Single administration of ultra-low-dose lipopolysaccharide in rat early pregnancy induces TLR4 activation in the placenta contributing to preeclampsia

PLoS One. 2015 Apr 8;10(4):e0124001. doi: 10.1371/journal.pone.0124001. eCollection 2015.

Abstract

Balanced immune responses are essential for the maintenance of successful pregnancy. Aberrant responses of immune system during pregnancy increase the risk of preeclampsia. Toll-like receptor 4 (TLR4) plays a crucial role in the activation of immune system at the maternal-fetal interface. This study aimed to generate a rat model of preeclampsia by lipopolysaccharide (LPS, a TLR4 agonist) administration on gestational day (GD) 5 as rats are subjected to placentation immediately after implantation between GDs 4 and 5, and to assess the contribution of TLR4 signaling to the development of preeclampsia. Single administration of 0.5 μg/kg LPS significantly increased blood pressure of pregnant rats since GD 6 (systolic blood pressure, 124.89 ± 1.79 mmHg versus 119.02 ± 1.80 mmHg, P < 0.05) and urinary protein level since GD 9 (2.02 ± 0.29 mg versus 1.11 ± 0.18 mg, P < 0.01), but barely affected blood pressure or proteinuria of virgin rats compared with those of saline-treated pregnant rats. This was accompanied with adverse pregnancy outcomes including fetal growth restriction. The expression of TLR4 and NF-κB p65 were both increased in the placenta but not the kidney from LPS-treated pregnant rats, with deficient trophoblast invasion and spiral artery remodeling. Furthermore, the levels of inflammatory cytokines were elevated systemically and locally in the placenta from pregnant rats treated with LPS. TLR4 signaling in the placenta was activated, to which that in the placenta of humans with preeclampsia changed similarly. In conclusion, LPS administration to pregnant rats in early pregnancy could elicit TLR4-mediated immune response at the maternal-fetal interface contributing to poor early placentation that may culminate in the preeclampsia-like syndrome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Pressure / drug effects
  • Disease Models, Animal*
  • Embryo Implantation / drug effects
  • Female
  • Fetal Growth Retardation / physiopathology
  • Fetus
  • Gene Expression Regulation
  • Humans
  • Injections, Intravenous
  • Lipopolysaccharides / administration & dosage*
  • Placenta / blood supply
  • Placenta / drug effects
  • Placenta / immunology*
  • Placenta / physiopathology
  • Placentation / drug effects
  • Pre-Eclampsia / chemically induced
  • Pre-Eclampsia / genetics
  • Pre-Eclampsia / immunology*
  • Pre-Eclampsia / physiopathology
  • Pregnancy
  • Rats*
  • Rats, Sprague-Dawley
  • Signal Transduction
  • Toll-Like Receptor 4 / agonists
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology*
  • Transcription Factor RelA / agonists
  • Transcription Factor RelA / genetics
  • Transcription Factor RelA / immunology

Substances

  • Lipopolysaccharides
  • Rela protein, rat
  • Tlr4 protein, rat
  • Toll-Like Receptor 4
  • Transcription Factor RelA

Grants and funding

This study was supported by the following grants: Chinese National Natural Science Foundation (81370724, 81070508); Maternal and Fetus Medicine Key Lab of Jiangsu Province, China (XK 201102); Innovative Research Program for Postgraduate in Higher Education Institutions of Jiangsu Province for the year 2013 (CXLX13_568). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.