Immunomodulation of host chitinase 3-like 1 during a mammary pathogenic Escherichia coli infection

Koen Breyne, Jonas Steenbrugge, Kristel Demeyere, Chun Geun Lee, Jack A. Elias, Wolfram Petzl, David George Emslie Smith, Pierre Germon, Evelyne Meyer

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4 Citations (Scopus)
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Abstract

Chitin is a N-acetyl-d-glucosamine biopolymer that can be recognized by chitin-binding proteins. Although mammals lack chitin synthase, they induce proteins responsible for detecting chitin in response to bacterial infections. Our aim was to investigate whether chitinase 3-like 1 (CHI3L1) has a potential role in the innate immunity of the Escherichia coli (E. coli) infected mammary gland. CHI3L1 protein was found to be secreted in whey of naturally coliform-affected quarters compared to whey samples isolated from healthy udders. In addition, gene expression of CHI3L1 was confirmed in udder tissue of cows experimentally infected with a mammary pathogenic E. coli (MPEC) strain. Despite the known anatomical differences, the bovine udders' innate immune response was mimicked by applying an experimental mouse model using MPEC or non-MPEC isolates. The effect of CHI3L1 expression in the murine mammary gland in response to coliform bacteria was investigated through the use of CHI3L1-/- mice as well as through treatment with either a pan-caspase inhibitor or chitin particles in wild-type mice. The local induction of CHI3L1 postinfection with different E. coli strains was demonstrated to be independent of both bacterial growth and mammary interleukin (IL)-8 levels. Indeed, CHI3L1 emerged as a regulator impacting on the transcytosis of Ly6G-positive cells from the interstitial space into the alveolar lumen of the mammary tissue. Furthermore, CHI3L1 was found to be upstream regulated by caspase activity and had a major downstream effect on the local pro-inflammatory cytokine profile, including IL-1beta, IL-6, and RANTES/CCL5. In conclusion, CHI3L1 was demonstrated to play a key role in the cytokine and caspase signaling during E. coli triggered inflammation of the mammary gland.

Original languageEnglish
Article number1143
JournalFrontiers in Immunology
Volume9
DOIs
Publication statusPublished - 28 May 2018

Keywords

  • Bovine mastitis
  • Chitinase 3-like 1
  • Escherichia coli
  • Immunomodulation
  • Mouse mammary gland infection model

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology

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  • Cite this

    Breyne, K., Steenbrugge, J., Demeyere, K., Lee, C. G., Elias, J. A., Petzl, W., Smith, D. G. E., Germon, P., & Meyer, E. (2018). Immunomodulation of host chitinase 3-like 1 during a mammary pathogenic Escherichia coli infection. Frontiers in Immunology, 9, [1143]. https://doi.org/10.3389/fimmu.2018.01143