Deregulation of NMDA-receptor function and down-stream signaling in APP[V717I] transgenic mice

Neurobiology of Aging

Volumn 30, Issue 2, 2009, Pages 241-256

  Dewachter, I ^a   Filipkowski, R K ^b   Priller, C ^c   Ris, L ^e   Neyton, J ^d   Croes, S ^a   Terwel, D ^a   Gysemans, M ^f   Devijver, H ^a   Borghgraef, P ^a   Godaux, E ^e   Kaczmarek, L ^b   Herms, J ^c   Van Leuven, F ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c UNIVERSITY OF MUNICH   (Germany)

^d ECOLE NORMALE SUPÉRIEURE   (France)

^e UNIVERSITY OF MONS   (Belgium)

^f KU LEUVEN   (Belgium)

Author keywords

Amyloid peptides; APP transgenic mice; c Fos; NMDA receptor; Oligomeric; Synaptic plasticity

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; AMYLOID PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; POSTSYNAPTIC DENSITY PROTEIN 95;

ANIMAL CELL; ARTICLE; BRAIN CELL; CALCIUM TRANSPORT; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MEMORY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYNAPSE; TRANSGENIC MOUSE; XENOPUS;

AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELLS, CULTURED; MICE; MICE, TRANSGENIC; NEURONS; PEPTIDE FRAGMENTS; RECEPTORS, CELL SURFACE; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION;

EID: 57749192464     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2007.06.011     Document Type: Article

References (58)

