Self‐assembled human placental model from trophoblast stem cells in a dynamic organ‐on‐a‐chip system

The placental barrier plays a key role in protecting the developing fetus from xenobiotics and exchanging substances between the fetus and mother. However, the trophoblast cell lines and animal models are often inadequate to recapitulate the key architecture and functional characteristics of human p...

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Vydané v:	Cell proliferation Ročník 56; číslo 5; s. e13469 - n/a
Hlavní autori:	Cao, Rongkai, Wang, Yaqing, Liu, Jiayue, Rong, Lujuan, Qin, Jianhua
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	England John Wiley & Sons, Inc 01.05.2023 John Wiley and Sons Inc
Predmet:	Animal models Animals Biochips Biomimetics Cell culture Cell Differentiation Cell lines Chorionic gonadotropin Chorionic Gonadotropin - analysis Chorionic Gonadotropin - metabolism Chorionic Gonadotropin - pharmacology Collagen Endocrine disruptors Endothelial cells Endothelial Cells - metabolism Endothelium Epithelium External stimuli Female Fetuses Fluid flow Gene expression Glucose transport Gonadotropins Humans Microphysiological Systems Original Permeability Pituitary (anterior) Placenta Placenta - metabolism Pregnancy RNA transport Scanning electron microscopy Self-assembly Signal transduction Stem Cells Structure-function relationships Toxicants Trophoblasts - metabolism Xenobiotics
ISSN:	0960-7722, 1365-2184, 1365-2184
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Abstract	The placental barrier plays a key role in protecting the developing fetus from xenobiotics and exchanging substances between the fetus and mother. However, the trophoblast cell lines and animal models are often inadequate to recapitulate the key architecture and functional characteristics of human placental barrier. Here, we described a biomimetic placental barrier model from human trophoblast stem cells (hTSCs) in a perfused organ chip system. The placental barrier was constructed by co‐culture of hTSCs and endothelial cells on the opposite sides of a collagen‐coated membrane on chip. hTSCs can differentiate into cytotrophoblasts (CT) and syncytiotrophoblast (ST), which self‐assembled into bilayered trophoblastic epithelium with placental microvilli‐like structure under dynamic cultures. The formed placental barrier displayed dense microvilli, higher level secretion of human chorionic gonadotropin (hCG), enhanced glucose transport activity. Moreover, RNA‐seq analysis revealed upregulated ST expression and activation of trophoblast differentiation‐related signalling pathways. These results indicated the key role of fluid flow in promoting trophoblast syncytialization and placental early development. After exposure to mono‐2‐ethylhexyl phthalate, one of the endocrine disrupting chemicals, the model showed inhibited hCG production and disturbed ST formation in trophoblastic epithelium, suggesting impaired placental structure and function elicited by environmental toxicants. Collectively, the hTSCs‐derived placental model can recapitulate placenta physiology and pathological response to external stimuli in a biomimetic manner, which is useful for the study of placental biology and associated diseases. Human placental barrier is consisted of trophoblastic layer, basal lamina, and the fetal capillaries in vivo. We developed a biomimetic placental barrier‐on‐a‐chip model by self‐assembly of human trophoblast stem cells in a dynamic microenvironment, recapitulating the key architecture and functions of human placental villi.
AbstractList	The placental barrier plays a key role in protecting the developing fetus from xenobiotics and exchanging substances between the fetus and mother. However, the trophoblast cell lines and animal models are often inadequate to recapitulate the key architecture and functional characteristics of human placental barrier. Here, we described a biomimetic placental barrier model from human trophoblast stem cells (hTSCs) in a perfused organ chip system. The placental barrier was constructed by co‐culture of hTSCs and endothelial cells on the opposite sides of a collagen‐coated membrane on chip. hTSCs can differentiate into cytotrophoblasts (CT) and syncytiotrophoblast (ST), which self‐assembled into bilayered trophoblastic epithelium with placental microvilli‐like structure under dynamic cultures. The formed placental barrier displayed dense microvilli, higher level secretion of human chorionic gonadotropin (hCG), enhanced glucose transport activity. Moreover, RNA‐seq analysis revealed upregulated ST expression and activation of trophoblast differentiation‐related signalling pathways. These results indicated the key role of fluid flow in promoting trophoblast syncytialization and placental early development. After exposure to mono‐2‐ethylhexyl phthalate, one of the endocrine disrupting chemicals, the model showed inhibited hCG production and disturbed ST formation in trophoblastic epithelium, suggesting impaired placental structure and function elicited by environmental toxicants. Collectively, the hTSCs‐derived placental model can recapitulate placenta physiology and pathological response to external stimuli in a biomimetic manner, which is useful for the study of placental biology and associated diseases. Human placental barrier is consisted of trophoblastic layer, basal lamina, and the fetal capillaries in vivo. We developed a biomimetic placental barrier‐on‐a‐chip model by self‐assembly of human trophoblast stem cells in a dynamic microenvironment, recapitulating the key architecture and functions of human placental villi. The placental barrier plays a key role in protecting the developing fetus from xenobiotics and exchanging substances between the fetus and mother. However, the trophoblast cell lines and animal models are often inadequate to recapitulate the key architecture and functional characteristics of human placental barrier. Here, we described a biomimetic placental barrier model from human trophoblast stem cells (hTSCs) in a perfused organ chip system. The placental barrier was constructed by co-culture of hTSCs and endothelial cells on the opposite sides of a collagen-coated membrane on chip. hTSCs can differentiate into cytotrophoblasts (CT) and syncytiotrophoblast (ST), which self-assembled into bilayered trophoblastic epithelium with placental microvilli-like structure under dynamic