Manipulation of the toll-like receptor 7 signaling pathway by Epstein-Barr virus

J Virol. 2007 Sep;81(18):9748-58. doi: 10.1128/JVI.01122-07. Epub 2007 Jul 3.

Abstract

Epstein-Barr virus (EBV) infection of primary B cells causes B-cell activation and proliferation. Activation of B cells requires binding of antigen to the B-cell receptor and a survival signal from ligand-bound CD40, signals that are provided by the EBV LMP1 and LMP2A latency proteins. Recently, Toll-like receptor (TLR) signaling has been reported to provide a third B-cell activation stimulus. The interaction between the EBV and TLR pathways was therefore investigated. Both UV-inactivated and untreated EBV upregulated the expression of TLR7 and downregulated the expression of TLR9 in naive B cells. UV-inactivated virus transiently stimulated naive B-cell proliferation in the presence of the TLR7 ligand R837, while addition of the TLR7 antagonist IRS 661 impaired cell growth induced by untreated EBV. Interferon regulatory factor 5 (IRF-5) is a downstream mediator of TLR7 signaling. IRF-5 was induced following EBV infection, and IRF-5 was expressed in B-cell lines with type III latency. Expression of IRF-5 in this setting is surprising since IRF-5 has tumor suppressor and antiviral properties. B-cell proliferation assays provided evidence that EBV modulates TLR7 signaling responses. Examination of IRF-5 transcripts identified a novel splice variant, V12, that was induced by EBV infection, was constitutively nuclear, and acted as a dominant negative form in IRF-5 reporter assays. IRF-4 negatively regulates IRF-5 activation, and IRF-4 was also present in type III latently infected cells. EBV therefore initially uses TLR7 signaling to enhance B-cell proliferation and subsequently modifies the pathway to regulate IRF-5 activity.

Publication types

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

MeSH terms

  • Adjuvants, Immunologic / pharmacology
  • Alternative Splicing / drug effects
  • Alternative Splicing / genetics
  • Alternative Splicing / physiology
  • Aminoquinolines / pharmacology
  • B-Lymphocytes / metabolism*
  • B-Lymphocytes / virology
  • CD40 Antigens / genetics
  • CD40 Antigens / metabolism
  • CD40 Ligand / genetics
  • CD40 Ligand / metabolism
  • Cell Line, Transformed
  • Cell Proliferation / radiation effects
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Cell Survival / radiation effects
  • Epstein-Barr Virus Infections / genetics
  • Epstein-Barr Virus Infections / metabolism*
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • Gene Expression Regulation / radiation effects
  • HeLa Cells
  • Herpesvirus 4, Human / genetics
  • Herpesvirus 4, Human / metabolism*
  • Humans
  • Imiquimod
  • Interferon Regulatory Factors / genetics
  • Interferon Regulatory Factors / metabolism
  • Lymphocyte Activation* / drug effects
  • Lymphocyte Activation* / genetics
  • Lymphocyte Activation* / radiation effects
  • Signal Transduction* / drug effects
  • Signal Transduction* / genetics
  • Signal Transduction* / radiation effects
  • Toll-Like Receptor 7 / agonists
  • Toll-Like Receptor 7 / metabolism*
  • Toll-Like Receptor 9 / genetics
  • Toll-Like Receptor 9 / metabolism
  • Ultraviolet Rays
  • Viral Matrix Proteins / genetics
  • Viral Matrix Proteins / metabolism
  • Virus Latency / drug effects
  • Virus Latency / genetics
  • Virus Latency / radiation effects

Substances

  • Adjuvants, Immunologic
  • Aminoquinolines
  • CD40 Antigens
  • EBV-associated membrane antigen, Epstein-Barr virus
  • IRF5 protein, human
  • Interferon Regulatory Factors
  • TLR7 protein, human
  • TLR9 protein, human
  • Toll-Like Receptor 7
  • Toll-Like Receptor 9
  • Viral Matrix Proteins
  • interferon regulatory factor-4
  • CD40 Ligand
  • Imiquimod