Artifactual strain-specific signs of incipient brain amyloidosis in APP transgenic mice

Neurobiology of Aging

Volumn 17, Issue 2, 1996, Pages 223-234

  Ali, S M ^a,d   Siedlak, S L ^b   Gonzalez DeWhitt, P A ^a,c   Altman, R A ^a,f   Glendening, J M ^a,g   Lowery, D E ^a   Savage, M J ^c   Polites, H G ^a,e   Perry, G ^b   Greenberg, B D ^a,c  

^a PFIZER INC   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c CEPHALON INC   (United States)

^d GLAXOSMITHKLINE   (United Kingdom)

^e SANOFI   (France)

^f BAYER AG   (Germany)

^g UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Alzheimer's Discase; Amyloid precursor protein; A ; Immunocytochemistry; In situ hybridization; Pathology

Indexed keywords

AMYLOID PRECURSOR PROTEIN;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

EID: 0029951778     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/0197-4580(95)02065-9     Document Type: Article

References (70)

1. Bahmanyar, S.; Higgins, G. A.; Goldgaber, D.; Lewis, D. A.; Morrison, J. H.; Wilson, M. C.; Shankar, S. K.; Gajdusek, D. C. Localization of amyloid protein messenger RNA in brains from patients with Alzheimer's disease. Science 237:77-80; 1987.
2. Brinster, R. L.; Allen, J. M.; Behringer, R. R.; Gelinas, R. E.; Palmiter, R. D. Introns increase transcriptional efficiency in transgenic mice. Proc. Natl. Acad. Sci. USA 85:836-840; 1988.
3. Busciglio, J.; Gabuzda, D. H.; Matsudaira, P.; Yankner, B. A. Generation of β-amyloid in the secretory pathway in neuronal and nonneuronal cells. Proc. Natl. Acad. Sci. USA 90:2092-2096; 1993.
4. Cai, X. D.; Golde, T. E.; Younkin, S. G. Release of excess amyloid β protein from a mutant amyloid β protein precursor. Science 259:514-516; 1993.
5. Chartier-Harlin, M.-C.; Crawford, F.; Houlden, H.; Warren, A.; Hughes, D.; Fidani, L.; Goate, A.; Rossor, M.; Roques, P.; Hardy, J.; Mullan, M. Early onset Alzheimer's disease caused by mutations at codon 717 of the β-amyloid precursor protein gene. Nature 353:844-846; 1991.
6. Choi, T.; Huang, M.; Gorman, C.; Jaenisch, R. A generic intron increases gene expression in transgenic mice. Mol. Cell. Biol. 11:3070-3074; 1991.
7. Chomczynski, P.; Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159; 1987.
8. Citron, M.; Oltersdorf, T.; Haass, C.; McConlogue, L.; Hung, A. Y.; Seubert, P.; Vigo-Pelfrey, C.; Lieberburg, I.; Selkoe, D. J. Mutation of the β-amyloid precursor protein in familial Alzheimer's disease increases β-protein production. Nature 360:672-674; 1992.
9. Citron, M.; Vigo-Pelfrey, C.; Teplow, D. B.; Miller, C.; Schenk, D.; Johnston, J.; Winblad, B.; Venizelos, N.; Lannfelt, L.; Selkoe, D. J. Excessive production of amyloid β-protein by peripheral cells of symptomatic and presymptomatic patients carrying the Swedish familial Alzheimer disease mutation. Proc. Natl. Acad. Sci. USA 91:11993-11997; 1994.
10. Citron, M.; Teplow, D. B.; Selkoe, D. J. Generation of amyloid protein from its precursor is sequence specific. Neuron 14:661-670; 1995.
11. Coria, F.; Moreno, A.; Torres, A.; Ahmad, I.; Ghiso, J. Distribution of Alzheimer's disease amyloid protein precursor in normal human and rat nervous system. Neuropathol. Appl. Neurobiol. 18:27-35; 1992.
