An EG-VEGF-dependent decrease in homeobox gene NKX3.1 contributes to cytotrophoblast dysfunction: a possible mechanism in human fetal growth restriction.
Identifieur interne : 002B16 ( PubMed/Curation ); précédent : 002B15; suivant : 002B17An EG-VEGF-dependent decrease in homeobox gene NKX3.1 contributes to cytotrophoblast dysfunction: a possible mechanism in human fetal growth restriction.
Auteurs : P. Murthi [Australie] ; S. Brouillet [France] ; A. Pratt [Australie] ; Aj Borg [Australie] ; B. Kalionis [Belgique] ; F. Goffin [Belgique] ; V. Tsatsaris [France] ; C. Munaut [Belgique] ; Jj Feige [France] ; M. Benharouga [France] ; T. Fournier [France] ; N. Alfaidy [France]Source :
- Molecular medicine (Cambridge, Mass.) [ 1528-3658 ] ; 2015.
Abstract
Idiopathic fetal growth restriction (FGR) is frequently associated with placental insufficiency. Previous reports have provided evidence that EG-VEGF (endocrine gland derived-vascular endothelial growth factor), a placental secreted protein, is expressed during the first trimester of pregnancy, controls both trophoblast proliferation and invasion, and its increased expression is associated with human FGR. In this study, we hypothesise that EG-VEGF-dependent change in placental homeobox gene expressions contribute to trophoblast dysfunction in idiopathic FGR. The changes in EG-VEGF-dependent homeobox gene expressions were determined using a Homeobox gene cDNA array on placental explants of 8-12 weeks' gestation after stimulation with EG-VEGF in vitro for 24 hours. The Homeobox gene array identified a >5-fold increase in HOXA9, HOXC8, HOXC10, HOXD1, HOXD8, HOXD9 and HOXD11, while NKX 3.1 showed a >2 fold-decrease in mRNA expression compared to untreated controls. Homeobox gene NKX3.1 was selected as a candidate because it is a downstream target of EG-VEGF and its expression and functional role are largely unknown in control and idiopathic FGR-affected placentae. Real-time PCR and immunoblotting showed a significant decrease in NKX3.1 mRNA and protein levels, respectively, in placentae from FGR compared to control pregnancies. Gene inactivation in vitro using short-interference RNA specific for NKX3.1 demonstrated an increase in BeWo cell differentiation and a decrease in HTR8-SVneo proliferation. We conclude that the decreased expression of homeobox gene NKX3.1 down-stream of EG-VEGF may contribute to the trophoblast dysfunction associated with idiopathic FGR pregnancies.
DOI: 10.2119/molmed.2015.00071
PubMed: 26208047
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Murthi</name><affiliation wicri:level="1"><nlm:affiliation>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052</wicri:regionArea></affiliation></author><author><name sortKey="Brouillet, S" sort="Brouillet, S" uniqKey="Brouillet S" first="S" last="Brouillet">S. Brouillet</name><affiliation wicri:level="3"><nlm:affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 1036, Grenoble. 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Benharouga</name><affiliation wicri:level="1"><nlm:affiliation>Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5249, Laboratoire de Chimie et Biologie des Métaux, Grenoble, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5249, Laboratoire de Chimie et Biologie des Métaux, Grenoble</wicri:regionArea></affiliation></author><author><name sortKey="Fournier, T" sort="Fournier, T" uniqKey="Fournier T" first="T" last="Fournier">T. Fournier</name><affiliation wicri:level="1"><nlm:affiliation>INSERM, U1139, Paris, F-75006, France, Universite Paris Descartes, UMR-S1139, Sorbonne Paris Cite, Paris, F-75006, France, PremUp Foundation, Paris, F-75006, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INSERM, U1139, Paris, F-75006, France, Universite Paris Descartes, UMR-S1139, Sorbonne Paris Cite, Paris, F-75006, France, PremUp Foundation, Paris, F-75006</wicri:regionArea></affiliation></author><author><name sortKey="Alfaidy, N" sort="Alfaidy, N" uniqKey="Alfaidy N" first="N" last="Alfaidy">N. Alfaidy</name><affiliation wicri:level="3"><nlm:affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 1036, Grenoble. France.