CITED2 is a conserved regulator of the uterine-placental interface

Establishment of the hemochorial uterine-placental interface requires exodus of trophoblast cells from the placenta and their transformative actions on the uterus, which represent processes critical for a successful pregnancy, but are poorly understood. We examined the involvement of CBP/p300-intera...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 120; no. 3; p. e2213622120
Main Authors Kuna, Marija, Dhakal, Pramod, Iqbal, Khursheed, Dominguez, Esteban M, Kent, Lindsey N, Muto, Masanaga, Moreno-Irusta, Ayelen, Kozai, Keisuke, Varberg, Kaela M, Okae, Hiroaki, Arima, Takahiro, Sucov, Henry M, Soares, Michael J
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LanguageEnglish
Published United States National Academy of Sciences 17.01.2023
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Abstract Establishment of the hemochorial uterine-placental interface requires exodus of trophoblast cells from the placenta and their transformative actions on the uterus, which represent processes critical for a successful pregnancy, but are poorly understood. We examined the involvement of CBP/p300-interacting transactivator with glutamic acid/aspartic acid-rich carboxyl-terminal domain 2 (CITED2) in rat and human trophoblast cell development. The rat and human exhibit deep hemochorial placentation. CITED2 was distinctively expressed in the junctional zone (JZ) and invasive trophoblast cells of the rat. Homozygous gene deletion resulted in placental and fetal growth restriction. Small null placentas were characterized by disruptions in the JZ, delays in intrauterine trophoblast cell invasion, and compromised plasticity. In the human placentation site, CITED2 was uniquely expressed in the extravillous trophoblast (EVT) cell column and importantly contributed to the development of the EVT cell lineage. We conclude that CITED2 is a conserved regulator of deep hemochorial placentation.
AbstractList The process of establishing the uterine–placental interface is a poorly understood tissue reengineering event that involves genetically foreign trophoblast cells breaching the immunologically secure uterus. When optimal, mother and fetus thrive, whereas failures represent the root cause of life-threatening diseases of pregnancy. CBP/p300-interacting transactivator with glutamic acid/aspartic acid-rich carboxyl-terminal domain 2 (CITED2) is a transcriptional coregulator with a conspicuous presence in trophoblast cell lineages infiltrating the uterine parenchyma. CITED2 helps coordinate the differentiation of rat and human trophoblast cells into invasive/extravillous trophoblast cells capable of transforming the uterus. These actions ensure requisite placental development and adaptations to physiological stressors. CITED2 exemplifies a conserved regulator of transcriptional events essential for establishing the uterine–placental interface. Establishment of the hemochorial uterine–placental interface requires exodus of trophoblast cells from the placenta and their transformative actions on the uterus, which represent processes critical for a successful pregnancy, but are poorly understood. We examined the involvement of CBP/p300-interacting transactivator with glutamic acid/aspartic acid-rich carboxyl-terminal domain 2 (CITED2) in rat and human trophoblast cell development. The rat and human exhibit deep hemochorial placentation. CITED2 was distinctively expressed in the junctional zone (JZ) and invasive trophoblast cells of the rat. Homozygous Cited2 gene deletion resulted in placental and fetal growth restriction. Small Cited2 null placentas were characterized by disruptions in the JZ, delays in intrauterine trophoblast cell invasion, and compromised plasticity. In the human placentation site, CITED2 was uniquely expressed in the extravillous trophoblast (EVT) cell column and importantly contributed to the development of the EVT cell lineage. We conclude that CITED2 is a conserved regulator of deep hemochorial placentation.
Establishment of the hemochorial uterine–placental interface requires exodus of trophoblast cells from the placenta and their transformative actions on the uterus, which represent processes critical for a successful pregnancy, but are poorly understood. We examined the involvement of CBP/p300-interacting transactivator with glutamic acid/aspartic acid-rich carboxyl-terminal domain 2 (CITED2) in rat and human trophoblast cell development. The rat and human exhibit deep hemochorial placentation. CITED2 was distinctively expressed in the junctional zone (JZ) and invasive trophoblast cells of the rat. Homozygous Cited2 gene deletion resulted in placental and fetal growth restriction. Small Cited2 null placentas were characterized by disruptions in the JZ, delays in intrauterine trophoblast cell invasion, and compromised plasticity. In the human placentation site, CITED2 was uniquely expressed in the extravillous trophoblast (EVT) cell column and importantly contributed to the development of the EVT cell lineage. We conclude that CITED2 is a conserved regulator of deep hemochorial placentation.
Establishment of the hemochorial uterine-placental interface requires exodus of trophoblast cells from the placenta and their transformative actions on the uterus, which represent processes critical for a successful pregnancy, but are poorly understood. We examined the involvement of CBP/p300-interacting transactivator with glutamic acid/aspartic acid-rich carboxyl-terminal domain 2 (CITED2) in rat and human trophoblast cell development. The rat and human exhibit deep hemochorial placentation. CITED2 was distinctively expressed in the junctional zone (JZ) and invasive trophoblast cells of the rat. Homozygous gene deletion resulted in placental and fetal growth restriction. Small null placentas were characterized by disruptions in the JZ, delays in intrauterine trophoblast cell invasion, and compromised plasticity. In the human placentation site, CITED2 was uniquely expressed in the extravillous trophoblast (EVT) cell column and importantly contributed to the development of the EVT cell lineage. We conclude that CITED2 is a conserved regulator of deep hemochorial placentation.
Author Dhakal, Pramod
Moreno-Irusta, Ayelen
Iqbal, Khursheed
Kuna, Marija
Muto, Masanaga
Okae, Hiroaki
Arima, Takahiro
Sucov, Henry M
Soares, Michael J
Varberg, Kaela M
Kozai, Keisuke
Dominguez, Esteban M
Kent, Lindsey N
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Copyright Copyright National Academy of Sciences Jan 17, 2023
Copyright © 2023 the Author(s). Published by PNAS. 2023
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Issue 3
Keywords stem cells
placenta
trophoblast
CITED2
pregnancy
Language English
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content type line 23
3Present address: Eurofins BioPharma, Columbia, MO 65202.
5Present address: Department of Stem Cells and Human Disease Models, Research Center for Animal Life Science, Shiga University of Medical Science, Seta, Tsukinowa-cho, Otsu 520-2192, Japan.
Edited by Thomas Spencer, University of Missouri, Columbia, MO; received August 11, 2022; accepted December 6, 2022
6Present address: Department of Obstetrics and Gynecology, University of Missouri-Kansas City School of Medicine, Kansas City, MO 64108.
4Present address: Center for Reproductive Health Sciences, Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO 63110.
1M.K. and P.D. contributed equally to this work.
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Snippet Establishment of the hemochorial uterine-placental interface requires exodus of trophoblast cells from the placenta and their transformative actions on the...
Establishment of the hemochorial uterine–placental interface requires exodus of trophoblast cells from the placenta and their transformative actions on the...
The process of establishing the uterine–placental interface is a poorly understood tissue reengineering event that involves genetically foreign trophoblast...
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StartPage e2213622120
SubjectTerms Animals
Aspartic acid
Biological Sciences
Cell lineage
CITED2 gene
Female
Fetuses
Gene deletion
Glutamic acid
Humans
Placenta
Placentation - genetics
Pregnancy
Rats
Repressor Proteins - genetics
Trans-Activators - genetics
Trophoblasts
Uterus
Title CITED2 is a conserved regulator of the uterine-placental interface
URI https://www.ncbi.nlm.nih.gov/pubmed/36626551
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https://search.proquest.com/docview/2763332307
https://pubmed.ncbi.nlm.nih.gov/PMC9934066
Volume 120
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