12. Cotner, T.; Pious, D. HLA-DR beta chains enter into an aggregated complex containing GRP-78/BiP prior to their degradation by the pre-Golgi degradative pathway. J. Biol. Chem. 270:2379-2386; 1995.
13. Cras, P.; Kawai, M.; Siedlak, S.; Mulvihill, P.; Gambetti, P.; Lowery, D.; Gonzalez-DeWhitt, P.; Greenberg, B.; Perry, G. Neuronal and microglial involvement in β-amyloid protein deposition in Alzheimer's disease. Am. J. Pathol. 137:241-246; 1990.
14. Cummings, B. J.; Su, J. H.; Geddes, J. W.; Van Nostrand, W. E.; Wagner, S. L.; Cunningham. D. D.; Cotman. C. W. Aggregation of the amyloid precursor protein within degenerating neurons and dystrophic neuntes in Alzheimer's disease. Neuroscience 48:763-777; 1992.
15. De Strooper, B.; Craessaerts, K.; Dewachter, I.; Moechars, D.; Greenberg, B.; Van Leuven, F.; Van Den Berghe, H. 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; 1995.
16. Dovey, H. F.; Suomensaari-Chrysler, S.; Lieberburg, I.; Sinha, S.; Keim, P. S. Cells with a familial Alzheimer's disease mutation produce authentic β-peptide. NeuroReport 4:1039-1042; 1993.
17. Evans, R. M; Weinberger, C.; Hollenberg, S.; Swanson, L.; Nelson, C.; Rosenfeld, M. G. Inducible and developmental control of neuroendocrine genes. Cold Spring Harb. Symp. Quant. Biol. 50:389-397; 1985.
18. Gabuzda, D.; Busciglio, J.; Chen, L. B.; Matsudaira, P.; Yankner, B. A. Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative. J. Biol. Chem. 269:13623-13628; 1994.
19. 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.; Liebowitz, P.; Lieberburg, I.; Little, S.; Masliah, E.; McConlogue, L.; 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.; Zhao, J. Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373:523-527; 1995.
20. Goate, A.; Chartier-Harlin, M.-C.; Mullan, M.; Brown, J.; Crawford, F.; Fidani, L.; Giuffra, L.; Haynes, A.; Irving, N.; James, L.; Mant, R.; Newton, P.; Rooke, K.; Roques, P.; Talbot, C.; Pericak-Vance, M.; Roses, A.; Williamson, R.; Rossor, M.; Owen, M.; Hardy, J. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349:704-706; 1991.
21. Goedert, M. Neuronal localization of amyloid beta protein precursor mRNA in normal human brain and in Alzheimer's disease. EMBO J. 6:3627-3632; 1987.
22. Goldgaber, D.; Lerman, M. I.; McBride, O. W.; Saffioti, U.; Gajdusek, D. C. Characterization and chromosomal localization of a cDNA encoding brain amyloid of Alzheimer's disease. Science 235:877-880; 1987.
23. Greenberg, B. D.; Kezdy, F. J.; Kisilevsky, R. Amyloidogenesis as a therapeutic target in Alzheimer's Disease. Ann. Rep. Med. Chem. 26:229-238; 1991.
24. Greenberg, B. D. Differences in the length of the A COOH-terminus influence the process of amyloid deposition in Alzheimer brain, and tell us something about relationships among parenchymal and vessel-associated amyloid deposits. Amyloid: Int. J. Exp. Clin. Invest. 2: 195-203; 1995
25. Haass, C.; Selkoe, D. J. Cellular processing of β-amyloid precursor protein and the genesis of amyloid β-peptide. Cell 75:1039-1042; 1993.
26. Haass, C.; Hung, A. Y.; Selkoe, D. J.; Teplow, D. B. Mutations associated with a locus for familial Alzheimer's disease result in alternative processing of amyloid β-protein precursor. J. Biol. Chem. 269:17741-17748; 1994.
