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274, 99-102.
23. Ida N., Hartmann T., Pantel J., Schroder J., Zerfass R., Forstl H., Sandbrink R., Masters C. L., and Beyreuther K. (1996) Analysis of heterogeneous βA4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive western blot assay. J. Biol. Chem. 271, 22908-22914.
24. Jarrett J. T., Berger E. P., and Lansbury P. T. Jr. (1993) The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32, 4693-4697.
25. 695 mRNA is predominantly produced in rat and human brain. Biochem. Biophys. Res. Commun. 166, 1192-1200.
26. Kang J., Lemaire H., Unterbeck A., Salbaum J. M., Masters C. L., Grzeschik K., Multhaup G., Beyreuther K., and Müller-Hill B. (1987) The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325, 733-736.
27. Klafki H. W., Abramowski D., Swoboda R., Paganetti P. A., and Staufenbiel M. (1996a) The carboxyl termini of β-amyloid peptides 1-40 and 1-42 are generated by distinct γ-secretase activities. J. Biol. Chem. 271, 28655-28659.
28. Klafki H. W., Wiltfang J., and Staufenbiel M. (1996b) Electrophoretic separation of βA4 peptides (1-40) and (1-42). Anal. Biochem. 237, 24-29.
29. Kuo Y. M., Emmerling M. R., Vigopelfrey C., Kasunic T. C., Kirkpatrick J. B., Murdoch G. H., Ball M. J., and Roher A. E. (1996) Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer disease brains. J. Biol. Chem. 271, 4077-4081.
30. Li Q.-X., Evin G., Small D. H., Multhaup G., Beyreuther K., and Masters C. L. (1995a) Proteolytic processing of Alzheimer's disease amyloid protein precursor in human platelets. J. Biol. Chem. 270, 14140-14147.
31. Li Q.-X., Whyte S., Birchall I., Beyreuther K., and Masters C. L. (1995b) The amyloid protein precursor of Alzheimer's disease in human platelets and kidney, in Non-Neuronal Cells in Alzheimer's Disease (Zatta P. and Nicolini M., eds), pp. 62-70. World Scientific, Singapore.
32. Li Q.-X., Cappai R., Evin G., Tanner J. E., Gray C. W., Beyreuther K., and Masters C. L. (1998a) Products of the Alzheimer's disease amyloid precursor protein generated by β-secretase are present in human platelets, and secreted upon degranulation. Am. J. Alzheimer's Dis. 13, 236-244.
33. Li Q.-X., Whyte S., Tanner J. E., Evin G., Beyreuther K., and Masters C. L. (1998b) Secretion of Alzheimer's disease Aβ amyloid peptide by activated human platelets. Lab. Invest. 78, 461-469.
34. Masters C. L., Multhaup G., Simms G., Pottgiesser J., Martíns R. N., and Beyreuther K. (1985) Neuronal origin of a cerebral amyloid: neurofibrillary tangles of Alzheimer's disease contain the same protein as the amyloid of plaque cores and blood vessels. EMBO J. 4, 2757-2763.
35. McPhie D. L., Lee R. K. K., Eckman C. B., Olstein D. H., Durham S .P., Yager D., Younkin S. G., Wurtman R. J., and Neve R. L. (1997) Neuronal expression of β-amyloid precursor protein Alzheimer mutations causes intracellular accumulation of a C-terminal fragment containing both the amyloid β and cytoplasmic domains. J. Biol. Chem. 272, 24743-24746.
36. Moir R. D., Martins R. N., Bush A. I., Small D. H., Milward E. A., Rumble B. A., Multhaup G., Beyreuther K., and Masters C. L. (1992) Human brain βA4 amyloid protein precursor of Alzheimer's disease: purification and partial characterization. J. Neurochem. 59, 1490-1498.
37. Morishima-Kawashima M. and Ihara Y. (1998) The presence of amyloid β-protein in the detergent-insoluble membrane compartment of human neuroblastoma cells. Biochemistry 37, 15247-15235.
38. Nalbantoglu J., Tiradosantiago G., Lahsaini A., Poirier J., Goncalves O., Verge A., Momoli F., Welner S. A., Massicotte G., Julien J. P., and Shapiro M. L. (1997) Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature 387, 500-505.
