Alzheimer's disease proteins in cerebellar and hippocampal synapses during postnatal development and aging of the rat

Neuroscience

Volumn 120, Issue 2, 2003, Pages 405-423

  Ribaut Barassin, C ^a   Dupont, J L ^a   Haeberle A M ^a   Bombarde, G ^a   Huber, G ^b   Moussaoui, S ^c   Mariani, J ^d   Bailly, Y ^a  

^a Centre de Neurochimie   (France)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c SANOFI   (France)

^d Groupe Enzymologie Moléculaire et Fonctionnelle   (France)

Author keywords

Amyloid precursor protein; Brain; Electron microscopy; Immunocytochemistry; Presenilins

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BRAIN PROTEIN; PRESENILIN 1; PRESENILIN 2; MEMBRANE PROTEIN;

AGING; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL ULTRASTRUCTURE; CEREBELLUM CORTEX; CONTROLLED STUDY; FLUORESCENCE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; QUALITATIVE ANALYSIS; RAT; SYNAPTIC MEMBRANE; UPREGULATION; ANIMAL; CELL COUNT; CELL CULTURE; CEREBELLUM; COMPARATIVE STUDY; DISEASE MODEL; ELECTRON MICROSCOPY; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INSTRUMENTATION; LONG EVANS RAT; METABOLISM; METHODOLOGY; NEWBORN; PATHOLOGY; SYNAPSE; TIME; ULTRASTRUCTURE;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; CELL COUNT; CELLS, CULTURED; CEREBELLUM; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; PRESENILIN-1; PRESENILIN-2; RATS; RATS, LONG-EVANS; SYNAPSES; TIME FACTORS;

EID: 0141957935     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00332-4     Document Type: Article

References (100)

