Neurobiology of Aging
Volume 29, Issue 5 , Pages 639-652 , May 2008

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

  • I. Dewachter

      Affiliations

    • Experimental Genetics Group, K.U.Leuven, 3000 Leuven, Belgium
    • ,
  • L. Ris

      Affiliations

    • Laboratory of Neurosciences, University of Mons-Hainaut, 7000 Mons, Belgium
    • ,
  • S. Croes

      Affiliations

    • Experimental Genetics Group, K.U.Leuven, 3000 Leuven, Belgium
    • ,
  • P. Borghgraef

      Affiliations

    • Experimental Genetics Group, K.U.Leuven, 3000 Leuven, Belgium
    • ,
  • H. Devijver

      Affiliations

    • Experimental Genetics Group, K.U.Leuven, 3000 Leuven, Belgium
    • ,
  • T. Voets

      Affiliations

    • Laboratory of Physiology, K.U.Leuven, 3000 Leuven, Belgium
    • ,
  • B. Nilius

      Affiliations

    • Laboratory of Physiology, K.U.Leuven, 3000 Leuven, Belgium
    • ,
  • E. Godaux

      Affiliations

    • Laboratory of Neurosciences, University of Mons-Hainaut, 7000 Mons, Belgium
    • ,
  • F. Van Leuven

      Affiliations

    • Experimental Genetics Group, K.U.Leuven, 3000 Leuven, Belgium
    • Corresponding Author InformationCorresponding author at: Experimental Genetics Group (LEGT_EGG), K.U.Leuven, Campus Gasthuisberg, ON1-06.602, 3000 Leuven, Belgium. Tel.: +32 16 34 58 88; fax: +32 16 34 58 71.

Received 7 August 2006 ,Revised 9 November 2006 ,Accepted 25 November 2006.