</nlm:affiliation><country>France</country><placeName><settlement type="city">Grenoble</settlement><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><wicri:orgArea>Institut National de la Santé et de la Recherche Médicale, Unité 1036</wicri:orgArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2015">2015</date><idno type="RBID">pubmed:26208047</idno><idno type="pmid">26208047</idno><idno type="doi">10.2119/molmed.2015.00071</idno><idno type="wicri:Area/PubMed/Corpus">002B89</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">002B89</idno><idno type="wicri:Area/PubMed/Curation">002B16</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Curation">002B16</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">An EG-VEGF-dependent decrease in homeobox gene NKX3.1 contributes to cytotrophoblast dysfunction: a possible mechanism in human fetal growth restriction.</title><author><name sortKey="Murthi, P" sort="Murthi, P" uniqKey="Murthi P" first="P" last="Murthi">P. Murthi</name><affiliation wicri:level="1"><nlm:affiliation>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052</wicri:regionArea></affiliation></author><author><name sortKey="Brouillet, S" sort="Brouillet, S" uniqKey="Brouillet S" first="S" last="Brouillet">S. Brouillet</name><affiliation wicri:level="3"><nlm:affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 1036, Grenoble. France.</nlm:affiliation><country>France</country><placeName><settlement type="city">Grenoble</settlement><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><wicri:orgArea>Institut National de la Santé et de la Recherche Médicale, Unité 1036</wicri:orgArea></affiliation></author><author><name sortKey="Pratt, A" sort="Pratt, A" uniqKey="Pratt A" first="A" last="Pratt">A. Pratt</name><affiliation wicri:level="1"><nlm:affiliation>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052</wicri:regionArea></affiliation></author><author><name sortKey="Borg, Aj" sort="Borg, Aj" uniqKey="Borg A" first="Aj" last="Borg">Aj Borg</name><affiliation wicri:level="1"><nlm:affiliation>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052</wicri:regionArea></affiliation></author><author><name sortKey="Kalionis, B" sort="Kalionis, B" uniqKey="Kalionis B" first="B" last="Kalionis">B. Kalionis</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Tumor and Developmental Biology University of Liège, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Laboratory of Tumor and Developmental Biology University of Liège</wicri:regionArea></affiliation></author><author><name sortKey="Goffin, F" sort="Goffin, F" uniqKey="Goffin F" first="F" last="Goffin">F. Goffin</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Tumor and Developmental Biology University of Liège, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Laboratory of Tumor and Developmental Biology University of Liège</wicri:regionArea></affiliation></author><author><name sortKey="Tsatsaris, V" sort="Tsatsaris, V" uniqKey="Tsatsaris V" first="V" last="Tsatsaris">V. Tsatsaris</name><affiliation wicri:level="1"><nlm:affiliation>Department of Obstetrics and Gynecology, Hôpital Cochin, Maternité Port-Royal, Université Rene Descartes, F-75014 Paris, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Department of Obstetrics and Gynecology, Hôpital Cochin, Maternité Port-Royal, Université Rene Descartes, F-75014 Paris</wicri:regionArea></affiliation></author><author><name sortKey="Munaut, C" sort="Munaut, C" uniqKey="Munaut C" first="C" last="Munaut">C. Munaut</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Tumor and Developmental Biology University of Liège, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Laboratory of Tumor and Developmental Biology University of Liège</wicri:regionArea></affiliation></author><author><name sortKey="Feige, Jj" sort="Feige, Jj" uniqKey="Feige J" first="Jj" last="Feige">Jj Feige</name><affiliation wicri:level="3"><nlm:affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 1036, Grenoble. France.</nlm:affiliation><country>France</country><placeName><settlement type="city">Grenoble</settlement><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><wicri:orgArea>Institut National de la Santé et de la Recherche Médicale, Unité 1036</wicri:orgArea></affiliation></author><author><name sortKey="Benharouga, M" sort="Benharouga, M" uniqKey="Benharouga M" first="M" last="Benharouga">M. Benharouga</name><affiliation wicri:level="1"><nlm:affiliation>Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5249, Laboratoire de Chimie et Biologie des Métaux, Grenoble, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5249, Laboratoire de Chimie et Biologie des Métaux, Grenoble</wicri:regionArea></affiliation></author><author><name sortKey="Fournier, T" sort="Fournier, T" uniqKey="Fournier T" first="T" last="Fournier">T. Fournier</name><affiliation wicri:level="1"><nlm:affiliation>INSERM, U1139, Paris, F-75006, France, Universite Paris Descartes, UMR-S1139, Sorbonne Paris Cite, Paris, F-75006, France, PremUp Foundation, Paris, F-75006, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INSERM, U1139, Paris, F-75006, France, Universite Paris Descartes, UMR-S1139, Sorbonne Paris Cite, Paris, F-75006, France, PremUp Foundation, Paris, F-75006</wicri:regionArea></affiliation></author><author><name sortKey="Alfaidy, N" sort="Alfaidy, N" uniqKey="Alfaidy N" first="N" last="Alfaidy">N. Alfaidy</name><affiliation wicri:level="3"><nlm:affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 1036, Grenoble. France.