1. Adams I. Plasticity of the synaptic contact zone following loss of synapses in the cerebral cortex of aging humans. Brain Res. 424:1987;343-351.
2. Allinquant B., Hantraye P., Mailleux P., Moya K., Bouillot C., Prochiantz A. Down-regulation of amyloid precursor protein inhibits neurite outgrowth in vitro. J Cell Biol. 128:1995;919-927.
3. Altman J., Bayer S. Development of the cerebellar system in relation to its evolution, structure and functions. 1997;CRC Press, Inc. Boca Raton.
4. Apert C., Czech C., Faivre-Bauman A., Loudes C., Pradier L., Epelbaum J. Profiles of amyloid precursor and presenilin 2-like proteins are correlated during development of the mouse hypothalamus. J Neuroendocrinol. 10:1998;101-109.
5. Bayer T.A., Cappai R., Masters C.L., Beyreuther K., Multhaup G. It all sticks together the APP-related family of proteins and Alzheimer's disease . Mol Psychiatry. 4:1999;524-528.
6. Bayer T.A., Paliga K., Wegen S., Wiestler O.D., Beyreuther K., Multhaup G. Amyloid precursor-like protein 1 accumulates in neuritic plaques in Alzheimer's disease. Acta Neuropathol (Berl). 94:1997;519-524.
7. Beeson J.G., Shelton E.R., Chan H.W., Gage F.H. Age and damage induces changes in amyloid protein precursor immunohistochemistry in the rat brain. J Comp Neurol. 342:1994;69-77.
8. Beher D., Elle C., Underwood J., Davis J.B., Ward R., Karran E., Masters C.L., Beyreuther K., Multhaup G. Proteolytic fragments of Alzheimer's disease associated proteins are present in synaptic organelles and growth cones membranes of rat brain. J Neurochem. 72:1999;1564-1573.
9. Berezovska O., Xia M., Page K., Wasco W., Tanzi R.E., Hyman B.T. Developmental regulation of presenilin mRNA expression parallels Notch expression. J Neuropath Exp Neurol. 56:1997;40-44.
10. Berezovska O., Jack C., Deng A., Gastineau N., Rebeck G.W., Hyman B.T. Notch1 and amyloid precursor protein are competitive substrates for presenilin 1-dependent gamma-secretase cleavage. J Biol Chem. 276:2001;30018-30023.
11. Blanchard V., Czech C., Bonici B., Clavel C., Gohin M., Dalet K., Revah F., Pradier L., Imperato A., Moussaoui S. Immunohistochemical analysis of presenilin 2 expression in the mouse brain, distribution pattern and co localization with PS1 protein. Brain Res. 758:1997;209-217.
12. Breen K.C., Bruce M., Anderton B.H. Beta amyloid precursor protein mediates neuronal cell-cell and cell-surface adhesion. J Neurosci Res. 28:1991;90-100.
13. Buxbaum J., Thinakaran G., Koliatsos V., O'Callahan J., Slunt H., Price D., Sisodia G. Alzheimer amyloid precursor protein in the rat hippocampus transport and processing through the perforant path . J Neurosci. 18:1998;9629-9637.
14. Capell A., Saffrich R., Olivi J.C., Meyn L., Watter J., Grunberg J., Matthews P., Nixon R., Dotti C., Haas C. Cellular expression and proteolytic processing of PS1 protein is developmentally regulated during neuronal differentiation. J Neurochem. 69:1997;2432-2440.
15. Capell A., Steiner H., Romig H., Keck S., Baader M., Grim M.G., Baumeister R., Haass C. Presenilin-1 differentially facilitates endoproteolysis of the beta-amyloid precursor protein and Notch. Nat Cell Biol. 2:2000;205-211.
16. Chapman P., White G., Jones M., Cooper-Blacketer D., Marshall V., Irizarry M., Younkin L., Good M., Bliss T., Hyman B., Younkin S., Hsiao K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci. 2:1999;271-276.
17. Chen S., Hillman D.E. Dying back of Purkinje cell dendrites with synapse loss in aging rats. J Neurocytol. 28:1999;187-196.
18. Cheng G., Yu Z., Zhou D., Mattson M.P. Phosphatidylinositol-3-kinase-Akt kinase and p42/p44 mitogen-activated protein kinases mediate neurotrophic and excitoprotective actions of a secreted form of amyloid precursor protein. Exp Neurol. 175:2002;407-414.
19. Chishti M. PS2 transgenes rescue skeletal abnormalities in PS1 knock out mice but not deficits in APP processing. Soc Neurosci Abstr USA. 25:1999;1856.
20. Choi J.H., Yu B.P. Brain synaptosomal aging free radicals and membrane fluidity . Free Radic Biol Med. 18:1995;133-139.
21. Coulson E.J., Paliga K., Beyreuther K., Masters C.L. What the evolution of the amyloid protein precursor tells us about its function. Neurochem Int. 36:2000;175-184.