References 

  1. Baki L, Shioi J, Wen P, Shao Z, Schwarzman A, Gama-Sosa M, et al. PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: effects of FAD mutations. EMBO J. 2004;23(13):2586–2596
  2. Barria A, Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron. 2005;48(2):289–301
  3. Barrow PA, Empson RM, Gladwell SJ, Anderson CM, Killick R, Yu X, et al. Functional phenotype in transgenic mice expressing mutant human presenilin-1. Neurobiol. Dis. 2000;7(2):119–126
  4. Berberich S, Punnakkal P, Jensen V, Pawlak V, Seeburg PH, Hvalby O, et al. Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J. Neurosci. 2005;25(29):6907–6910
  5. Buee-Scherrer V, Condamines O, Mourton-Gilles C, Jakes R, Goedert M, Pau B, et al. AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease. Brain Res. Mol. Brain Res. 1996;39(1/2):79–88
  6. Carlin RK, Grab DJ, Cohen RS, Siekevitz P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell. Biol. 1980;86:831–843
  7. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, Annaert W, et al. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature. 1998;391:339–340
  8. Dewachter I, Van Dorpe J, Smeijers L, Gilis M, Kuiperi C, Laenen I, et al. 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. 2000;20:6452–6458
  9. Dewachter I, Reverse D, Caluwaerts N, Ris L, Kuiperi C, Van den Haute C, 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. 2002;22:3445–3453
  10. Dobrunz LE, Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron. 1997;18(6):995–1008
  11. Doglio LE, Kanwar R, Jackson GR, Perez M, Avila J, Dingwall C, et al. Gamma-cleavage-independent functions of presenilin, nicastrin, and Aph-1 regulate cell-junction organization and prevent tau toxicity in vivo. Neuron. 2006;50(3):359–375
  12. Feng R, Rampon C, Tang YP, Shrom D, Jin J, Kyin M, et al. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron. 2001;32(5):911–926
  13. Feng R, Wang H, Wang J, Shrom D, Zeng X, Tsien JZ. Forebrain degeneration and ventricle enlargement caused by double knockout of Alzheimer's presenilin-1 and presenilin-2. Proc. Natl. Acad. Sci. U.S.A. 2004;101(21):8162–8167
  14. Fleischmann A, Hvalby O, Jensen V, Strekalova T, Zacher C, Layer LE, et al. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J. Neurosci. 2003;23(27):9116–9122
  15. Herms J, Tings T, Gall S, Madlung A, Giese A, Siebert H, et al. Evidence of presynaptic location and function of the prion protein. J. Neurosci. 1999;19:8866–8875
  16. Herms J, Schneider I, Dewachter I, Caluwaerts N, Kretzschmar H, 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. 2003;278:2484–2489
  17. Huang XG, Yee BK, Nag S, Chan ST, 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. 2003;183(2):673–681
  18. Huang KP, Huang FL, Jager T, Li J, Reymann KG, Balschun D. Neurogranin/RC3 enhances long-term potentiation and learning by promoting calcium-mediated signaling. J. Neurosci. 2004;24(47):10660–10669
  19. Hutton M, Hardy J. The presenilins and Alzheimer's disease. Hum. Mol. Genet. 1997;6:1639–1646
  20. Iwatsubo T. The gamma-secretase complex: machinery for intramembrane proteolysis. Curr. Opin. Neurobiol. 2004;14:379–383
  21. Janus C, D’Amelio S, Amitay O, Chishti MA, Strome R, Fraser P, et al. Spatial learning in transgenic mice expressing human presenilin 1 (PS1) transgenes. Neurobiol. Aging. 2000;21(4):541–549
  22. Kennedy MB. The postsynaptic density at glutamatergic synapses. Trends Neurosci. 1997;20:264–268
  23. Peters A, Palay S, Webster H. The Fine Structure of the Nervous System. Oxford: Oxford University Press; 1991;
  24. Koo EH, Kopan R. Potential role of presenilin-regulated signaling pathways in sporadic neurodegeneration. Nat. Med. 2004;10:26–33
  25. Kopan R, Ilagan MXG. Gamma-secretase: proteasome of the membrane?. Nat. Rev. Mol. Cell Biol. 2004;5:499–504
  26. Leissring MA, Akbari Y, Fanger CM, Cahalan MD, Mattson MP, LaFerla FM. Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice. J. Cell Biol. 2000;149:793–798
  27. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, et al. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science. 2004;304(5673):1021–1024
  28. Malleret G, Haditsch U, Genoux D, Jones MW, Bliss TV, Vanhoose AM, et al. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell. 2001;104:675–686
  29. Maren S, Holt W. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav. Brain Res. 2000;110:97–108
  30. Maren S, Quirk GJ. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 2004;5:844–852
  31. Marjaux E, Hartmann D, De Strooper B. Presenilins in memory, Alzheimer's disease, and therapy. Neuron. 2004;42:189–192
