Extracellular Vesicles in Feto–Maternal Crosstalk and Pregnancy Disorders

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Abstract

Extracellular vesicles (EVs) actively participate in inter-cellular crosstalk and have progressively emerged as key players of organized communities of cells within multicellular organisms in health and disease. For these reasons, EVs are attracting the attention of many investigators across different biomedical fields. In this scenario, the possibility to study specific placental-derived EVs in the maternal peripheral blood may open novel perspectives in the development of new early biomarkers for major obstetric pathological conditions. Here we reviewed the involvement of EVs in feto–maternal crosstalk mechanisms, both in physiological and pathological conditions (preeclampsia, fetal growth restriction, preterm labor, gestational diabetes mellitus), also underlining the usefulness of EV characterization in maternal–fetal medicine.

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Most cited references 65

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Extracellular Vesicle Heterogeneity: Subpopulations, Isolation Techniques, and Diverse Functions in Cancer Progression

Eduard Willms, Carlos Cabañas, Imre Mäger … (2018)

Cells release membrane enclosed nano-sized vesicles termed extracellular vesicles (EVs) that function as mediators of intercellular communication by transferring biological information between cells. Tumor-derived EVs have emerged as important mediators in cancer development and progression, mainly through transfer of their bioactive content which can include oncoproteins, oncogenes, chemokine receptors, as well as soluble factors, transcripts of proteins and miRNAs involved in angiogenesis or inflammation. This transfer has been shown to influence the metastatic behavior of primary tumors. Moreover, tumor-derived EVs have been shown to influence distant cellular niches, establishing favorable microenvironments that support growth of disseminated cancer cells upon their arrival at these pre-metastatic niches. It is generally accepted that cells release a number of major EV populations with distinct biophysical properties and biological functions. Exosomes, microvesicles, and apoptotic bodies are EV populations most widely studied and characterized. They are discriminated based primarily on their intracellular origin. However, increasing evidence suggests that even within these EV populations various subpopulations may exist. This heterogeneity introduces an extra level of complexity in the study of EV biology and function. For example, EV subpopulations could have unique roles in the intricate biological processes underlying cancer biology. Here, we discuss current knowledge regarding the role of subpopulations of EVs in cancer development and progression and highlight the relevance of EV heterogeneity. The position of tetraspanins and integrins therein will be highlighted. Since addressing EV heterogeneity has become essential for the EV field, current and novel techniques for isolating EV subpopulations will also be discussed. Further dissection of EV heterogeneity will advance our understanding of the critical roles of EVs in health and disease.

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Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro.

Christian Weber, Mihail Hristov, Stefan Linder … (2004)

Endothelial progenitor cells (EPCs) play a role in the repair of ischemic or injured tissue. Because endothelial injury can be associated with apoptosis, we have investigated whether apoptotic bodies from mature endothelial cells (ECs) may affect growth and differentiation of EPCs in vitro. A 24-hour incubation of isolated human EPCs with apoptotic bodies-rich medium (ABRM) from ECs led to a significant increase in the number of spindle-shaped attached cells. EPCs were characterized by DiI-Ac-LDL/lectin staining and measurement of CD34 and kinase insert domain receptor (KDR) expression. The treatment with ABRM resulted in a 2-fold increase of DiI-Ac-LDL/lectin-positive cells and up-regulation of CD34 (22% +/- 2% versus 13% +/- 3%, P < .05 and KDR (49% +/- 12% versus 19% +/- 7%, P < .05). Fluorescence and confocal laser microscopy demonstrated the uptake of apoptotic bodies by the EPCs. Apoptotic bodies-depleted medium had no effect, whereas the incubation with suspension of apoptotic bodies induced effects similar to those of ABRM. Our results suggest that apoptotic bodies from ECs are taken up by EPCs, increasing their number and differentiation state. Such a mechanism may facilitate the repair of injured endothelium and may represent a new signaling pathway between progenitor and damaged somatic cells.

