MAPK mutations and cigarette smoke promote the pathogenesis of pulmonary Langerhans cell histiocytosis

JCI Insight. 2020 Feb 27;5(4):e132048. doi: 10.1172/jci.insight.132048.

Abstract

Pulmonary Langerhans cell histiocytosis (PLCH) is a rare smoking-related lung disease characterized by dendritic cell (DC) accumulation, bronchiolocentric nodule formation, and cystic lung remodeling. Approximately 50% of patients with PLCH harbor somatic BRAF-V600E mutations in cells of the myeloid/monocyte lineage. However, the rarity of the disease and lack of animal models have impeded the study of PLCH pathogenesis. Here, we establish a cigarette smoke-exposed (CS-exposed) BRAF-V600E-mutant mouse model that recapitulates many hallmark characteristics of PLCH. We show that CD11c-targeted expression of BRAF-V600E increases DC responsiveness to stimuli, including the chemokine CCL20, and that mutant cell accumulation in the lungs of CS-exposed mice is due to both increased cellular viability and enhanced recruitment. Moreover, we report that the chemokine CCL7 is secreted from DCs and human peripheral blood monocytes in a BRAF-V600E-dependent manner, suggesting a possible mechanism for recruitment of cells known to dominate PLCH lesions. Inflammatory lesions and airspace dilation in BRAF-V600E mice in response to CS are attenuated by transitioning animals to filtered air and treatment with a BRAF-V600E inhibitor, PLX4720. Collectively, this model provides mechanistic insights into the role of myelomonocytic cells and the BRAF-V600E mutation and CS exposure in PLCH pathogenesis and provides a platform to develop biomarkers and therapeutic targets.

Keywords: Chemokines; Dendritic cells; Immunology; Molecular pathology; Pulmonology.

Publication types

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

MeSH terms

  • Animals
  • CD11c Antigen / genetics
  • Disease Models, Animal
  • Histiocytosis, Langerhans-Cell / etiology*
  • Lung Diseases / etiology*
  • Mice
  • Mitogen-Activated Protein Kinases / genetics*
  • Mutation*
  • Proto-Oncogene Proteins B-raf / genetics
  • Smoke / adverse effects*
  • Tobacco Products*

Substances

  • CD11c Antigen
  • Smoke
  • Proto-Oncogene Proteins B-raf
  • Mitogen-Activated Protein Kinases