Site-Specific Siderocalin Binding to Ferric and Ferric-Free Enterobactin As Revealed by Mass Spectrometry

ACS Chem Biol. 2020 May 15;15(5):1154-1160. doi: 10.1021/acschembio.9b00741. Epub 2020 Jan 13.

Abstract

Both host and pathogen competitively manipulate coordination environments during bacterial infections. Human cells release the innate immune protein siderocalin (Scn, also known as lipocalin-2/Lcn2, neutrophil gelatinase-associated lipocalin/NGAL) that can inhibit bacterial growth by sequestering iron in a ferric complex with enterobactin (Ent), the ubiquitous Escherichia coli siderophore. Pathogenic E. coli use the virulence-associated esterase IroE to linearize the Ent cyclic trilactone to linear enterobactin (lin-Ent). We characterized lin-Ent interactions with Scn by using native mass spectrometry (MS) with hydrogen-deuterium exchange (HDX) and Lys/Arg specific covalent footprinting. These approaches support 1:1 binding of both Fe(III)-lin-Ent to Scn and iron-free lin-Ent to Scn. Both ferric and nonferric lin-Ent localize to all three pockets of the Scn calyx, consistent with Scn capture of lin-Ent both before and after Fe(III) chelation. These findings raise the possibility that Scn neutralizes both siderophores and siderophore-bound iron during infections. This integrated, MS-based approach circumvents the limitations that frustrate traditional structural approaches to examining Scn interactions with enterobactin-based ligands.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acids / chemistry*
  • Binding Sites
  • Carrier Proteins / chemistry*
  • Coordination Complexes / chemistry
  • Deuterium / chemistry
  • Enterobactin / chemistry*
  • Escherichia coli / chemistry
  • Ferric Compounds / chemistry*
  • Humans
  • Isotope Labeling
  • Ligands
  • Lipocalin-2
  • Mass Spectrometry / methods*
  • Peptides / chemistry
  • Protein Conformation
  • Siderophores / chemistry

Substances

  • Amino Acids
  • Carrier Proteins
  • Coordination Complexes
  • Ferric Compounds
  • LCN2 protein, human
  • Ligands
  • Lipocalin-2
  • Peptides
  • Siderophores
  • Enterobactin
  • ferrienterochelin
  • Deuterium