Trophoblast organoids as a model for maternal–fetal interactions during human placentation

The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of funct...

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Published in:Nature (London) Vol. 564; no. 7735; pp. 263 - 267
Main Authors: Turco, Margherita Y., Gardner, Lucy, Kay, Richard G., Hamilton, Russell S., Prater, Malwina, Hollinshead, Michael S., McWhinnie, Alasdair, Esposito, Laura, Fernando, Ridma, Skelton, Helen, Reimann, Frank, Gribble, Fiona M., Sharkey, Andrew, Marsh, Steven G. E., O’Rahilly, Stephen, Hemberger, Myriam, Burton, Graham J., Moffett, Ashley
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 01.12.2018
Nature Publishing Group
Subjects:
13
14
38
631/136
631/1647
Analysis
Antigens
Bioinformatics
Cell Differentiation
Cell Movement
Chorionic gonadotropin
Chorionic Gonadotropin - metabolism
Chorionic gonadotropins
Decidua
Decidua - cytology
Deoxyribonucleic acid
DNA
DNA Methylation
Epithelium
Female
Fetuses
Glycoproteins
Gonadotropins
Growth Differentiation Factor 15 - metabolism
Histocompatibility antigen HLA
HLA antigens
HLA Antigens - metabolism
Hormones
Humanities and Social Sciences
Humans
Implantation
Letter
Leukocytes
Mass spectrometry
Mass spectroscopy
Maternal-fetal exchange
Maternal-Fetal Relations
Models, Biological
multidisciplinary
Organoids
Organoids - cytology
Organoids - metabolism
Organoids - physiology
Peptides
Physiological aspects
Physiological research
Pituitary (anterior)
Placenta
Placental hormones
Placentation
Pregnancy
Pregnancy-Specific beta 1-Glycoproteins - metabolism
Principal components analysis
Science
Science (multidisciplinary)
Scientific imaging
Secretion
Spectroscopy
Stem cells
Surgical implants
Three dimensional analysis
Tissue Culture Techniques
Tissue typing
Transcriptome - genetics
Transplants & implants
Trophectoderm
Trophoblasts
Trophoblasts - cytology
Trophoblasts - metabolism
Trophoblasts - physiology
ISSN:0028-0836, 1476-4687, 1476-4687
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Abstract The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of functional experimental models 1 . After implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, proliferative villous cytotrophoblast cells differentiate into two main sub-populations: syncytiotrophoblast, the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast cells, which anchor the placenta to the maternal decidua and transform the maternal spiral arteries 2 . Here we describe the generation of long-term, genetically stable organoid cultures of trophoblast that can differentiate into both syncytiotrophoblast and extravillous trophoblast. We used human leukocyte antigen (HLA) typing to confirm that the organoids were derived from the fetus, and verified their identities against four trophoblast-specific criteria 3 . The cultures organize into villous-like structures, and we detected the secretion of placental-specific peptides and hormones, including human chorionic gonadotropin (hCG), growth differentiation factor 15 (GDF15) and pregnancy-specific glycoprotein (PSG) by mass spectrometry. The organoids also differentiate into HLA-G + extravillous trophoblast cells, which vigorously invade in three-dimensional cultures. Analysis of the methylome reveals that the organoids closely resemble normal first trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment. An in vitro system that generates three-dimensional cultures of extraembryonic fetal trophoblast cells that differentiate into the two main types of trophoblast can be used to study human placental development.
AbstractList The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of functional experimental models.sup.1. After implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, proliferative villous cytotrophoblast cells differentiate into two main sub-populations: syncytiotrophoblast, the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast cells, which anchor the placenta to the maternal decidua and transform the maternal spiral arteries.sup.2. Here we describe the generation of long-term, genetically stable organoid cultures of trophoblast that can differentiate into both syncytiotrophoblast and extravillous trophoblast. We used human leukocyte antigen (HLA) typing to confirm that the organoids were derived from the fetus, and verified their identities against four trophoblast-specific criteria.sup.3. The cultures organize into villous-like structures, and we detected the secretion of placental-specific peptides and hormones, including human chorionic gonadotropin (hCG), growth differentiation factor 15 (GDF15) and pregnancy-specific glycoprotein (PSG) by mass spectrometry. The organoids also differentiate into HLA-G.sup.+ extravillous trophoblast cells, which vigorously invade in three-dimensional cultures. Analysis of the methylome reveals that the organoids closely resemble normal first trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment.
