IL-33-mediated IL-13 secretion by ST2+ Tregs controls inflammation after lung injury

JCI Insight. 2019 Mar 21;4(6):e123919. doi: 10.1172/jci.insight.123919.

Abstract

Acute respiratory distress syndrome is an often fatal disease that develops after acute lung injury and trauma. How released tissue damage signals, or alarmins, orchestrate early inflammatory events is poorly understood. Herein we reveal that IL-33, an alarmin sequestered in the lung epithelium, is required to limit inflammation after injury due to an unappreciated capacity to mediate Foxp3+ Treg control of local cytokines and myeloid populations. Specifically, Il33-/- mice are more susceptible to lung damage-associated morbidity and mortality that is typified by augmented levels of the proinflammatory cytokines and Ly6Chi monocytes in the bronchoalveolar lavage fluid. Local delivery of IL-33 at the time of injury is protective but requires the presence of Treg cells. IL-33 stimulates both mouse and human Tregs to secrete IL-13. Using Foxp3Cre × Il4/Il13fl/fl mice, we show that Treg expression of IL-13 is required to prevent mortality after acute lung injury by controlling local levels of G-CSF, IL-6, and MCP-1 and inhibiting accumulation of Ly6Chi monocytes. Our study identifies a regulatory mechanism involving IL-33 and Treg secretion of IL-13 in response to tissue damage that is instrumental in limiting local inflammatory responses and may shape the myeloid compartment after lung injury.

Keywords: Cytokines; Immunology; Macrophages; Pulmonology; T cells.

Publication types

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

MeSH terms

  • Acute Lung Injury / metabolism
  • Acute Lung Injury / pathology
  • Animals
  • Bronchoalveolar Lavage Fluid
  • Chemokine CCL2
  • Cytokines / metabolism
  • Disease Models, Animal
  • Forkhead Transcription Factors / genetics
  • Granulocyte Colony-Stimulating Factor
  • Humans
  • Inflammation / metabolism*
  • Interleukin-1 Receptor-Like 1 Protein / genetics
  • Interleukin-1 Receptor-Like 1 Protein / metabolism*
  • Interleukin-13 / metabolism*
  • Interleukin-33 / genetics
  • Interleukin-33 / metabolism*
  • Interleukin-6
  • Lung / metabolism
  • Lung / pathology
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Respiratory Distress Syndrome / metabolism
  • T-Lymphocytes, Regulatory / metabolism*
  • Transcriptome

Substances

  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Cytokines
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Il1rl1 protein, mouse
  • Il33 protein, mouse
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-13
  • Interleukin-33
  • Interleukin-6
  • Granulocyte Colony-Stimulating Factor