22. Crain B.J., Hu W., Sze C.I., Slunt H.H., Koo E.H., Price D.L., Thinakaran G., Sisodia S.S. Expression and distribution of amyloid precursor protein-like protein-2 in Alzheimer's disease and in normal brain. Am J Pathol. 149:1996;1087-1095.
23. Davidsson P., Bogdanovic N., Lannfelt L., Blennow K. Reduced expression of amyloid precursor protein, presenilin-1 and rab3a in cortical brain regions in Alzheimer's disease. Dement Geriatr Cogn Disord. 12:2001;243-250.
24. Dawson G.R., Seabrook G.R., Zheng H., Smith D.W., Graham S., O'Dowd G., Bowery B.J., Boyce S., Trumbauer M.E., Chen H.Y., Van der Ploeg L.H., Sirinathsinghji D.J. Age related cognitive deficits, impaired long term potentiation and reduction in synaptic marker density in mice lacking the beta amyloid precursor protein. Neuroscience. 90:1999;1-13.
25. De Strooper B., Annaert W., Cupers P., Saftig P., Craessaerts K., Mumm J.S., Schroeter E.H., Schrijvers V., Wolfe M.S., Ray W.J., Goate A., Kopan R. A PS1 dependant gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 398:1999;518-522.
26. De Strooper B., Annaert W. Proteolytic processing and cell biological functions of the amyloid precursor protein. J Cell Sci. 113:2000;1857-1870.
27. Edbauer D., Winkler E., Haass C., Steiner H. Presenilin and nicastrin regulate each other and determine amyloid beta-peptide production via complex formation. Proc Natl Acad Sci USA. 99:2002;8666-8671.
28. Fakla I., Kovacs I., Yamaguchi H., Geula C., Kasa P. Expressions of amyloid precursor protein, synaptophysin and presenilin-1 in the different areas of the developing cerebellum of rat. Neurochem Int. 36:2000;143-151.
29. Francis R., McGrath G., Zhang J., Ruddy D.A., Sym M., Apfeld J., Nicoll M., Maxwell M., Hai B., Ellis M.C., Parks A.L., Xu W., Li J., Gurney M., Myers R.L., Himes C.S., Hiebsch R., Ruble C., Nye J.S., Curtis D. Aph-1 and pen-2 are required for Notch pathway signalling, gamma-secretase cleavage of beta APP, and presenilin protein accumulation. Dev Cell. 3:2002;6-7.
30. Gao Y., Pimplikar S.W. The γ-secretase-cleaved C-terminal fragment of amyloid precursor protein mediates signalling to the nucleus. Proc Natl Acad Sci USA. 98:2001;14979-14984.
31. Georgakopoulos A., Marambaud P., Friedrich V.L. Jr, Shioi J., Efthimiopoulos S., Robakis N.K. Presenilin-1 a component of synaptic and endothelial adherens junctions . Ann NY Acad Sci. 920:2000;209-214.
32. Giacchino J., Criado J.R., Games D., Henriksen S. In vivo synaptic transmission in young and aged amyloid precursor protein transgenic mice. Brain Res. 876:2000;185-190.
33. Handler M., Yang X., Shen J. Presenilin-1 regulates neuronal differentiation during neurogenesis. Development. 127:2000;2593-2606.
34. Heber S., Herms J., Gajic V., Hainfellner J., Aguzzi A., Rülicke T., Kretzschmar H., von Koch C., Sisodia S., Tremml P., Lipp H.-P., Wolfer D.P., Müller U. Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J Neurosci. 20:2000;7951-7963.
35. Heinonen O., Soininen H., Sorvari H., Kosunen O., Paljarvi L., Koivisto E., Riekkinen P. Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease. Neuroscience. 64:1995;375-384.
36. Higgins G.A., Oyler G.A., Neve R.L., Chen K.S., Gage F.H. Altered levels of amyloid precursor transcripts in the basal forebrain of behaviourally impaired aged rats. Proc Natl Acad Sci USA. 87:1990;3032-3036.
37. Hsu S.M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. J Histochem Cytochem. 29:1981;77-580.
38. Huber G., Martin J.R., Löffler J., Moreau J.L. Involvement of amyloid precursor protein in memory formation in the rat an indirect antibody approach . Brain Res. 603:1993;348-352.
39. Huber G., Bailly Y., Martin J., Mariani J., Brugg B. Synaptic APPs increase with learning capacity. Neuroscience. 80:1997;313-320.
40. Johnston J.A., Norgren S., Ravid R., Wasco W., Winblad B., Lannfelt L., Cowburn R.F. Quantification of APP and APLP2 mRNA in APOE genotyped Alzheimer's disease brains. Brain Res Mol Brain Res. 43:1996;85-95.
41. Jung S., Nalbantoglu J., Cashman N. Alzheimer's beta-amyloid precursor protein is expressed on the surface of immediately ex vivo brain cells a flow cytometric study . J Neurosci Res. 46:1996;336-348.
