Blocking IL-10 receptor signaling ameliorates Mycobacterium tuberculosis infection during influenza-induced exacerbation

JCI Insight. 2019 Apr 18;5(10):e126533. doi: 10.1172/jci.insight.126533.

Abstract

Epidemiological findings indicate that coinfection with influenza viruses is associated with an increased risk of death in patients suffering from tuberculosis but the underlying pathomechanisms are not well understood. In this study, we demonstrate that influenza A virus (IAV) coinfection rapidly impairs control of Mycobacterium tuberculosis (Mtb) in C57BL/6 mice. IAV coinfection was associated with significantly increased bacterial loads, reduced survival and a substantial modulation of innate and adaptive immune defenses including an impaired onset and development of Mtb-specific CD4+ T cell responses and the accumulation of macrophages with increased arginase-1 production in the lungs. Our findings strongly indicate that IAV coinfection compromises the host's ability to control Mtb infection via the production of IL-10 which was rapidly induced upon viral infection. The blockade of IL-10 receptor signaling reduced the bacterial load in coinfected mice to a level comparable with that in Mtb-only-infected animals. Taken together, our data suggest that IL-10 signaling constitutes a major pathway that enhances susceptibility to Mtb during concurrent IAV infection.

Keywords: Immunology; Infectious disease; Influenza; Mouse models; Tuberculosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity / immunology*
  • Animals
  • Arginase / metabolism
  • Bacterial Load
  • CD4-Positive T-Lymphocytes / immunology
  • Coinfection / immunology*
  • Immunity, Innate / immunology*
  • Influenza A Virus, H1N1 Subtype
  • Interferon-gamma / immunology
  • Interleukin-10 / immunology*
  • Lung / immunology*
  • Lung / metabolism
  • Macrophages, Alveolar / immunology
  • Macrophages, Alveolar / metabolism
  • Mice
  • Mycobacterium tuberculosis
  • Orthomyxoviridae Infections / immunology*
  • Receptors, Interleukin-10 / antagonists & inhibitors
  • Receptors, Interleukin-10 / immunology*
  • Survival Rate
  • T-Lymphocytes, Regulatory / immunology
  • Tuberculosis, Pulmonary / immunology*
  • Tumor Necrosis Factor-alpha / immunology
  • Viral Load

Substances

  • IFNG protein, mouse
  • IL10 protein, mouse
  • Receptors, Interleukin-10
  • Tnf protein, mouse
  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Interferon-gamma
  • Arg1 protein, mouse
  • Arginase

Grants and funding

This study was funded by the Leibniz Center Infection. Research in DS laboratory was supported by the German Center for Infection (DZIF – TTU TB, BMBF) and funds of the German Research Foundation (Cluster of Excellence 306, CL X).