Burkholderia pseudomallei suppresses Caenorhabditis elegans immunity by specific degradation of a GATA transcription factor

Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):15067-72. doi: 10.1073/pnas.1311725110. Epub 2013 Aug 26.

Abstract

Burkholderia pseudomallei is a Gram-negative soil bacterium that infects both humans and animals. Although cell culture studies have revealed significant insights into factors contributing to virulence and host defense, the interactions between this pathogen and its intact host remain to be elucidated. To gain insights into the host defense responses to B. pseudomallei infection within an intact host, we analyzed the genome-wide transcriptome of infected Caenorhabditis elegans and identified ∼6% of the nematode genes that were significantly altered over a 12-h course of infection. An unexpected feature of the transcriptional response to B. pseudomallei was a progressive increase in the proportion of down-regulated genes, of which ELT-2 transcriptional targets were significantly enriched. ELT-2 is an intestinal GATA transcription factor with a conserved role in immune responses. We demonstrate that B. pseudomallei down-regulation of ELT-2 targets is associated with degradation of ELT-2 protein by the host ubiquitin-proteasome system. Degradation of ELT-2 requires the B. pseudomallei type III secretion system. Together, our studies using an intact host provide evidence for pathogen-mediated host immune suppression through the destruction of a host transcription factor.

Keywords: innate immunity; ubiquitin–proteosomal system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Burkholderia pseudomallei / genetics
  • Burkholderia pseudomallei / immunology
  • Burkholderia pseudomallei / pathogenicity*
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / immunology*
  • Caenorhabditis elegans / microbiology*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Down-Regulation
  • GATA Transcription Factors / genetics
  • GATA Transcription Factors / metabolism*
  • Host-Pathogen Interactions / immunology
  • RNA Processing, Post-Transcriptional
  • RNA, Helminth / genetics
  • RNA, Helminth / metabolism
  • Ubiquitin-Protein Ligases / metabolism
  • Virulence / immunology

Substances

  • Caenorhabditis elegans Proteins
  • ELT-2 protein, C elegans
  • GATA Transcription Factors
  • RNA, Helminth
  • Ubiquitin-Protein Ligases