39. Neve R. L., Boyce F. M., McPhie D. L., Greenan J., and Oster-Granite M. L. (1996) Transgenic mice expressing APP-C100 in the brain. Neurobiol. Aging 17, 191-203.
40. Oster-Granite M. L., McPhie D. L., Greenan J., and Neve R. L. (1996) Age-dependent neuronal and synaptic degeneration in mice transgenic for the C terminus of the amyloid precursor protein. J. Neurosci. 16, 6732-6741.
41. Ouimet C. C., Baerwald K. D., Gandy S. E., and Greengard P. (1994) Immunocytochemical localization of amyloid precursor protein in rat brain. j. Comp. Neurol. 348, 244-260.
42. Roher A. E., Lowenson J. D., Clarke S., Wolkow C., Wang R., Cotter R. J., Reardon I. M., Zürcher-Neely H. A., Heinrikson R. L., Ball M. J., and Greenberg B. D. (1993) Structural alterations in the peptide backbone of β-amyloid core protein may account for its deposition and stability in Alzheimer's disease. J. Biol. Chem. 268, 3072-3083.
43. Roher A. E., Chaney M. O., Kuo Y. M., Webster S. D., Stine W. B., Haverkamp L. J., Woods A. S., Cotter R. J., Tuohy J. M., Krafft G. A., Bonnell B. S., and Emmerling M. R. (1996) Morphology and toxicity of Aβ-(1-42) dimer derived from neuritic and vascular amyloid deposits of Alzheimer's disease. J. Biol. Chem. 271, 20631-20635.
44. Sberna G., Sáez-Valero J., Li Q.-X., Czech C., Beyreuther K., Masters C. L., McLean C. A., and Small D. H. (1998) Acetylcholinesterase is increased in the brains of transgenic mice expressing the C-terminal fragment (CT100) of the β-amyloid protein precursor of Alzheimer's disease. J. Neurochem. 71, 723-731.
45. Seubert P., Oltersdorf T., Lee M. G., Barbour R., Blomquist C., Davis D. L., Bryant K., Britz L. C., Galasko D., Thai L. J., Lieberburg I., and Schenk D. B. (1993) Secretion of β-amyloid precursor protein cleaved at the amino terminus of the β-amyloid peptide. Nature 361, 260-263.
46. Simons M., De Strooper B., Multhaup G., Tienar 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.
47. Sisodia S. S., Koo E. H., Beyreuther K., Unterbeck A., and Price D. L. (1990) Evidence that β-amyloid protein in Alzheimer's disease is not derived by normal processing. Science 248, 492-495.
48. Sopher B. L., Fukuchi K., Smith A. C., Leppig K. A., Furlong C. E., and Martin G. M. (1994) Cytotoxicity mediated by conditional expression of a carboxyl-terminal derivative of β-amyloid precursor protein. Mol. Brain Res. 26, 207-217.
49. Sturchler-Pierrat C., Abramowski D.; Duke M., Wiederhold K. H., Mistl C., Rothacher S., Ledermann B., Burki K., Frey P., Paganetti P. A., Waridel C., Calhoun M. E., Jucker M., Probst A., Staufenbiel M., and Sommer B. (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc. Natl. Acad. Sci. USA 94, 13287-13292.
50. Suzuki N., Cheung T. T., Cai X. D., Odaka A., Otvos L. Jr., Eckman C., Golde T. E., and Younkin S. G. (1994) An increased percentage of long amyloid β protein secreted by familial amyloid β protein precursor (βAPP717) mutants. Science 264, 1336-1340.
51. Vassilacopoulou D., Ripellino J. A., Tezapsidis N., Hook V. Y. H., and Robakis N. K. (1995) Full-length and truncated Alzheimer's amyloid precursors in chromaffin granules: solubilization of membrane amyloid precursor is mediated by an enzyme mechanism. J. Neurochem. 64, 2140-2146.
52. Yankner B. A., Dawes L. R., Fisher S., Villa-Komaroff L., Oster-Granite M. L., and Neve R. L. (1989) Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease. Science 245, 417-420.