Alveolar Macrophages Provide an Early Mycobacterium tuberculosis Niche and Initiate Dissemination

Cell Host Microbe. 2018 Sep 12;24(3):439-446.e4. doi: 10.1016/j.chom.2018.08.001. Epub 2018 Aug 23.

Abstract

Mycobacterium tuberculosis (Mtb) infection is initiated in the distal airways, but the bacteria ultimately disseminate to the lung interstitium. Although various cell types, including alveolar macrophages (AM), neutrophils, and permissive monocytes, are known to be infected with Mtb, the initially infected cells as well as those that mediate dissemination from the alveoli to the lung interstitium are unknown. In this study, using a murine infection model, we reveal that early, productive Mtb infection occurs almost exclusively within airway-resident AM. Thereafter Mtb-infected, but not uninfected, AM localize to the lung interstitium through mechanisms requiring an intact Mtb ESX-1 secretion system. Relocalization of infected AM precedes Mtb uptake by recruited monocyte-derived macrophages and neutrophils. This dissemination process is driven by non-hematopoietic host MyD88/interleukin-1 receptor inflammasome signaling. Thus, interleukin-1-mediated crosstalk between Mtb-infected AM and non-hematopoietic cells promotes pulmonary Mtb infection by enabling infected cells to disseminate from the alveoli to the lung interstitium.

Keywords: ESX-1; IL-1; alveolar macrophages; granuloma; innate immunity; lung; pulmonary tuberculosis.

Publication types

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

MeSH terms

  • Animals
  • Bacterial Proteins / metabolism
  • Granuloma / microbiology
  • Granuloma / pathology
  • Immunity, Innate / immunology
  • Inflammation / immunology
  • Macrophages, Alveolar / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mycobacterium tuberculosis / immunology*
  • Myeloid Differentiation Factor 88 / metabolism
  • Pulmonary Alveoli / immunology*
  • Pulmonary Alveoli / microbiology*
  • Receptors, Interleukin-1 / metabolism
  • Tuberculosis / immunology*
  • Tuberculosis / microbiology*

Substances

  • Bacterial Proteins
  • EspI protein, Mycobacterium tuberculosis
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Receptors, Interleukin-1