Lymphatic mimicry in maternal endothelial cells promotes placental spiral artery remodeling

Molecular heterogeneity of endothelial cells underlies their highly specialized functions during changing physiological conditions within diverse vascular beds. For example, placental spiral arteries (SAs) undergo remarkable remodeling to meet the ever-growing demands of the fetus - a process which...

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Published inThe Journal of clinical investigation Vol. 129; no. 11; pp. 4912 - 4921
Main Authors Pawlak, John B, Bálint, László, Lim, Lillian, Ma, Wanshu, Davis, Reema B, Benyó, Zoltán, Soares, Michael J, Oliver, Guillermo, Kahn, Mark L, Jakus, Zoltán, Caron, Kathleen M
Format Journal Article
LanguageEnglish
Published United States American Society for Clinical Investigation 01.11.2019
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Abstract Molecular heterogeneity of endothelial cells underlies their highly specialized functions during changing physiological conditions within diverse vascular beds. For example, placental spiral arteries (SAs) undergo remarkable remodeling to meet the ever-growing demands of the fetus - a process which is deficient in preeclampsia. The extent to which maternal endothelial cells coordinate with immune cells and pregnancy hormones to promote SA remodeling remains largely unknown. Here we found that remodeled SAs expressed the lymphatic markers PROX1, LYVE1, and VEGFR3, mimicking lymphatic identity. Uterine natural killer (uNK) cells, which are required for SA remodeling and secrete VEGFC, were both sufficient and necessary for VEGFR3 activation in vitro and in mice lacking uNK cells, respectively. Using Flt4Chy/+ mice with kinase inactive VEGFR3 and Vegfcfl/fl Vav1-Cre mice, we demonstrated that SA remodeling required VEGFR3 signaling, and that disrupted maternal VEGFR3 signaling contributed to late-gestation fetal growth restriction. Collectively, we identified a novel instance of lymphatic mimicry by which maternal endothelial cells promote SA remodeling, furthering our understanding of the vascular heterogeneity employed for the mitigation of pregnancy complications such as fetal growth restriction and preeclampsia.
AbstractList Molecular heterogeneity of endothelial cells underlies their highly specialized functions during changing physiological conditions within diverse vascular beds. For example, placental spiral arteries (SAs) undergo remarkable remodeling to meet the ever-growing demands of the fetus--a process which is deficient in preeclampsia. The extent to which maternal endothelial cells coordinate with immune cells and pregnancy hormones to promote SA remodeling remains largely unknown. Here we found that remodeled SAs expressed the lymphatic markers PROX1, LYVE1, and VEGFR3, mimicking lymphatic identity. Uterine natural killer (uNK) cells, which are required for SA remodeling and secrete VEGFC, were both sufficient and necessary for VEGFR3 activation in vitro and in mice lacking uNK cells, respectively. Using [Flt4.sup.Chy/+] mice with kinase inactive VEGFR3 and [Vegfc.sup.fl/fl] Vav1-Cre mice, we demonstrated that SA remodeling required VEGFR3 signaling, and that disrupted maternal VEGFR3 signaling contributed to late-gestation fetal growth restriction. Collectively, we identified a novel instance of lymphatic mimicry by which maternal endothelial cells promote SA remodeling, furthering our understanding of the vascular heterogeneity employed for the mitigation of pregnancy complications such as fetal growth restriction and preeclampsia.
Molecular heterogeneity of endothelial cells underlies their highly specialized functions during changing physiological conditions within diverse vascular beds. For example, placental spiral arteries (SAs) undergo remarkable remodeling to meet the ever-growing demands of the fetus - a process which is deficient in preeclampsia. The extent to which maternal endothelial cells coordinate with immune cells and pregnancy hormones to promote SA remodeling remains largely unknown. Here we found that remodeled SAs expressed the lymphatic markers PROX1, LYVE1, and VEGFR3, mimicking lymphatic identity. Uterine natural killer (uNK) cells, which are required for SA remodeling and secrete VEGFC, were both sufficient and necessary for VEGFR3 activation in vitro and in mice lacking uNK cells, respectively. Using Flt4Chy/+ mice with kinase inactive VEGFR3 and Vegfcfl/fl Vav1-Cre mice, we demonstrated that SA remodeling required VEGFR3 signaling, and that disrupted maternal VEGFR3 signaling contributed to late-gestation fetal growth restriction. Collectively, we identified a novel instance of lymphatic mimicry by which maternal endothelial cells promote SA remodeling, furthering our understanding of the vascular heterogeneity employed for the mitigation of pregnancy complications such as fetal growth restriction and preeclampsia.