</nlm:affiliation><country>France</country><placeName><settlement type="city">Grenoble</settlement><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region></placeName><wicri:orgArea>Institut National de la Santé et de la Recherche Médicale, Unité 1036</wicri:orgArea></affiliation></author></analytic><series><title level="j">Molecular medicine (Cambridge, Mass.)</title><idno type="eISSN">1528-3658</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Idiopathic fetal growth restriction (FGR) is frequently associated with placental insufficiency. Previous reports have provided evidence that EG-VEGF (endocrine gland derived-vascular endothelial growth factor), a placental secreted protein, is expressed during the first trimester of pregnancy, controls both trophoblast proliferation and invasion, and its increased expression is associated with human FGR. In this study, we hypothesise that EG-VEGF-dependent change in placental homeobox gene expressions contribute to trophoblast dysfunction in idiopathic FGR. The changes in EG-VEGF-dependent homeobox gene expressions were determined using a Homeobox gene cDNA array on placental explants of 8-12 weeks' gestation after stimulation with EG-VEGF in vitro for 24 hours. The Homeobox gene array identified a >5-fold increase in HOXA9, HOXC8, HOXC10, HOXD1, HOXD8, HOXD9 and HOXD11, while NKX 3.1 showed a >2 fold-decrease in mRNA expression compared to untreated controls. Homeobox gene NKX3.1 was selected as a candidate because it is a downstream target of EG-VEGF and its expression and functional role are largely unknown in control and idiopathic FGR-affected placentae. Real-time PCR and immunoblotting showed a significant decrease in NKX3.1 mRNA and protein levels, respectively, in placentae from FGR compared to control pregnancies. Gene inactivation in vitro using short-interference RNA specific for NKX3.1 demonstrated an increase in BeWo cell differentiation and a decrease in HTR8-SVneo proliferation. We conclude that the decreased expression of homeobox gene NKX3.1 down-stream of EG-VEGF may contribute to the trophoblast dysfunction associated with idiopathic FGR pregnancies.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">26208047</PMID><DateCreated><Year>2015</Year><Month>07</Month><Day>24</Day></DateCreated><DateRevised><Year>2017</Year><Month>02</Month><Day>20</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1528-3658</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2015</Year><Month>Jul</Month><Day>21</Day></PubDate></JournalIssue><Title>Molecular medicine (Cambridge, Mass.)</Title><ISOAbbreviation>Mol. Med.</ISOAbbreviation></Journal><ArticleTitle>An EG-VEGF-dependent decrease in homeobox gene NKX3.1 contributes to cytotrophoblast dysfunction: a possible mechanism in human fetal growth restriction.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.2119/molmed.2015.00071</ELocationID><Abstract><AbstractText>Idiopathic fetal growth restriction (FGR) is frequently associated with placental insufficiency. Previous reports have provided evidence that EG-VEGF (endocrine gland derived-vascular endothelial growth factor), a placental secreted protein, is expressed during the first trimester of pregnancy, controls both trophoblast proliferation and invasion, and its increased expression is associated with human FGR. In this study, we hypothesise that EG-VEGF-dependent change in placental homeobox gene expressions contribute to trophoblast dysfunction in idiopathic FGR. The changes in EG-VEGF-dependent homeobox gene expressions were determined using a Homeobox gene cDNA array on placental explants of 8-12 weeks' gestation after stimulation with EG-VEGF in vitro for 24 hours. The Homeobox gene array identified a >5-fold increase in HOXA9, HOXC8, HOXC10, HOXD1, HOXD8, HOXD9 and HOXD11, while NKX 3.1 showed a >2 fold-decrease in mRNA expression compared to untreated controls. Homeobox gene NKX3.1 was selected as a candidate because it is a downstream target of EG-VEGF and its expression and functional role are largely unknown in control and idiopathic FGR-affected placentae. Real-time PCR and immunoblotting showed a significant decrease in NKX3.1 mRNA and protein levels, respectively, in placentae from FGR compared to control pregnancies. Gene inactivation in vitro using short-interference RNA specific for NKX3.1 demonstrated an increase in BeWo cell differentiation and a decrease in HTR8-SVneo proliferation. We conclude that the decreased expression of homeobox gene NKX3.1 down-stream of EG-VEGF may contribute to the trophoblast dysfunction associated with idiopathic FGR pregnancies.