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A Gestational Profile of Placental Exosomes in Maternal Plasma and Their Effects on Endothelial Cell Migration

Carlos Salomon, María Torres Parra, Miharu Kobayashi … (2014)

Studies completed to date provide persuasive evidence that placental cell-derived exosomes play a significant role in intercellular communication pathways that potentially contribute to placentation and development of materno-fetal vascular circulation. The aim of this study was to establish the gestational-age release profile and bioactivity of placental cell-derived exosome in maternal plasma. Plasma samples (n = 20 per pregnant group) were obtained from non-pregnant and pregnant women in the first (FT, 6–12 weeks), second (ST, 22–24 weeks) and third (TT, 32–38 weeks) trimester. The number of exosomes and placental exosome contribution were determined by quantifying immunoreactive exosomal CD63 and placenta-specific marker (PLAP), respectively. The effect of exosomes isolated from FT, ST and TT on endothelial cell migration were established using a real-time, live-cell imaging system (Incucyte). Exosome plasma concentration was more than 50-fold greater in pregnant women than in non-pregnant women (p<0.001). During normal healthy pregnancy, the number of exosomes present in maternal plasma increased significantly with gestational age by more that two-fold (p<0.001). Exosomes isolated from FT, ST and TT increased endothelial cell migration by 1.9±0.1, 1.6±0.2 and 1.3±0.1-fold, respectively compared to the control. Pregnancy is associated with a dramatic increase in the number of exosomes present in plasma and maternal plasma exosomes are bioactive. While the role of placental cell-derived exosome in regulating maternal and/or fetal vascular responses remains to be elucidated, changes in exosome profile may be of clinical utility in the diagnosis of placental dysfunction.

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Journal

Journal ID (nlm-ta): Int J Mol Sci

Journal ID (iso-abbrev): Int J Mol Sci

Journal ID (publisher-id): ijms

Title: International Journal of Molecular Sciences

Publisher: MDPI

ISSN (Electronic): 1422-0067

Publication date (Electronic): 19 March 2020

Publication date Collection: March 2020

Volume: 21

Issue: 6

Electronic Location Identifier: 2120

Affiliations

[1 ]Department of Obstetrics and Gynecology, University of Chieti, 66100 Chieti, Italy; alicedamico91@ 123456gmail.com (A.D.); liberati@ 123456unich.it (M.L.)

[2 ]Department of Medicine and Aging Sciences, University “G. d’Annunzio” of Chieti-Pescara, 66100 Chieti, Italy; giuseppina.bologna@ 123456hotmail.it (G.B.); simeone.pasquale@ 123456gmail.com (P.S.); evitacolonna@ 123456unich.it (E.V.); s.miscia@ 123456unich.it (S.M.); p.lanuti@ 123456unich.it (P.L.)

[3 ]Centre on Aging Sciences and Translational Medicine (Ce.S.I.-Me.T.), University “G. D’Annunzio” of Chieti-Pescara, 66100 Chieti, Italy

[4 ]School of Medicine and Health Science, G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy; saracugini@ 123456hotmail.it (S.C.); franc3scamusca@ 123456gmail.com (F.M.); melania.febbo@ 123456gmail.com (M.F.); dolores.darcangelo@ 123456gmail.com (D.D.)

[5 ]Department of Molecular Medicine and Development, University of Siena, 53100 Siena, Italy; bucadavide@ 123456gmail.com

[6 ]Fetal Medicine Unit, Department of Medical and Surgical Sciences, Department of Obstetrics and Gynecology, University of Foggia, 71121 Foggia, Italy; dantoniofra@ 123456gmail.com

Author notes

[* ]Correspondence: danilobuca@ 123456gmail.com

[†]

These authors contributed equally to this work.

Author information

Pasquale Simeone https://orcid.org/0000-0003-4430-480X

Ester Vitacolonna https://orcid.org/0000-0003-1756-661X

Article

Publisher ID: ijms-21-02120

DOI: 10.3390/ijms21062120

PMC ID: 7139847

PubMed ID: 32204473

SO-VID: 51d8a684-aa69-4aa9-b029-c87607daac2f

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Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

Extracellular Vesicles in Feto–Maternal Crosstalk and Pregnancy Disorders

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Higher order chromatin architecture

Most cited references 65

Extracellular Vesicle Heterogeneity: Subpopulations, Isolation Techniques, and Diverse Functions in Cancer Progression

Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro.

A Gestational Profile of Placental Exosomes in Maternal Plasma and Their Effects on Endothelial Cell Migration

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