Pharmacological and genetic reversal of age-dependent cognitive deficits attributable to decreased presenilin function

Journal of Neuroscience

Volumn 30, Issue 28, 2010, Pages 9510-9522

  McBride, Sean M J ^a   Choi, Catherine H ^a,b   Schoenfeld, Brian P ^a   Bell, Aaron J ^a   Liebelt, David A ^a   Ferreiro, David ^a   Choi, Richard J ^a   Hinchey, Paul ^a   Kollaros, Maria ^a   Terlizzi, Allison M ^a   Ferrick, Neal J ^a   Koenigsberg, Eric ^a   Rudominer, Rebecca L ^a   Sumida, Ai ^c   Chiorean, Stephanie ^c   Siwicki, Kathleen K ^d   Nguyen, Hanh T ^a   Fortini, Mark E ^e   McDonald, Thomas V ^a   Jongens, Thomas A ^c  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d SWARTHMORE COLLEGE   (United States)

^e THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; ALPHA METHYL 4 TETRAZOLYLPHENYLGLYCINE; ALPHA METHYLSERINE O PHOSPHATE; FLAVINE ADENINE NUCLEOTIDE; INOSITOL POLYPHOSPHATE; INOSITOL POLYPHOSPHATE 1 PHOSPHATASE; INOSITOL TRISPHOSPHATE; LITHIUM; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR ANTAGONIST; PRESENILIN; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN TISSUE; CALCIUM TRANSPORT; COGNITION; CONTROLLED STUDY; COURTSHIP; DFMR1 GENE; DROSOPHILA MELANOGASTER; GENE; GENE FUNCTION; GENE INTERACTION; HETEROZYGOSITY; LEARNING DISORDER; MALE; MEMORY DISORDER; MORPHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SHORT TERM MEMORY;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; COGNITION; COURTSHIP; DROSOPHILA MELANOGASTER; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LEARNING; LITHIUM; MALE; MEMORY; MUSHROOM BODIES; PHOSPHORIC MONOESTER HYDROLASES; PRESENILINS; RANDOM ALLOCATION; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 77954723280     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1017-10.2010     Document Type: Article

References (104)

1. Acharya JK, Labarca P, Delgado R, Jalink K, Zuker CS (1998) Synaptic defects and compensatory regulation of inositol metabolism in inositol polyphosphate 1-phosphatase mutants. Neuron 20:1219-1229. (Pubitemid 28293138)
2. Ackerman SL, Siegel RW (1986) Chemically reinforced conditioned courtship in Drosophila: responses of wild-type and the dunce, amnesiac and don giovanni mutants. J Neurogenet 3:111-123.
3. Alzheimer A (1907) Über eine eigenartige Erkrankung der Hirnrinde. Allg Zschr Psychiatr psych-gerichtl Med 64:146-148.
4. Amtul Z, Lewis PA, Piper S, Crook R, Baker M, Findlay K, Singleton A, Hogg M, Younkin L, Younkin SG, Hardy J, Hutton M, Boeve BF, Tang-Wai D, Golde TE (2002) A presenilin 1 mutation associated with familial frontotemporal dementia inhibits gamma-secretase cleavage of APP and notch. Neurobiol Dis 9:269-273. (Pubitemid 34261221)
5. Baki L, Shioi J, Wen P, Shao Z, Schwarzman A, Gama-Sosa M, Neve R, Robakis NK (2004) PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: effects of FAD mutations. EMBO J 23:2586-2596. (Pubitemid 38988230)
6. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361:315-325.
7. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45:675-688. (Pubitemid 40320703)
8. Bogdanik L, Mohrmann R, Ramaekers A, Bockaert J, Grau Y, Broadie K, Parmentier ML (2004) The Drosophila metabotropic glutamate receptor DmGluRA regulates activity-dependent synaptic facilitation and fine synaptic morphology. J Neurosci 24:9105-9116.
9. Bolduc FV, Bell K, Cox H, Broadie KS, Tully T (2008) Excess protein synthesis in Drosophila fragile X mutants impairs long-term memory. Nat Neurosci 11:1143-1145.