42. Kaufmann W.A., Barnas U., Humpel C., Nowakowski K., De Col C., Gurka P., Ransmayr G., Hinterhuber H., Winkler H., Marksteiner J. Synaptic loss reflected by secretoneurin-like immunoreactivity in the human hippocampus in Alzheimer's disease. Eur J Neurosci. 10:1998;1084-1094.
43. Kasa P., Papp H., Pakaski M. Presenilin-1 and its N-terminal and C-terminal fragments are transported in the sciatic nerve of rat. Brain Res. 909:2001;159-169.
44. Kim T.-W., Wu K., Xu J.-L., McAuliffe G., Tanzi R.E., Wasco W., Black I.B. Selective localization of amyloid precursor-like protein 1 in the cerebral cortex postsynaptic density. Mol Brain Res. 32:1995;36-44.
45. Kimberly W.T., Xia W., Rahmati T., Wolfe M.S., Selkoe D.J. The transmembrane aspartates in presenilin 1 and 2 are obligatory for gamma-secretase activity and amyloid beta-protein generation. J Biol Chem. 275:2000;3173-3178.
46. Kinoshita A., Whelan C.M., Smith C.J., Berezovska O., Hyman B.T. Direct visualization of the gamma secretase-generated carboxyl-terminal domain of the amyloid precursor protein association with Fe65 and translocation to the nucleus . J Neurochem. 82:2002;839-847.
47. Kirazov E., Kirazov L., Bigl V., Schliebs R. Ontogenetic changes in protein level of amyloid precursor protein (APP) in growth cones and synaptosomes from rat brain and prenatal expression pattern of APP mRNA isoforms in developing rat embryo. Int J Dev Neurosci. 19:2001;287-296.
48. Lah J., Heilman C., Nash N., Rees H., Yi Y., Courts S. Light and electron microscopy localisation of PS1 in primate brain. J Neurosci. 17:1997;1971-1980.
49. Levitan D., Lee J., Song L., Manning R., Wong G., Parker E., Zhang L. PS1 N- and C-terminal fragments form a complex that functions in APP processing and Notch signalling. Proc Natl Acad Sci USA. 98:2001;12186-12190.
50. Li Y.M., Xu M., Lai M.T., Huang Q., Catsro J.L., DiMuzo-Mower J., Harrison T., Lellis C., Nadin A., Neduvelil J.G., Registrer R.B., Sardana M.K., Shearman M.S., Smith A.L., Shi X.P., Yin K.C., Shafer J.A., Gardell S.J. Photo activated gamma-secretase inhibitors directed to the active sites covalently label presenilin 1. Nature. 405:2000;689-694.
51. Liu X., Erikson C., Brun A. Cortical synaptic changes and gliosis in normal aging, Alzheimer's disease and frontal lobe degeneration. Dementia. 7:1996;128-134.
52. Löffler J., Huber G. Amyloid precursor protein isoforms in various rat brain regions and during brain development. J Neurochem. 59:1992;1316-1324.
53. Lorenzo A., Yuan M., Zhang Z., Paganetti P.A., Sturchler-Pierrat C., Staufenbiel M., Mautino J., Vigo F.S., Sommer B., Yankner B.A. Amyloid beta interacts with the amyloid precursor protein a potential toxic mechanism in Alzheimer's disease . Nat Neurosci. 3:2000;460-464.
54. Luo J.J., Wallace M.S., Hawver D.B., Kusiack J.W., Wallace W.C. Characterization of the neurotrophic interaction between nerve growth factor and secreted alpha-amyloid precursor protein. J Neurosci Res. 63:2001;410-420.
55. Masliah E., Westland C., Rockenstein E.M., Abraham C.R., Mallory M., Veinberg I., Sheldon E., Mucke L. Amyloid precursor proteins protect neurons of transgenic mice against acute and chronic excitotoxic injuries in vivo. Neuroscience. 78:1997;135-146.
56. Mattson M.P., Gary D.S., Chan S.L., Duan W. Perturbed endoplasmic reticulum function, synaptic apoptosis and the pathogenesis of Alzheimer's disease. Biochem Soc Symp. 67:2001;151-162.
57. McLaughlin M., Breen K. Protein kinase C activation potentiates the rapid secretion of amyloid precursor protein from rat cortical synaptosomes. J Neurochem. 72:1999;273-281.
58. McNamara M.J., Ruff C.T., Wasco W., Tanzi R.E., Thinakaran G., Hyman B.T. Immunohistochemical and in situ analysis of amyloid precursor-like protein-1 and amyloid precursor-like protein-2 expression in Alzheimer disease and aged control brains. Brain Res. 804:1998;45-51.
59. Mezziane H., Dodart J.C., Mathis C., Little S., Clemens J., Paul S., Ungerer A. Memory enhancement effects of secreted forms of the APP in normal and amnestic mice. Proc Natl Acad Sci USA. 95:1999;12683-12688.
60. Mileusnic R., Lancashire C.L., Johnston A.N., Rose S.P. APP is required during an early phase of memory formation. Eur J Neurosci. 12:2000;4487-4495.
