B Cells Producing Type I IFN Modulate Macrophage Polarization in Tuberculosis

Am J Respir Crit Care Med. 2018 Mar 15;197(6):801-813. doi: 10.1164/rccm.201707-1475OC.

Abstract

Rationale: In addition to their well-known function as antibody-producing cells, B lymphocytes can markedly influence the course of infectious or noninfectious diseases via antibody-independent mechanisms. In tuberculosis (TB), B cells accumulate in lungs, yet their functional contribution to the host response remains poorly understood.

Objectives: To document the role of B cells in TB in an unbiased manner.

Methods: We generated the transcriptome of B cells isolated from Mycobacterium tuberculosis (Mtb)-infected mice and validated the identified key pathways using in vitro and in vivo assays. The obtained data were substantiated using B cells from pleural effusion of patients with TB.

Measurements and main results: B cells isolated from Mtb-infected mice displayed a STAT1 (signal transducer and activator of transcription 1)-centered signature, suggesting a role for IFNs in B-cell response to infection. B cells stimulated in vitro with Mtb produced type I IFN, via a mechanism involving the innate sensor STING (stimulator of interferon genes), and antagonized by MyD88 (myeloid differentiation primary response 88) signaling. In vivo, B cells expressed type I IFN in the lungs of Mtb-infected mice and, of clinical relevance, in pleural fluid from patients with TB. Type I IFN expression by B cells induced an altered polarization of macrophages toward a regulatory/antiinflammatory profile in vitro. In vivo, increased provision of type I IFN by B cells in a murine model of B cell-restricted Myd88 deficiency correlated with an enhanced accumulation of regulatory/antiinflammatory macrophages in Mtb-infected lungs.

Conclusions: Type I IFN produced by Mtb-stimulated B cells favors macrophage polarization toward a regulatory/antiinflammatory phenotype during Mtb infection.

Keywords: B lymphocytes; IFN; macrophages; tuberculosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes / metabolism*
  • Disease Models, Animal
  • Humans
  • Interferon Type I / metabolism*
  • Lung / metabolism
  • Lung / microbiology
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mycobacterium tuberculosis
  • Signal Transduction
  • Spleen / metabolism
  • Spleen / microbiology
  • Tuberculosis / metabolism*

Substances

  • Interferon Type I