Active immunization with amyloid-beta 1-42 impairs memory performance through TLR2/4-dependent activation of the innate immune system

J Immunol. 2010 Nov 15;185(10):6338-47. doi: 10.4049/jimmunol.1001765. Epub 2010 Oct 13.

Abstract

Active immunization with amyloid-β (Aβ) peptide 1-42 reverses amyloid plaque deposition in the CNS of patients with Alzheimer's disease and in amyloid precursor protein transgenic mice. However, this treatment may also cause severe, life-threatening meningoencephalitis. Physiological responses to immunization with Aβ(1-42) are poorly understood. In this study, we characterized cognitive and immunological consequences of Aβ(1-42)/CFA immunization in C57BL/6 mice. In contrast to mice immunized with myelin oligodendrocyte glycoprotein (MOG)(35-55)/CFA or CFA alone, Aβ(1-42)/CFA immunization resulted in impaired exploratory activity, habituation learning, and spatial-learning abilities in the open field. As morphological substrate of this neurocognitive phenotype, we identified a disseminated, nonfocal immune cell infiltrate in the CNS of Aβ(1-42)/CFA-immunized animals. In contrast to MOG(35-55)/CFA and PBS/CFA controls, the majority of infiltrating cells in Aβ(1-42)/CFA-immunized mice were CD11b(+)CD14(+) and CD45(high), indicating their blood-borne monocyte/macrophage origin. Immunization with Aβ(1-42)/CFA was significantly more potent than immunization with MOG(35-55)/CFA or CFA alone in activating macrophages in the secondary lymphoid compartment and peripheral tissues. Studies with TLR2/4-deficient mice revealed that the TLR2/4 pathway mediated the Aβ(1-42)-dependent proinflammatory cytokine release from cells of the innate immune system. In line with this, TLR2/4 knockout mice were protected from cognitive impairment upon immunization with Aβ(1-42)/CFA. Thus, this study identifies adjuvant effects of Aβ(1-42), which result in a clinically relevant neurocognitive phenotype highlighting potential risks of Aβ immunotherapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic / pharmacology
  • Alzheimer Vaccines / adverse effects*
  • Alzheimer Vaccines / immunology
  • Amyloid beta-Peptides / immunology*
  • Amyloid beta-Peptides / pharmacology
  • Animals
  • Behavior, Animal / drug effects
  • Brain / immunology
  • Brain / pathology
  • Cell Separation
  • Cytokines / biosynthesis
  • Enzyme-Linked Immunosorbent Assay
  • Female
  • Flow Cytometry
  • Freund's Adjuvant / immunology
  • Freund's Adjuvant / pharmacology
  • Humans
  • Immunity, Innate / immunology*
  • Macrophages / immunology
  • Memory Disorders / immunology*
  • Memory Disorders / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Monocytes / immunology
  • Peptide Fragments / immunology*
  • Peptide Fragments / pharmacology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Toll-Like Receptor 2 / biosynthesis
  • Toll-Like Receptor 2 / immunology
  • Toll-Like Receptor 4 / biosynthesis
  • Toll-Like Receptor 4 / immunology
  • Vaccination / adverse effects*

Substances

  • Adjuvants, Immunologic
  • Alzheimer Vaccines
  • Amyloid beta-Peptides
  • Cytokines
  • Peptide Fragments
  • Tlr2 protein, mouse
  • Tlr4 protein, mouse
  • Toll-Like Receptor 2
  • Toll-Like Receptor 4
  • amyloid beta-protein (1-42)
  • Freund's Adjuvant