Molecular heterogeneity of endothelial cells underlies their highly specialized functions during changing physiological conditions within diverse vascular beds. For example, placental spiral arteries (SAs) undergo remarkable remodeling to meet the ever-growing demands of the fetus — a process which is deficient in preeclampsia. The extent to which maternal endothelial cells coordinate with immune cells and pregnancy hormones to promote SA remodeling remains largely unknown. Here we found that remodeled SAs expressed the lymphatic markers PROX1, LYVE1, and VEGFR3, mimicking lymphatic identity. Uterine natural killer (uNK) cells, which are required for SA remodeling and secrete VEGFC, were both sufficient and necessary for VEGFR3 activation in vitro and in mice lacking uNK cells, respectively. Using Flt4 Chy/+ mice with kinase inactive VEGFR3 and Vegfc fl/fl Vav1-Cre mice, we demonstrated that SA remodeling required VEGFR3 signaling, and that disrupted maternal VEGFR3 signaling contributed to late-gestation fetal growth restriction. Collectively, we identified a novel instance of lymphatic mimicry by which maternal endothelial cells promote SA remodeling, furthering our understanding of the vascular heterogeneity employed for the mitigation of pregnancy complications such as fetal growth restriction and preeclampsia.
Audience Academic
Author Pawlak, John B
Caron, Kathleen M
Bálint, László
Jakus, Zoltán
Ma, Wanshu
Kahn, Mark L
Lim, Lillian
Oliver, Guillermo
Davis, Reema B
Benyó, Zoltán
Soares, Michael J
AuthorAffiliation 7 Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USA
1 Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, North Carolina, USA
2 Department of Physiology, Semmelweis University School of Medicine, Budapest, Hungary
5 Northwestern University, Feinberg School of Medicine, Chicago, Illinois, USA
8 Center for Perinatal Research, Children’s Research Institute, Children’s Mercy, Kansas City, Missouri, USA
4 Department of Medicine and Cardiovascular Institute, University of Pennsylvania, Philadelphia, Pennsylvania, USA
6 Institute of Clinical Experimental Research, Semmelweis University, Budapest, Hungary
3 MTA-SE “Lendület” Lymphatic Physiology Research Group of the Hungarian Academy of Sciences and the Semmelweis University, Budapest, Hungary
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Snippet Molecular heterogeneity of endothelial cells underlies their highly specialized functions during changing physiological conditions within diverse vascular...
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StartPage 4912
SubjectTerms Animals
Antigens, Differentiation
Arteries
Arteries - immunology
Arteries - pathology
Biomedical research
Cancer
Cell adhesion & migration
Endothelial cells
Endothelium
Endothelium, Lymphatic - immunology
Endothelium, Lymphatic - pathology
Extracellular matrix
Female
Fetal development
Fetal Growth Retardation - immunology
Fetal Growth Retardation - pathology
Fetuses
Gestation
Hormones
Humans
Kinases
Mice
Mimicry
Molecular Mimicry
Natural killer cells
Novels
Phosphorylation
Physiological aspects
Physiology
Placenta
Placenta - blood supply
Placenta - immunology
Placenta - pathology
Pre-eclampsia
Pre-Eclampsia - immunology
Pre-Eclampsia - pathology
Preeclampsia
Pregnancy
Pregnancy complications
Smooth muscle
Sunitinib
Uterus
Uterus - blood supply
Uterus - immunology
Uterus - pathology
Vascular endothelial growth factor
Vascular endothelial growth factor receptors
Vascular Remodeling - immunology
Veins & arteries
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Title Lymphatic mimicry in maternal endothelial cells promotes placental spiral artery remodeling
URI https://www.ncbi.nlm.nih.gov/pubmed/31415243
https://www.proquest.com/docview/2313334702
https://search.proquest.com/docview/2275255871
https://pubmed.ncbi.nlm.nih.gov/PMC6819089
Volume 129
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