27. Hanger, D. P.; Mann, D. M. A.; Neary, D.; Anderton, B. H. Molecular pathology of Alzheimer's disease in sporadic and familial Alzheimer's disease with mutations in the amyloid precursor protein. Biochem. Soc. Trans. 20:642-645; 1992.
28. Higaki, J.; Quon, D.; Zhong, Z.; Cordell, B. Inhibition of β-amyloid formation identifies proteolytic precursors and subcellular site of catabolism. Neuron 14:651-659; 1995.
29. Hogan, B.; Costantini, F.; Lacy, E. Manipulating the mouse embryo. Cold Spring Harbor Laboratory, NY: Cold Spring Harbor Laboratory Press; 1986.
30. Howland, D. S.; Greenberg, B. D.; Savage, M. J.; Siman, R.; Scott, R. W. Author's response to commentaries. Neurobiol. Aging 16:715-718; 1995.
31. Iwatsubo, T.; Okada, A.; Suzuki, N.; Mizusawa, H.; Nukina, N.; Ihara, Y. Visualization of Aβ42(43) and Aβ40 in senile plaques with end-specific Aβ monoclonals: Evidence that an initially deposited species is Aβ42(43). Neuron 13:45-53; 1994.
32. Johnston, J. A.; Cowburn, R. F.; Norgren, S.; Wiehager, B.; Venizelos, N.; Winblad, B.; Vigo-Pelfrey, C.; Schenk, D.; Lannfelt, L.; O'Neill, C. Increased β-amyloid release and levels of amyloid precursor protein (APP) in fibroblast cell lines from family members with the Swedish Alzheimer's disease APP670/671 mutation. FEBS Lett. 354:274-278; 1994.
33. Kang, J.; Lemaire, H.-G.; Unterbeck, A.; Salbaum, J, M.; Masters, C. L.; Grzeschik, K.-H.; Multhaup, G.; Beyreuther, K.; Müller-Hill, B. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325:733-736; 1987.
34. Kelder, B.; Chen, H.; Kopchick, J. J. Activation of the mouse metallothionein-I promoter in transiently transfected avian cells. Gene 76: 75-80; 1989.
35. Klausner, R. D.; Sitia, R. Protein degradation in the endoplasmic reticulum. Cell 62:611-614; 1990.
36. Knittler, M. R.; Dirks, S.; Haas, I. G. Molecular chaperones involved in protein degradation in the endoplasmic reticulum: Quantitative interaction of the heat shock cognate protein BiP with partially folded immunoglobulin light chains that are degraded in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 92:1764-1768; 1995.
37. Knops, J.; Suomensaari, S.; Lee, M.; McConlogue, L.; Seubert, P.; Sinha, S. Cell-type and amyloid precursor protein-type specific inhibition of Aβ release by bafilomycin A1, a selective inhibitor of vacuolar ATPases. J. Biol. Chem. 270:2419-2422; 1995.
38. Koo, E. H.; Squazzo, S. L. Evidence that production and release of amyloid β-protein involves the endocytic pathway. J. Biol. Chem. 269:17386-17389; 1994.
39. Kuentzel, S. L.; Greenberg, B. D.; Gonzalez-DeWhitt, P. A.; Lowery, D. E.; Raub, T. J. Overexpression of a C-terminal fragment of β-amyloid protein precursor in HeLa cells results in accumulation in a pre-Golgi compartment and generation of A4. Amyloid: Int. J. Exp. Clin. Invest. (in press).
40. LaFerla, F. M.; Tinkle, B. T.; Bieberich, C. J.; Haudenschild, C. C.; Jay, G. The Alzheimer's AB peptide induces neurodegeneration and apoptotic cell death in transgenic mice. Nat. Genet. 9:21-29; 1995.
