Human Cytomegalovirus Infection Changes the Pattern of Surface Markers of Small Extracellular Vesicles Isolated From First Trimester Placental Long-Term Histocultures

Extracellular vesicles (EVs) have increasingly been recognized as key players in a wide variety of physiological and pathological contexts, including during pregnancy. Notably, EVs appear both as possible biomarkers and as mediators involved in the communication of the placenta with the maternal and...

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Main Authors: Mathilde Bergamelli, Hélène Martin, Mélinda Bénard, Jérôme Ausseil, Jean-Michel Mansuy, Ilse Hurbain, Maïlys Mouysset, Marion Groussolles, Géraldine Cartron, Yann Tanguy le Gac, Nathalie Moinard, Elsa Suberbielle, Jacques Izopet, Charlotte Tscherning, Graça Raposo, Daniel Gonzalez-Dunia, Gisela D’Angelo, Cécile E. Malnou
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2021.689122/full
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author Mathilde Bergamelli
Hélène Martin
Mélinda Bénard
Mélinda Bénard
Jérôme Ausseil
Jérôme Ausseil
Jean-Michel Mansuy
Ilse Hurbain
Ilse Hurbain
Maïlys Mouysset
Marion Groussolles
Marion Groussolles
Marion Groussolles
Géraldine Cartron
Yann Tanguy le Gac
Nathalie Moinard
Nathalie Moinard
Elsa Suberbielle
Jacques Izopet
Jacques Izopet
Charlotte Tscherning
Graça Raposo
Graça Raposo
Daniel Gonzalez-Dunia
Gisela D’Angelo
Cécile E. Malnou
author_facet Mathilde Bergamelli
Hélène Martin
Mélinda Bénard
Mélinda Bénard
Jérôme Ausseil
Jérôme Ausseil
Jean-Michel Mansuy
Ilse Hurbain
Ilse Hurbain
Maïlys Mouysset
Marion Groussolles
Marion Groussolles
Marion Groussolles
Géraldine Cartron
Yann Tanguy le Gac
Nathalie Moinard
Nathalie Moinard
Elsa Suberbielle
Jacques Izopet
Jacques Izopet
Charlotte Tscherning
Graça Raposo
Graça Raposo
Daniel Gonzalez-Dunia
Gisela D’Angelo
Cécile E. Malnou
author_sort Mathilde Bergamelli
collection DOAJ
description Extracellular vesicles (EVs) have increasingly been recognized as key players in a wide variety of physiological and pathological contexts, including during pregnancy. Notably, EVs appear both as possible biomarkers and as mediators involved in the communication of the placenta with the maternal and fetal sides. A better understanding of the physiological and pathological roles of EVs strongly depends on the development of adequate and reliable study models, specifically at the beginning of pregnancy where many adverse pregnancy outcomes have their origin. In this study, we describe the isolation of small EVs from a histoculture model of first trimester placental explants in normal conditions as well as upon infection by human cytomegalovirus. Using bead-based multiplex cytometry and electron microscopy combined with biochemical approaches, we characterized these small EVs and defined their associated markers and ultrastructure. We observed that infection led to changes in the expression level of several surface markers, without affecting the secretion and integrity of small EVs. Our findings lay the foundation for studying the functional role of EVs during early pregnancy, along with the identification of new predictive biomarkers for the severity and outcome of this congenital infection, which are still sorely lacking.
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spelling doaj.art-3c6c7a0436584794b1360c2aaacebf182022-12-21T20:02:14ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-09-01910.3389/fcell.2021.689122689122Human Cytomegalovirus Infection Changes the Pattern of Surface Markers of Small Extracellular Vesicles Isolated From First Trimester Placental Long-Term HistoculturesMathilde Bergamelli0Hélène Martin1Mélinda Bénard2Mélinda Bénard3Jérôme Ausseil4Jérôme Ausseil5Jean-Michel Mansuy6Ilse Hurbain7Ilse Hurbain8Maïlys Mouysset9Marion Groussolles10Marion Groussolles11Marion Groussolles12Géraldine Cartron13Yann Tanguy le Gac14Nathalie Moinard15Nathalie Moinard16Elsa Suberbielle17Jacques Izopet18Jacques Izopet19Charlotte Tscherning20Graça Raposo21Graça Raposo22Daniel Gonzalez-Dunia23Gisela D’Angelo24Cécile E. Malnou25Institut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceService de Néonatalogie, CHU Toulouse, Hôpital des Enfants, Toulouse, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceLaboratoire de Biochimie, CHU Toulouse, Hôpital Rangueil, Toulouse, FranceLaboratoire de Virologie, CHU Toulouse, Hôpital Purpan, Toulouse, FranceCNRS UMR 144, Structure et Compartiments Membranaires, Institut Curie, Université Paris Sciences et Lettres, Paris, FranceCNRS UMR 144, Plateforme d’Imagerie Cellulaire et Tissulaire (PICT-IBiSA), Institut Curie, Université Paris Sciences et Lettres, Paris, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceService de Diagnostic Prénatal, CHU Toulouse, Hôpital Paule de Viguier, Toulouse, FranceINSERM UMR 1027, UPS, Equipe SPHERE