The alveolar immune cell landscape is dysregulated in checkpoint inhibitor pneumonitis

J Clin Invest. 2019 Jul 16;129(10):4305-4315. doi: 10.1172/JCI128654.

Abstract

Background: Checkpoint inhibitor pneumonitis (CIP) is a highly morbid complication of immune checkpoint immunotherapy (ICI), one which precludes the continuation of ICI. Yet, the mechanistic underpinnings of CIP are unknown.

Methods: To better understand the mechanism of lung injury in CIP, we prospectively collected bronchoalveolar lavage (BAL) samples in ICI-treated patients with (n=12) and without CIP (n=6), prior to initiation of first-line therapy for CIP (high dose corticosteroids. We analyzed BAL immune cell populations using a combination of traditional multicolor flow cytometry gating, unsupervised clustering analysis and BAL supernatant cytokine measurements.

Results: We found increased BAL lymphocytosis, predominantly CD4+ T cells, in CIP. Specifically, we observed increased numbers of BAL central memory T-cells (Tcm), evidence of Type I polarization, and decreased expression of CTLA-4 and PD-1 in BAL Tregs, suggesting both activation of pro-inflammatory subsets and an attenuated suppressive phenotype. CIP BAL myeloid immune populations displayed enhanced expression of IL-1β and decreased expression of counter-regulatory IL-1RA. We observed increased levels of T cell chemoattractants in the BAL supernatant, consistent with our pro-inflammatory, lymphocytic cellular landscape.

Conclusion: We observe several immune cell subpopulations that are dysregulated in CIP, which may represent possible targets that could lead to therapeutics for this morbid immune related adverse event.

Keywords: Cancer immunotherapy; Immunology; Lung cancer; Pulmonology; Th1 response.

Publication types

  • Clinical Trial
  • Multicenter Study
  • Observational Study
  • 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

  • Aged
  • Bronchoalveolar Lavage
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / pathology
  • Cytokines / immunology
  • Female
  • Humans
  • Immunotherapy / adverse effects*
  • Male
  • Middle Aged
  • Neoplasms / immunology*
  • Neoplasms / pathology
  • Neoplasms / therapy
  • Pneumonia / chemically induced
  • Pneumonia / immunology*
  • Pneumonia / pathology
  • Programmed Cell Death 1 Receptor / immunology
  • Prospective Studies
  • Pulmonary Alveoli / immunology*
  • Pulmonary Alveoli / pathology

Substances

  • Cytokines
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor