Evidence map›Paper›PMID 28904069›Full record

ArticleCirculation2017

Disturbed Placental Imprinting in Preeclampsia Leads to Altered Expression of DLX5, a Human-Specific Early Trophoblast Marker.

Julianna Zadora, Manvendra Singh, Florian Herse, Lukasz Przybyl, Nadine Haase, Michaela Golic, Hong Wa Yung, Berthold Huppertz, Judith E Cartwright, Guy Whitley and 10 more

Erratum issuedOpen access · greenAbstract read
PubMed Full text at PMC Publisher
In one paragraph

Article in Circulation, 2017. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 49 papers.

0numbers the graph read from it
0cells of the map it votes in
49citing papers in PubMed
4.4field-weighted citation impact, top 6% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

49 citing papers in PubMed, 78 citations in OpenAlex.

  1. Article
  2. Review
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  4. Article
  5. Application of single-cell RNA sequencing in preeclampsia.Frontiers in global women's health · 2026
    Review
  6. Review
  7. Article
  8. Article
  9. Super-Enhancers in Placental Development and Diseases.Journal of developmental biology · 2025
    Review
  10. Article
  11. Article
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  14. Article
  15. Review
  16. Article
  17. Article
  18. Review
  19. Article
  20. Machine-learning predictive model of pregnancy-induced hypertension in the first trimester.Hypertension research : official journal of the Japanese Society of Hypertension · 2023
    Article
4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

20 authors at 5 institutions in 4 countries.

Julianna ZadoraFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Manvendra SinghFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Florian HerseFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Lukasz PrzybylFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Nadine HaaseFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Michaela GolicFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Hong Wa YungFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Berthold HuppertzFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Judith E CartwrightFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Guy WhitleyFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Guro M JohnsenFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Giovanni LeviFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Annette IsbruchFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Herbert SchulzFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Friedrich C LuftFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Dominik N MüllerFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Anne Cathrine StaffFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.).
Laurence D HurstFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.). zizsvak@mdc-berlin.de l.d.hurst@bath.ac.uk ralf.dechend@charite.de.
Ralf DechendFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.). zizsvak@mdc-berlin.de l.d.hurst@bath.ac.uk ralf.dechend@charite.de.
Zsuzsanna IzsvákFrom Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany (J.Z., M.S., F.H., N.H., D.N.M., Z.I.); Experimental and Clinical Research Center, a joint cooperation between the Max-Delbrück Center for Molecular Medicine in the Helmholtz Association and the Charité-Universitätsmedizin Berlin, Germany (J.Z., F.H., L.P., N.H., M.G., H.S., F.C.L., D.N.M., R.D.); Berlin Institute of Health, Germany (J.Z., F.H., L.P., N.H., M.G., F.C.L., D.N.M., R.D., Z.I.); Department of Obstetrics and Department of Gynecology, Charité-Universitätsmedizin Berlin, Germany (M.G.); German Centre for Cardiovascular Research, partner site Berlin, Germany (N.H., D.N.M.); Centre for Trophoblast Research, University of Cambridge, UK (H.W.Y.); Institute of Cell Biology, Histology and Embryology, Medical University of Graz, Austria (B.H.); Molecular and Clinical Sciences Research Institute, St George's University of London, UK (J.E.C., G.W.); Division of Obstetrics and Gynaecology, Oslo University Hospital, Norway (G.M.J., A.C.S.); University of Oslo, Norway (G.M.J., A.C.S.); Évolution des Régulations Endocriniennes, Muséum Nationale d'Histoire Naturelle, Paris, France (G.L.); HELIOS-Klinikum, Berlin, Germany (A.I., R.D.); Cologne Center for Genomics, University of Cologne, Germany (H.S.); and Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK (L.D.H.). zizsvak@mdc-berlin.de l.d.hurst@bath.ac.uk ralf.dechend@charite.de.
Oslo University Hospital · NOEvolution des Régulations Endocriniennes · FRGerman Centre for Cardiovascular Research · DEHelios Hospital Berlin-Buch · DEOffice of Basic Energy Sciences · US

Funding

European Research Council 294742European Research Council 669207
6 · The paper itself

Abstract

backgroundPreeclampsia is a complex and common human-specific pregnancy syndrome associated with placental pathology. The human specificity provides both intellectual and methodological challenges, lacking a robust model system. Given the role of imprinted genes in human placentation and the vulnerability of imprinted genes to loss of imprinting changes, there has been extensive speculation, but no robust evidence, that imprinted genes are involved in preeclampsia. Our study aims to investigate whether disturbed imprinting contributes to preeclampsia.

methodsWe first aimed to confirm that preeclampsia is a disease of the placenta by generating and analyzing genome-wide molecular data on well-characterized patient material. We performed high-throughput transcriptome analyses of multiple placenta samples from healthy controls and patients with preeclampsia. Next, we identified differentially expressed genes in preeclamptic placentas and intersected them with the list of human imprinted genes. We used bioinformatics/statistical analyses to confirm association between imprinting and preeclampsia and to predict biological processes affected in preeclampsia. Validation included epigenetic and cellular assays. In terms of human specificity, we established an in vitro invasion-differentiation trophoblast model. Our comparative phylogenetic analysis involved single-cell transcriptome data of human, macaque, and mouse preimplantation embryogenesis.

resultsWe found disturbed placental imprinting in preeclampsia and revealed potential candidates, including

conclusionsOur analysis provides evidence of a true association among disturbed imprinting, gene expression, and preeclampsia. As a result of disturbed imprinting, the upregulated

Indexed as

Genomic ImprintingAnimalsCase-Control StudiesCell MovementCell ProliferationCells, CulturedCell SurvivalComputational BiologyDatabases, GeneticFemaleGene Expression ProfilingGene Expression Regulation, DevelopmentalGenome-Wide Association StudyHigh-Throughput Nucleotide SequencingHomeodomain ProteinsHumansDLX5 protein, humanHomeodomain ProteinsTranscription Factorsepigeneticsgene expression and regulationgenomic imprintingpreeclampsiatrophoblasts

Identifiers

PMID28904069
PMCPMC5671803
OpenAlexW2756050015

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