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

Koen Breyne (UGent) , Jonas Steenbrugge (UGent) , Kristel Demeyere (UGent) , Chun Geun Lee, Jack A Elias, Wolfram Petzl, David GE Smith, Pierre Germon and Evelyne Meyer (UGent)
(2018) FRONTIERS IN IMMUNOLOGY. 9.
Author
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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.
Keywords
chitinase 3-like 1, Escherichia coli, bovine mastitis, immunomodulation, mouse mammary gland infection model, COLONIC EPITHELIAL-CELLS, TISSUE RESPONSES, PROTEINS, MASTITIS, MILK, INFLAMMATION, CHITOTRIOSIDASE, APOPTOSIS, MODEL, WHEY

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MLA
Breyne, Koen et al. “Immunomodulation of Host Chitinase 3-like 1 During a Mammary Pathogenic Escherichia Coli Infection.” FRONTIERS IN IMMUNOLOGY 9 (2018): n. pag. Print.
APA
Breyne, K., Steenbrugge, J., Demeyere, K., Lee, C. G., Elias, J. A., Petzl, W., Smith, D. G., et al. (2018). Immunomodulation of host chitinase 3-like 1 during a mammary pathogenic Escherichia coli infection. FRONTIERS IN IMMUNOLOGY, 9.
Chicago author-date
Breyne, Koen, Jonas Steenbrugge, Kristel Demeyere, Chun Geun Lee, Jack A Elias, Wolfram Petzl, David GE Smith, Pierre Germon, and Evelyne Meyer. 2018. “Immunomodulation of Host Chitinase 3-like 1 During a Mammary Pathogenic Escherichia Coli Infection.” Frontiers in Immunology 9.
Chicago author-date (all authors)
Breyne, Koen, Jonas Steenbrugge, Kristel Demeyere, Chun Geun Lee, Jack A Elias, Wolfram Petzl, David GE Smith, Pierre Germon, and Evelyne Meyer. 2018. “Immunomodulation of Host Chitinase 3-like 1 During a Mammary Pathogenic Escherichia Coli Infection.” Frontiers in Immunology 9.
Vancouver
1.
Breyne K, Steenbrugge J, Demeyere K, Lee CG, Elias JA, Petzl W, et al. Immunomodulation of host chitinase 3-like 1 during a mammary pathogenic Escherichia coli infection. FRONTIERS IN IMMUNOLOGY. 2018;9.
IEEE
[1]
K. Breyne et al., “Immunomodulation of host chitinase 3-like 1 during a mammary pathogenic Escherichia coli infection,” FRONTIERS IN IMMUNOLOGY, vol. 9, 2018.
@article{8586588,
  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.},
  articleno    = {1143},
  author       = {Breyne, Koen and Steenbrugge, Jonas and Demeyere, Kristel and Lee, Chun Geun and Elias, Jack A and Petzl, Wolfram and Smith, David GE and Germon, Pierre and Meyer, Evelyne},
  issn         = {1664-3224},
  journal      = {FRONTIERS IN IMMUNOLOGY},
  keywords     = {chitinase 3-like 1,Escherichia coli,bovine mastitis,immunomodulation,mouse mammary gland infection model,COLONIC EPITHELIAL-CELLS,TISSUE RESPONSES,PROTEINS,MASTITIS,MILK,INFLAMMATION,CHITOTRIOSIDASE,APOPTOSIS,MODEL,WHEY},
  language     = {eng},
  pages        = {12},
  title        = {Immunomodulation of host chitinase 3-like 1 during a mammary pathogenic Escherichia coli infection},
  url          = {http://dx.doi.org/10.3389/fimmu.2018.01143},
  volume       = {9},
  year         = {2018},
}
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