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Murthi</LastName><ForeName>P</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Medicine, Monash University, Clayton, Victoria 3168, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brouillet</LastName><ForeName>S</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 1036, Grenoble. France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Univ. Grenoble-Alpes, 38000, Grenoble, France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Commissariat à l'Energie Atomique (CEA), iRTSV-Biology of Cancer and infection, Grenoble, France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Centre Hospitalier Universitaire de Grenoble, Hôpital Couple-Enfant, Centre Clinique et Biologique d'Assistance Médicale à la Procréation, 38700, La Tronche, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pratt</LastName><ForeName>A</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Borg</LastName><ForeName>Aj</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Perinatal Medicine Pregnancy Research Centre, The Royal Women's Hospital and The University of Melbourne Department of Obstetrics and Gynaecology, The Royal Women's Hospital, Parkville, Victoria 3052, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kalionis</LastName><ForeName>B</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Laboratory of Tumor and Developmental Biology University of Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Goffin</LastName><ForeName>F</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Laboratory of Tumor and Developmental Biology University of Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tsatsaris</LastName><ForeName>V</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Department of Obstetrics and Gynecology, Hôpital Cochin, Maternité Port-Royal, Université Rene Descartes, F-75014 Paris, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Munaut</LastName><ForeName>C</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Laboratory of Tumor and Developmental Biology University of Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feige</LastName><ForeName>Jj</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 1036, Grenoble. France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Univ. Grenoble-Alpes, 38000, Grenoble, France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Commissariat à l'Energie Atomique (CEA), iRTSV-Biology of Cancer and infection, Grenoble, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Benharouga</LastName><ForeName>M</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5249, Laboratoire de Chimie et Biologie des Métaux, Grenoble, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fournier</LastName><ForeName>T</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>INSERM, U1139, Paris, F-75006, France, Universite Paris Descartes, UMR-S1139, Sorbonne Paris Cite, Paris, F-75006, France, PremUp Foundation, Paris, F-75006, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Alfaidy</LastName><ForeName>N</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 1036, Grenoble. France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Univ. Grenoble-Alpes, 38000, Grenoble, France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Commissariat à l'Energie Atomique (CEA), iRTSV-Biology of Cancer and infection, Grenoble, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2015</Year><Month>07</Month><Day>21</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Mol Med</MedlineTA><NlmUniqueID>9501023</NlmUniqueID><ISSNLinking>1076-1551</ISSNLinking></MedlineJournalInfo><CommentsCorrectionsList><CommentsCorrections RefType="Cites"><RefSource>Placenta. 2011 Oct;32(10):745-51</RefSource><PMID Version="1">21802725</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Semin Fetal Neonatal Med. 2004 Oct;9(5):395-401</RefSource><PMID 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