The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of functional experimental models 1 . After implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, proliferative villous cytotrophoblast cells differentiate into two main sub-populations: syncytiotrophoblast, the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast cells, which anchor the placenta to the maternal decidua and transform the maternal spiral arteries 2 . Here we describe the generation of long-term, genetically stable organoid cultures of trophoblast that can differentiate into both syncytiotrophoblast and extravillous trophoblast. We used human leukocyte antigen (HLA) typing to confirm that the organoids were derived from the fetus, and verified their identities against four trophoblast-specific criteria 3 . The cultures organize into villous-like structures, and we detected the secretion of placental-specific peptides and hormones, including human chorionic gonadotropin (hCG), growth differentiation factor 15 (GDF15) and pregnancy-specific glycoprotein (PSG) by mass spectrometry. The organoids also differentiate into HLA-G + extravillous trophoblast cells, which vigorously invade in three-dimensional cultures. Analysis of the methylome reveals that the organoids closely resemble normal first trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment. An in vitro system that generates three-dimensional cultures of extraembryonic fetal trophoblast cells that differentiate into the two main types of trophoblast can be used to study human placental development.
The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of functional experimental models . After implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, proliferative villous cytotrophoblast cells differentiate into two main sub-populations: syncytiotrophoblast, the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast cells, which anchor the placenta to the maternal decidua and transform the maternal spiral arteries . Here we describe the generation of long-term, genetically stable organoid cultures of trophoblast that can differentiate into both syncytiotrophoblast and extravillous trophoblast. We used human leukocyte antigen (HLA) typing to confirm that the organoids were derived from the fetus, and verified their identities against four trophoblast-specific criteria . The cultures organize into villous-like structures, and we detected the secretion of placental-specific peptides and hormones, including human chorionic gonadotropin (hCG), growth differentiation factor 15 (GDF15) and pregnancy-specific glycoprotein (PSG) by mass spectrometry. The organoids also differentiate into HLA-G extravillous trophoblast cells, which vigorously invade in three-dimensional cultures. Analysis of the methylome reveals that the organoids closely resemble normal first trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment.
The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of functional experimental models.sup.1. After implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, proliferative villous cytotrophoblast cells differentiate into two main sub-populations: syncytiotrophoblast, the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast cells, which anchor the placenta to the maternal decidua and transform the maternal spiral arteries.sup.2. Here we describe the generation of long-term, genetically stable organoid cultures of trophoblast that can differentiate into both syncytiotrophoblast and extravillous trophoblast. We used human leukocyte antigen (HLA) typing to confirm that the organoids were derived from the fetus, and verified their identities against four trophoblast-specific criteria.sup.3. The cultures organize into villous-like structures, and we detected the secretion of placental-specific peptides and hormones, including human chorionic gonadotropin (hCG), growth differentiation factor 15 (GDF15) and pregnancy-specific glycoprotein (PSG) by mass spectrometry. The organoids also differentiate into HLA-G.sup.+ extravillous trophoblast cells, which vigorously invade in three-dimensional cultures. Analysis of the methylome reveals that the organoids closely resemble normal first trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment.An in vitro system that generates three-dimensional cultures of extraembryonic fetal trophoblast cells that differentiate into the two main types of trophoblast can be used to study human placental development.
The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of functional experimental models1. After implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, proliferative villous cytotrophoblast cells differentiate into two main sub-populations: syncytiotrophoblast, the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast cells, which anchor the placenta to the maternal decidua and transform the maternal spiral arteries2. Here we describe the generation of long-term, genetically stable organoid cultures of trophoblast that can differentiate into both syncytiotrophoblast and extravillous trophoblast. We used human leukocyte antigen (HLA) typing to confirm that the organoids were derived from the fetus, and verified their identities against four trophoblast-specific criteria3. The cultures organize into villouslike structures, and we detected the secretion of placental-specific peptides and hormones, including human chorionic gonadotropin (hCG), growth differentiation factor 15 (GDF15) and pregnancyspecific glycoprotein (PSG) by mass spectrometry. The organoids also differentiate into HLA-G+ extravillous trophoblast cells, which vigorously invade in three-dimensional cultures. Analysis of the methylome reveals that the organoids closely resemble normal first trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment.
