Comprehensive analysis of clinical Burkholderia pseudomallei isolates demonstrates conservation of unique lipid A structure and TLR4-dependent innate immune activation

PLoS Negl Trop Dis. 2018 Feb 23;12(2):e0006287. doi: 10.1371/journal.pntd.0006287. eCollection 2018 Feb.

Abstract

Burkholderia pseudomallei is an environmental bacterium that causes melioidosis, a major community-acquired infection in tropical regions. Melioidosis presents with a range of clinical symptoms, is often characterized by a robust inflammatory response, may relapse after treatment, and results in high mortality rates. Lipopolysaccharide (LPS) of B. pseudomallei is a potent immunostimulatory molecule comprised of lipid A, core, and O-polysaccharide (OPS) components. Four B. pseudomallei LPS types have been described based on SDS-PAGE patterns that represent the difference of OPS-type A, type B, type B2 and rough LPS. The majority of B. pseudomallei isolates are type A. We used matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) followed by electrospray ionization quadrupole time-of-flight mass spectrometry (ESI-QqTOF MS) and gas chromatography to characterize the lipid A of B. pseudomallei within LPS type A isolates. We determined that B. pseudomallei lipid A is represented by penta- and tetra-acylated species modified with 4-amino-4-deoxy-arabinose (Ara4N). The MALDI-TOF profiles from 171 clinical B. pseudomallei isolates, including 68 paired primary and relapse isolates and 35 within-host isolates were similar. We did not observe lipid A structural changes when the bacteria were cultured in different growth conditions. Dose-dependent NF-κB activation in HEK cells expressing TLR4 was observed using multiple heat-killed B. pseudomallei isolates and corresponding purified LPS. We demonstrated that TLR4-dependent NF-κB activation induced by heat-killed bacteria or LPS prepared from OPS deficient mutant was significantly greater than those induced by wild type B. pseudomallei. These findings suggest that the structure of B. pseudomallei lipid A is highly conserved in a wide variety of clinical and environmental circumstances but that the presence of OPS may modulate LPS-driven innate immune responses in melioidosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Sugars / chemistry
  • Burkholderia pseudomallei / chemistry
  • Burkholderia pseudomallei / growth & development
  • Burkholderia pseudomallei / immunology*
  • Burkholderia pseudomallei / isolation & purification*
  • HEK293 Cells
  • Humans
  • Immunity, Innate*
  • Lipid A / chemistry*
  • Lipid A / immunology*
  • Lipopolysaccharides / chemistry
  • Melioidosis / immunology
  • Melioidosis / microbiology*
  • NF-kappa B / immunology
  • Signal Transduction
  • Spectrometry, Mass, Electrospray Ionization
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization / methods
  • Toll-Like Receptor 4 / immunology*

Substances

  • Amino Sugars
  • Lipid A
  • Lipopolysaccharides
  • NF-kappa B
  • Toll-Like Receptor 4
  • lipopolysaccharide B
  • 4-amino-4-deoxyarabinose