Activated Neutrophils Propagate Fetal Membrane Inflammation and Weakening through ERK and Neutrophil Extracellular Trap-Induced TLR-9 Signaling

J Immunol. 2021 Mar 1;206(5):1039-1045. doi: 10.4049/jimmunol.2001268. Epub 2021 Jan 20.

Abstract

Preterm birth is associated with significant neonatal mortality and morbidity worldwide. Chorioamnionitis, inflammation of the fetal membranes (FMs), is a major risk factor and is characterized by neutrophil infiltration. However, the role of neutrophils at the FMs remains unclear. We recently reported that FMs exposed to bacterial LPS recruited more neutrophils compared with resting FMs and activated them to degranulate and release reactive oxygen species, chemokines/cytokines, and neutrophil extracellular traps. We posit that under resting conditions, neutrophils play a protective surveillance role, whereas during infection/inflammation, they induce FM tissue injury. To test this, human FM explants were exposed to neutrophil conditioned media (CM). We demonstrate that CM from neutrophils exposed to resting FM-CM did not affect FM viability or function. Conversely, CM from neutrophils activated by LPS-stimulated FM-CM significantly increased FM secretion of inflammatory IL-6, IL-8, GRO-α, and the markers of membrane weakening, MMP-9 and PGE2 This FM response was partially mediated by ERK signaling and neutrophil extracellular traps through the activation of the DNA sensor, TLR-9. Thus, neutrophils recruited by FMs during infection can propagate FM inflammation and weakening, acting in a feed-forward mechanism to propagate tissue injury at the maternal-fetal interface, increasing the risk of premature FM rupture and preterm birth in women with intrauterine infection.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Chorioamnionitis / immunology
  • Cytokines / immunology
  • Extracellular Traps / immunology*
  • Extraembryonic Membranes / immunology*
  • Female
  • Humans
  • Infant, Newborn
  • Inflammation / immunology*
  • MAP Kinase Signaling System / immunology*
  • Maternal-Fetal Relations
  • Neutrophil Activation / immunology*
  • Neutrophil Infiltration / immunology
  • Neutrophils / immunology*
  • Pregnancy
  • Premature Birth / immunology
  • Reactive Oxygen Species / immunology
  • Signal Transduction / immunology
  • Toll-Like Receptor 9 / immunology*

Substances

  • Cytokines
  • Reactive Oxygen Species
  • TLR9 protein, human
  • Toll-Like Receptor 9