Activation of the noncanonical NF-κB pathway by HIV controls a dendritic cell immunoregulatory phenotype

Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):14122-7. doi: 10.1073/pnas.1204032109. Epub 2012 Aug 9.

Abstract

HIV modulates plasmacytoid dendritic cell (pDC) activation via Toll-like receptor 7, inducing type I IFN and inflammatory cytokines. Simultaneously, pDCs up-regulate the expression of indoleamine 2,3 dioxygenase (IDO), which is essential for the induction of regulatory T cells (Tregs), which function to down-modulate immune activation. Here we demonstrate the crucial importance of the noncanonical NF-κB pathway in the establishment of this immunoregulatory phenotype in pDCs. In response to HIV, the noncanonical NF-κB pathway directly induces IDO and involves the recruitment of TNF receptor-associated factor-3 to the Toll-like receptor/MyD88 complex, NF-κB-inducing kinase-dependent IκB kinase-α activation, and p52/RelB nuclear translocation. We also show that pDC-induced Tregs can inhibit conventional DC (cDC) maturation partially through cytotoxic T-lymphocyte antigen (CTLA)-4 engagement. Furthermore, CTLA-4 induces IDO in cDCs in a NF-κB-inducing kinase-dependent way. These CTLA-4-conditioned cDCs can in turn induce Treg differentiation in an IDO-dependent manner. Thus, the noncanonical NF-κB pathway is integral in controlling immunoregulatory phenotypes of both pDCs and cDCs.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Dendritic Cells / immunology*
  • Dendritic Cells / virology*
  • Gene Expression / immunology
  • Gene Knockdown Techniques
  • HIV Infections / immunology*
  • HIV Infections / metabolism
  • Humans
  • I-kappa B Kinase / genetics
  • I-kappa B Kinase / immunology
  • I-kappa B Kinase / metabolism
  • Immunophenotyping
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / genetics
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / immunology
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
  • Myeloid Differentiation Factor 88 / immunology
  • Myeloid Differentiation Factor 88 / metabolism
  • NF-kappa B p52 Subunit / immunology*
  • NF-kappa B p52 Subunit / metabolism
  • NF-kappaB-Inducing Kinase
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / immunology
  • Protein Serine-Threonine Kinases / metabolism
  • Signal Transduction / immunology
  • T-Lymphocytes, Cytotoxic / immunology
  • T-Lymphocytes, Cytotoxic / virology
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / virology*
  • TNF Receptor-Associated Factor 3 / immunology
  • TNF Receptor-Associated Factor 3 / metabolism

Substances

  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • MYD88 protein, human
  • Myeloid Differentiation Factor 88
  • NF-kappa B p52 Subunit
  • TNF Receptor-Associated Factor 3
  • TRAF3 protein, human
  • Protein Serine-Threonine Kinases
  • I-kappa B Kinase