1. Almeida C.G., Tampellini D., Takahashi R.H., Greengard P., Lin M.T., Snyder E.M., and Gouras G.K. Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol. Dis. 20 2 (2005) 187-198
2. Aronin N., Chase K., Sagar S.M., Sharp F.R., and DiFiglia M. N-methyl-d-aspartate receptor activation in the neostriatum increases c-fos and fos-related antigens selectively in medium-sized neurons. Neuroscience 44 (1991) 409-420
3. Bliss T.V., and Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
4. 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
5. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V., Hyman B.T., Younkin S.G., and Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci. 2 3 (1999) 271-276
6. Cleary J.P., Walsh D.M., Hofmeister J.J., Shankar G.M., Kuskowski M.A., Selkoe D.J., and Ashe K.H. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci. 8 1 (2005) 79-84
7. Cole A.J., Saffen D.W., Baraban J.M., and Worley P.F. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340 (1989) 474-476
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 17 (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 9 (2002) 3445-3453
10. Dewachter I., Ris L., Croes S., Borghgraef P., Devijver H., Voets T., Nilius B., Godaux E., and Van Leuven F. Modulation of synaptic plasticity and Tau phosphorylation by wild-type and mutant presenilin1. Neurobiol. Aging 29 (2008) 639-652
11. Dineley K.T., Westerman M., Bui D., Bell K., Ashe K.H., and Sweatt J.D. Beta-amyloid activates the mitogen-activated protein kinase cascade via hippocampal alpha7 nicotinic acetylcholine receptors: In vitro and in vivo mechanisms related to Alzheimer's disease. J. Neurosci. 21 12 (2001) 4125-4133
12. 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., and Paul S.M. Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat. Neurosci. 5 5 (2002) 452-457
13. Filipkowski R.K., Rydz M., Berdel B., Morys J., and Kaczmarek L. Tactile experience induces c-fos expression in rat barrel cortex. Learn. Mem. 7 2 (2000) 116-122
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. Gong Y., Chang L., Viola K.L., Lacor P.N., Lambert M.P., Finch C.E., Krafft G.A., and Klein W.L. Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl. Acad. Sci. U.S.A. 100 18 (2003) 10417-10422
16. Gong B., Cao Z., Zheng P., Vitolo O.V., Liu S., Staniszewski A., Moolman D., Zhang H., Shelanski M., and Arancio O. Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 126 4 (2006) 775-788
17. Goto Y., Niidome T., Akaike A., Kihara T., and Sugimoto H. Amyloid beta-peptide preconditioning reduces glutamate-induced neurotoxicity by promoting endocytosis of NMDA receptor. Biochem. Biophys. Res. Commun. 351 1 (2006) 259-265
18. Hering H., and Sheng M. Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2 (2001) 880-888
19. Herrera D.G., and Robertson H.A. N-methyl-d-aspartate receptors mediate activation of the c-fos proto-oncogene in a model of brain injury. Neuroscience 35 (1990) 273-281
20. Hsieh H., Boehm J., Sato C., Iwatsubo T., Tomita T., Sisodia S., and Malinow R. AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52 5 (2006) 831-843
21. Kaczmarek L. c-Fos in learning: beyond the mapping of neuronal activity. Immediate Early Genes and Inducible Transcription Factors in Mapping of the Central Nervous System Function and Dysfunction. In: Kaczmarek L., and Robertson H.A. (Eds). Handbook of Chemical Neuroanatomy vol. 19 (2002), Elsevier, Amsterdam, Boston, London, New York, Oxford, Paris, San Diego, San Francisco, Singapore, Sydney, Tokyo 189-216
22. Kaczmarek L., and Chaudhuri A. Sensory regulation of immediate-early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity. Brain Res. Brain Res. Rev. 23 (1997) 237-256
23. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., and Malinow R. APP processing and synaptic function. Neuron 37 6 (2003) 925-937
24. Kayed R., Sokolov Y., Edmonds B., McIntire T.M., Milton S.C., Hall J.E., and Glabe C.G. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem. 279 45 (2004) 46363-46366
25. Klyubin I., Walsh D.M., Lemere C.A., Cullen W.K., Shankar G.M., Betts V., Spooner E.T., Jiang L., Anwyl R., Selkoe D.J., and Rowan M.J. Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat. Med. 11 5 (2005) 556-561
26. Lacor P.N., Buniel M.C., Chang L., Fernandez S.J., Gong Y., Viola K.L., Lambert M.P., Velasco P.T., Bigio E.H., Finch C.E., Krafft G.A., and Klein W.L. Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J. Neurosci. 24 45 (2004) 10191-10200
27. Lacor P.N., Buniel M.C., Furlow P.W., Clemente A.S., Velasco P.T., Wood M., Viola K.L., and Klein W.L. Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J. Neurosci. 27 4 (2007) 796-807
28. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., and Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95 11 (1998) 6448-6453
29. Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., and Ashe K.H. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440 7082 (2006) 352-357
30. Maren S., and Holt W. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav. Brain Res. 110 1-2 (2000 Jun. 1) 97-108
