Pro-angiogenic effects of pregnancy-specific glycoproteins in endothelial and extravillous trophoblast cells

in Reproduction
Authors:
Shemona Rattila Department of Pathology, Uniformed Services University of Health Sciences, Bethesda, Maryland, USA

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Florian Kleefeldt Institute of Anatomy and Cell Biology, Julius-Maximilians-University Würzburg, Würzburg, Germany

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Angela Ballesteros Molecular Physiology and Biophysics Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA

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Jimena S Beltrame Laboratory of Physiology and Pharmacology of Reproduction, Centre for Pharmacological and Botanical Studies (CONICET – School of Medicine, University of Buenos Aires), Buenos Aires, Argentina

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Maria L Ribeiro Laboratory of Physiology and Pharmacology of Reproduction, Centre for Pharmacological and Botanical Studies (CONICET – School of Medicine, University of Buenos Aires), Buenos Aires, Argentina

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Süleyman Ergün Institute of Anatomy and Cell Biology, Julius-Maximilians-University Würzburg, Würzburg, Germany

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Gabriela Dveksler Department of Pathology, Uniformed Services University of Health Sciences, Bethesda, Maryland, USA

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Correspondence should be addressed to G Dveksler; Email: gabriela.dveksler@usuhs.edu
DOI:
https://doi.org/10.1530/REP-20-0169
Volume/Issue:
Volume 160: Issue 5
Page Range:
737–750
Article Type:
Research Article
Online Publication Date:
Nov 2020
Copyright:
© 2020 Society for Reproduction and Fertility 2020
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We previously reported that binding to heparan sulfate (HS) is required for the ability of the placentally secreted pregnancy-specific glycoprotein 1 (PSG1) to induce endothelial tubulogenesis. PSG1 is composed of four immunoglobulin-like domains but which domains of the protein bind to HS remains unknown. To analyze the interaction of PSG1 with HS, we generated several recombinant proteins, including the individual domains, chimeric proteins between two PSG1 domains, and mutants. Using flow cytometric and surface plasmon resonance studies, we determined that the B2 domain of PSG1 binds to HS and that the positively charged amino acids encompassed between amino acids 43–59 are required for this interaction. Furthermore, we showed that the B2 domain of PSG1 is required for the increase in the formation of tubes by endothelial cells (EC) including a human endometrial EC line and two extravillous trophoblast (EVT) cell lines and for the pro-angiogenic activity of PSG1 observed in an aortic ring assay. PSG1 enhanced the migration of ECs while it increased the expression of matrix metalloproteinase-2 in EVTs, indicating that the pro-angiogenic effect of PSG1 on these two cell types may be mediated by different mechanisms. Despite differences in amino acid sequence, we observed that all human PSGs bound to HS proteoglycans and confirmed that at least two other members of the family, PSG6 and PSG9, induce tube formation. These findings contribute to a better understanding of the pro-angiogenic activity of human PSGs and strongly suggest conservation of this function among all PSG family members.

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Print ISSN:
1470-1626
Online ISSN:
1741-7899

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