Cis-acting lnc-Cxcl2 restrains neutrophil-mediated lung inflammation by inhibiting epithelial cell CXCL2 expression in virus infection

Proc Natl Acad Sci U S A. 2021 Oct 12;118(41):e2108276118. doi: 10.1073/pnas.2108276118.

Abstract

Chemokine production by epithelial cells is important for neutrophil recruitment during viral infection, the appropriate regulation of which is critical for restraining inflammation and attenuating subsequent tissue damage. Epithelial cell expression of long noncoding RNAs (lncRNAs), RNA-binding proteins, and their functional interactions during viral infection and inflammation remain to be fully understood. Here, we identified an inducible lncRNA in the Cxcl2 gene locus, lnc-Cxcl2, which could selectively inhibit Cxcl2 expression in mouse lung epithelial cells but not in macrophages. lnc-Cxcl2-deficient mice exhibited increased Cxcl2 expression, enhanced neutrophils recruitment, and more severe inflammation in the lung after influenza virus infection. Mechanistically, nucleus-localized lnc-Cxcl2 bound to Cxcl2 promoter, recruited a ribonucleoprotein La, which inhibited the chromatin accessibility of chemokine promoters, and consequently inhibited Cxcl2 transcription in cis However, unlike mouse lnc-Cxcl2, human lnc-CXCL2-4-1 inhibited multiple immune cytokine expressions including chemokines in human lung epithelial cells. Together, our results demonstrate a self-protecting mechanism within epithelial cells to restrain chemokine and neutrophil-mediated inflammation, providing clues for better understanding chemokine regulation and epithelial cell function in lung viral infection.

Keywords: chemokine CXCL2; epithelial cell; lung inflammation; neutrophil.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Animals
  • Cell Line, Tumor
  • Chemokine CXCL2 / genetics*
  • Chemokine CXCL2 / metabolism
  • Chromatin / metabolism
  • Epithelial Cells / metabolism
  • HEK293 Cells
  • Heterogeneous-Nuclear Ribonucleoprotein L / genetics
  • Humans
  • Inflammation / prevention & control
  • Inflammation Mediators
  • Influenza A virus / immunology
  • Lung / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutrophil Infiltration / immunology*
  • Neutrophils / immunology*
  • Orthomyxoviridae Infections / immunology
  • Orthomyxoviridae Infections / pathology
  • Pneumonia / immunology
  • Pneumonia / pathology
  • Pneumonia / virology
  • Promoter Regions, Genetic / genetics
  • RAW 264.7 Cells
  • RNA, Long Noncoding / genetics*
  • Vesicular Stomatitis / immunology
  • Vesicular Stomatitis / pathology
  • Vesicular stomatitis Indiana virus / immunology

Substances

  • CXCL2 protein, human
  • Chemokine CXCL2
  • Chromatin
  • Cxcl2 protein, mouse
  • Heterogeneous-Nuclear Ribonucleoprotein L
  • Inflammation Mediators
  • RNA, Long Noncoding