10. Boulianne GL, Livne-Bar I, Humphreys JM, Liang Y, Lin C, Rogaev E, St George-Hyslop P (1997) Cloning and characterization of the Drosophila presenilin homologue. Neuroreport 8:1025-1029.
11. Bullock BP, Habener JF (1998) Phosphorylation of the cAMP response element binding protein CREB by cAMP-dependent protein kinase A and glycogen synthase kinase-3 alters DNA-binding affinity, conformation, and increases net charge. Biochemistry 37:3795-3809.
12. Caccamo A, Oddo S, Tran LX, LaFerla FM (2007) Lithium reduces tau phosphorylation but not A beta or working memory deficits in a transgenic model with both plaques and tangles. Am J Pathol 170:1669-1675. (Pubitemid 47339311)
13. 2+ disruption in Alzheimer's disease by presenilin regulation of InsP3 receptor channel gating. Neuron 58:871-883.
14. Coleman PD, Yao PJ (2003) Synaptic slaughter in Alzheimer's disease. Neurobiol Aging 24:1023-1027.
15. Crowther DC, Kinghorn KJ, Miranda E, Page R, Curry JA, Duthie FA, Gubb DC, Lomas DA (2005) Intraneuronal Abeta, non-amyloid aggregates and neurodegeneration in a Drosophila model of Alzheimer's disease. Neuroscience 132:123-135.
16. Davies CA, Mann DM, Sumpter PQ, Yates PO (1987) A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease. J Neurol Sci 78:151-164.
17. DeKosky ST, Scheff SW (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 27:457-464.
18. Dermaut B, Kumar-Singh S, Engelborghs S, Theuns J, Rademakers R, Saerens J, Pickut BA, Peeters K, van den Broeck M, Vennekens K, Claes S, Cruts M, Cras P, Martin JJ, Van Broeckhoven C, De Deyn PP (2004) A novel presenilin 1 mutation associated with Pick's disease but not beta-amyloid plaques. Ann Neurol 55:617-626.
19. Deshpande M, Venkatesh K, Rodrigues V, Hasan G (2000) The inositol 1,4,5-trisphosphate receptor is required for maintenance of olfactory adaptation in Drosophila antennae. J Neurobiol 43:282-288. (Pubitemid 30350628)
20. De Strooper B (2003) Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron 38:9-12.
21. De Strooper B (2007) Loss-of-function presenilin mutations in Alzheimer disease. Talking point on the role of presenilin mutations in Alzheimer disease. EMBO Rep 8:141-146.
22. Dölen G, Osterweil E, Rao BS, Smith GB, Auerbach BD, Chattarji S, Bear MF (2007) Correction of fragile X syndrome in mice. Neuron 56:955-962.
23. Ejima A, Smith BP, Lucas C, Levine JD, Griffith LC (2005) Sequential learning of pheromonal cues modulates memory consolidation in trainer-specific associative courtship conditioning. Curr Biol 15:194-206. (Pubitemid 40205699)
24. Ejima A, Smith BP, Lucas C, van der Goes van Naters W, Miller CJ, Carlson JR, Levine JD, Griffith LC (2007) Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 17:599-605.
25. Etcheberrigaray R, Hirashima N, Nee L, Prince J, Govoni S, Racchi M, Tanzi RE, Alkon DL (1998) Calcium responses in fibroblasts from asymptomatic members of Alzheimer's disease families. Neurobiol Dis 5:37-45. (Pubitemid 28361650)
26. Gong B, Vitolo OV, Trinchese F, Liu S, Shelanski M, Arancio O (2004) Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J Clin Invest 114:1624-1634. (Pubitemid 40385553)
27. Gould TD, Manji HK (2005) Glycogen synthase kinase-3: a putative molecular target for lithium mimetic drugs. Neuropsychopharmacology 30:1223-1237.
28. Grimes CA, Jope RS (2001) CREB DNA binding activity is inhibited by glycogen synthase kinase-3 beta and facilitated by lithium. J Neurochem 78:1219-1232.
29. Hall JC (1994) The mating of a fly. Science 264:1702-1714.
30. Halliday GM, Song YJ, Lepar G, Brooks WS, Kwok JB, Kersaitis C, Gregory G, Shepherd CE, Rahimi F, Schofield PR, Kril JJ (2005) Pick bodies in a family with presenilin-1 Alzheimer's disease. Ann Neurol 57:139-143. (Pubitemid 40053327)
31. Hansen TO, Rehfeld JF, Nielsen FC (2004) GSK-3beta reduces cAMP-induced cholecystokinin gene expression by inhibiting CREB binding. Neuroreport 15:841-845.
