Engineering neprilysin activity and specificity to create a novel therapeutic for Alzheimer's disease

PLoS One. 2014 Aug 4;9(8):e104001. doi: 10.1371/journal.pone.0104001. eCollection 2014.

Abstract

Neprilysin is a transmembrane zinc metallopeptidase that degrades a wide range of peptide substrates. It has received attention as a potential therapy for Alzheimer's disease due to its ability to degrade the peptide amyloid beta. However, its broad range of peptide substrates has the potential to limit its therapeutic use due to degradation of additional peptides substrates that tightly regulate many physiological processes. We sought to generate a soluble version of the ectodomain of neprilysin with improved activity and specificity towards amyloid beta as a potential therapeutic for Alzheimer's disease. Extensive amino acid substitutions were performed at positions surrounding the active site and inner surface of the enzyme and variants screened for activity on amyloid beta 1-40, 1-42 and a variety of other physiologically relevant peptides. We identified several mutations that modulated and improved both enzyme selectivity and intrinsic activity. Neprilysin variant G399V/G714K displayed an approximately 20-fold improved activity on amyloid beta 1-40 and up to a 3,200-fold reduction in activity on other peptides. Along with the altered peptide substrate specificity, the mutant enzyme produced a markedly altered series of amyloid beta cleavage products compared to the wild-type enzyme. Crystallisation of the mutant enzyme revealed that the amino acid substitutions result in alteration of the shape and size of the pocket containing the active site compared to the wild-type enzyme. The mutant enzyme offers the potential for the more efficient degradation of amyloid beta in vivo as a therapeutic for the treatment of Alzheimer's disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / drug therapy
  • Amino Acid Sequence
  • Amino Acid Substitution
  • Amyloid beta-Peptides / chemistry*
  • Gene Expression
  • Humans
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation
  • Neprilysin / chemistry*
  • Neprilysin / genetics
  • Peptide Fragments / chemistry*
  • Peptides / chemistry*
  • Peptides / genetics
  • Protein Engineering*
  • Protein Structure, Tertiary
  • Proteolysis
  • Recombinant Proteins / chemistry*
  • Recombinant Proteins / genetics
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Structure-Activity Relationship

Substances

  • Amyloid beta-Peptides
  • Peptide Fragments
  • Peptides
  • Recombinant Proteins
  • amyloid beta-protein (1-40)
  • amyloid beta-protein (1-42)
  • Neprilysin

Grants and funding

All work was funded by AstraZeneca and MedImmune (a wholly owned subsidiary of AstraZeneca). The funders or Bayer HealthCare AG provided support in the form of salaries for all authors, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.