cultures. The formed placental barrier displayed dense microvilli, higher level secretion of human chorionic gonadotropin (hCG), enhanced glucose transport activity. Moreover, RNA-seq analysis revealed upregulated ST expression and activation of trophoblast differentiation-related signalling pathways. These results indicated the key role of fluid flow in promoting trophoblast syncytialization and placental early development. After exposure to mono-2-ethylhexyl phthalate, one of the endocrine disrupting chemicals, the model showed inhibited hCG production and disturbed ST formation in trophoblastic epithelium, suggesting impaired placental structure and function elicited by environmental toxicants. Collectively, the hTSCs-derived placental model can recapitulate placenta physiology and pathological response to external stimuli in a biomimetic manner, which is useful for the study of placental biology and associated diseases. The placental barrier plays a key role in protecting the developing fetus from xenobiotics and exchanging substances between the fetus and mother. However, the trophoblast cell lines and animal models are often inadequate to recapitulate the key architecture and functional characteristics of human placental barrier. Here, we described a biomimetic placental barrier model from human trophoblast stem cells (hTSCs) in a perfused organ chip system. The placental barrier was constructed by co-culture of hTSCs and endothelial cells on the opposite sides of a collagen-coated membrane on chip. hTSCs can differentiate into cytotrophoblasts (CT) and syncytiotrophoblast (ST), which self-assembled into bilayered trophoblastic epithelium with placental microvilli-like structure under dynamic cultures. The formed placental barrier displayed dense microvilli, higher level secretion of human chorionic gonadotropin (hCG), enhanced glucose transport activity. Moreover, RNA-seq analysis revealed upregulated ST expression and activation of trophoblast differentiation-related signalling pathways. These results indicated the key role of fluid flow in promoting trophoblast syncytialization and placental early development. After exposure to mono-2-ethylhexyl phthalate, one of the endocrine disrupting chemicals, the model showed inhibited hCG production and disturbed ST formation in trophoblastic epithelium, suggesting impaired placental structure and function elicited by environmental toxicants. Collectively, the hTSCs-derived placental model can recapitulate placenta physiology and pathological response to external stimuli in a biomimetic manner, which is useful for the study of placental biology and associated diseases.The placental barrier plays a key role in protecting the developing fetus from xenobiotics and exchanging substances between the fetus and mother. However, the trophoblast cell lines and animal models are often inadequate to recapitulate the key architecture and functional characteristics of human placental barrier. Here, we described a biomimetic placental barrier model from human trophoblast stem cells (hTSCs) in a perfused organ chip system. The placental barrier was constructed by co-culture of hTSCs and endothelial cells on the opposite sides of a collagen-coated membrane on chip. hTSCs can differentiate into cytotrophoblasts (CT) and syncytiotrophoblast (ST), which self-assembled into bilayered trophoblastic epithelium with placental microvilli-like structure under dynamic cultures. The formed placental barrier displayed dense microvilli, higher level secretion of human chorionic gonadotropin (hCG), enhanced glucose transport activity. Moreover, RNA-seq analysis revealed upregulated ST expression and activation of trophoblast differentiation-related signalling pathways. These results indicated the key role of fluid flow in promoting trophoblast syncytialization and placental early development. After exposure to mono-2-ethylhexyl phthalate, one of the endocrine disrupting chemicals, the model showed inhibited hCG production and disturbed ST formation in trophoblastic epithelium, suggesting impaired placental structure and function elicited by environmental toxicants. Collectively, the hTSCs-derived placental model can recapitulate placenta physiology and pathological response to external stimuli in a biomimetic manner, which is useful for the study of placental biology and associated diseases. The placental barrier plays a key role in protecting the developing fetus from xenobiotics and exchanging substances between the fetus and mother. However, the trophoblast cell lines and animal models are often inadequate to recapitulate the key architecture and functional characteristics of human placental barrier. Here, we described a biomimetic placental barrier model from human trophoblast stem cells (hTSCs) in a perfused organ chip system. The placental barrier was constructed by co‐culture of hTSCs and endothelial cells on the opposite sides of a collagen‐coated membrane on chip. hTSCs can differentiate into cytotrophoblasts (CT) and syncytiotrophoblast (ST), which self‐assembled into bilayered trophoblastic epithelium with placental microvilli‐like structure under dynamic cultures. The formed placental barrier displayed dense microvilli, higher level secretion of human chorionic gonadotropin (hCG), enhanced glucose transport activity. Moreover, RNA‐seq analysis revealed upregulated ST expression and activation of trophoblast differentiation‐related signalling pathways. These results indicated the key role of fluid flow in promoting trophoblast syncytialization and placental early development. After exposure to mono‐2‐ethylhexyl phthalate, one of the endocrine disrupting chemicals, the model showed inhibited hCG production and disturbed ST formation in trophoblastic epithelium, suggesting impaired placental structure and function elicited by environmental toxicants. Collectively, the hTSCs‐derived placental model can recapitulate placenta physiology and pathological response to external stimuli in a biomimetic manner, which is useful for the study of placental biology and associated diseases. Human placental barrier is consisted of trophoblastic layer, basal lamina, and the fetal capillaries in vivo. We developed a biomimetic placental barrier‐on‐a‐chip model by self‐assembly of human trophoblast stem cells in a dynamic microenvironment, recapitulating the key architecture and functions of human placental villi.