32. Hardy J (2006) A hundred years of Alzheimer's disease research. Neuron 52:3-13. (Pubitemid 44472602)
33. Hardy J (2007) Putting presenilins centre stage. Introduction to the Talking point on the role of presenilin mutations in Alzheimer disease. EMBO Rep 8:134-135.
34. Hériché JK, Ang D, Bier E, O'Farrell PH (2003) Involvement of an SCFSlmb complex in timely elimination of E2F upon initiation of DNA replication in Drosophila. BMC Genet 4:9.
35. Hirashima N, Etcheberrigaray R, Bergamaschi S, Racchi M, Battaini F, Binetti G, Govoni S, Alkon DL (1996) Calcium responses in human fibroblasts: a diagnostic molecular profile for Alzheimer's disease. Neurobiol Aging 17:549-555. (Pubitemid 26274254)
36. Hong CS, Koo EH (1997) Isolation and characterization of Drosophila presenilin homolog. Neuroreport 8:665-668.
37. Hu Y, Fortini ME (2003) Different cofactor activities in gamma-secretase assembly: evidence for a nicastrin-Aph-1 subcomplex. J Cell Biol 161:685-690. (Pubitemid 36648751)
38. Huang HC, Klein PS (2006) Multiple roles for glycogen synthase kinase-3 as a drug target in Alzheimer's disease. Curr Drug Targets 7:1389-1397.
39. Huang HM, Toral-Barza L, Thaler H, Tofel-Grehl B, Gibson GE (1991) Inositol phosphates and intracellular calcium after bradykinin stimulation in fibroblasts from young, normal aged and Alzheimer donors. Neurobiol Aging 12:469-473.
40. Huang LQ, Rowan MJ, Anwyl R (1997) mGluR II agonist inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyrus in vitro. Neuroreport 8:687-693.
41. Huang L, Killbride J, Rowan MJ, Anwyl R (1999a) Activation of mGluRII induces LTD via activation of protein kinase A and protein kinase C in the dentate gyrus of the hippocampus in vitro. Neuropharmacology 38:73-83. (Pubitemid 29073528)
42. Huang LQ, Rowan MJ, Anwyl R (1999b) Role of protein kinases A and C in the induction of mGluR-dependent long-term depression in the medial perforant path of the rat dentate gyrus in vitro. Neurosci Lett 274:71-74.
43. Huber KM, Gallagher SM, Warren ST, Bear MF (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci U S A 99:7746-7750. (Pubitemid 34568762)
44. Iijima K, Liu HP, Chiang AS, Hearn SA, Konsolaki M, Zhong Y (2004) Dissecting the pathological effects of human Abeta40 and Abeta42 in Drosophila: a potential model for Alzheimer's disease. Proc Natl Acad Sci U S A 101:6623-6628.
45. Isoo N, Sato C, Miyashita H, Shinohara M, Takasugi N, Morohashi Y, Tsuji S, Tomita T, Iwatsubo T (2007) Abeta42 overproduction associated with structural changes in the catalytic pore of gamma-secretase: common effects of Pen-2 N-terminal elongation and fenofibrate. J Biol Chem 282:12388-12396. (Pubitemid 47100594)
46. Ito E, Oka K, Etcheberrigaray R, Nelson TJ, McPhie DL, Tofel-Grehl B, Gibson GE, Alkon DL (1994) Internal Ca2+ mobilization is altered in fibroblasts from patients with Alzheimer disease. Proc Natl Acad Sci U S A 91:534-538. (Pubitemid 2042532)
47. Joiner MA, Griffith LC (1997) CaM kinase II and visual input modulate memory formation in the neuronal circuit controlling courtship conditioning. J Neurosci 17:9384-9391.
48. Joiner MA, Griffith LC (1999) Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. Learn Mem 6:177-192.
49. Jope RS, Roh MS (2006) Glycogen synthase kinase-3 (GSK3) in psychiatric diseases and therapeutic interventions. Curr Drug Targets 7:1421-1434.
