Toll-like receptor 7 and 9 defects in common variable immunodeficiency

J Allergy Clin Immunol. 2009 Aug;124(2):349-56, 356.e1-3. doi: 10.1016/j.jaci.2009.05.019. Epub 2009 Jul 9.

Abstract

Background: Common variable immunodeficiency (CVID) is characterized by hypogammaglobulinemia, reduced numbers of peripheral blood isotype-switched memory B cells, and loss of plasma cells.

Objective: Because Toll-like receptor (TLR) activation of B cells can initiate and potentially sustain normal B cell functions, we examined functional outcomes of TLR7 and TLR9 signaling in CVID B cells.

Methods: TLR7-mediated, TLR7/8-mediated, and TLR9-mediated cell proliferation, isotype switch, and immunoglobulin production by control and CVID B cells or isolated naive and memory B cell subsets were examined. We quantitated TNF-alpha, IL-6, and IL-12 production in response to TLR1-9 ligands and measured IFN-alpha production by TLR7-stimulated PBMCs and isolated plasmacytoid dendritic cells (pDCs). IFN-beta mRNA expression by TLR3-stimulated fibroblasts was assessed.

Results: Unlike CD27(+) B cells of controls, TLR7-activated, TLR7/8-activated, or TLR9-activated CVID B cells or isolated CD27(+) B cells did not proliferate, upregulate CD27, or shed surface IgD. TLR-stimulated CVID B cells failed to upregulate activation-induced cytosine deaminase mRNA or produce IgG and IgA. TLR7-stimulated PBMCs and pDCs produced little or no IFN-alpha. Reconstituting IFN-alpha in TLR7-stimulated CVID B-cell cultures facilitated proliferation, CD27 upregulation, and isotype switch. These TLR defects are restricted because CVID PBMCs stimulated with TLR ligands produced normal amounts of TNF-alpha, IL-6, and IL-12; TLR3-mediated expression of IFN-beta by CVID fibroblasts was normal.

Conclusion: Defective TLR7 and TLR9 signaling in CVID B cells and pDCs, coupled with deficient IFN-alpha, impairs CVID B cell functions and prevents TLR-mediated augmentation of humoral immunity in vivo.

Publication types

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

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • B-Lymphocyte Subsets / drug effects
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocyte Subsets / metabolism
  • Cell Differentiation / drug effects
  • Cell Differentiation / immunology
  • Cell Proliferation / drug effects
  • Common Variable Immunodeficiency / immunology
  • Common Variable Immunodeficiency / metabolism*
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Female
  • Fibroblasts / drug effects
  • Fibroblasts / immunology
  • Fibroblasts / metabolism
  • Guanosine / analogs & derivatives
  • Guanosine / pharmacology
  • Humans
  • Immunoglobulin Class Switching / drug effects
  • Immunoglobulin Class Switching / immunology
  • Interferon-alpha / biosynthesis
  • Interferon-alpha / immunology
  • Interferon-alpha / pharmacology
  • Interferon-beta / biosynthesis
  • Interferon-beta / immunology
  • Interleukin-12 / biosynthesis
  • Interleukin-12 / immunology
  • Interleukin-6 / biosynthesis
  • Interleukin-6 / immunology
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / immunology
  • Leukocytes, Mononuclear / metabolism
  • Ligands
  • Lymphocyte Activation / drug effects
  • Lymphocyte Activation / immunology
  • Male
  • Middle Aged
  • Poly I-C / pharmacology
  • Toll-Like Receptor 7 / agonists
  • Toll-Like Receptor 7 / immunology
  • Toll-Like Receptor 7 / metabolism*
  • Toll-Like Receptor 9 / agonists
  • Toll-Like Receptor 9 / immunology
  • Toll-Like Receptor 9 / metabolism*
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Tumor Necrosis Factor-alpha / immunology
  • Young Adult

Substances

  • Interferon-alpha
  • Interleukin-6
  • Ligands
  • TLR7 protein, human
  • TLR9 protein, human
  • Toll-Like Receptor 7
  • Toll-Like Receptor 9
  • Tumor Necrosis Factor-alpha
  • Guanosine
  • Interleukin-12
  • Interferon-beta
  • loxoribine
  • Poly I-C