Modulation of synaptic plasticity and Tau phosphorylation by wild-type and mutant presenilin1

Neurobiology of Aging

Volumn 29, Issue 5, 2008, Pages 639-652

  Dewachter, I ^a   Ris, L ^b   Croes, S ^a   Borghgraef, P ^a   Devijver, H ^a   Voets, T ^a   Nilius, B ^a   Godaux, E ^b   Van Leuven, F ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF MONS   (Belgium)

Author keywords

FAD mutation; NMDA receptor; Postsynaptic; Presenilin; Presynaptic; Synaptic plasticity; Synaptic vesicles; Tau

Indexed keywords

ALPHA PROTEIN KINASE (CALCIUM,CALMODULIN) II; GLYCOGEN SYNTHASE KINASE 3BETA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PRESENILIN 1; PROTEIN KINASE (CALCIUM,CALMODULIN) II; TAU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SYNAPSE VESICLE;

ANIMALS; CELLS, CULTURED; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; PRESENILIN-1; SYNAPSES; SYNAPTIC TRANSMISSION; TAU PROTEINS;

EID: 40849115110     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2006.11.019     Document Type: Article

References (59)

1. Baki L., Shioi J., Wen P., Shao Z., Schwarzman A., Gama-Sosa M., Neve R., and Robakis N.K. PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: effects of FAD mutations. EMBO J. 23 13 (2004) 2586-2596
2. Barria A., and Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48 2 (2005) 289-301
3. Barrow P.A., Empson R.M., Gladwell S.J., Anderson C.M., Killick R., Yu X., Jefferys J.G., and Duff K. Functional phenotype in transgenic mice expressing mutant human presenilin-1. Neurobiol. Dis. 7 2 (2000) 119-126
4. Berberich S., Punnakkal P., Jensen V., Pawlak V., Seeburg P.H., Hvalby O., and Kohr G. Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J. Neurosci. 25 29 (2005) 6907-6910
5. Buee-Scherrer V., Condamines O., Mourton-Gilles C., Jakes R., Goedert M., Pau B., and Delacourte A. AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease. Brain Res. Mol. Brain Res. 39 1/2 (1996) 79-88
6. Carlin R.K., Grab D.J., Cohen R.S., and Siekevitz P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell. Biol. 86 (1980) 831-843
7. De Strooper B., Saftig P., Craessaerts K., Vanderstichele H., Guhde G., Annaert W., Von Figura K., and Van Leuven F. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391 (1998) 339-340
8. Dewachter I., Van Dorpe J., Smeijers L., Gilis M., Kuiperi C., Laenen I., Caluwaerts N., Moechars D., Checler F., Vanderstichele H., and Van Leuven F. Aging increased amyloid peptide and caused amyloid plaques in brain of old APP/V717I transgenic mice by a different mechanism than mutant presenilin1. J. Neurosci. 20 (2000) 6452-6458
9. Dewachter I., Reverse D., Caluwaerts N., Ris L., Kuiperi C., Van den Haute C., Spittaels K., Umans L., Serneels L., Thiry E., Moechars D., Mercken M., Godaux E., and Van Leuven F. 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
10. Dobrunz L.E., and Stevens C.F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18 6 (1997) 995-1008
11. Doglio L.E., Kanwar R., Jackson G.R., Perez M., Avila J., Dingwall C., Dotti C.G., Fortini M.E., and Feiguin F. Gamma-cleavage-independent functions of presenilin, nicastrin, and Aph-1 regulate cell-junction organization and prevent tau toxicity in vivo. Neuron 50 3 (2006) 359-375
12. Feng R., Rampon C., Tang Y.P., Shrom D., Jin J., Kyin M., Sopher B., Miller M.W., Ware C.B., Martin G.M., Kim S.H., Langdon R.B., Sisodia S.S., and Tsien J.Z. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 32 5 (2001) 911-926
13. Feng R., Wang H., Wang J., Shrom D., Zeng X., and Tsien J.Z. Forebrain degeneration and ventricle enlargement caused by double knockout of Alzheimer's presenilin-1 and presenilin-2. Proc. Natl. Acad. Sci. U.S.A. 101 21 (2004) 8162-8167
14. Fleischmann A., Hvalby O., Jensen V., Strekalova T., Zacher C., Layer L.E., Kvello A., Reschke M., Spanagel R., Sprengel R., Wagner E.F., and Gass P. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J. Neurosci. 23 27 (2003) 9116-9122
15. Herms J., Tings T., Gall S., Madlung A., Giese A., Siebert H., Schurmann P., Windl O., Brose N., and Kretzschmar H. Evidence of presynaptic location and function of the prion protein. J. Neurosci. 19 (1999) 8866-8875