50. Kane NS, Robichon A, Dickinson JA, Greenspan RJ (1997) Learning without performance in PKC-deficient Drosophila. Neuron 18:307-314.
51. Klein PS, Melton DA (1996) A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 93:8455-8459.
52. Kreibich TA, Chalasani SH, Raper JA (2004) The neurotransmitter glutamate reduces axonal responsiveness to multiple repellents through the activation of metabotropic glutamate receptor 1. J Neurosci 24:7085-7095.
53. Kumar-Singh S, Theuns J, Van Broeck B, Pirici D, Vennekens K, Corsmit E, Cruts M, Dermaut B, Wang R, Van Broeckhoven C (2006) Mean age-of-onset of familial alzheimer disease caused by presenilin mutations correlates with both increased Abeta42 and decreased Abeta40. Hum Mutat 27:686-695.
54. Mai L, Jope RS, Li X (2002) BDNF-mediated signal transduction is modulated by GSK3beta and mood stabilizing agents. J Neurochem 82:75-83. (Pubitemid 34755251)
55. Malherbe P, Kratochwil N, Zenner MT, Piussi J, Diener C, Kratzeisen C, Fischer C, Porter RH (2003) Mutational analysis and molecular modeling of the binding pocket of the metabotropic glutamate 5 receptor negative modulator 2-methyl-6-(phenylethynyl)-pyridine. Mol Pharmacol 64:823-832. (Pubitemid 37153050)
56. Malm TM, Iivonen H, Goldsteins G, Keksa-Goldsteine V, Ahtoniemi T, Kanninen K, Salminen A, Auriola S, Van Groen T, Tanila H, Koistinaho J (2007) Pyrrolidine dithiocarbamate activates Akt and improves spatial learning in APP/PS1 mice without affecting β-amyloid burden. J Neurosci 27:3712-3721. (Pubitemid 46557689)
57. Mattson MP (2004) Pathways towards and away from Alzheimer's disease. Nature 430:631-639. (Pubitemid 39061671)
58. McBride SM, Giuliani G, Choi C, Krause P, Correale D, Watson K, Baker G, Siwicki KK (1999) Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24:967-977. (Pubitemid 30017675)
59. McBride SM, Choi CH, Wang Y, Liebelt D, Braunstein E, Ferreiro D, Sehgal A, Siwicki KK, Dockendorff TC, Nguyen HT, McDonald TV, Jongens TA (2005) Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile X syndrome. Neuron 45:753-764.
60. Mershin A, Pavlopoulos E, Fitch O, Braden BC, Nanopoulos DV, Skoulakis EM (2004) Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons. Learn Mem 11:277-287.
61. Moehlmann T, Winkler E, Xia X, Edbauer D, Murrell J, Capell A, Kaether C, Zheng H, Ghetti B, Haass C, Steiner H (2002) Presenilin-1 mutations of leucine 166 equally affect the generation of the Notch and APP intracellular domains independent of their effect on Abeta 42 production. Proc Natl Acad Sci U S A 99:8025-8030. (Pubitemid 34650999)
62. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39:409-421. (Pubitemid 36937044)
63. Otani S, Auclair N, Desce JM, Roisin MP, Crépel F (1999) Dopamine receptors and groups I and II mGluRs cooperate for long-term depression induction in rat prefrontal cortex through converging postsynaptic activation of MAP kinases. J Neurosci 19:9788-9802. (Pubitemid 30226652)
64. Otani S, Daniel H, Takita M, Crépel F (2002) Long-term depression induced by postsynaptic group II metabotropic glutamate receptors linked to phospholipase C and intracellular calcium rises in rat prefrontal cortex. J Neurosci 22:3434-3444. (Pubitemid 37465749)
65. Pagano A, Ruegg D, Litschig S, Stoehr N, Stierlin C, Heinrich M, Floersheim P, Prezèau L, Carroll F, Pin JP, Cambria A, Vranesic I, Flor PJ, Gasparini F, Kuhn R (2000) Thenon-competitive antagonists2-methyl-6- (phenylethynyl) pyridine and 7-hydroxyiminocyclopropan[b]chromen-1a-carboxylic acid ethyl ester interact with overlapping binding pockets in the transmembrane region of group I metabotropic glutamate receptors. J Biol Chem 275:33750-33758.