Author	Qin, Jianhua Liu, Jiayue Wang, Yaqing Cao, Rongkai Rong, Lujuan
AuthorAffiliation	4 Suzhou Institute for Advanced Research University of Science and Technology of China Suzhou China 1 Division of Biotechnology Dalian Institute of Chemical Physics, Chinese Academy of Sciences Dalian China 3 School of Biomedical Engineering University of Science and Technology of China Hefei China 2 University of Chinese Academy of Sciences Beijing China 6 Beijing Institute for Stem Cell and Regeneration, Chinese Academy of Sciences Beijing China 5 Kunming University of Science and Technology Kunming China
AuthorAffiliation_xml	– name: 2 University of Chinese Academy of Sciences Beijing China – name: 4 Suzhou Institute for Advanced Research University of Science and Technology of China Suzhou China – name: 1 Division of Biotechnology Dalian Institute of Chemical Physics, Chinese Academy of Sciences Dalian China – name: 6 Beijing Institute for Stem Cell and Regeneration, Chinese Academy of Sciences Beijing China – name: 3 School of Biomedical Engineering University of Science and Technology of China Hefei China – name: 5 Kunming University of Science and Technology Kunming China
Author_xml	– sequence: 1 givenname: Rongkai surname: Cao fullname: Cao, Rongkai organization: University of Chinese Academy of Sciences – sequence: 2 givenname: Yaqing surname: Wang fullname: Wang, Yaqing organization: University of Science and Technology of China – sequence: 3 givenname: Jiayue surname: Liu fullname: Liu, Jiayue organization: University of Science and Technology of China – sequence: 4 givenname: Lujuan surname: Rong fullname: Rong, Lujuan organization: Kunming University of Science and Technology – sequence: 5 givenname: Jianhua orcidid: 0000-0001-5735-6436 surname: Qin fullname: Qin, Jianhua email: jhqin@dicp.ac.cn organization: Beijing Institute for Stem Cell and Regeneration, Chinese Academy of Sciences
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CitedBy_id	crossref_primary_10_1080_10408444_2023_2295349 crossref_primary_10_1016_j_jpsychores_2023_111380 crossref_primary_10_1039_D5LC00014A crossref_primary_10_1016_j_placenta_2024_02_006 crossref_primary_10_1186_s12951_024_02651_w crossref_primary_10_1111_cpr_13729 crossref_primary_10_1177_02611929251349465 crossref_primary_10_3390_ijms26062818 crossref_primary_10_1002_adhm_202301067 crossref_primary_10_1038_s41467_024_45279_y crossref_primary_10_1016_j_ecoenv_2024_117051 crossref_primary_10_1038_s42003_025_08057_0 crossref_primary_10_1016_j_mtbio_2025_102053 crossref_primary_10_1016_j_bea_2025_100172 crossref_primary_10_1038_s41598_024_61747_3 crossref_primary_10_1016_j_ebiom_2023_104780 crossref_primary_10_1016_j_mtbio_2025_102222
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Copyright	2023 The Authors. published by Beijing Institute for Stem Cell and Regenerative Medicine and John Wiley & Sons Ltd. 2023 The Authors. Cell Proliferation published by Beijing Institute for Stem Cell and Regenerative Medicine and John Wiley & Sons Ltd. 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Snippet	The placental barrier plays a key role in protecting the developing fetus from xenobiotics and exchanging substances between the fetus and mother. However, the...
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SubjectTerms	Animal models Animals Biochips Biomimetics Cell culture Cell Differentiation Cell lines Chorionic gonadotropin Chorionic Gonadotropin - analysis Chorionic Gonadotropin - metabolism Chorionic Gonadotropin - pharmacology Collagen Endocrine disruptors Endothelial cells Endothelial Cells - metabolism Endothelium Epithelium External stimuli Female Fetuses Fluid flow Gene expression Glucose transport Gonadotropins Humans Microphysiological Systems Original Permeability Pituitary (anterior) Placenta Placenta - metabolism Pregnancy RNA transport Scanning electron microscopy Self-assembly Signal transduction Stem Cells Structure-function relationships Toxicants Trophoblasts - metabolism Xenobiotics
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Title	Self‐assembled human placental model from trophoblast stem cells in a dynamic organ‐on‐a‐chip system
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