Microanatomic Distribution of Myeloid Heme Oxygenase-1 Protects against Free Radical-Mediated Immunopathology in Human Tuberculosis

Cell Rep. 2018 Nov 13;25(7):1938-1952.e5. doi: 10.1016/j.celrep.2018.10.073.

Abstract

Heme oxygenase-1 (HO-1) is a cytoprotective enzyme that controls inflammatory responses and redox homeostasis; however, its role during pulmonary tuberculosis (TB) remains unclear. Using freshly resected human TB lung tissue, we examined the role of HO-1 within the cellular and pathological spectrum of TB. Flow cytometry and histopathological analysis of human TB lung tissues showed that HO-1 is expressed primarily in myeloid cells and that HO-1 levels in these cells were directly proportional to cytoprotection. HO-1 mitigates TB pathophysiology by diminishing myeloid cell-mediated oxidative damage caused by reactive oxygen and/or nitrogen intermediates, which control granulocytic karyorrhexis to generate a zonal HO-1 response. Using whole-body or myeloid-specific HO-1-deficient mice, we demonstrate that HO-1 is required to control myeloid cell infiltration and inflammation to protect against TB progression. Overall, this study reveals that zonation of HO-1 in myeloid cells modulates free-radical-mediated stress, which regulates human TB immunopathology.

Keywords: free radical; heme oxygenase-1; histopathological spectrum; human TB pathology; human pulmonary tuberculosis; karyorrhexis; macrophage; mycobacterium tuberculosis; myeloid cell inflammation; neutrophil.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase / metabolism
  • CD4-Positive T-Lymphocytes / immunology
  • Cytokines / metabolism
  • Free Radicals / metabolism*
  • Granuloma / pathology
  • Heme Oxygenase-1 / deficiency
  • Heme Oxygenase-1 / metabolism*
  • Humans
  • Inflammation / pathology
  • Lung / pathology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mycobacterium tuberculosis / physiology
  • Myeloid Cells / enzymology
  • NF-E2-Related Factor 2 / metabolism
  • Neutrophils / metabolism
  • Nitric Oxide Synthase Type II / metabolism
  • Tuberculosis / enzymology
  • Tuberculosis / immunology*
  • Tuberculosis / microbiology
  • Tuberculosis / pathology*

Substances

  • Cytokines
  • Free Radicals
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • Nitric Oxide Synthase Type II
  • Heme Oxygenase-1
  • Arginase