66. Palladino MJ, Keegan LP, O'Connell MA, Reenan RA (2000) A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell 102:437-449.
67. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L (2003) Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci U S A 100:9572-9577. (Pubitemid 37033969)
68. Pan L, Broadie KS (2007) Drosophila fragile X mental retardation protein and metabotropic glutamate receptor A convergently regulate the synaptic ratio of ionotropic glutamate receptor subclasses. J Neurosci 27:12378-12389.
69. Pan L, Woodruff E 3rd, Liang P, Broadie K (2008) Mechanistic relationships between Drosophila fragile X mental retardation protein and metabotropic glutamate receptor A signaling. Mol Cell Neurosci 37:747-760.
70. Parmentier ML, Pin JP, Bockaert J, Grau Y (1996) Cloning and functional expression of a Drosophila metabotropic glutamate receptor expressed in the embryonic CNS. J Neurosci 16:6687-6694.
71. Peterson C, Ratan RR, Shelanski ML, Goldman JE (1988) Altered response of fibroblasts from aged and Alzheimer donors to drugs that elevate cytosolic free calcium. Neurobiol Aging 9:261-266. (Pubitemid 19268091)
72. Qi-Takahara Y, Morishima-Kawashima M, Tanimura Y, Dolios G, Hirotani N, Horikoshi Y, Kametani F, Maeda M, Saido TC, Wang R, Ihara Y (2005) Longer forms of amyloid β protein: implications for the mechanism of intramembrane cleavage by γ-secretase. J Neurosci 25:436-445. (Pubitemid 40105614)
73. Raux G, Gantier R, Martin C, Pothin Y, Brice A, Frebourg T, Campion D (2000) A novel presenilin 1 missense mutation (L153V) segregating with early-onset autosomal dominant Alzheimer's disease. Hum Mutat 16:95.
74. Sambamurti K, Suram A, Venugopal C, Prakasam A, Zhou Y, Lahiri DK, Greig NH (2006) A partial failure of membrane protein turnover may cause Alzheimer's disease: a new hypothesis. Curr Alzheimer Res 3:81-90.
75. Saura CA, Choi SY, Beglopoulos V, Malkani S, Zhang D, Shankaranarayana Rao BS, Chattarji S, Kelleher RJ 3rd, Kandel ER, Duff K, Kirkwood A, Shen J (2004) Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42:23-36. (Pubitemid 38456965)
76. Schroeter EH, Ilagan MX, Brunkan AL, Hecimovic S, Li YM, Xu M, Lewis HD, Saxena MT, De Strooper B, Coonrod A, Tomita T, Iwatsubo T, Moore CL, Goate A, Wolfe MS, Shearman M, Kopan R (2003) A presenilin dimer at the core of the gamma-secretase enzyme: insights from parallel analysis of Notch 1 and APP proteolysis. Proc Natl Acad Sci U S A 100:13075-13080. (Pubitemid 37340028)
77. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298:789-791.
78. Serban G, Kouchi Z, Baki L, Georgakopoulos A, Litterst CM, Shioi J, Robakis NK (2005) Cadherins mediate both the association between PS1 and beta-catenin and the effects of PS1 on beta-catenin stability. J Biol Chem 280:36007-36012. (Pubitemid 41633870)
79. Shen J, Kelleher RJ 3rd (2007) The presenilin hypothesis of Alzheimer's disease: evidence for a loss-of-function pathogenic mechanism. Proc Natl Acad Sci U S A 104:403-409. (Pubitemid 46123039)
80. Shioi J, Georgakopoulos A, Mehta P, Kouchi Z, Litterst CM, Baki L, Robakis NK (2007) FAD mutants unable to increase neurotoxic Abeta 42 suggest that mutation effects on neurodegeneration may be independent of effects on Abeta. J Neurochem 101:674-681. (Pubitemid 46633320)
81. Siegel RW, Hall JC (1979) Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc Natl Acad Sci U S A 76:3430-3434.
82. Siwicki KK, Riccio P, Ladewski L, Marcillac F, Dartevelle L, Cross SA, Ferveur JF (2005) The role of cuticular pheromones in courtship conditioning of Drosophila males. Learn Mem 12:636-645.