16. Herms J., Schneider I., Dewachter I., Caluwaerts N., Kretzschmar H., and Van Leuven F. Capacitive calcium entry is directly attenuated by mutant presenilin-1, independent of the expression of the amyloid precursor protein. J. Biol. Chem. 278 (2003) 2484-2489
17. Huang X.G., Yee B.K., Nag S., Chan S.T., and Tang F. Behavioral and neurochemical characterization of transgenic mice carrying the human presenilin-1 gene with or without the leucine-to-proline mutation at codon 235. Exp. Neurol. 183 2 (2003) 673-681
18. Huang K.P., Huang F.L., Jager T., Li J., Reymann K.G., and Balschun D. Neurogranin/RC3 enhances long-term potentiation and learning by promoting calcium-mediated signaling. J. Neurosci. 24 47 (2004) 10660-10669
19. Hutton M., and Hardy J. The presenilins and Alzheimer's disease. Hum. Mol. Genet. 6 (1997) 1639-1646
20. Iwatsubo T. The gamma-secretase complex: machinery for intramembrane proteolysis. Curr. Opin. Neurobiol. 14 (2004) 379-383
21. Janus C., D'Amelio S., Amitay O., Chishti M.A., Strome R., Fraser P., Carlson G.A., Roder J.C., St George-Hyslop P., and Westaway D. Spatial learning in transgenic mice expressing human presenilin 1 (PS1) transgenes. Neurobiol. Aging 21 4 (2000) 541-549
22. Kennedy M.B. The postsynaptic density at glutamatergic synapses. Trends Neurosci. 20 (1997) 264-268
23. Peters A., Palay S., and Webster H. The Fine Structure of the Nervous System (1991), Oxford University Press, Oxford
24. Koo E.H., and Kopan R. Potential role of presenilin-regulated signaling pathways in sporadic neurodegeneration. Nat. Med. 10 (2004) 26-33
25. Kopan R., and Ilagan M.X.G. Gamma-secretase: proteasome of the membrane?. Nat. Rev. Mol. Cell Biol. 5 (2004) 499-504
26. Leissring M.A., Akbari Y., Fanger C.M., Cahalan M.D., Mattson M.P., and LaFerla F.M. Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice. J. Cell Biol. 149 (2000) 793-798
27. Liu L., Wong T.P., Pozza M.F., Lingenhoehl K., Wang Y., Sheng M., Auberson Y.P., and Wang Y.T. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304 5673 (2004) 1021-1024
28. Malleret G., Haditsch U., Genoux D., Jones M.W., Bliss T.V., Vanhoose A.M., Weitlauf C., Kandel E.R., Winder D.G., and Mansuy I.M. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell 104 (2001) 675-686
29. Maren S., and Holt W. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav. Brain Res. 110 (2000) 97-108
30. Maren S., and Quirk G.J. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 5 (2004) 844-852
31. Marjaux E., Hartmann D., and De Strooper B. Presenilins in memory, Alzheimer's disease, and therapy. Neuron 42 (2004) 189-192
32. Miyamoto E. Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J. Pharmacol. Sci. 100 5 (2006) 433-442 (Review)
33. Moechars D., Dewachter I., Lorent K., Reverse D., Baekelandt V., Naidu A., Tesseur I., Spittaels K., Van Den Haute C., Checler F., Godaux E., Cordell B., and Van Leuven F. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J. Biol. Chem. 274 (1999) 6483-6492
34. Murayama O., Tomita T., Nihonmatsu N., Murayama M., Sun X., Honda T., Iwatsubo T., and Takashima A. Enhancement of amyloid beta 42 secretion by 28 different presenilin 1 mutations of familial Alzheimer's disease. Neurosci. Lett. 265 (1999) 61-63
35. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., and LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39 3 (2003) 409-421
36. Parent A.T., Linden D.J., Sisodia S.S., and Borchelt D.R. Synaptic transmission and hippocampal long-term potentiation in transgenic mice expressing FAD-linked presenilin 1. Neurobiol. Dis. 6 (1999) 56-62
37. Parent A.T., Barnes N.Y., Taniguchi Y., Thinakaran G., and Sisodia S.S. Presenilin attenuates receptor-mediated signaling and synaptic function. J. Neurosci. 25 6 (2005) 1540-1549
38. Pozzo-Miller L., Gottschalk W.A., Zhang L., McDermott K., Du J., Gopalakrishnan R., Oho C., Shen Z., and Lu B. Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J. Neurosci. 19 (1999) 4972-4983
39. Rampon C., Tang Y.P., Goodhouse J., Shimizu E., Kyin M., and Tsien J.Z. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 3 (2000) 238-244
