HIV-1-triggered release of type I IFN by plasmacytoid dendritic cells induces BAFF production in monocytes

J Immunol. 2015 Mar 1;194(5):2300-8. doi: 10.4049/jimmunol.1402147. Epub 2015 Jan 30.

Abstract

HIV-1 infection leads to numerous B cell abnormalities, including hypergammaglobulinemia, nonspecific B cell activation, nonspecific class switching, increased cell turnover, breakage of tolerance, increased immature/transitional B cells, B cell malignancies, as well as a loss of capacity to generate and maintain memory, all of which contribute to a global impairment of the immune humoral compartment. Several cytokines and soluble factors, which are increased in sera of HIV-1-infected individuals, have been suggested to directly or indirectly contribute to these B cell dysfunctions, and one of these is the B cell-activating factor (BAFF). We report in this study that HIV-1 (X4- and R5-tropic) upregulates BAFF expression and secretion by human monocytes. Moreover, we show that the virus-mediated production of BAFF by monocytes relies on a type I IFN response by a small percentage of plasmacytoid dendritic cells (pDCs) present in the monocyte cultures. HIV-1-induced type I IFN by pDCs triggers BAFF production in both classical and intermediate monocytes, but not in nonclassical monocytes, which nonetheless display a very strong basal BAFF production. We report also that basal BAFF secretion was higher in monocytes obtained from females compared with those from male donors. This study provides a novel mechanistic explanation for the increased BAFF levels observed during HIV-1 infection and highlights the importance of pDC/monocyte crosstalk to drive BAFF secretion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • B-Cell Activating Factor / genetics
  • B-Cell Activating Factor / immunology*
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology
  • B-Lymphocytes / virology
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology
  • Dendritic Cells / virology*
  • Female
  • Gene Expression Regulation
  • HEK293 Cells
  • HIV-1 / immunology*
  • Humans
  • Interferon-alpha / biosynthesis
  • Interferon-alpha / metabolism*
  • Interferon-beta / biosynthesis
  • Interferon-beta / metabolism*
  • Lymphocyte Activation
  • Male
  • Monocytes / drug effects
  • Monocytes / immunology
  • Monocytes / virology*
  • Poly I-C / pharmacology
  • Primary Cell Culture
  • Quinolines / pharmacology
  • Signal Transduction
  • Toll-Like Receptors / agonists
  • Toll-Like Receptors / genetics
  • Toll-Like Receptors / immunology

Substances

  • 1-(2-methylpropyl)-1H-imidazo(4,5-c)quinolin 4-amine
  • B-Cell Activating Factor
  • Interferon-alpha
  • Quinolines
  • TNFSF13B protein, human
  • Toll-Like Receptors
  • Interferon-beta
  • Poly I-C