Galectin-3 Interacts with the CHI3L1 Axis and Contributes to Hermansky-Pudlak Syndrome Lung Disease

J Immunol. 2018 Mar 15;200(6):2140-2153. doi: 10.4049/jimmunol.1701442. Epub 2018 Feb 2.

Abstract

Hermansky-Pudlak syndrome (HPS) comprises a group of inherited disorders caused by mutations that alter the function of lysosome-related organelles. Pulmonary fibrosis is the major cause of morbidity and mortality in HPS-1 and HPS-4 patients. However, the mechanisms that underlie the exaggerated injury and fibroproliferative repair responses in HPS have not been adequately defined. In particular, although Galectin-3 (Gal-3) is dysregulated in HPS, its roles in the pathogenesis of HPS have not been adequately defined. In addition, although chitinase 3-like 1 (CHI3L1) and its receptors play major roles in the injury and repair responses in HPS, the ability of Gal-3 to interact with or alter the function of these moieties has not been evaluated. In this article, we demonstrate that Gal-3 accumulates in exaggerated quantities in bronchoalveolar lavage fluids, and traffics abnormally and accumulates intracellularly in lung fibroblasts and macrophages from bleomycin-treated pale ear, HPS-1-deficient mice. We also demonstrate that Gal-3 drives epithelial apoptosis when in the extracellular space, and stimulates cell proliferation and myofibroblast differentiation when accumulated in fibroblasts and M2-like differentiation when accumulated in macrophages. Biophysical and signaling evaluations also demonstrated that Gal-3 physically interacts with IL-13Rα2 and CHI3L1, and competes with TMEM219 for IL-13Rα2 binding. By doing so, Gal-3 diminishes the antiapoptotic effects of and the antiapoptotic signaling induced by CHI3L1 in epithelial cells while augmenting macrophage Wnt/β-catenin signaling. Thus, Gal-3 contributes to the exaggerated injury and fibroproliferative repair responses in HPS by altering the antiapoptotic and fibroproliferative effects of CHI3L1 and its receptor complex in a tissue compartment-specific manner.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Bleomycin / pharmacology
  • Bronchoalveolar Lavage Fluid / chemistry
  • Cell Differentiation / drug effects
  • Cell Proliferation / drug effects
  • Cell Proliferation / physiology
  • Chitinase-3-Like Protein 1 / metabolism*
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Galectin 3 / metabolism*
  • Hermanski-Pudlak Syndrome / metabolism*
  • Lung / drug effects
  • Lung / metabolism*
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Pulmonary Fibrosis / metabolism
  • Wnt Signaling Pathway / drug effects
  • beta Catenin / metabolism

Substances

  • Chitinase-3-Like Protein 1
  • Galectin 3
  • beta Catenin
  • Bleomycin