Mechanism of bacterial interference with TLR4 signaling by Brucella Toll/interleukin-1 receptor domain-containing protein TcpB

J Biol Chem. 2014 Jan 10;289(2):654-68. doi: 10.1074/jbc.M113.523274. Epub 2013 Nov 21.

Abstract

Upon activation of Toll-like receptors (TLRs), cytoplasmic Toll/interleukin-1 receptor (TIR) domains of the receptors undergo homo- or heterodimerization. This in turn leads to the recruitment of adaptor proteins, activation of transcription factors, and the secretion of pro-inflammatory cytokines. Recent studies have described the TIR domain-containing protein from Brucella melitensis, TcpB (BtpA/Btp1), to be involved in virulence and suppression of host innate immune responses. TcpB interferes with TLR4 and TLR2 signaling pathways by a mechanism that remains controversial. In this study, we show using co-immunoprecipitation analyses that TcpB interacts with MAL, MyD88, and TLR4 but interferes only with the MAL-TLR4 interaction. We present the crystal structure of the TcpB TIR domain, which reveals significant structural differences in the loop regions compared with other TIR domain structures. We demonstrate that TcpB forms a dimer in solution, and the crystal structure reveals the dimerization interface, which we validate by mutagenesis and biophysical studies. Our study advances the understanding of the molecular mechanisms of host immunosuppression by bacterial pathogens.

Keywords: Adaptor Proteins; Innate Immunity; Protein Structure; Toll IL-1 Receptor (TIR) Domain; Toll-like Receptors (TLR).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Binding Sites / genetics
  • Brucella melitensis / genetics
  • Brucella melitensis / metabolism
  • HEK293 Cells
  • Humans
  • Immunoblotting
  • Immunoprecipitation
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation
  • Myelin and Lymphocyte-Associated Proteolipid Proteins / genetics
  • Myelin and Lymphocyte-Associated Proteolipid Proteins / metabolism
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism
  • Protein Binding
  • Protein Conformation
  • Protein Multimerization
  • Protein Structure, Tertiary*
  • Receptors, Interleukin-1 / metabolism
  • Scattering, Small Angle
  • Sequence Homology, Amino Acid
  • Signal Transduction
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / metabolism*
  • Virulence Factors / chemistry*
  • Virulence Factors / genetics
  • Virulence Factors / metabolism*
  • X-Ray Diffraction

Substances

  • Bacterial Proteins
  • MAL protein, human
  • Myelin and Lymphocyte-Associated Proteolipid Proteins
  • Myeloid Differentiation Factor 88
  • Receptors, Interleukin-1
  • TLR4 protein, human
  • TcpB protein, Brucella melitensis
  • Toll-Like Receptor 4
  • Virulence Factors