CD74-Downregulation of Placental Macrophage-Trophoblastic Interactions in Preeclampsia

Circ Res. 2016 Jun 24;119(1):55-68. doi: 10.1161/CIRCRESAHA.116.308304. Epub 2016 May 19.

Abstract

Rationale: We hypothesized that cluster of differentiation 74 (CD74) downregulation on placental macrophages, leading to altered macrophage-trophoblast interaction, is involved in preeclampsia.

Objective: Preeclamptic pregnancies feature hypertension, proteinuria, and placental anomalies. Feto-placental macrophages regulate villous trophoblast differentiation during placental development. Disturbance of this well-balanced regulation can lead to pathological pregnancies.

Methods and results: We performed whole-genome expression analysis of placental tissue. CD74 was one of the most downregulated genes in placentas from preeclamptic women. By reverse transcriptase-polymerase chain reaction, we confirmed this finding in early-onset (<34 gestational week, n=26) and late-onset (≥34 gestational week, n=24) samples from preeclamptic women, compared with healthy pregnant controls (n=28). CD74 protein levels were analyzed by Western blot and flow cytometry. We identified placental macrophages to express CD74 by immunofluorescence, flow cytometry, and RT-PCR. CD74-positive macrophages were significantly reduced in preeclamptic placentas compared with controls. CD74-silenced macrophages showed that the adhesion molecules ALCAM, ICAM4, and Syndecan-2, as well as macrophage adhesion to trophoblasts were diminished. Naive and activated macrophages lacking CD74 showed a shift toward a proinflammatory signature with an increased secretion of tumor necrosis factor-α, chemokine (C-C motif) ligand 5, and monocyte chemotactic protein-1, when cocultured with trophoblasts compared with control macrophages. Trophoblasts stimulated by these factors express more CYP2J2, sFlt1, TNFα, and IL-8. CD74-knockout mice showed disturbed placental morphology, reduced junctional zone, smaller placentas, and impaired spiral artery remodeling with fetal growth restriction.

Conclusions: CD74 downregulation in placental macrophages is present in preeclampsia. CD74 downregulation leads to altered macrophage activation toward a proinflammatory signature and a disturbed crosstalk with trophoblasts.

Keywords: immunology; macrophages; preeclampsia; pregnancy; trophoblasts.

MeSH terms

  • Animals
  • Antigens, Differentiation, B-Lymphocyte / genetics
  • Antigens, Differentiation, B-Lymphocyte / metabolism*
  • Case-Control Studies
  • Cell Adhesion Molecules / metabolism
  • Cells, Cultured
  • Chemokine CXCL5 / metabolism
  • Cytochrome P-450 CYP2J2
  • Cytochrome P-450 Enzyme System / metabolism
  • Down-Regulation
  • Female
  • Histocompatibility Antigens Class II / genetics
  • Histocompatibility Antigens Class II / metabolism*
  • Humans
  • Interleukin-8 / metabolism
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Pre-Eclampsia / genetics
  • Pre-Eclampsia / metabolism*
  • Pre-Eclampsia / pathology
  • Pregnancy
  • Syndecan-2 / metabolism
  • Trophoblasts / cytology
  • Trophoblasts / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism
  • Vascular Endothelial Growth Factor Receptor-1 / metabolism

Substances

  • Antigens, Differentiation, B-Lymphocyte
  • CYP2J2 protein, human
  • Cell Adhesion Molecules
  • Chemokine CXCL5
  • Histocompatibility Antigens Class II
  • Interleukin-8
  • Tumor Necrosis Factor-alpha
  • invariant chain
  • Syndecan-2
  • Cytochrome P-450 Enzyme System
  • Cytochrome P-450 CYP2J2
  • Vascular Endothelial Growth Factor Receptor-1