Human IL-32 expression protects mice against a hypervirulent strain of Mycobacterium tuberculosis

Proc Natl Acad Sci U S A. 2015 Apr 21;112(16):5111-6. doi: 10.1073/pnas.1424302112. Epub 2015 Mar 27.

Abstract

Silencing of interleukin-32 (IL-32) in a differentiated human promonocytic cell line impairs killing of Mycobacterium tuberculosis (MTB) but the role of IL-32 in vivo against MTB remains unknown. To study the effects of IL-32 in vivo, a transgenic mouse was generated in which the human IL-32γ gene is expressed using the surfactant protein C promoter (SPC-IL-32γTg). Wild-type and SPC-IL-32γTg mice were infected with a low-dose aerosol of a hypervirulent strain of MTB (W-Beijing HN878). At 30 and 60 d after infection, the transgenic mice had 66% and 85% fewer MTB in the lungs and 49% and 68% fewer MTB in the spleens, respectively; the transgenic mice also exhibited greater survival. Increased numbers of host-protective innate and adaptive immune cells were present in SPC-IL-32γTg mice, including tumor necrosis factor-alpha (TNFα) positive lung macrophages and dendritic cells, and IFN-gamma (IFNγ) and TNFα positive CD4(+) and CD8(+) T cells in the lungs and mediastinal lymph nodes. Alveolar macrophages from transgenic mice infected with MTB ex vivo had reduced bacterial burden and increased colocalization of green fluorescent protein-labeled MTB with lysosomes. Furthermore, mouse macrophages made to express IL-32γ but not the splice variant IL-32β were better able to limit MTB growth than macrophages capable of producing both. The lungs of patients with tuberculosis showed increased IL-32 expression, particularly in macrophages of granulomas and airway epithelial cells but also B cells and T cells. We conclude that IL-32γ enhances host immunity to MTB.

Keywords: cytokine; host immunity; interleukin-32; transgenic mouse; tuberculosis.

Publication types

  • Research Support, American Recovery and Reinvestment Act
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptive Immunity / immunology
  • Animals
  • Antigens, Ly / metabolism
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Cells, Cultured
  • Humans
  • Immunity, Innate / immunology
  • Interferon-gamma
  • Interleukins / metabolism*
  • Lung / immunology
  • Lung / microbiology
  • Lung / pathology
  • Lymph Nodes / immunology
  • Lymph Nodes / pathology
  • Macrophages, Alveolar / immunology
  • Mice, Transgenic
  • Mutation / genetics
  • Mycobacterium tuberculosis / pathogenicity*
  • NK Cell Lectin-Like Receptor Subfamily B / metabolism
  • Pulmonary Surfactant-Associated Protein C / metabolism
  • RNA Splice Sites / genetics
  • T-Lymphocytes, Regulatory / immunology
  • Transfection
  • Transgenes
  • Tuberculosis / immunology*
  • Tuberculosis / microbiology
  • Tuberculosis / prevention & control*
  • Tumor Necrosis Factor-alpha / metabolism
  • Virulence / immunology

Substances

  • Antigens, Ly
  • IL32 protein, human
  • Interleukins
  • Klrb1c protein, mouse
  • NK Cell Lectin-Like Receptor Subfamily B
  • Pulmonary Surfactant-Associated Protein C
  • RNA Splice Sites
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma