BACE1 Deficiency Rescues Memory Deficits and Cholinergic Dysfunction in a Mouse Model of Alzheimer's Disease

Neuron

Volumn 41, Issue 1, 2004, Pages 27-33

  Ohno, Masuo ^a   Sametsky, Evgeny A ^a   Younkin, Linda H ^b   Oakley, Holly ^a   Younkin, Steven G ^b   Citron, Martin ^c   Vassar, Robert ^a   Disterhoft, John F ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b MAYO CLINIC   (United States)

^c AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN DYSFUNCTION; BRAIN ELECTROPHYSIOLOGY; CHOLINERGIC ACTIVITY; CHOLINERGIC SYSTEM; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE MODEL; DRUG TARGETING; GENE OVEREXPRESSION; GENETIC ENGINEERING; HIPPOCAMPUS; MALE; MEMORY DISORDER; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEFICIENCY; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM;

EID: 0346055155     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00810-9     Document Type: Article

References (61)

1. Ashe K.H. Learning and memory in transgenic mice modeling Alzheimer's disease. Learn. Mem. 8:2001;301-308.
2. Auld D.S., Kar S., Quirion R. β-amyloid peptides as direct cholinergic neuromodulators. a missing link? Trends Neurosci. 21:1998;43-49.
3. Cai H., Wang Y., McCarthy D., Wen H., Borchelt D.R., Price D.L., Wong P.C. BACE1 is the major β-secretase for generation of Aβ peptides by neurons. Nat. Neurosci. 4:2001;233-234.
4. Citron M. Alzheimer's disease. treatments in discovery and development Nat. Neurosci. 5:2002;1055-1057.
5. + currents Neurosci. Lett. 209:1996;49-52.
6. Coyle J.T., Price D.L., DeLong M.R. Alzheimer's disease. a disorder of cortical cholinergic innervation Science. 219:1983;1184-1190.
7. Dewachter I., Reverse D., Caluwaerts N., Ris L., Kuiperi C., Van Den Haute C., Spittaels K., Umans L., Serneels L., Thiry E.et al. Neuronal deficiency of presenilin 1 Inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V717I] transgenic mice. J. Neurosci. 22:2002;3445-3453.
8. Dineley K.T., Xia X., Bui D., Sweatt J.D., Zheng H. Accelerated plaque accumulation, associative learning deficits, and up-regulation of α7 nicotinic receptor protein in transgenic mice co-expressing mutant human presenilin 1 and amyloid precursor proteins. J. Biol. Chem. 277:2002;22768- 22780.
9. Dodart J.C., Bales K.R., Gannon K.S., Greene S.J., DeMattos R.B., Mathis C., DeLong C.A., Wu S., Wu X., Holtzman D.M., Paul S.M. Immunization reverses memory deficits without reducing brain Aβ burden in Alzheimer's disease model. Nat. Neurosci. 5:2002;452-457.
10. Dodel R.C., Hampel H., Du Y. Immunotherapy for Alzheimer's disease. Lancet Neurol. 2:2003;215-220.
11. Duff K., Eckman C., Zehr C., Yu X., Prada C.M., Perez-tur J., Hutton M., Buee L., Harigaya Y., Yager D.et al. Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1. Nature. 383:1996;710-713.
12. Ferguson J.N., Young L.J., Insel T.R. The neuroendocrine basis of social recognition. Front. Neuroendocrinol. 23:2002;200-224.
13. Gong Y., Chang L., Viola K.L., Lacor P.N., Lambert M.P., Finch C.E., Krafft G.A., Klein W.L. Alzheimer's disease-affected brain. presence of oligomeric Aβ ligands (ADDLs) suggests a molecular basis for reversible memory loss Proc. Natl. Acad. Sci. USA. 100:2003;10417-10422.
14. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease. progress and problems on the road to therapeutics Science. 297:2002;353-356.
15. Hartley D.M., Walsh D.M., Ye C.P., Diehl T., Vasquez S., Vassilev P.M., Teplow D.B., Selkoe D.J. Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J. Neurosci. 19:1999;8876-8884.
16. Hock C., Konietzko U., Streffer J.R., Tracy J., Signorell A., Muller-Tillmanns B., Lemke U., Henke K., Moritz E., Garcia E.et al. Antibodies against β-amyloid slow cognitive decline in Alzheimer's disease. Neuron. 38:2003;547-554.
17. Holcomb L., Gordon M.N., McGowan E., Yu X., Benkovic S., Jantzen P., Wright K., Saad I., Mueller R., Morgan D.et al. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat. Med. 4:1998;97-100.