83. Skoulakis EM, Grammenoudi S (2006) Dunces and da Vincis: the genetics of learning and memory in Drosophila. Cell Mol Life Sci 63:975-988.
84. Small SA, Gandy S (2006) Sorting through the cell biology of Alzheimer's disease: intracellular pathways to pathogenesis. Neuron 52:15-31.
85. Struhl G, Greenwald I (1999) Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 398:522-525. (Pubitemid 129523591)
86. 2+ signals and altered membrane excitability. J Neurosci 24:508-513.
87. Takasugi N, Tomita T, Hayashi I, Tsuruoka M, Niimura M, Takahashi Y, Thinakaran G, Iwatsubo T (2003) The role of presenilin cofactors in the gamma-secretase complex. Nature 422:438-441. (Pubitemid 36411397)
88. Takei K, Shin RM, Inoue T, Kato K, Mikoshiba K (1998) Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science 282:1705-1708. (Pubitemid 28549285)
89. Tanji C, Yamamoto H, Yorioka N, Kohno N, Kikuchi K, Kikuchi A (2002) A-kinase anchoring protein AKAP220 binds to glycogen synthase kinase-3beta (GSK-3beta) and mediates protein kinase A-dependent inhibition of GSK-3beta. J Biol Chem 277:36955-36961.
90. Tatebayashi Y, Takeda M, Kashiwagi Y, Okochi M, Kurumadani T, Sekiyama A, Kanayama G, Hariguchi S, Nishimura T (1995) Cell-cycle-dependent abnormal calcium response in fibroblasts from patients with familial Alzheimer's disease. Dementia 6:9-16.
91. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572-580.
92. Tompkins L, Siegel RW, Gailey DA, Hall JC (1983) Conditioned courtship in Drosophila and its mediation by association of chemical cues. Behav Genet 13:565-578.
93. Venkatesh K, Hasan G (1997) Disruption of the IP3 receptor gene of Drosophila affects larval metamorphosis and ecdysone release. Curr Biol 7:500-509.
94. Walker ES, Martinez M, Brunkan AL, Goate A (2005) Presenilin 2 familial Alzheimer's disease mutations result in partial loss of function and dramatic changes in Abeta 42/40 ratios. J Neurochem 92:294-301. (Pubitemid 40194020)
95. Walsh DM, Selkoe DJ (2004) Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44:181-193. (Pubitemid 39348839)
96. Westphalen RI, Scott HL, Dodd PR (2003) Synaptic vesicle transport and synaptic membrane transporter sites in excitatory amino acid nerve terminals in Alzheimer disease. J Neural Transm 110:1013-1027.
97. Williams RS, Cheng L, Mudge AW, Harwood AJ (2002) A common mechanism of action for three mood-stabilizing drugs. Nature 417:292-295. (Pubitemid 34534711)
98. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, Feany MB (2001) Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 293:711-714.
99. Wolfe MS (2007) When loss is gain: reduced presenilin proteolytic function leads to increased Abeta42/Abeta40. Talking point on the role of presenilin mutations in Alzheimer disease. EMBO Rep 8:136-140.
100. Yan QJ, Rammal M, Tranfaglia M, Bauchwitz RP (2005) Suppression of two major Fragile X Syndrome mouse model phenotypes by the mGluR5 antagonist MPEP. Neuropharmacology 49:1053-1066. (Pubitemid 41503304)
101. Yao PJ, Zhu M, Pyun EI, Brooks AI, Therianos S, Meyers VE, Coleman PD (2003) Defects in expression of genes related to synaptic vesicle trafficking in frontal cortex of Alzheimer's disease. Neurobiol Dis 12:97-109. (Pubitemid 36355860)
102. Ye Y, Fortini ME (1998) Characterization of Drosophila Presenilin and its colocalization with Notch during development. Mech Dev 79:199-211.
103. Ye Y, Fortini ME (1999) Apoptotic activities of wild-type and Alzheimer's disease-related mutant presenilins in Drosophila melanogaster. J Cell Biol 146:1351-1364.
104. Ye Y, Lukinova N, Fortini ME (1999) Neurogenic phenotypes and altered Notch processing in Drosophila Presenilin mutants. Nature 398:525-529.