Neurobiology of Aging
Volume 32, Issue 12 , Pages 2219-2228 , December 2011

Early neuronal dysfunction by amyloid β oligomers depends on activation of NR2B-containing NMDA receptors

  • Raik Rönicke

      Affiliations

    • Project Group Neuropharmacology, Leibniz Institute for Neurobiology, Brenneckestrasse 6, 39118 Magdeburg, Germany
    • German Center for Neurodegenerative Diseases (DZNE), Location Magdeburg, Germany
  • ,
  • Marina Mikhaylova

      Affiliations

    • Project Group Neuroplasticity, Leibniz Institute for Neurobiology, Brenneckestrasse 6, 39118 Magdeburg, Germany
  • ,
  • Sabine Rönicke

      Affiliations

    • Institute for Neurobiochemistry, Otto-von-Guericke-University Magdeburg, Leipziger Strasse 44, D-39120 Magdeburg, Germany
  • ,
  • Jessica Meinhardt

      Affiliations

    • Leibniz Institute for Age Research, Beutenbergstraβe 11, 07745 Jena, Germany
  • ,
  • Ulrich H. Schröder

      Affiliations

    • Project Group Neuropharmacology, Leibniz Institute for Neurobiology, Brenneckestrasse 6, 39118 Magdeburg, Germany
  • ,
  • Marcus Fändrich

      Affiliations

    • Max Planck Research Unit for Enzymology of Protein Folding, Weinbergweg 22, 06120 Halle (Saale), Germany
    • Martin-Luther University Halle-Wittenberg, Germany
  • ,
  • Georg Reiser

      Affiliations

    • Institute for Neurobiochemistry, Otto-von-Guericke-University Magdeburg, Leipziger Strasse 44, D-39120 Magdeburg, Germany
  • ,
  • Michael R. Kreutz

      Affiliations

    • Project Group Neuroplasticity, Leibniz Institute for Neurobiology, Brenneckestrasse 6, 39118 Magdeburg, Germany
    • German Center for Neurodegenerative Diseases (DZNE), Location Magdeburg, Germany
  • ,
  • Klaus G. Reymann

      Affiliations

    • Project Group Neuropharmacology, Leibniz Institute for Neurobiology, Brenneckestrasse 6, 39118 Magdeburg, Germany
    • German Center for Neurodegenerative Diseases (DZNE), Location Magdeburg, Germany
    • Corresponding Author InformationCorresponding author at: Leibniz Institute for Neurobiology, Project Group Neuropharmacology, Brenneckestrasse 6, 39118 Magdeburg, Germany. Tel.: +49 3916263437.

Received 15 July 2009 ,Revised 12 January 2010 ,Accepted 14 January 2010.

