Chronic NF-κB activation links COPD and lung cancer through generation of an immunosuppressive microenvironment in the lungs

Oncotarget. 2016 Feb 2;7(5):5470-82. doi: 10.18632/oncotarget.6562.

Abstract

Nuclear Factor (NF)-κB is positioned to provide the interface between COPD and carcinogenesis through regulation of chronic inflammation in the lungs. Using a tetracycline-inducible transgenic mouse model that conditionally expresses activated IκB kinase β (IKKβ) in airway epithelium (IKTA), we found that sustained NF-κB signaling results in chronic inflammation and emphysema by 4 months. By 11 months of transgene activation, IKTA mice develop lung adenomas. Investigation of lung inflammation in IKTA mice revealed a substantial increase in M2-polarized macrophages and CD4+/CD25+/FoxP3+ regulatory T lymphocytes (Tregs). Depletion of alveolar macrophages in IKTA mice reduced Tregs, increased lung CD8+ lymphocytes, and reduced tumor numbers following treatment with the carcinogen urethane. Alveolar macrophages from IKTA mice supported increased generation of inducible Foxp3+ Tregs ex vivo through expression of TGFβ and IL-10. Targeting of TGFβ and IL-10 reduced the ability of alveolar macrophages from IKTA mice to induce Foxp3 expression on T cells. These studies indicate that sustained activation of NF-κB pathway links COPD and lung cancer through generation and maintenance of a pro-tumorigenic inflammatory environment consisting of alternatively activated macrophages and regulatory T cells.

Keywords: COPD; NF-κB; lung cancer; macrophage; tregs.

Publication types

  • 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

  • Animals
  • Blotting, Western
  • CD8-Positive T-Lymphocytes / immunology
  • Cells, Cultured
  • Epithelium / immunology*
  • Female
  • Flow Cytometry
  • Humans
  • I-kappa B Kinase / physiology
  • Immunosuppressive Agents / immunology
  • Inflammation / immunology*
  • Interleukin-10 / genetics
  • Interleukin-10 / metabolism
  • Lung / immunology*
  • Lung / metabolism
  • Lung / pathology
  • Lung Neoplasms / immunology*
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / pathology
  • Macrophages, Alveolar / immunology*
  • Male
  • Mice
  • Mice, Transgenic
  • NF-kappa B / genetics
  • NF-kappa B / metabolism*
  • Pulmonary Disease, Chronic Obstructive / immunology*
  • Pulmonary Disease, Chronic Obstructive / metabolism
  • Pulmonary Disease, Chronic Obstructive / pathology
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • T-Lymphocytes, Regulatory / immunology
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism

Substances

  • Immunosuppressive Agents
  • NF-kappa B
  • RNA, Messenger
  • Transforming Growth Factor beta
  • Interleukin-10
  • I-kappa B Kinase