40. Ris L., Dewachter I., Reverse D., Godaux E., and Van Leuven F. Capacitative calcium entry induces hippocampal long term potentiation in the absence of presenilin-1. J. Biol. Chem. 278 (2003) 44393-44399
41. Rumpel S., LeDoux J., Zador A., and Malinow R. Postsynaptic receptor trafficking underlying a form of associative learning. Science 308 (2005) 83-88
42. Saura C., Choi S., Beglopoulos V., Malkani S., Zhang D., Shankaranarayana Rao B., Chattarji S., Kelleher III R.J., Kandel E., Duff K., Kirkwood A., and Shen J. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42 (2004) 23-36
43. Schellenberg G.D., D'Souza I., and Poorkaj P. The genetics of Alzheimer's disease. Curr. Psychiatry Rep. 2 (2000) 158-164
44. Schikorski T., and Stevens C.F. Morphological correlates of functionally defined synaptic vesicle populations. Nat. Neurosci. 4 4 (2001) 391-395
45. Schneider I., Reverse D., Dewachter I., Ris L., Caluwaerts N., Kuiperi C., Gilis M., Geerts H., Kretzschmar H., Godaux E., Moechars D., Van Leuven F., and Herms J. Mutant presenilins disturb neuronal calcium homeostasis in the brain of transgenic mice, decreasing the threshold for excitotoxicity and facilitating long-term potentiation. J. Biol. Chem. 276 (2001) 11539-11544
46. Spittaels K., Van den Haute C., Van Dorpe J., Geerts H., Mercken M., Bruynseels K., Lasrado R., Vandezande K., Laenen I., Boon T., Van Lint J., Vandenheede J., Moechars D., Loos R., and Van Leuven F. Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J. Biol. Chem. 275 52 (2000) 41340-41349
47. Steiner H. Uncovering gamma-secretase. Curr. Alzheimer Res. 1 (2004) 175-181
48. Tanemura K., Chui D.H., Fukuda T., Murayama M., Park J.M., Akagi T., Tatebayashi Y., Miyasaka T., Kimura T., Hashikawa T., Nakano Y., Kudo T., Takeda M., and Takashima A. Formation of tau inclusions in knock-in mice with familial Alzheimer disease (FAD) mutation of presenilin 1 (PS1). J. Biol. Chem. 281 8 (2006) 5037-5041
49. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., and Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature 401 (1999) 63-69
50. Tartaglia N., Du J., Tyler W.J., Neale E., Pozzo-Miller L., and Lu B. Protein synthesis-dependent and -independent regulation of hippocampal synapses by brain-derived neurotrophic factor. J. Biol. Chem. 276 40 (2001) 37585-37593
51. Thinakaran G., and Parent A.T. Identification of the role of presenilins beyond Alzheimer's disease. Pharmacol. Res. 50 (2004) 411-418
52. Tischmeyer W., and Grimm R. Activation of immediate early genes and memory formation. Cell Mol. Life Sci. 55 4 (1999) 564-574 (Review)
53. Vaucher E., Fluit P., Chishti M.A., Westaway D., Mount H.T., and Kar S. Object recognition memory and cholinergic parameters in mice expressing human presenilin 1 transgenes. Exp. Neurol. 175 2 (2002) 398-406
54. Walikonis R.S., Jensen O.N., Mann M., Provance Jr. D.W., Mercer J.A., and Kennedy M.B. Identification of proteins in the postsynaptic density fraction by mass spectrometry. J. Neurosci. 20 (2000) 4069-4080
55. Wang R., Dineley K.T., Sweatt J.D., and Zheng H. Presenilin 1 familial Alzheimer's disease mutation leads to defective associative learning and impaired adult neurogenesis. Neuroscience 126 2 (2004) 305-312
56. Wong R.W., Setou M., Teng J., Takei Y., and Hirokawa N. Overexpression of motor protein KIF17 enhances spatial and working memory in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 14500-14505
57. Yoo A.S., Cheng I., Chung S., Grenfell T.Z., Lee H., Pack-Chung E., Handler M., Shen J., Xia W., Tesco G., Saunders A.J., Ding K., Frosch M.P., Tanzi R.E., and Kim T.W. Presenilin-mediated modulation of capacitative calcium entry. Neuron 27 (2000) 411-412
58. Yu H., Saura C.A., Choi S.Y., Sun L.D., Yang X., Handler M., Kawarabayashi T., Younkin L., Fedeles B., Wilson M.A., Younkin S., Kandel E.R., Kirkwood A., and Shen J. APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron 31 5 (2001) 713-726
59. Zhao M.G., Toyoda H., Lee Y.S., Wu L.J., Ko S.W., Zhang X.H., Jia Y., Shum F., Xu H., Li B.M., Kaang B.K., and Zhuo M. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47 6 (2005) 859-872