Functional selection of protease inhibitory antibodies

Proc Natl Acad Sci U S A. 2019 Aug 13;116(33):16314-16319. doi: 10.1073/pnas.1903330116. Epub 2019 Jul 30.

Abstract

Critical for diverse biological processes, proteases represent one of the largest families of pharmaceutical targets. To inhibit pathogenic proteases with desired selectivity, monoclonal antibodies (mAbs) hold great promise as research tools and therapeutic agents. However, identification of mAbs with inhibitory functions is challenging because current antibody discovery methods rely on binding rather than inhibition. This study developed a highly efficient selection method for protease inhibitory mAbs by coexpressing 3 recombinant proteins in the periplasmic space of Escherichia coli-an antibody clone, a protease of interest, and a β-lactamase modified by insertion of a protease cleavable peptide sequence. During functional selection, inhibitory antibodies prevent the protease from cleaving the modified β-lactamase, thereby allowing the cell to survive in the presence of ampicillin. Using this method to select from synthetic human antibody libraries, we isolated panels of mAbs inhibiting 5 targets of 4 main protease classes: matrix metalloproteinases (MMP-14, a predominant target in metastasis; MMP-9, in neuropathic pain), β-secretase 1 (BACE-1, an aspartic protease in Alzheimer's disease), cathepsin B (a cysteine protease in cancer), and Alp2 (a serine protease in aspergillosis). Notably, 37 of 41 identified binders were inhibitory. Isolated mAb inhibitors exhibited nanomolar potency, exclusive selectivity, excellent proteolytic stability, and desired biological functions. Particularly, anti-Alp2 Fab A4A1 had a binding affinity of 11 nM and inhibition potency of 14 nM, anti-BACE1 IgG B2B2 reduced amyloid beta (Aβ40) production by 80% in cellular assays, and IgG L13 inhibited MMP-9 but not MMP-2/-12/-14 and significantly relieved neuropathic pain development in mice.

Keywords: BACE-1; MMP; functional selection; monoclonal antibody; protease inhibitor.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alzheimer Disease / immunology
  • Alzheimer Disease / therapy
  • Amino Acid Sequence / genetics
  • Amyloid Precursor Protein Secretases / genetics
  • Amyloid Precursor Protein Secretases / immunology
  • Amyloid beta-Peptides / antagonists & inhibitors
  • Amyloid beta-Peptides / genetics
  • Amyloid beta-Peptides / immunology
  • Animals
  • Antibodies, Monoclonal / biosynthesis
  • Antibodies, Monoclonal / immunology*
  • Antibodies, Monoclonal / pharmacology
  • Aspartic Acid Endopeptidases / genetics
  • Aspartic Acid Endopeptidases / immunology
  • Aspergillosis / immunology
  • Aspergillosis / therapy
  • Cathepsin B / genetics
  • Cathepsin B / immunology
  • Escherichia coli / genetics
  • Humans
  • Matrix Metalloproteinase 14 / genetics
  • Matrix Metalloproteinase 14 / immunology
  • Matrix Metalloproteinase 9 / genetics
  • Matrix Metalloproteinase 9 / immunology
  • Matrix Metalloproteinase Inhibitors / immunology
  • Matrix Metalloproteinase Inhibitors / metabolism
  • Mice
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Peptide Hydrolases / chemistry
  • Peptide Hydrolases / genetics*
  • Peptide Hydrolases / immunology
  • Periplasm / genetics
  • Protease Inhibitors / immunology*
  • Protease Inhibitors / pharmacology
  • Proteolysis / drug effects
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / genetics
  • Recombinant Proteins / immunology*
  • Recombinant Proteins / pharmacology
  • Serine Proteases / genetics
  • Serine Proteases / immunology

Substances

  • Amyloid beta-Peptides
  • Antibodies, Monoclonal
  • Matrix Metalloproteinase Inhibitors
  • Protease Inhibitors
  • Recombinant Proteins
  • Amyloid Precursor Protein Secretases
  • Peptide Hydrolases
  • Serine Proteases
  • Cathepsin B
  • Aspartic Acid Endopeptidases
  • BACE1 protein, human
  • Matrix Metalloproteinase 9
  • Matrix Metalloproteinase 14