  32. Miyamoto E. Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J. Pharmacol. Sci. 2006;100(5):433–442(Review)
  33. Moechars D, Dewachter I, Lorent K, Reverse D, Baekelandt V, Naidu A, et al. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J. Biol. Chem. 1999;274:6483–6492
  34. Murayama O, Tomita T, Nihonmatsu N, Murayama M, Sun X, Honda T, et al. Enhancement of amyloid beta 42 secretion by 28 different presenilin 1 mutations of familial Alzheimer's disease. Neurosci. Lett. 1999;265:61–63
  35. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron. 2003;39(3):409–421
  36. Parent AT, Linden DJ, Sisodia SS, Borchelt DR. Synaptic transmission and hippocampal long-term potentiation in transgenic mice expressing FAD-linked presenilin 1. Neurobiol. Dis. 1999;6:56–62
  37. Parent AT, Barnes NY, Taniguchi Y, Thinakaran G, Sisodia SS. Presenilin attenuates receptor-mediated signaling and synaptic function. J. Neurosci. 2005;25(6):1540–1549
  38. Pozzo-Miller L, Gottschalk WA, Zhang L, McDermott K, Du J, Gopalakrishnan R, et al. Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J. Neurosci. 1999;19:4972–4983
  39. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 2000;3:238–244
  40. Ris L, Dewachter I, Reverse D, Godaux E, Van Leuven F. Capacitative calcium entry induces hippocampal long term potentiation in the absence of presenilin-1. J. Biol. Chem. 2003;278:44393–44399
  41. Rumpel S, LeDoux J, Zador A, Malinow R. Postsynaptic receptor trafficking underlying a form of associative learning. Science. 2005;308:83–88
  42. Saura C, Choi S, Beglopoulos V, Malkani S, Zhang D, Shankaranarayana Rao B, et al. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron. 2004;42:23–36
  43. Schellenberg GD, D'Souza I, Poorkaj P. The genetics of Alzheimer's disease. Curr. Psychiatry Rep. 2000;2:158–164
  44. Schikorski T, Stevens CF. Morphological correlates of functionally defined synaptic vesicle populations. Nat. Neurosci. 2001;4(4):391–395
  45. Schneider I, Reverse D, Dewachter I, Ris L, Caluwaerts N, Kuiperi C, et al. 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. 2001;276:11539–11544
  46. Spittaels K, Van den Haute C, Van Dorpe J, Geerts H, Mercken M, Bruynseels K, et al. 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. 2000;275(52):41340–41349
  47. Steiner H. Uncovering gamma-secretase. Curr. Alzheimer Res. 2004;1:175–181
  48. Tanemura K, Chui DH, Fukuda T, Murayama M, Park JM, Akagi T, et al. Formation of tau inclusions in knock-in mice with familial Alzheimer disease (FAD) mutation of presenilin 1 (PS1). J. Biol. Chem. 2006;281(8):5037–5041
  49. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, et al. Genetic enhancement of learning and memory in mice. Nature. 1999;401:63–69
  50. Tartaglia N, Du J, Tyler WJ, Neale E, Pozzo-Miller L, Lu B. Protein synthesis-dependent and -independent regulation of hippocampal synapses by brain-derived neurotrophic factor. J. Biol. Chem. 2001;276(40):37585–37593
  51. Thinakaran G, Parent AT. Identification of the role of presenilins beyond Alzheimer's disease. Pharmacol. Res. 2004;50:411–418
  52. Tischmeyer W, Grimm R. Activation of immediate early genes and memory formation. Cell Mol. Life Sci. 1999;55(4):564–574(Review)
  53. Vaucher E, Fluit P, Chishti MA, Westaway D, Mount HT, Kar S. Object recognition memory and cholinergic parameters in mice expressing human presenilin 1 transgenes. Exp. Neurol. 2002;175(2):398–406
  54. Walikonis RS, Jensen ON, Mann M, Provance DW, Mercer JA, Kennedy MB. Identification of proteins in the postsynaptic density fraction by mass spectrometry. J. Neurosci. 2000;20:4069–4080
  55. Wang R, Dineley KT, Sweatt JD, Zheng H. Presenilin 1 familial Alzheimer's disease mutation leads to defective associative learning and impaired adult neurogenesis. Neuroscience. 2004;126(2):305–312
  56. Wong RW, Setou M, Teng J, Takei Y, Hirokawa N. Overexpression of motor protein KIF17 enhances spatial and working memory in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 2002;99:14500–14505
  57. Yoo AS, Cheng I, Chung S, Grenfell TZ, Lee H, Pack-Chung E, et al. Presenilin-mediated modulation of capacitative calcium entry. Neuron. 2000;27:411–412
  58. Yu H, Saura CA, Choi SY, Sun LD, Yang X, Handler M, et al. APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron. 2001;31(5):713–726
  59. Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, et al. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron. 2005;47(6):859–872

PII: S0197-4580(06)00441-6

doi: 10.1016/j.neurobiolaging.2006.11.019

Neurobiology of Aging
Volume 29, Issue 5 , Pages 639-652 , May 2008

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