Role of mesothelial cell-derived granulocyte colony-stimulating factor in interleukin-17-induced neutrophil accumulation in the peritoneum

J. Witowski, K. Ksia̧zek, C. Warnecke, M. Kuźlan, K. Korybalska, H. Tayama, J. Wiśniewska-Elnur, K. Pawlaczyk, J. Trómińska, A. Brȩborowicz, A. Jörres

Research output: Contribution to journalArticle

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Abstract

Recent studies suggest that peritoneal CD4+ T lymphocytes may control recruitment of polymorphonuclear leukocytes (PMN) during peritonitis by an interleukin-17 (IL-17)-dependent mechanism. IL-17 and granulocyte colony-stimulating factor (G-CSF) have been proposed to form an axis that regulates PMN transmigration. Here we report on the role of G-CSF released by human peritoneal mesothelial cells (HPMCs) in IL-17A-mediated peritoneal PMN accumulation. In vitro exposure of HPMCs to IL-17A resulted in a time- and dose-dependent release of G-CSF. This effect was related to the induction of G-CSF mRNA and mediated through the nuclear factor-κB (NF-κB) pathway. The novel observation was that IL-17A-stimulated NF-κB activation in HPMCs followed a biphasic profile, with an early induction (45 min), followed by the return to basal levels (90 min), and a delayed induction (3 h). Tumor necrosis factor α synergistically amplified IL-17A-induced G-CSF production by enhanced NF-κB activation and through stabilization of G-CSF mRNA. Intraperitoneal (i.p.) administration of IL-17A in Balb/c mice resulted in increased local levels of G-CSF and selective PMN accumulation. Administration of anti-G-CSF blocking antibody before IL-17A injection significantly reduced the IL-17A-triggered PMN infiltration. This effect occurred despite increased i.p. levels of PMN-specific chemokines KC and macrophage inflammatory protein-2 seen in animals treated with anti-G-CSF antibody. These data demonstrate that the mesothelium-derived G-CSF plays an important role in IL-17A-induced PMN recruitment into the peritoneum.

Original languageEnglish (US)
Pages (from-to)514-525
Number of pages12
JournalKidney International
Volume71
Issue number6
DOIs
StatePublished - Mar 13 2007
Externally publishedYes

Fingerprint

Interleukin-17
Peritoneum
Granulocyte Colony-Stimulating Factor
Neutrophils
Chemokine CXCL2
Messenger RNA
Blocking Antibodies
Peritonitis
Chemokines
Epithelium
Tumor Necrosis Factor-alpha
Observation
T-Lymphocytes
Injections

Keywords

  • Chemokines
  • G-CSF
  • IL-17
  • Mesothelium
  • Neutrophils
  • Peritoneum

ASJC Scopus subject areas

  • Nephrology

Cite this

Role of mesothelial cell-derived granulocyte colony-stimulating factor in interleukin-17-induced neutrophil accumulation in the peritoneum. / Witowski, J.; Ksia̧zek, K.; Warnecke, C.; Kuźlan, M.; Korybalska, K.; Tayama, H.; Wiśniewska-Elnur, J.; Pawlaczyk, K.; Trómińska, J.; Brȩborowicz, A.; Jörres, A.

In: Kidney International, Vol. 71, No. 6, 13.03.2007, p. 514-525.

Research output: Contribution to journalArticle

Witowski, J, Ksia̧zek, K, Warnecke, C, Kuźlan, M, Korybalska, K, Tayama, H, Wiśniewska-Elnur, J, Pawlaczyk, K, Trómińska, J, Brȩborowicz, A & Jörres, A 2007, 'Role of mesothelial cell-derived granulocyte colony-stimulating factor in interleukin-17-induced neutrophil accumulation in the peritoneum', Kidney International, vol. 71, no. 6, pp. 514-525. https://doi.org/10.1038/sj.ki.5002082
Witowski, J. ; Ksia̧zek, K. ; Warnecke, C. ; Kuźlan, M. ; Korybalska, K. ; Tayama, H. ; Wiśniewska-Elnur, J. ; Pawlaczyk, K. ; Trómińska, J. ; Brȩborowicz, A. ; Jörres, A. / Role of mesothelial cell-derived granulocyte colony-stimulating factor in interleukin-17-induced neutrophil accumulation in the peritoneum. In: Kidney International. 2007 ; Vol. 71, No. 6. pp. 514-525.
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abstract = "Recent studies suggest that peritoneal CD4+ T lymphocytes may control recruitment of polymorphonuclear leukocytes (PMN) during peritonitis by an interleukin-17 (IL-17)-dependent mechanism. IL-17 and granulocyte colony-stimulating factor (G-CSF) have been proposed to form an axis that regulates PMN transmigration. Here we report on the role of G-CSF released by human peritoneal mesothelial cells (HPMCs) in IL-17A-mediated peritoneal PMN accumulation. In vitro exposure of HPMCs to IL-17A resulted in a time- and dose-dependent release of G-CSF. This effect was related to the induction of G-CSF mRNA and mediated through the nuclear factor-κB (NF-κB) pathway. The novel observation was that IL-17A-stimulated NF-κB activation in HPMCs followed a biphasic profile, with an early induction (45 min), followed by the return to basal levels (90 min), and a delayed induction (3 h). Tumor necrosis factor α synergistically amplified IL-17A-induced G-CSF production by enhanced NF-κB activation and through stabilization of G-CSF mRNA. Intraperitoneal (i.p.) administration of IL-17A in Balb/c mice resulted in increased local levels of G-CSF and selective PMN accumulation. Administration of anti-G-CSF blocking antibody before IL-17A injection significantly reduced the IL-17A-triggered PMN infiltration. This effect occurred despite increased i.p. levels of PMN-specific chemokines KC and macrophage inflammatory protein-2 seen in animals treated with anti-G-CSF antibody. These data demonstrate that the mesothelium-derived G-CSF plays an important role in IL-17A-induced PMN recruitment into the peritoneum.",
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