Epidémiologie et Analyses en Santé Publique: Risques, Maladies Chroniques et Handicaps, Université de Toulouse, Toulouse, FranceService de Gynécologie Obstétrique, CHU Toulouse, Hôpital Paule de Viguier, Toulouse, FranceService de Gynécologie Obstétrique, CHU Toulouse, Hôpital Paule de Viguier, Toulouse, France0Développement Embryonnaire, Fertilité, Environnement (DEFE), INSERM UMR 1203, Université de Toulouse et Université de Montpellier, Montpellier, France1CECOS, Groupe d’Activité de Médecine de la Reproduction, CHU Toulouse, Hôpital Paule de Viguier, Toulouse, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceLaboratoire de Virologie, CHU Toulouse, Hôpital Purpan, Toulouse, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceCNRS UMR 144, Structure et Compartiments Membranaires, Institut Curie, Université Paris Sciences et Lettres, Paris, FranceCNRS UMR 144, Plateforme d’Imagerie Cellulaire et Tissulaire (PICT-IBiSA), Institut Curie, Université Paris Sciences et Lettres, Paris, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceCNRS UMR 144, Structure et Compartiments Membranaires, Institut Curie, Université Paris Sciences et Lettres, Paris, FranceInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), INSERM, CNRS, UPS, Université de Toulouse, Toulouse, FranceExtracellular vesicles (EVs) have increasingly been recognized as key players in a wide variety of physiological and pathological contexts, including during pregnancy. Notably, EVs appear both as possible biomarkers and as mediators involved in the communication of the placenta with the maternal and fetal sides. A better understanding of the physiological and pathological roles of EVs strongly depends on the development of adequate and reliable study models, specifically at the beginning of pregnancy where many adverse pregnancy outcomes have their origin. In this study, we describe the isolation of small EVs from a histoculture model of first trimester placental explants in normal conditions as well as upon infection by human cytomegalovirus. Using bead-based multiplex cytometry and electron microscopy combined with biochemical approaches, we characterized these small EVs and defined their associated markers and ultrastructure. We observed that infection led to changes in the expression level of several surface markers, without affecting the secretion and integrity of small EVs. Our findings lay the foundation for studying the functional role of EVs during early pregnancy, along with the identification of new predictive biomarkers for the severity and outcome of this congenital infection, which are still sorely lacking.https://www.frontiersin.org/articles/10.3389/fcell.2021.689122/fullearly placentaextracellular vesiclescongenital infectionhuman cytomegalovirusplacental histoculture
spellingShingle Mathilde Bergamelli
Hélène Martin
Mélinda Bénard
Mélinda Bénard
Jérôme Ausseil
Jérôme Ausseil
Jean-Michel Mansuy
Ilse Hurbain
Ilse Hurbain
Maïlys Mouysset
Marion Groussolles
Marion Groussolles
Marion Groussolles
Géraldine Cartron
Yann Tanguy le Gac
Nathalie Moinard
Nathalie Moinard
Elsa Suberbielle
Jacques Izopet
Jacques Izopet
Charlotte Tscherning
Graça Raposo
Graça Raposo
Daniel Gonzalez-Dunia
Gisela D’Angelo
Cécile E. Malnou
Human Cytomegalovirus Infection Changes the Pattern of Surface Markers of Small Extracellular Vesicles Isolated From First Trimester Placental Long-Term Histocultures
Frontiers in Cell and Developmental Biology
early placenta
extracellular vesicles
congenital infection
human cytomegalovirus
placental histoculture
title Human Cytomegalovirus Infection Changes the Pattern of Surface Markers of Small Extracellular Vesicles Isolated From First Trimester Placental Long-Term Histocultures
title_full Human Cytomegalovirus Infection Changes the Pattern of Surface Markers of Small Extracellular Vesicles Isolated From First Trimester Placental Long-Term Histocultures
title_fullStr Human Cytomegalovirus Infection Changes the Pattern of Surface Markers of Small Extracellular Vesicles Isolated From First Trimester Placental Long-Term Histocultures
title_full_unstemmed Human Cytomegalovirus Infection Changes the Pattern of Surface Markers of Small Extracellular Vesicles Isolated From First Trimester Placental Long-Term Histocultures
title_short Human Cytomegalovirus Infection Changes the Pattern of Surface Markers of Small Extracellular Vesicles Isolated From First Trimester Placental Long-Term Histocultures
title_sort human cytomegalovirus infection changes the pattern of surface markers of small extracellular vesicles isolated from first trimester placental long term histocultures
topic early placenta
extracellular vesicles
congenital infection
human cytomegalovirus
placental histoculture
url https://www.frontiersin.org/articles/10.3389/fcell.2021.689122/full
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