41. Lamb, B. T.; Sisodia, S. S.; Lawler, A. M.; Slunt, H. H.; Kitt, C. A.; Kearns, W. G.; Pearson, P. L.; Price, D. L.; Gearhart, J. D. Introduction and expression of the 400 kilobase precursor amyloid protein gene in transgenic mice. Nat. Genet. 5:22-30; 1993.
42. Lannfelt, L.; Bogdanovic, N.; Appelgren, H.; Axelman, K.; Lilius, L.; Hansson, G.; Schenk, D.; Hardy, J.; Winblad, B. Amyloid precursor protein mutation causes Alzheimer's disease in a Swedish family. Neurosci. Lett. 168:254-256; 1994.
43. Liepnieks, J. J.; Ghetti, B.; Farlow, M.; Roses, A. D.; Benson, M. D. Characterization of amyloid fibril β-peptide in familial Alzheimer's disease with APP717 mutations. Biochem. Biophys. Res. Commun. 197:386-392; 1993.
44. Lowery, D. E.; Pasternack, J.; Gonzalez-DeWhitt, P. A.; Zürcher-Neely, H.; Tomich, C.-S. C.; Altman, R. A.; Fairbanks, M. B.; Heinrikson, R. L.; Younkin, S.; Greenberg, B. D. Alzheimer amyloid precursor protein produced by recombinant baculovirus expression: Proteolytic processing and protease inhibitory properties. J. Biol. Chem. 266:19842-19850; 1991.
45. Mann, D. M. A. The pathologic association between Down's syndrome and Alzheimer's disease. Mech. Ageing Dev. 43:99-136; 1988.
46. Mullan, M.; Crawford, F.; Axelman, K.; Houlden, H.; Lilus, L.; Winblad, B.; Lannfelt, L. A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of β-amyloid. Nat. Genet. 1:345-347; 1992.
47. Murrell, J.; Farlow, M.; Ghetti, B.; Benson, M. D. A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease. Science 254:97-99; 1991.
48. Neve, R. L.; Finch, E. A.; Dawes, L. R. Expression of the Alzheimer amyloid precursor protein gene transcripts in the human brain. Neuron 1:669-677; 1988.
49. Palmiter, R. D.; Sandgren, E. P.; Avarbock, M. R.; Allen, D. D.; Brinster, R. L. Heterologous introns can enhance expression of transgenes in mice. Proc. Natl. Acad. Sci. USA 88:478-482; 1991.
50. Pearson, B. E.; Choi, T. K. Expression of the human beta-amyloid precursor protein gene from a yeast artificial chromosome in transgenic mice. Proc. Natl. Acad. Sci. USA 90:10578-10582; 1993.
51. Pelham, H. R. Control of protein exit from the endoplasmic reticulum. Annu. Rev. Cell Biol. 5:1-23; 1989.
52. Russo, A. F.; Crenshaw, B. E.; Lira, S. A.; Simmons, D. M.; Swanson, L. W.; Rosenfeld, M. G. Neuronal expression of chimeric genes in transgenic mice. Neuron 1:311-320; 1988.
53. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular cloning. A laboratory manual, 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989.
54. Savage, M. J.; Howland, D. S.; Ali, S. M.; Siedlak, S.; Perry, G.; Siman, R.; Scott, R. W.; Greenberg, B. D. APP transgenesis: Approaches toward the development of animal models for Alzheimer disease neuropathology. In: Dawbarn, D.; Allen, S., eds. Neurobiology of Alzheimer's disease. Oxford: BIOS Scientific Publishers, Ltd.; (in press).
55. 42 in cerebrovascular deposits. Amyloid: Int. J. Exp. Clin. Invest. 2:234-240; 1995.
56. Schellenberg, G. D.; Bird, T. D.; Wijsman, E. M.; Orr, H. T.; Anderson, L.; Nemens, E.; White, J. A.; Bonnycastle, L.; Weber, J. L.; Alonson, M. E.; Potter, H.; Heston, L. L.; Martin, G. M. Genetic linkage evidence for a familial Alzheimer's disease locus on chromosome 14. Science 258:668-671; 1992.