61. Moir R.D., Lynch T., Bush A.I., Henry A., Portbury S., Multhaup G., Small D.H., Tanzi R.E., Beyreuther K., Masters C.L. Relative increase in Alzheimer's disease of soluble forms of cerebral A beta amyloid precursor protein containing the Kunitz protease inhibitory domain. J Biol Chem. 273:1998;5013-5019.
62. Moreno-Flores M., Medina W., Wandosell F. Expression of presenilin 1 in nervous system during rat development. J Comp Neurol. 410:1999;556-570.
63. Morley J.E., Kumar V.B., Bernardo A.E., Farr S.A., Uezu K., Tumosa N., Flood J.F. Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides. 21:2000;1761-1767.
64. Moussaoui S., Czech C., Pradier L., Blanchard V., Bonici B., Gohin M., Imperato A., Revah F. Immunohistochemical analysis of presenilin 1 expression in the mouse brain. FEBS Lett. 383:1996;219-222.
65. Moya K., Benowitz L., Schneider G., Allinquant B. The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Dev Biol. 16:1994;597-603.
66. Moya K., Confaloni A., Allinquant B. In vivo neuronal synthesis and axonal transport of KPI-containing forms of the amyloid precursor protein. Neurosci Lett. 206:1994;113-116.
67. Mucke L., Masliah E., Johnson W., Ruppe M.D., Alford M., Rockenstein E.M., Forss-Peter S., Pietropaulo M., Mallory M., Abraham C.R. Synaptotrophic effects of human amyloid beta protein precursors in the cortex of transgenic mice. Brain Res. 666:1994;151-167.
68. Mucke L., Abraham C., Masliah E. Neurotrophic and neuroprotective effects of hAPP in transgenic mice. Ann NY Acad Sci. 777:1996;82-88.
69. Nakamura Y., Takeda M., Niigawa H., Kametani F., Harigushi S., Yoshida I., Kitajima S., Nishimura T. Accumulation of amyloid beta protein precursor (APP) in Purkinje cells and increase of amino-terminal fragments of APP in cerebrum and cerebellum of aged rats. Brain Res. 643:1994;319-323.
70. Nalbantoglu J., Tirado-Santiago G., Lahsaini A., Poirier A., Goncalves O., Verge G., Momoli F., Welner S., Massicotte G., Julien J.P., Shapiro M. Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature. 387:1997;500-505.
71. Ohta M., Kitamoto T., Oghami T., Fukui M., Tateishi J. Immunohistochemical distribution of amyloid precursor protein during normal rat development. Brain Res Dev Brain Res. 75:1993;151-161.
72. Parvathy S., Hussain I., Karran E.H., Turner A.J., Hooper N.M. Cleavage of Alzheimer's amyloid precursor protein by alpha-secretase occurs at the surface of neuronal cells. Biochemistry. 38:1999;9728-9734.
73. Pigino G., Pelsman A., Mori H., Busciglio J. Presenilin-1 mutations reduce cytoskeletal association, deregulate neurite growth, and potentiate neuronal dystrophy and tau phosphorylation. J Neurosci. 21:2001;834-842.
74. Pokorny J., Yamamoto T. Postnatal ontogenesis of hippocampal CA1 area in rats Part II . Development of ultrastructure in stratum lacunosum and moleculare. Brain Res Bull. 7:1981;121-130.
75. Ramirez M.J., Heslop K.E., Francis P.T., Rattray M. Expression of amyloid precursor protein, tau and presenilin RNAs in rat hippocampus following deafferentation lesions. Brain Res. 907:2001;222-232.
76. Ray W.J., Yao M., Mumm J., Schroeter E.H., Saftig P., Wolfe M., Selkoe D.J., Kopan R., Goate A.M. Cell surface presenilin-1 participates in the gamma-secretase-like proteolysis of Notch. J Biol Chem. 17:1999;36801-36807.
77. Ribaut-Barassin C., Moussaoui S., Brugg B., Haeberlé A.-M., Huber G., Imperato A., Delhaye-Bouchaud N., Mariani J., Bailly Y. Hemisynaptic distribution patterns of presenilins and βAPP isoforms in the rodent cerebellum and hippocampus. Synapse. 35:2000;96-110.
78. Roch J.M., Masliah E., Roch-Levecq A.C., Sundsmo M.P., Otero D., Veinberg I., Saitoh T. Increase of synaptic density and memory retention by a peptide representing the trophic domain of the amyloid βA4 precursor protein. Proc Natl Acad Sci USA. 91:1994;7450-7454.
79. Schubert W., Prior R., Weideman A., Dircksen H., Multhaup G., Masters C., Beyreuther K. Localisation of βA4 amyloid precursor at central and peripheral synaptic sites. Brain Res. 563:1991;184-194.
80. Schubert D., Behl C. The expression of amyloid precursor protein protects nerve cells from beta amyloid and glutamate toxicity and alters their interaction with the extracellular matrix. Brain Res. 629:1993;275-282.
