Massive antibody discovery used to probe structure-function relationships of the essential outer membrane protein LptD

Elife. 2019 Jun 25:8:e46258. doi: 10.7554/eLife.46258.

Abstract

Outer membrane proteins (OMPs) in Gram-negative bacteria dictate permeability of metabolites, antibiotics, and toxins. Elucidating the structure-function relationships governing OMPs within native membrane environments remains challenging. We constructed a diverse library of >3000 monoclonal antibodies to assess the roles of extracellular loops (ECLs) in LptD, an essential OMP that inserts lipopolysaccharide into the outer membrane of Escherichia coli. Epitope binning and mapping experiments with LptD-loop-deletion mutants demonstrated that 7 of the 13 ECLs are targeted by antibodies. Only ECLs inaccessible to antibodies were required for the structure or function of LptD. Our results suggest that antibody-accessible loops evolved to protect key extracellular regions of LptD, but are themselves dispensable. Supporting this hypothesis, no α-LptD antibody interfered with essential functions of LptD. Our experimental workflow enables structure-function studies of OMPs in native cellular environments, provides unexpected insight into LptD, and presents a method to assess the therapeutic potential of antibody targeting.

Keywords: E. coli; K. pneumoniae; LPS; LptD; infectious disease; microbiology; molecular biophysics; monoclonal antibodies; outer membrane; structural biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Antibodies, Monoclonal / metabolism*
  • Bacterial Outer Membrane Proteins / chemistry*
  • Bacterial Outer Membrane Proteins / metabolism*
  • Binding Sites
  • Epitope Mapping
  • Epitopes / metabolism
  • Escherichia coli / growth & development
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / chemistry*
  • Escherichia coli Proteins / metabolism*
  • Mice, Inbred BALB C
  • Protein Structure, Secondary
  • Rats, Sprague-Dawley
  • Structure-Activity Relationship

Substances

  • Anti-Bacterial Agents
  • Antibodies, Monoclonal
  • Bacterial Outer Membrane Proteins
  • Epitopes
  • Escherichia coli Proteins
  • LptD protein, E coli

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.