Control of neutrophil influx during peritonitis by transcriptional cross-regulation of chemokine CXCL1 by IL-17 and IFN-γ.
Adult
Aged
Aged, 80 and over
Cells, Cultured
Chemokine CXCL1
/ genetics
Female
Humans
Interferon-gamma
/ metabolism
Interleukin-17
/ metabolism
Male
Middle Aged
Neutrophil Infiltration
/ drug effects
Neutrophils
/ drug effects
Peritoneum
/ drug effects
Peritonitis
/ genetics
STAT1 Transcription Factor
/ metabolism
Signal Transduction
Sp1 Transcription Factor
/ genetics
Transcription, Genetic
CXCL1
IFN-γ
IL-17
mesothelial cells
peritoneal dialysis
peritonitis
Journal
The Journal of pathology
ISSN: 1096-9896
Titre abrégé: J Pathol
Pays: England
ID NLM: 0204634
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
06
06
2019
revised:
08
02
2020
accepted:
23
03
2020
pubmed:
2
4
2020
medline:
22
9
2020
entrez:
2
4
2020
Statut:
ppublish
Résumé
Neutrophil infiltration is a hallmark of peritoneal inflammation, but mechanisms regulating neutrophil recruitment in patients with peritoneal dialysis (PD)-related peritonitis are not fully defined. We examined 104 samples of PD effluent collected during acute peritonitis for correspondence between a broad range of soluble parameters and neutrophil counts. We observed an association between peritoneal IL-17 and neutrophil levels. This relationship was evident in effluent samples with low but not high IFN-γ levels, suggesting a differential effect of IFN-γ concentration on neutrophil infiltration. Surprisingly, there was no association of neutrophil numbers with the level of CXCL1, a key IL-17-induced neutrophil chemoattractant. We investigated therefore the production of CXCL1 by human peritoneal mesothelial cells (HPMCs) under in vitro conditions mimicking clinical peritonitis. Stimulation of HPMCs with IL-17 increased CXCL1 production through induction of transcription factor SP1 and activation of the SP1-binding region of the CXCL1 promoter. These effects were amplified by TNFα. In contrast, IFN-γ dose-dependently suppressed IL-17-induced SP1 activation and CXCL1 production through a transcriptional mechanism involving STAT1. The SP1-mediated induction of CXCL1 was also observed in HPMCs exposed to PD effluent collected during peritonitis and containing IL-17 and TNFα, but not IFN-γ. Supplementation of the effluent with IFN-γ led to a dose-dependent activation of STAT1 and a resultant inhibition of SP1-induced CXCL1 expression. Transmesothelial migration of neutrophils in vitro increased upon stimulation of HPMCs with IL-17 and was reduced by IFN-γ. In addition, HPMCs were capable of binding CXCL1 at their apical cell surface. These observations indicate that changes in relative peritoneal concentrations of IL-17 and IFN-γ can differently engage SP1-STAT1, impacting on mesothelial cell transcription of CXCL1, whose release and binding to HPMC surface may determine optimal neutrophil recruitment and retention during peritonitis. © 2020 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of Pathological Society of Great Britain and Ireland.
Substances chimiques
CXCL1 protein, human
0
Chemokine CXCL1
0
IFNG protein, human
0
Interleukin-17
0
STAT1 Transcription Factor
0
STAT1 protein, human
0
Sp1 Transcription Factor
0
SP1 protein, human
0
Interferon-gamma
82115-62-6
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
175-186Subventions
Organisme : Medical Research Council
ID : MR/N023145/1
Pays : United Kingdom
Informations de copyright
© 2020 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of Pathological Society of Great Britain and Ireland.
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