57. Selkoe, D. J. The molecular pathology of Alzheimer's disease. Neuron 6:487-498; 1991.
58. Selkoe, D. J. Physiological production of the β-amyloid protein and the mechanism of Alzheimer's disease. Trends Neurosci. 16:403-409; 1993.
59. Seubert, P.; Vigo-Pelfrey, C.; Esch, F.; Lee, M.; Dovey, H.; Davis, D.; Sinha, S.; Schlossmacher, M.; Whaley, J.; Swindlehurst, C.; McCormack, R.; Wolfert, R.; Selkoe, D.; Lieberburg, I.; Schenk, D. Isolation and quantification of soluble Alzheimer's β-peptide from biological fluids. Nature 359:325-327; 1992.
60. Shigematsu, K.; McGeer, P. L. Accumulation of amyloid precursor protein in neurons after intraventricular injection of colchicine. Am. J. Pathol. 140:787-794; 1992.
61. Shoji, M.; Golde, T. E.; Ghiso, J.; Cheung, T. T.; Estus, S.; Shaffer, L. M.; Cai, X.-D.; McKay, D. M.; Tintner, R.; Frangione, B.; Younkin, S. G. Production of the Alzheimer amyloid protein by normal proteolytic processing. Science 258:126-129; 1992.
62. Siman, R.; Mistretta, S.; Durkin, J. T.; Savage, M. J.; Loh, T.; Trusko, S.; Scott, R. W. Processing of the β-amyloid precursor: Multiple proteases generate and degrade potentially amyloidogenic fragments. J. Biol. Chem. 268:16602-16609; 1993.
63. Siman, R.; Greenberg B. D. Alzheimer's disease. In: Pullan, L.; Patel, J., eds. Neurotherapeutics: emerging strategies. Totowa, NJ: Humana Press; 1995:389-428.
64. Stem, R. A.; Ötvös, L.; Trojanowski, J. Q.; Lee, V. M.-Y. Monoclonal antibodies to a synthetic peptide homologous with the first 28 amino acids of Alzheimer's disease β-protein recognized amyloid and diverse glial and neuronal cell types in the central nervous system. Am. J. Pathol. 134:973-978; 1989.
65. Suzuki, N.; Cheung, T. T.; Cai, X.-D.; Odaka, A.; Ötvös, L.; Eckman, C.; Golde, T. E.; Younkin, S. G. An increased percentage of long amyloid β protein secreted by familial amyloid b protein precursor (βAPP717) mutants. Science 264:1336-1340; 1994.
66. Suzuki, N.; Iwatsubo, T.; Odaka, A.; Ishibashi, Y.; Kitada, C.; Ihara, Y. High tissue content of soluble β1-40 is linked to cerebral amyloid angiopathy. Am. J. Pathol. 145:452-460; 1994.
67. Suzuki, N.; Cheung, T. T.; Cai, X.-D.; Ötvös, L.; Gillespie, S. L.; Ho, L.; Eckman, C. B.; Golde, T. E.; Younkin, S. G. Factors affecting production of secreted amyloid β protein ending at Aβ42,43. Soc. Neurosci. Abstr. 20:437; 1994.
68. Swanson, L. W.; Simmons, D. M.; Arriza, J.; Hammer, R.; Brinster, R.; Rosenfeld, M. G.; Evans, R. M. Novel developmental specificity in the nervous system of transgenic animals expressing growth hormone fusion genes. Nature 317:363-366; 1985.
69. Tabaton, M.; Nunzi, M. G.; Xue, R.; Usiak, M.; Autilio-Gambetti, L.; Gambetti, P. Soluble amyloid β-protein is a marker of Alzheimer amyloid in brain but not cerebrospinal fluid. Biochem. Biophys. Res. Commun. 200:1592-1603; 1994.
70. Tamaoka, A.; Odaka, A.; Ishibashi, Y.; Usami, M.; Sahara, N.; Suzuki, N.; Nukina, N.; Mizusawa, H.; Shoji, S.; Kanazawa, I.; Mori, H. APP717 missense mutation affects the ratio of amyloid β protein species (Aβ1-42/43 and Aβ1-40) in familial Alzheimer's disease brain. J. Biol. Chem. 269:32721-32724; 1994.