Loss of placental growth factor ameliorates maternal hypertension and preeclampsia in mice

Preeclampsia remains a clinical challenge due to its poorly understood pathogenesis. A prevailing notion is that increased placental production of soluble fms-like tyrosine kinase-1 (sFlt-1) causes the maternal syndrome by inhibiting proangiogenic placental growth factor (PlGF) and VEGF. However, th...

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Published inThe Journal of clinical investigation Vol. 128; no. 11; pp. 5008 - 5017
Main Authors Parchem, Jacqueline G, Kanasaki, Keizo, Kanasaki, Megumi, Sugimoto, Hikaru, Xie, Liang, Hamano, Yuki, Lee, Soo Bong, Gattone, Vincent H, Parry, Samuel, Strauss, Jerome F, Garovic, Vesna D, McElrath, Thomas F, Lu, Karen H, Sibai, Baha M, LeBleu, Valerie S, Carmeliet, Peter, Kalluri, Raghu
Format Journal Article
LanguageEnglish
Published United States American Society for Clinical Investigation 01.11.2018
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Abstract Preeclampsia remains a clinical challenge due to its poorly understood pathogenesis. A prevailing notion is that increased placental production of soluble fms-like tyrosine kinase-1 (sFlt-1) causes the maternal syndrome by inhibiting proangiogenic placental growth factor (PlGF) and VEGF. However, the significance of PlGF suppression in preeclampsia is uncertain. To test whether preeclampsia results from the imbalance of angiogenic factors reflected by an abnormal sFlt-1/PlGF ratio, we studied PlGF KO (Pgf-/-) mice and noted that the mice did not develop signs or sequelae of preeclampsia despite a marked elevation in circulating sFLT-1. Notably, PlGF KO mice had morphologically distinct placentas, showing an accumulation of junctional zone glycogen. We next considered the role of placental PlGF in an established model of preeclampsia (pregnant catechol-O-methyltransferase-deficient [COMT-deficient] mice) by generating mice with deletions in both the Pgf and Comt genes. Deletion of placental PlGF in the context of COMT loss resulted in a reduction in maternal blood pressure and increased placental glycogen, indicating that loss of PlGF might be protective against the development of preeclampsia. These results identify a role for PlGF in placental development and support a complex model for the pathogenesis of preeclampsia beyond an angiogenic factor imbalance.
AbstractList Preeclampsia remains a clinical challenge due to its poorly understood pathogenesis. A prevailing notion is that increased placental production of soluble fms-like tyrosine kinase-1 (sFlt-1) causes the maternal syndrome by inhibiting proangiogenic placental growth factor (PlGF) and VEGF. However, the significance of PlGF suppression in preeclampsia is uncertain. To test whether preeclampsia results from the imbalance of angiogenic factors reflected by an abnormal sFlt-1/PlGF ratio, we studied PlGF KO (Pgf-/-) mice and noted that the mice did not develop signs or sequelae of preeclampsia despite a marked elevation in circulating sFLT-1. Notably, PlGF KO mice had morphologically distinct placentas, showing an accumulation of junctional zone glycogen. We next considered the role of placental PlGF in an established model of preeclampsia (pregnant catechol-O-methyltransferase-deficient [COMT-deficient] mice) by generating mice with deletions in both the Pgf and Comt genes. Deletion of placental PlGF in the context of COMT loss resulted in a reduction in maternal blood pressure and increased placental glycogen, indicating that loss of PlGF might be protective against the development of preeclampsia. These results identify a role for PlGF in placental development and support a complex model for the pathogenesis of preeclampsia beyond an angiogenic factor imbalance.