References 

  1. Berberich S, Jensen V, Hvalby Ø, Seeburg PH, Köhr G. The role of NMDAR subtypes and charge transfer during hippocampal LTP induction. Neuropharmacology. 2007;52:77–86
  2. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, et al. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science. 2008;321:1686–1689
  3. Calabrese B, Shaked GM, Tabarean IV, Braga J, Koo EH, Halpain S. Rapid, concurrent alterations in pre- and postsynaptic structure induced by naturally-secreted amyloid-beta protein. Mol. Cell. Neurosci. 2007;35:183–193
  4. Christie BR, Stellwagen D, Abraham WC . Reduction of the threshold for long-term potentiation by prior theta-frequency synaptic activity. Hippocampus. 1995;5:52–59
  5. Cohen E, Ivenshitz M, Amor-Baroukh V, Greenberger V, Segal M. Determinants of spontaneous activity in networks of cultured hippocampus. Brain Res. 2008;1235:21–30
  6. De Felice FG, Velasco PT, Lambert MP, Viola K, Fernandez SJ, Ferreira ST, et al. Abeta oligomers induce neuronal oxidative stress through an N-methyl-d-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J. Biol. Chem. 2007;282:11590–11601
  7. Dieterich DC, Karpova A, Mikhaylova M, Zdobnova I, Konig I, Landwehr M, et al. Caldendrin-Jacob: a protein liaison that couples NMDA receptor signalling to the nucleus. PLoS Biol. 2008;6:e34
  8. Eckert A, Hauptmann S, Meinhardt J, Rhein V, Dröse S, Brandt U, et al. Oligomeric and fibrillar species of β-amyloid (Aβ42) both impair mitochondrial function in P301L tau transgenic mice. J. Mol. Med. 2008;86:1255–1267
  9. Fändrich M. On the structural definition of amyloid fibrils and other polypeptide aggregates. Cell. Mol. Life Sci. 2007;64:2066–2078
  10. Gortz P, Opatz J, Siebler M, Funke SA, Willbold D, Lange-Asschenfeldt C. Transient reduction of spontaneous neuronal network activity by sublethal amyloid beta (1-42) peptide concentrations. J. Neural Transm. 2009;116:351–355
  11. Habicht G, Haupt C, Friedrich RP, Hortschansky P, Sachse C, Meinhardt J, et al. Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing A protofibrils. Proc. Natl. Acad. Sci. U.S.A. 2007;104:19232–19237
  12. Hardingham GE, Fukunaga Y, Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 2002;5:405–414
  13. Harris AZ, Pettit DL. Recruiting extrasynaptic NMDA receptors augments synaptic signaling. J. Neurophysiol. 2008;2:524–533
  14. Hein S, Schonfeld P, Kahlert S, Reiser G. Toxic effects of X-linked adrenoleukodystrophy-associated, very long chain fatty acids on glial cells and neurons from rat hippocampus in culture. Hum. Mol. Genet. 2008;17:1750–1761
  15. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, et al. AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron. 2006;52:831–843
  16. Hu NW, Klyubin I, Anwy R, Rowan MJ. GluN2B subunit-containing NMDA receptor antagonists prevent Abeta-mediated synaptic plasticity disruption in vivo. Proc. Natl. Acad. Sci. U.S.A. 2009;106:20504–20509
  17. Hynd MR, Scott HL, Dodd PR. Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer's disease. Neurochem. Int. 2004;45:583–595
  18. Klein WL. Abeta toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem. Int. 2002;41:345–352
  19. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT, Wood M, et al. Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J. Neurosci. 2007;27:796–807
  20. Li S, Hong S, Shepardson NE, Walsh DM, Shankar GM, Selkoe D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron. 2009;62:788–801
  21. Liu Y, Wong TP, Aarts M, Rooyakkers A, Liu L, Lai TW, et al. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J. Neurosci. 2007;27:2846–2857
  22. Lynch AM, Loane DJ, Minogue AM, Clarke R, Kilroy D, Nally RE, et al. Eicosapentaenoic acid confers neuroprotection in the amyloid-beta challenged aged hippocampus. Neurobiol. Aging. 2007;28:845–855
  23. Papadia S, Hardingham GE. The dichotomy of NMDA receptor signaling. Neuroscientist. 2007;13:572–579
  24. Raymond CR, Ireland DR, Abraham WC. NMDA receptor regulation by amyloid-beta does not account for its inhibition of LTP in rat hippocampus. Brain Res. 2003;968:263–272
  25. Ronicke R, Klemm A, Meinhardt J, Schroder UH, Fandrich M, Reymann KG. Abeta mediated diminution of MTT reduction—an artefact of single cell culture?. PLoS ONE. 2008;3:e3236
  26. Rowan MJ, Klyubin I, Wang Q, Hu NW, Anwyl R. Synaptic memory mechanisms: Alzheimer's disease amyloid beta-peptide-induced dysfunction. Biochem. Soc. Trans. 2007;35:1219–1223
  27. Santos SF, Pierrot N, Morel N, Gailly P, Sindic C, Octave JN. Expression of human amyloid precursor protein in rat cortical neurons inhibits calcium oscillations. J. Neurosci. 2009;15:4708–4718
  28. Schroder UH, Muller T, Schreiber R, Stolle A, Zuschratter W, Balschun D, et al. The potent non-competitive mGlu1 receptor antagonist BAY 36-7620 differentially affects synaptic plasticity in area cornu ammonis 1 of rat hippocampal slices and impairs acquisition in the water maze task in mice. Neuroscience. 2008;157:385–395
  29. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J. Neurosci. 2007;27:2866–2875
  30. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 2008;14:837–842
  31. Sheng M, Cummings J, Roldan LA, Jan YN, Yeh L. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature. 1994;368:144–147
  32. Small DH. Network dysfunction in Alzheimer's disease: does synaptic scaling drive disease progression?. Trends Mol. Med. 2008;3:103–108
  33. Tanaka J, Horiike Y, Matsuzaki M, Miyazaki T, Ellis-Davies GC, Kasai H. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science. 2008;319:1683–1687
  34. Ting JT, Kelley BG, Lambert TJ, Cook DG, Sullivan JM. Amyloid precursor protein overexpression depresses excitatory transmission through both presynaptic and postsynaptic mechanisms. Proc. Natl. Acad. Sci. U.S.A. 2007;104:353–358
  35. Tong L, Thornton PL, Balazs R, Cotman CW. Beta-amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival is not compromised. J. Biol. Chem. 2001;276:17301–17306
  36. Viola KL, Velasco PT, Klein WL. Why Alzheimer's is a disease of memory: the attack on synapses by A beta oligomers (ADDLs). J. Nutr. Health Aging. 2008;12:51S–57S
  37. Walsh DM, Selkoe DJ. A beta oligomers—a decade of discovery. J. Neurochem. 2007;101:1172–1184

PII: S0197-4580(10)00041-2

doi: 10.1016/j.neurobiolaging.2010.01.011

Neurobiology of Aging
Volume 32, Issue 12 , Pages 2219-2228 , December 2011