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Angiogenic activity of human chorionic gonadotropin through LH receptor activation on endothelial and epithelial cells of the endometrium

Sarah Berndt^*, Sophie Perrier d’Hauterive^,, Silvia Blacher^*, Christel Péqueux^*, Sophie Lorquet^*,, Carine Munaut^*, Martine Applanat, Marie Astrid Hervé, Noël Lamandé^||, Pierre Corvol^||, Frédéric van den Brûle^*,, Françis Frankenne^*, Matti Poutanen^¶, Ilpo Huhtaniemi^¶,#, Vincent Geenen, Agnès Noël^* and Jean-Michel Foidart^*,

^* Laboratory of Tumor and Development Biology, Centre de recherche en cancérologie expérimentale (CRCE), Université de Liège, Liège, Belgium;

Center of Immunology, Université de Liège, Liège, Belgium;

Department of Gynecology and Obstetrics, CHR-Citadelle, Liège, Belgium;

INSERM U135, Paris, France;

^|| Collège de France, INSERM U36, Paris, France;

^¶ Institute of Reproductive and Developmental Biology, Imperial College Faculty of Medicine, Hammersmith Campus, London, UK;

^# Department of Physiology, University of Turku, Turku, Finland

¹Correspondence: University of Liège, Laboratory of Tumor Biology and Development, Institute of Pathology CHU-B23, B-4000 Liège, Sart-Tilman, Belgium. E-mail: jmfoidart{at}ulg.ac.be

ABSTRACT

Successful embryo development requires an extensive endometrial angiogenesis in proximity of implantation site. The glycoprotein hCG is produced even before implantation by trophoblast in normal pregnancy. In this manuscript, we demonstrate an angiogenic effect of hCG in several in vivo (chick chorioallantoïc membrane, matrigel plug assay, aortic ring assay) and in vitro experimental models. In contrast, human placental lactogen (hPL) did not display angiogenic properties. LH/hCG receptor was detected in endothelial cells by reverse-transcriptase polymerase chain reaction (RT-PCR) and by Western blotting. In mice aortic ring assay, angiostimulation by hCG was abrogated by deletion of LH/hCG receptor (LuRKO mice). Use of recombinant hCG and anti–hCG antibody (Ab) further confirmed the specificity of this angiogenic activity. By using dibutyryl cAMP, adenylate cyclase, or protein kinase A inhibitors, we demonstrate that hCG-mediated angiogenesis involves adenylyl-cyclase–protein kinase A activation. Addition of hCG to endometrial epithelial epithelial cells, but not to cultured endothelial cells, stimulated vascular endothelial growth factor (VEGF). VEGF and hCG also displayed additive activities. Altogether, these data demonstrate that peritrophoblastic angiostimulation may result from a paracrine dialogue between trophoblast, epithelial, and endothelial cells through hCG and VEGF.—Berndt, S., Perrier d’Hauterive, S., Blacher, S., Péqueux, C., Lorquet, S., Munaut, C., Applanat, M., Hervé, M. A., Lamandé, N., Corvol, P., van den Brûle, F., Frankenne, F., Poutanen, M., Huhtaniemi, I., Geenen, V., Noël, A., Foidart, J.-M. Angiogenic activity of human chorionic gonadotropin through LH receptor activation on endothelial and epithelial cells of the endometrium.

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