Neurobiology of Aging
Volume 30, Issue 10 , Pages 1608-1613 , October 2009

Inhibition of LTP by beta-amyloid is prevented by activation of β2 adrenoceptors and stimulation of the cAMP/PKA signalling pathway

  • Qin-wen Wang

      Affiliations

    • Department of Physiology, Trinity College, Dublin 2, Ireland
    • Department of Physiology and Pharmacology, Medical School, Ningbo University, Ningbo, China
  • ,
  • Michael J. Rowan

      Affiliations

    • Department of Experimental Therapeutics, Trinity College, Dublin 2, Ireland
  • ,
  • Roger Anwyl

      Affiliations

    • Department of Physiology, Trinity College, Dublin 2, Ireland
    • Corresponding Author InformationCorresponding author. Tel.: +353 1 8961624; fax: +353 1 6793545.

Received 31 August 2007 ,Revised 10 December 2007 ,Accepted 11 December 2007.

References 

  1. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol. Aging. 2000;21:383–421
  2. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE. A cell surface receptor complex for fibrillar β-amyloid mediates microglial activation. J. Neurosci. 2003;23:2665–2674
  3. Bondareff W, Mountjoy CO, Roth M, Rossor MN, Iversen LL, Reynolds GP, et al. Neuronal degeneration in locus coeruleus and cortical correlates of Alzheimers disease. Alzheimer Dis. Assoc. Disord. 1987;1:256–262
  4. Colton CA, Chernyshev ON. Inhibition of microglial superoxide anion production by isoproterenol and dexamethasone. Neurochem. Int. 1996;29:43–53
  5. Combs CK, Johnson DJ, Cannady SB, Lehman TM, Landreth GE. Inflammatory mechanism in Alzheimers disease: inhibition of β-amyloid-stimulated proinflammatory responses and neurotoxicity by PPAR-gamma agonist. J. Neurosci. 2000;21:1179–1181
  6. Cotman CW, Su JH. Mechanisms of neuronal death in Alzheimer's disease. Brain Pathol. 1996;4:493–506
  7. Cullen WK, Suh YH, Anwyl R, Rowan MJ. Block of LTP in rat hippocampus in vivo by beta-amyloid precursor protein fragments. Neuroreport. 1997;8:3213–3217
  8. Dello Rosso C, Boullerne AI, Gavrilyuk V, Feinstein DL. Inhibition of microglial inflammatory responses by norepinephrine: effects on nitric oxide and interleukin 1beta production. J. Neuroinflamm. 2004;1:11–19
  9. Eikelenboom P, Zahn SS, van Gool WA, Allsop D. Inflammatory mechanisms in Alzheimer's disease. Trends Pharmacol. Sci. 1994;15:447–450
  10. Feinstein DL. Suppression of astroglial nitric oxide synthase expression by norepinephrine results from decreased NOS-2 promoter activity. J. Neurochem. 1998;70:1484–1496
  11. Feinstein DL, Heneka MT, Gavrilyuk V, Dello Russo C, Weinberg G, Galea E. Noradrenergic regulation of inflammatory gene expression in brain. Neurochem. Int. 2002;41:357–365
  12. Fujita H, Tanaka J, Maeda N, Sakanaka M. Adrenergic agonists suppress the proliferation of microglia through β2 adrenergic receptor. Neurosci. Lett. 1996;242:37–40
  13. German DC, Manaye KF, White CL, Woodward DJ, McIntire DD, Smith WK, et al. Disease-specific patterns of locus coeruleus cell loss. Ann. Neurol. 1992;32:667–676
  14. Griffin WS, Sheng JC, Royston MC, Gentleman SM, McKenzie JE, Graham DI, et al. Glial–neuronal interactions in Alzheimer's disease: the potential role of a cytokine cycle in disease progression. Brain Pathol. 1998;8:65–72
  15. Heneka MT, Galea E, Gavriluyk V, Dumitrescu-Ozimek L, Daeschner J, O’Banion MK, et al. Noradrenergic depletion potentiates beta-amyloid-induced cortical inflammation: implications for Alzheimer's disease. J. Neurosci. 2002;22:2434–2442
  16. Hu XX, Goldmuntz EA, Brosnan CF. The effect of norepinephrine on endotoxin-mediated macrophage activation. J. Neuroimmunol. 1991;31:35–42
  17. Kalinin S, Gavrilyuk V, Polak PE, Heneka MT, Feinstein DL. Noradrenaline deficiency in brain increases beta-amyloid plaque burden in an animal model of Alzheimers disease. Neurobiol. Aging. 2007;28:1206–1214
  18. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, et al. Diffusible nonfibrillar ligands derived from Aβ1–42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. 1998;95:6448–6453
  19. MacKenzie IR, Munoz DG. Nonsteroidal anti-inflammatory use and Alzheimer-type pathology in ageing. Neurology. 1998;50:986–990
  20. Madrigal JL, Feinstein DL, Dello Russo C. Norepinephrine protects cortical neurons against microglial induced cell death. J. Neurosci. Res. 2005;81:390–396
  21. McGeer PL, McGeer EG. The inflammatory response system of the brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res. Rev. 1995;21:195–218
  22. Mori K, Ozaki E, Zhang B, Yang L, Yokoyama A, Takeda I, et al. Effects of norepinephrine on rat cultured microglial cells that express alpha1, alpha2, beta1 and beta2 adrenergic receptors. Neuropharmacology. 2002;43:1026–1034
  23. Small DH, Mok SS, Bornstein JC. Alzheimer's disease and Abeta toxicity: from top to bottom. Nat. Rev. Neurosci. 2002;8:595–598
  24. Stanton PK, Sarvey JM. Norepinephrine regulates long-term potentiation of both the population spike and dendritic EPSP in hippocampal dentate gyrus. Brain Res. Bull. 1987;18:115–119
  25. Tan J, et al. Microglial activation resulting from CD40–CD40L interaction after beta-amyloid stimulation. Science. 1999;286:2352–2355
  26. Vitolo OV, Sant’Angelo A, Costanzo V, Battaglia F, Arancio O, 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. 2002;99:13217–13221
  27. Walsh DM, Klyubuin I, Fadeeva J, Cullen WK, Anwyl R, Wolfe MS, et al. Naturally secreted oligomers of the Alzheimer amyloid β-protein potently inhibit long-term potentiation in vivo. Nature. 2002;416:535–539
  28. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, 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. 2004;24:3370–3378
  29. Wang Q, Rowan MJ, Anwyl R. Beta-amyloid-mediated inhibition of NMDA receptor-dependent long-term potentiation induction involves activation of microglia and stimulation of inducible nitric oxide synthase and superoxide. J. Neurosci. 2004;24:6049–6056
  30. Wang Q, Wu J, Rowan MJ, Anwyl R. Beta-amyloid inhibition of long-term potentiation is mediated via tumor necrosis factor. Eur. J. Neurosci. 2005;22:2827–2832
  31. Willis SA, Nisen PD. Inhibition of lipopolysaccharide-induced IL-1 beta transcription by cyclic adenosine monophosphate in human astrocytic cells. J. Immunol. 1995;154:1399–1406
  32. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, et al. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron. 1999;24:715–726
  33. Wu J, Rowan MJ, Anwyl R. Long-term potentiation is mediated by multiple kinase cascades involving CAMKII or p42/44 MAPK in the adult rat dentate gyrus in vitro. Neurophysiol. 2006;95:3519–3527

PII: S0197-4580(07)00470-8

doi: 10.1016/j.neurobiolaging.2007.12.004

Neurobiology of Aging
Volume 30, Issue 10 , Pages 1608-1613 , October 2009