Modulators of γ-secretase activity can facilitate the toxic side-effects and pathogenesis of Alzheimer's disease

PLoS One. 2013;8(1):e50759. doi: 10.1371/journal.pone.0050759. Epub 2013 Jan 7.

Abstract

Background: Selective modulation of different Aβ products of an intramembrane protease γ-secretase, could be the most promising strategy for development of effective therapies for Alzheimer's disease. We describe how different drug-candidates can modulate γ-secretase activity in cells, by studying how DAPT affects changes in γ-secretase activity caused by gradual increase in Aβ metabolism.

Results: Aβ 1-40 secretion in the presence of DAPT shows biphasic activation-inhibition dose-response curves. The biphasic mechanism is a result of modulation of γ-secretase activity by multiple substrate and inhibitor molecules that can bind to the enzyme simultaneously. The activation is due to an increase in γ-secretase's kinetic affinity for its substrate, which can make the enzyme increasingly more saturated with otherwise sub-saturating substrate. The noncompetitive inhibition that prevails at the saturating substrate can decrease the maximal activity. The synergistic activation-inhibition effects can drastically reduce γ-secretase's capacity to process its physiological substrates. This reduction makes the biphasic inhibitors exceptionally prone to the toxic side-effects and potentially pathogenic. Without the modulation, γ-secretase activity on it physiological substrate in cells is only 14% of its maximal activity, and far below the saturation.

Significance: Presented mechanism can explain why moderate inhibition of γ-secretase cannot lead to effective therapies, the pharmacodynamics of Aβ-rebound phenomenon, and recent failures of the major drug-candidates such as semagacestat. Novel improved drug-candidates can be prepared from competitive inhibitors that can bind to different sites on γ-secretase simultaneously. Our quantitative analysis of the catalytic capacity can facilitate the future studies of the therapeutic potential of γ-secretase and the pathogenic changes in Aβ metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / drug therapy*
  • Alzheimer Disease / enzymology*
  • Alzheimer Disease / metabolism
  • Alzheimer Disease / pathology
  • Amyloid Precursor Protein Secretases / antagonists & inhibitors*
  • Amyloid Precursor Protein Secretases / metabolism
  • Amyloid beta-Peptides / adverse effects
  • Amyloid beta-Peptides / metabolism*
  • Dipeptides / adverse effects
  • Dipeptides / pharmacology*
  • Enzyme Activation / drug effects
  • HeLa Cells
  • Humans
  • Models, Biological
  • Peptide Fragments / adverse effects
  • Peptide Fragments / metabolism*

Substances

  • Amyloid beta-Peptides
  • Dipeptides
  • N-(N-(3,5-difluorophenacetyl)alanyl)phenylglycine tert-butyl ester
  • Peptide Fragments
  • amyloid beta-protein (1-40)
  • Amyloid Precursor Protein Secretases

Grants and funding

The authors are funded by the Croatian Ministry of Health. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.