18. Holcomb L.A., Gordon M.N., Jantzen P., Hsiao K., Duff K., Morgan D. Behavioral changes in transgenic mice expressing both amyloid precursor protein and presenilin-1 mutations. lack of association with amyloid deposits Behav. Genet. 29:1999;177-185.
19. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science. 274:1996;99-102.
20. Huang H.M., Ou H.C., Hsieh S.J. Amyloid beta peptide impaired carbachol but not glutamate-mediated phosphoinositide pathways in cultured rat cortical neurons. Neurochem. Res. 25:2000;303-312.
21. Hussain I., Powell D., Howlett D.R., Tew D.G., Meek T.D., Chapman C., Gloger I.S., Murphy K.E., Southan C.D., Ryan D.M.et al. Identification of a novel aspartic protease (Asp 2) as β-secretase. Mol. Cell. Neurosci. 14:1999;419-427.
22. Janus C., Westaway D. Transgenic mouse models of Alzheimer's disease. Physiol. Behav. 73:2001;873-886.
23. John V., Beck J.P., Bienkowski M.J., Sinha S., Heinrikson R.L. Human β-secretase (BACE) and BACE inhibitors. J. Med. Chem. 46:2003;4625-4630.
24. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron. 37:2003;925-937.
25. Kawarabayashi T., Younkin L.H., Saido T.C., Shoji M., Ashe K.H., Younkin S.G. Age-dependent changes in brain, CSF, and plasma amyloid β protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J. Neurosci. 21:2001;372-381.
26. Kelly J.F., Furukawa K., Barger S.W., Rengen M.R., Mark R.J., Blanc E.M., Roth G.S., Mattson M.P. Amyloid β-peptide disrupts carbachol-induced muscarinic cholinergic signal transduction in cortical neurons. Proc. Natl. Acad. Sci. USA. 93:1996;6753-6758.
27. Kitazume S., Tachida Y., Oka R., Shirotani K., Saido T.C., Hashimoto Y. Alzheimer's β-secretase, β-site amyloid precursor protein-cleaving enzyme, is responsible for cleavage secretion of a Golgi-resident sialyltransferase. Proc. Natl. Acad. Sci. USA. 98:2001;13554-13559.
28. Kogan J.H., Frankland P.W., Silva A.J. Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus. 10:2000;47-56.
29. Lalonde R. The neurobiological basis of spontaneous alternation. Neurosci. Biobehav. Rev. 26:2002;91-104.
30. 1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA. 95:1998;6448-6453.
31. 4 receptor agonists, modulate spontaneous alternation deficits induced by scopolamine in the mouse. Naunyn Schmiedebergs Arch. Pharmacol. 367:2003;621-628.
32. Lin X., Koelsch G., Wu S., Downs D., Dashti A., Tang J. Human aspartic protease memapsin 2 cleaves the β-secretase site of β-amyloid precursor protein. Proc. Natl. Acad. Sci. USA. 97:2000;1456-1460.
33. Luo Y., Bolon B., Kahn S., Bennett B.D., Babu-Khan S., Denis P., Fan W., Kha H., Zhang J., Gong Y.et al. Mice deficient in BACE1, the Alzheimer's β-secretase, have normal phenotype and abolished β-amyloid generation. Nat. Neurosci. 4:2001;231-232.
34. Luo Y., Bolon B., Damore M.A., Fitzpatrick D., Liu H., Zhang J., Yan Q., Vassar R., Citron M. BACE1 (β-secretase) knockout mice do not acquire compensatory gene expression changes or develop neural lesions over time. Neurobiol. Dis. 14:2003;81-88.
35. Mallucci G.R., Ratte S., Asante E.A., Linehan J., Gowland I., Jefferys J.G., Collinge J. Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 21:2002;202-210.
36. Miller B.C., Eckman E.A., Sambamurti K., Dobbs N., Chow K.M., Eckman C.B., Hersh L.B., Thiele D.L. Amyloid-β peptide levels in brain are inversely correlated with insulysin activity levels in vivo. Proc. Natl. Acad. Sci. USA. 100:2003;6221-6226.
37. Nalbantoglu J., Tirado-Santiago G., Lahsaini A., Poirier J., Goncalves O., Verge G., Momoli F., Welner S.A., Massicotte G., Julien J.P., Shapiro M.L. Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature. 387:1997;500-505.
38. Nicoll J.A., Wilkinson D., Holmes C., Steart P., Markham H., Weller R.O. Neuropathology of human Alzheimer disease after immunization with amyloid-β peptide. a case report Nat. Med. 9:2003;389-390.
39. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles. intracellular Aβ and synaptic dysfunction Neuron. 39:2003;409-421.
40. Roberds S.L., Anderson J., Basi G., Bienkowski M.J., Branstetter D.G., Chen K.S., Freedman S.B., Frigon N.L., Games D., Hu K.et al. BACE knockout mice are healthy despite lacking the primary β-secretase activity in brain. implications for Alzheimer's disease therapeutics Hum. Mol. Genet. 10:2001;1317-1324.
41. Saar D., Grossman Y., Barkai E. Long-lasting cholinergic modulation underlies rule learning in rats. J. Neurosci. 21:2001;1385-1392.
42. Savage L.M., Chang Q., Gold P.E. Diencephalic damage decreases hippocampal acetylcholine release during spontaneous alternation testing. Learn. Mem. 10:2003;242-246.
43. Schenk D. Amyloid-β immunotherapy for Alzheimer's disease. the end of the beginning Nat. Rev. Neurosci. 3:2002;824-828.
44. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science. 298:2002;789-791.
45. Selkoe D.J., Schenk D. Alzheimer's disease. molecular understanding predicts amyloid-based therapeutics Annu. Rev. Pharmacol. Toxicol. 43:2003;545-584.
46. Sinha S., Anderson J.P., Barbour R., Basi G.S., Caccavello R., Davis D., Doan M., Dovey H.F., Frigon N., Hong J.et al. Purification and cloning of amyloid precursor protein β-secretase from human brain. Nature. 402:1999;537-540.
47. Suh Y.H. An etiological role of amyloidogenic carboxyl-terminal fragments of the β-amyloid precursor protein in Alzheimer's disease. J. Neurochem. 68:1997;1781-1791.
48. Tang J., Ghosh A.K., Hong L., Koelsch G., Turner R.T., Chang W. Study of memapsin 2 (β-secretase) and strategy of inhibitor design. J. Mol. Neurosci. 20:2003;299-304.
49. Tran M.H., Yamada K., Nabeshima T. Amyloid β-peptide induces cholinergic dysfunction and cognitive deficits. a minireview Peptides. 23:2002;1271-1283.
50. Turner P.R., O'Connor K., Tate W.P., Abraham W.C. Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog. Neurobiol. 70:2003;1-32.
51. Vassar R., Citron M. Aβ-generating enzymes. recent advances in β- and γ-secretase research Neuron. 27:2000;419-422.
52. Vassar R., Bennett B.D., Babu-Khan S., Kahn S., Mendiaz E.A., Denis P., Teplow D.B., Ross S., Amarante P., Loeloff R.et al. β-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science. 286:1999;735-741.
53. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature. 416:2002;535-539.
54. Westerman M.A., Cooper-Blacketer D., Mariash A., Kotilinek L., Kawarabayashi T., Younkin L.H., Carlson G.A., Younkin S.G., Ashe K.H. The relationship between Aβ and memory in the Tg2576 mouse model of Alzheimer's disease. J. Neurosci. 22:2002;1858-1867.
55. Winslow J.T., Camacho F. Cholinergic modulation of a decrement in social investigation following repeated contacts between mice. Psychopharmacology (Berl.). 121:1995;164-172.
56. Wolfe M.S. Therapeutic strategies for Alzheimer's disease. Nat. Rev. Drug Discov. 1:2002;859-866.
57. Wong P.C., Cai H., Borchelt D.R., Price D.L. Genetically engineered mouse models of neurodegenerative diseases. Nat. Neurosci. 5:2002;633-639.
58. Wu W.W., Oh M.M., Disterhoft J.F. Age-related biophysical alterations of hippocampal pyramidal neurons. implications for learning and memory Ageing Res. Rev. 1:2002;181-207.
59. Yan R., Bienkowski M.J., Shuck M.E., Miao H., Tory M.C., Pauley A.M., Brashier J.R., Stratman N.C., Mathews W.R., Buhl A.E.et al. Membrane-anchored aspartyl protease with Alzheimer's disease β-secretase activity. Nature. 402:1999;533-537.
60. Yu H., Saura C.A., Choi S.Y., Sun L.D., Yang X., Handler M., Kawarabayashi T., Younkin L., Fedeles B., Wilson M.A.et al. APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron. 31:2001;713-726.
61. Zhong P., Gu Z., Wang X., Jiang H., Feng J., Yan Z. Impaired modulation of GABAergic transmission by muscarinic receptors in a mouse transgenic model of Alzheimer's disease. J. Biol. Chem. 278:2003;26888-26896.