Preeclampsia remains a clinical challenge due to its poorly understood pathogenesis. A prevailing notion is that increased placental production of soluble fms-like tyrosine kinase-1 (sFlt-1) causes the maternal syndrome by inhibiting proangiogenic placental growth factor (PlGF) and VEGF. However, the significance of PlGF suppression in preeclampsia is uncertain. To test whether preeclampsia results from the imbalance of angiogenic factors reflected by an abnormal sFlt-1/PlGF ratio, we studied PlGF KO ( Pgf –/– ) mice and noted that the mice did not develop signs or sequelae of preeclampsia despite a marked elevation in circulating sFLT-1. Notably, PlGF KO mice had morphologically distinct placentas, showing an accumulation of junctional zone glycogen. We next considered the role of placental PlGF in an established model of preeclampsia (pregnant catechol-O-methyltransferase–deficient [COMT-deficient] mice) by generating mice with deletions in both the Pgf and Comt genes. Deletion of placental PlGF in the context of COMT loss resulted in a reduction in maternal blood pressure and increased placental glycogen, indicating that loss of PlGF might be protective against the development of preeclampsia. These results identify a role for PlGF in placental development and support a complex model for the pathogenesis of preeclampsia beyond an angiogenic factor imbalance.
Author Kanasaki, Megumi
Xie, Liang
Sibai, Baha M
Strauss, Jerome F
Kanasaki, Keizo
McElrath, Thomas F
LeBleu, Valerie S
Kalluri, Raghu
Garovic, Vesna D
Sugimoto, Hikaru
Gattone, Vincent H
Parchem, Jacqueline G
Hamano, Yuki
Parry, Samuel
Lee, Soo Bong
Carmeliet, Peter
Lu, Karen H
AuthorAffiliation 7 Department of Obstetrics and Gynecology, Virginia Commonwealth University School of Medicine, Richmond, Virginia, USA
5 Department of Anatomy and Cell Biology, Indiana University School of Medicine, Indianapolis, Indiana, USA
1 Department of Cancer Biology, Metastasis Research Center, University of Texas MD Anderson Cancer Center, Houston, Texas, USA
3 Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas, USA
10 Department of Gynecologic Oncology, University of Texas MD Anderson Cancer Center, Houston, Texas, USA
6 Department of Obstetrics and Gynecology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
8 Department of Internal Medicine, Mayo Clinic, Rochester, Minnesota, USA
4 Division of Matrix Biology, Department of Medicine, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts, USA
11 Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, Katholieke Universiteit (
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30179860$$D View this record in MEDLINE/PubMed
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Copyright Copyright American Society for Clinical Investigation Nov 2018
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PublicationDate_xml – month: 11
  year: 2018
  text: 2018-11-01
  day: 01
PublicationDecade 2010
PublicationPlace United States
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– name: Ann Arbor
PublicationTitle The Journal of clinical investigation
PublicationTitleAlternate J Clin Invest
PublicationYear 2018
Publisher American Society for Clinical Investigation
Publisher_xml – name: American Society for Clinical Investigation
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Snippet Preeclampsia remains a clinical challenge due to its poorly understood pathogenesis. A prevailing notion is that increased placental production of soluble...
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Aggregation Database
Index Database
StartPage 5008
SubjectTerms Angiogenesis
Animals
Biomedical research
Blood Pressure
Catechol
Catechol O-methyltransferase
Complications
Disease Models, Animal
Female
Genotype & phenotype
Glycogen
Glycogen - genetics
Glycogen - metabolism
Hypertension
Hypoxia
Ischemia
Kinases
Metabolism
Methyltransferase
Mice
Mice, Knockout
Models, Biological
Pathogenesis
Placenta
Placenta - metabolism
Placenta - pathology
Placenta Growth Factor - deficiency
Pre-eclampsia
Pre-Eclampsia - genetics
Pre-Eclampsia - metabolism
Pre-Eclampsia - pathology
Preeclampsia
Pregnancy
Protein-tyrosine kinase
Vascular endothelial growth factor
Vascular Endothelial Growth Factor Receptor-1 - genetics
Vascular Endothelial Growth Factor Receptor-1 - metabolism
Veins & arteries
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Title Loss of placental growth factor ameliorates maternal hypertension and preeclampsia in mice
URI https://www.ncbi.nlm.nih.gov/pubmed/30179860
https://www.proquest.com/docview/2133379903
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Volume 128
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