Myeloid-specific disruption of tyrosine phosphatase Shp2 promotes alternative activation of macrophages and predisposes mice to pulmonary fibrosis

J Immunol. 2014 Sep 15;193(6):2801-11. doi: 10.4049/jimmunol.1303463. Epub 2014 Aug 15.

Abstract

The alternative activation of M2 macrophages in the lungs has been implicated as a causative agent in pulmonary fibrosis; however, the mechanisms underlying M2 polarization are poorly characterized. In this study, we investigated the role of the ubiquitously expressed Src homology domain-containing tyrosine phosphatase Shp2 in this process. Shp2 inactivation augmented IL-4-mediated M2 polarization in vitro, suggesting that Shp2 regulates macrophage skewing and prevents a bias toward the M2 phenotype. Conditional removal of Shp2 in monocytes/macrophages with lysozyme M promoter-driven Cre recombinase caused an IL-4-mediated shift toward M2 polarization. Additionally, an increase in arginase activity was detected in Shp2(∆/∆) mice after i.p. injection of chitin, whereas Shp2-deficient macrophages showed enhanced M2 polarization and protection against schistosome egg-induced schistosomiasis. Furthermore, mutants were more sensitive than control mice to bleomycin-induced inflammation and pulmonary fibrosis. Shp2 was associated with IL-4Rα and inhibited JAK1/STAT6 signaling through its phosphatase activity; loss of Shp2 promoted the association of JAK1 with IL-4Rα, which enhanced IL-4-mediated JAK1/STAT6 activation that resulted in M2 skewing. Taken together, these findings define a role for Shp2 in alveolar macrophages and reveal that Shp2 is required to inhibit the progression of M2-associated pulmonary fibrosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase / biosynthesis
  • Bleomycin / adverse effects
  • Bleomycin / pharmacology
  • Bronchoalveolar Lavage Fluid / cytology
  • Bronchoalveolar Lavage Fluid / immunology
  • Cells, Cultured
  • Chitin / pharmacology
  • Inflammation / chemically induced
  • Interleukin-13 / biosynthesis
  • Interleukin-4 / biosynthesis
  • Interleukin-4 / immunology
  • Interleukin-5 / biosynthesis
  • Janus Kinase 1 / biosynthesis
  • Lung / immunology
  • Lung / pathology
  • Macrophage Activation / genetics
  • Macrophage Activation / immunology*
  • Macrophages, Alveolar / immunology
  • Mice
  • Mice, Knockout
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / genetics
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / immunology*
  • Pulmonary Fibrosis / chemically induced
  • Pulmonary Fibrosis / immunology*
  • RNA Interference
  • RNA, Small Interfering
  • Receptors, Cell Surface / immunology
  • STAT6 Transcription Factor / biosynthesis
  • Schistosoma japonicum / immunology*
  • Schistosomiasis japonica / immunology*
  • Schistosomiasis japonica / parasitology
  • Signal Transduction / genetics
  • Signal Transduction / immunology

Substances

  • Il4ra protein, mouse
  • Interleukin-13
  • Interleukin-5
  • RNA, Small Interfering
  • Receptors, Cell Surface
  • STAT6 Transcription Factor
  • Stat6 protein, mouse
  • Bleomycin
  • Chitin
  • Interleukin-4
  • Jak1 protein, mouse
  • Janus Kinase 1
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Ptpn11 protein, mouse
  • Arginase