Reciprocal upregulation of hypoxia-inducible factor-1α and persistently enhanced placental adenosine signaling contribute to the pathogenesis of preeclampsia

FASEB J. 2020 Mar;34(3):4041-4054. doi: 10.1096/fj.201902583R. Epub 2020 Jan 12.

Abstract

Recent evidence indicates that elevated placental adenosine signaling contributes to preeclampsia (PE). However, the molecular basis for the chronically enhanced placental adenosine signaling in PE remains unclear. Here, we report that hypoxia-inducible factor-1α (HIF-1α) is crucial for the enhancement of placental adenosine signaling. Utilizing a pharmacologic approach to reduce placental adenosine levels, we found that enhanced adenosine underlies increased placental HIF-1α in an angiotensin receptor type 1 receptor agonistic autoantibody (AT1 -AA)-induced mouse model of PE. Knockdown of placental HIF-1α in vivo suppressed the accumulation of adenosine and increased ecto-5'-nucleotidase (CD73) and adenosine A2B receptor (ADORA2B) in the placentas of PE mouse models induced by AT1 -AA or LIGHT, a TNF superfamily cytokine (TNFSF14). Human in vitro studies using placental villous explants demonstrated that increased HIF-1α resulting from ADORA2B activation facilitates the induction of CD73, ADORA2B, and FLT-1 expression. Overall, we demonstrated that (a) elevated placental HIF-1α by AT1 -AA or LIGHT upregulates CD73 and ADORA2B expression and (b) enhanced adenosine signaling through upregulated ADORA2B induces placental HIF-1α expression, which creates a positive feedback loop that promotes FLT-1 expression leading to disease development. Our results suggest that adenosine-based therapy targeting the malicious cycle of placental adenosine signaling may elicit therapeutic effects on PE.

Keywords: adenosine signaling; angiotensin II type I receptor agonistic autoantibody (AT1-AA); hypoxia-inducible factor-1α; preeclampsia; tumor necrosis factor superfamily member 14 (TNFSF14).

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine / metabolism*
  • Animals
  • Autoantibodies / genetics
  • Autoantibodies / metabolism*
  • Blood Pressure / genetics
  • Blood Pressure / physiology
  • Female
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Immunoblotting
  • Immunohistochemistry
  • Mice
  • Mice, Inbred C57BL
  • Placenta / metabolism*
  • Pre-Eclampsia / genetics
  • Pre-Eclampsia / metabolism*
  • Pregnancy
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Vascular Endothelial Growth Factor Receptor-1 / genetics
  • Vascular Endothelial Growth Factor Receptor-1 / metabolism

Substances

  • Autoantibodies
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • RNA, Small Interfering
  • Flt1 protein, mouse
  • Vascular Endothelial Growth Factor Receptor-1
  • Adenosine