31. Maren S., and Quirk G.J. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 5 11 (2004 Nov.) 844-852
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 10 (1999) 6483-6492
34. 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
35. Paoletti P., Ascher P., and Neyton J. High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J. Neurosci. 17 (1997) 5711-5725
36. Platenik J., Kuramoto N., and Yoneda Y. Molecular mechanisms associated with long-term consolidation of the NMDA signals. Life Sci. 67 (2000) 335-364
37. Postina R., Schroeder A., Dewachter I., Bohl J., Schmitt U., Kojro E., Prinzen C., Endres K., Hiemke C., Blessing M., Flamez P., Dequenne A., Godaux E., Van Leuven F., and Fahrenholz F. A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J. Clin. Invest. 113 10 (2004) 1456-1464
38. Priller C., Dewachter I., Vassallo N., Paluch S., Pace C., Kretzschmar H.A., Van Leuven F., and Herms J. Mutant presenilin 1 alters synaptic transmission in cultured hippocampal neurons. J. Biol. Chem. 282 2 (2007) 1119-1127
39. Puzzo D., Vitolo O., Trinchese F., Jacob J.P., Palmeri A., and Arancio O. Amyloid-beta peptide inhibits activation of the nitric oxide/cGMP/cAMP-responsive element-binding protein pathway during hippocampal synaptic plasticity. J. Neurosci. 25 29 (2005) 6887-6897
40. Savonenko A., Werka T., Nikolaev E., Zielinski K., and Kaczmarek L. Complex effects of NMDA receptor antagonist APV in the basolateral amygdala on acquisition of two-way avoidance reaction and long-term fear memory. Learn. Mem. 10 (2003) 293-303
41. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 298 5594 (2002) 789-791 (Review)
42. Shankar G.M., Bloodgood B.L., Townsend M., Walsh D.M., Selkoe D.J., and Sabatini B.L. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J. Neurosci. 27 11 (2007) 2866-2875
43. Sheng M., and Pak D.T. Glutamate receptor anchoring proteins and the molecular organization of excitatory synapses. Ann. N.Y. Acad. Sci. 868 (1999) 483-493
44. Small D.H. Mechanisms of synaptic homeostasis in Alzheimer's disease. Curr. Alzheimer Res. 1 1 (2004) 27-32 (Review)
45. Small D.H., Mok S.S., and Bornstein J.C. Alzheimer's disease and Abeta toxicity: from top to bottom. Nat. Rev. Neurosci. 2 8 (2001) 595-598 (Review)
46. Snyder E.M., Nong Y., Almeida C.G., Paul S., Moran T., Choi E.Y., Nairn A.C., Salter M.W., Lombroso P.J., Gouras G.K., and Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nat. Neurosci. 8 8 (2005) 1051-1058
47. Stine Jr. W.B., Dahlgren K.N., Krafft G.A., and LaDu M.J. In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J. Biol. Chem. 278 13 (2003) 11612-11622
48. Tischmeyer W., and Grimm R. Activation of immediate early genes and memory formation. Cell Mol. Life Sci. 55 4 (1999) 564-574 (Review)
49. Van Dorpe J., Smeijers L., Dewachter I., Nuyens D., Spittaels K., Van Den Haute C., Mercken M., Moechars D., Laenen I., Kuiperi C., Bruynseels K., Tesseur I., Loos R., Vanderstichele H., Checler F., Sciot R., and Van Leuven F. Prominent cerebral amyloid angiopathy in transgenic mice overexpressing the london mutant of human APP in neurons. Am. J. Pathol. 157 4 (2000) 1283-1298
50. Vitolo O.V., Sant'Angelo A., Costanzo V., Battaglia F., Arancio O., and Shelanski M. Amyloid beta -peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc. Natl. Acad. Sci. U.S.A. 99 20 (2002) 13217-13221
51. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., and Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416 6880 (2002) 535-539
52. Walsh D.M., and Selkoe D.J. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44 1 (2004) 181-193 (Review)
53. Walsh D.M., Townsend M., Podlisny M.B., Shankar G.M., Fadeeva J.V., Agnaf O.E., Hartley D.M., and Selkoe D.J. Certain inhibitors of synthetic amyloid beta-peptide (Abeta) fibrillogenesis block oligomerization of natural Abeta and thereby rescue long-term potentiation. J. Neurosci. 25 10 (2005) 2455-2462
54. Walsh D.M., Klyubin I., Shankar G.M., Townsend M., Fadeeva J.V., Betts V., Podlisny M.B., Cleary J.P., Ashe K.H., Rowan M.J., and Selkoe D.J. The role of cell-derived oligomers of Abeta in Alzheimer's disease and avenues for therapeutic intervention. Biochem. Soc. Trans. 33 Pt 5 (2005) 1087-1090 Review
55. Wang H.W., Pasternak J.F., Kuo H., Ristic H., Lambert M.P., Chromy B., Viola K.L., Klein W.L., Stine W.B., Krafft G.A., and Trommer B.L. soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res. 924 2 (2002) 133-140
56. Wang H.Y., Lee D.H., D'Andrea M.R., Peterson P.A., Shank R.P., and Reitz A.B. beta-Amyloid (1-42) binds to alpha7 nicotinic acetylcholine receptor with high affinity. Implications for Alzheimer's disease pathology. J. Biol. Chem. 275 8 (2000) 5626-5632
57. Wang Q., Walsh D.M., Rowan M.J., Selkoe D.J., and Anwyl R. Block of long-term potentiation by naturally secreted and synthetic amyloid beta-peptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogen-activated protein kinase as well as metabotropic glutamate receptor type 5. J. Neurosci. 24 13 (2004) 3370-3378
58. Whitlock J.R., Heynen A.J., Shuler M.G., and Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 313 5790 (2006) 1093-1097