Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence

J Exp Med. 2005 Mar 21;201(6):1007-18. doi: 10.1084/jem.20041442. Epub 2005 Mar 14.

Abstract

Viral immune evasion strategies target key aspects of the host antiviral response. Recently, it has been recognized that Toll-like receptors (TLRs) have a role in innate defense against viruses. Here, we define the function of the vaccinia virus (VV) protein A46R and show it inhibits intracellular signalling by a range of TLRs. TLR signalling is triggered by homotypic interactions between the Toll-like-interleukin-1 resistance (TIR) domains of the receptors and adaptor molecules. A46R contains a TIR domain and is the only viral TIR domain-containing protein identified to date. We demonstrate that A46R targets the host TIR adaptors myeloid differentiation factor 88 (MyD88), MyD88 adaptor-like, TIR domain-containing adaptor inducing IFN-beta (TRIF), and the TRIF-related adaptor molecule and thereby interferes with downstream activation of mitogen-activated protein kinases and nuclear factor kappaB. TRIF mediates activation of interferon (IFN) regulatory factor 3 (IRF3) and induction of IFN-beta by TLR3 and TLR4 and suppresses VV replication in macrophages. Here, A46R disrupted TRIF-induced IRF3 activation and induction of the TRIF-dependent gene regulated on activation, normal T cell expressed and secreted. Furthermore, we show that A46R is functionally distinct from another described VV TLR inhibitor, A52R. Importantly, VV lacking the A46R gene was attenuated in a murine intranasal model, demonstrating the importance of A46R for VV virulence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters
  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport / metabolism*
  • Amino Acid Sequence
  • Animals
  • Antigens, Differentiation / metabolism*
  • Cell Line
  • DNA-Binding Proteins / metabolism
  • Disease Models, Animal
  • Gene Expression Regulation, Viral / genetics
  • Gene Expression Regulation, Viral / physiology
  • Humans
  • Interferon Regulatory Factor-3
  • Interferon-beta / biosynthesis
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / physiology
  • MAP Kinase Signaling System / genetics
  • MAP Kinase Signaling System / physiology*
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Molecular Sequence Data
  • Myeloid Differentiation Factor 88
  • Periplasmic Binding Proteins
  • Protein Structure, Tertiary / genetics
  • Protein Structure, Tertiary / physiology
  • Receptors, Cell Surface / metabolism*
  • Receptors, Immunologic / metabolism*
  • T-Lymphocytes / physiology
  • Toll-Like Receptor 3
  • Toll-Like Receptor 4
  • Toll-Like Receptors
  • Transcription Factors / metabolism
  • Vaccinia virus / genetics
  • Vaccinia virus / metabolism*
  • Vaccinia virus / pathogenicity
  • Viral Proteins / genetics
  • Viral Proteins / metabolism*
  • Virus Diseases / genetics
  • Virus Diseases / physiopathology
  • Virus Replication / genetics
  • Virus Replication / physiology

Substances

  • A46R protein, vaccinia virus
  • A52R protein, vaccinia virus
  • ATP-Binding Cassette Transporters
  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport
  • Antigens, Differentiation
  • DNA-Binding Proteins
  • IRF3 protein, human
  • Interferon Regulatory Factor-3
  • Irf3 protein, mouse
  • MYD88 protein, human
  • Membrane Glycoproteins
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Periplasmic Binding Proteins
  • Receptors, Cell Surface
  • Receptors, Immunologic
  • TICAM1 protein, human
  • TLR3 protein, human
  • TLR4 protein, human
  • Toll-Like Receptor 3
  • Toll-Like Receptor 4
  • Toll-Like Receptors
  • Transcription Factors
  • TroA protein, Treponema pallidum
  • Viral Proteins
  • Interferon-beta