The amyloid cascade-inflammatory hypothesis of Alzheimer disease: implications for therapy

Acta Neuropathol. 2013 Oct;126(4):479-97. doi: 10.1007/s00401-013-1177-7. Epub 2013 Sep 20.

Abstract

The amyloid cascade hypothesis is widely accepted as the centerpiece of Alzheimer disease (AD) pathogenesis. It proposes that abnormal production of beta amyloid protein (Abeta) is the cause of AD and that the neurotoxicity is due to Abeta itself or its oligomeric forms. We suggest that this, in itself, cannot be the cause of AD because demonstrating such toxicity requires micromolar concentrations of these Abeta forms, while their levels in brain are a million times lower in the picomolar range. AD probably results from the inflammatory response induced by extracellular Abeta deposits, which later become enhanced by aggregates of tau. The inflammatory response, which is driven by activated microglia, increases over time as the disease progresses. Disease-modifying therapeutic attempts to date have failed and may continue to do so as long as the central role of inflammation is not taken into account. Multiple epidemiological and animal model studies show that NSAIDs, the most widely used antiinflammatory agents, have a substantial sparing effect on AD. These studies provide a proof of concept regarding the anti-inflammatory approach to disease modification. Biomarker studies have indicated that early intervention may be necessary. They have established that disease onset occurs more than a decade before it becomes clinically evident. By combining biomarker and pathological data, it is possible to define six phases of disease development, each separated by about 5 years. Phase one can be identified by decreases in Abeta in the CSF, phase 2 by increases of tau in the CSF plus clear evidence of Abeta brain deposits by PET scanning, phase 3 by slight decreases in brain metabolic rate by PET-FDG scanning, phase 4 by slight decreases in brain volume by MRI scanning plus minimal cognitive impairment, phase 5 by increased scanning abnormalities plus clinical diagnosis of AD, and phase 6 by advanced AD requiring institutional care. Utilization of antiinflammatory agents early in the disease process remains an overlooked therapeutic opportunity. Such agents, while not preventative, have the advantage of being able to inhibit the consequences of both Abeta and tau aggregation. Since there is more than a decade between disease onset and cognitive decline, a window of opportunity exists to introduce truly effective disease-modifying regimens. Taking advantage of this opportunity is the challenge for the future.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Alzheimer Disease / genetics*
  • Alzheimer Disease / metabolism
  • Alzheimer Disease / pathology
  • Alzheimer Disease / therapy*
  • Alzheimer Vaccines / therapeutic use
  • Amyloid / genetics*
  • Amyloid beta-Peptides / genetics
  • Amyloid beta-Protein Precursor / genetics
  • Animals
  • Animals, Genetically Modified
  • Anti-Inflammatory Agents / therapeutic use
  • Anti-Inflammatory Agents, Non-Steroidal / therapeutic use
  • Antioxidants / therapeutic use
  • Biomarkers
  • Diet
  • Humans
  • Immunization
  • Inflammation / genetics*
  • Inflammation / metabolism
  • Inflammation / pathology
  • Mutation / genetics
  • Peptide Fragments / genetics
  • Translational Research, Biomedical

Substances

  • Alzheimer Vaccines
  • Amyloid
  • Amyloid beta-Peptides
  • Amyloid beta-Protein Precursor
  • Anti-Inflammatory Agents
  • Anti-Inflammatory Agents, Non-Steroidal
  • Antioxidants
  • Biomarkers
  • Peptide Fragments
  • amyloid beta-protein (1-42)