81. Seabrook G.R., Smith D.W., Bowery B.J., Easter A., Reynolds T., Fitzjohn S.M., Morton R.A., Zheng H., Dawson G.R., Sirinathsinghji D.J., Davies C.H., Collingridge G.L., Hill R.G. Mechanisms contributing to the deficits in hippocampal synaptic plasticity in mice lacking amyloid precursor protein. Neuropharmacology. 38:1999;349-359.
82. Shen J., Bronson R.T., Chen D.F., Xia W., Selkoe D.J., Tonegawa S. Skeletal and CNS defects in presenilin 1 deficient mice. Cell. 89:1997;629-639.
83. Sherman C.A., Higgins G.A. Regulated splicing of the amyloid precursor protein gene during postnatal development of the rat basal forebrain. Dev Brain Res. 66:1992;63-69.
84. Shigematsu K., McGeer P.L., McGeer E.G. Localization of amyloid precursor protein in selective postsynaptic densities of rat cortical neurons. Brain Res. 592:1992;353-357.
85. Simons M., Ikonen E., Tienari P.J., Cidarregui A., Monning U., Beyreuther K., Dotti C.G. Intracellular routing of the human amyloid protein precursor axonal delivery followed by transport to the dendrites . J Neurosci Res. 41:1995;121-128.
86. Singh N., Talalayeva Y., Tsiper M., Romanov V., Dranovsky A., Colflesh D., Rudamen G., Vitek M.P., Shen J., Yang X., Goldgaber D., Schwarzman A.L. The role of Alzheimer's disease-related presenilin 1 in intercellular adhesion. Exp Cell Res. 263:2001;1-13.
87. Slunt H.H., Thinakaran G., von Koch C., Lo A.C., Tanzi R.E., Sisodia S.S. Expression of an ubiquitous, cross-reactive homologue of the mouse beta-amyloid precursor protein (APP). J Biol Chem. 28:1994;2637-2644.
88. Small D., Nurcombe V., Reed G., Clarris H., Moir R., Beyreuther K., Masters C. A heparin binding domain in the amyloid precursor protein of Alzheimer's disease is involved in the regulation of neurite outgrowth. J Neurosci. 14:1994;2117-2127.
89. Stewart R.R., Bossu J.-L., Muzet M., Dupont J.-L., Feltz A. Voltage-activated ionic current in differentiating rat cerebellar granular neurons from the external germinal layer. J Neurobiol. 28:1995;419-432.
90. Struhl G., Adachi A. Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol Cell. 6:2000;625-636.
91. Sze C.I., Hong B., Kleinschmidt-Demasters B.K., Filley C.M., Martin L.J. Selective regional loss of exocytotic presynaptic vesicle proteins in Alzheimer's disease brains. J Neurol Sci. 175:2000;81-90.
92. Tanaka S., Liu L., Kimura J., Shiojiri S., Takahashi Y., Kitagushi N., Nakamura S., Ueda K. Age related changes in the proportion of amyloid precursor protein mRNAs in Alzheimer's disease and other neurological disorders. Brain Res Mol Brain Res. 15:1992;303-310.
93. Thinakaran G. Metabolism of presenilins. J Mol Neurosci. 17:2001;183-192.
94. von Koch C.S., Zheng H., Chen H., Trumbauer M., Thinakaran G., van der Ploeg L.H.T., Price D.L., Sisodia S. Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol Aging. 18:1997;661-669.
95. Weidemann A., Konig G., Bunke D., Fischer P., Salbaum J.M., Masters C.L., Beyreuther K. Identification, biogenesis, and localisation of precursors of Alzheimer's disease A4 amyloid protein. Cell. 57:1989;115-126.
96. Wolfe M.S., Xia W., Ostaszewski B.L., Diehl T.S., Kimberly W.T., Selkoe D.J. Two transmembrane aspartates in PS1 required for PS endoproteolysis and gamma secretase activity. Nature. 398:1999;513-517.
97. Xia W., Ray W.J., Ostaszewski B.L., Rahmati T., Kimberly W.T., Wolfe M.S., Zhang J., Goate A.M., Selkoe D.J. Presenilin complexes with the C-terminal fragments of amyloid precursor protein at the sites of amyloid beta-protein generation. Proc Natl Acad Sci USA. 97:2000;9299-9304.
98. Xie Y.Y., Yao Z.B., Wu W.T. Survival of motor neurons and expression of beta-amyloid protein in aged rat spinal cord. Neuroreport. 11:2000;697-700.
99. Young M.J., Lee R.K., Jhaveri S., Wurtman R.J. Intracellular and cell-surface distribution of amyloid precursor protein in cortical astrocytes. Brain Res Bull. 50:1999;27-32.
100. Zhang Z., Nadeau P., Song W., Donoviel D., Yuan M., Bernstein A., Yankner B.A. Presenilins are required for gamma-secretase cleavage of beta-APP and transmembrane cleavage of Notch-1. Nat Cell Biol. 2:2000;463-465.