The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of functional experimental models1. After implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, proliferative villous cytotrophoblast cells differentiate into two main sub-populations: syncytiotrophoblast, the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast cells, which anchor the placenta to the maternal decidua and transform the maternal spiral arteries2. Here we describe the generation of long-term, genetically stable organoid cultures of trophoblast that can differentiate into both syncytiotrophoblast and extravillous trophoblast. We used human leukocyte antigen (HLA) typing to confirm that the organoids were derived from the fetus, and verified their identities against four trophoblast-specific criteria3. The cultures organize into villous-like structures, and we detected the secretion of placental-specific peptides and hormones, including human chorionic gonadotropin (hCG), growth differentiation factor 15 (GDF15) and pregnancy-specific glycoprotein (PSG) by mass spectrometry. The organoids also differentiate into HLA-G+ extravillous trophoblast cells, which vigorously invade in three-dimensional cultures. Analysis of the methylome reveals that the organoids closely resemble normal first trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment.The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for the mother and child, our knowledge of the human placenta is limited owing to a lack of functional experimental models1. After implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, proliferative villous cytotrophoblast cells differentiate into two main sub-populations: syncytiotrophoblast, the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast cells, which anchor the placenta to the maternal decidua and transform the maternal spiral arteries2. Here we describe the generation of long-term, genetically stable organoid cultures of trophoblast that can differentiate into both syncytiotrophoblast and extravillous trophoblast. We used human leukocyte antigen (HLA) typing to confirm that the organoids were derived from the fetus, and verified their identities against four trophoblast-specific criteria3. The cultures organize into villous-like structures, and we detected the secretion of placental-specific peptides and hormones, including human chorionic gonadotropin (hCG), growth differentiation factor 15 (GDF15) and pregnancy-specific glycoprotein (PSG) by mass spectrometry. The organoids also differentiate into HLA-G+ extravillous trophoblast cells, which vigorously invade in three-dimensional cultures. Analysis of the methylome reveals that the organoids closely resemble normal first trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment.
The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of pregnancy with immediate and lifelong consequences for both mother and child, our knowledge of the human placenta is limited due to lack of functional experimental models1. Upon implantation, the trophectoderm of the blastocyst rapidly proliferates and generates the trophoblast, the unique cell type of the placenta. In vivo, the proliferative villous cytotrophoblast cells (VCT) differentiate into two main sub-populations: syncytiotrophoblast (SCT), the multinucleated epithelium of the villi responsible for nutrient exchange and hormone production, and extravillous trophoblast (EVT) that anchor the placenta to the maternal decidua and transform the maternal spiral arteries2. Here, we describe the generation of long-term, genetically-stable organoid cultures of trophoblast cells that can differentiate to SCT and EVT. We used HLA-typing to confirm the organoids are fetally-derived, and verified their identity against four trophoblast-specific criteria3. The cultures organise into villous-like structures, and we detected secretion of placental-specific peptides and hormones, including hCG, GDF15, PSGs and PAPPA, by mass spectrometry. The organoids also differentiate to HLA-G+ EVT that vigorously invade in 3D. Analysis of the methylome reveals the organoids closely resemble normal first-trimester placentas. This organoid model will be transformative for studying human placental development and for investigating trophoblast interactions with the local and systemic maternal environment.
Audience Academic
Author O’Rahilly, Stephen
Reimann, Frank
Prater, Malwina
Turco, Margherita Y.
Kay, Richard G.
Marsh, Steven G. E.
Gardner, Lucy
Hamilton, Russell S.
McWhinnie, Alasdair
Sharkey, Andrew
Hemberger, Myriam
Gribble, Fiona M.
Esposito, Laura
Burton, Graham J.
Moffett, Ashley
Skelton, Helen
Fernando, Ridma
Hollinshead, Michael S.
AuthorAffiliation 1 Department of Pathology, University of Cambridge, UK
2 Department of Physiology, Neurobiology and Development, University of Cambridge, UK
3 Centre for Trophoblast Research, University of Cambridge, UK
6 UCL Cancer Institute, Royal Free Campus, London, UK
4 Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Wellcome Trust-MRC Institute of Metabolic Science, Addenbrooke’s Hospital, Cambridge, UK
7 Epigenetics Programme, The Babraham Institute, Cambridge, UK
5 Anthony Nolan Research Institute, Royal Free Hospital, London, UK
AuthorAffiliation_xml – name: 6 UCL Cancer Institute, Royal Free Campus, London, UK
– name: 5 Anthony Nolan Research Institute, Royal Free Hospital, London, UK
– name: 2 Department of Physiology, Neurobiology and Development, University of Cambridge, UK
– name: 3 Centre for Trophoblast Research, University of Cambridge, UK
– name: 7 Epigenetics Programme, The Babraham Institute, Cambridge, UK
– name: 1 Department of Pathology, University of Cambridge, UK
– name: 4 Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Wellcome Trust-MRC Institute of Metabolic Science, Addenbrooke’s Hospital, Cambridge, UK
Author_xml – sequence: 1
  givenname: Margherita Y.
  surname: Turco
  fullname: Turco, Margherita Y.
  email: myt25@cam.ac.uk
  organization: Department of Pathology, University of Cambridge, Department of Physiology, Development and Neuroscience, University of Cambridge, Centre for Trophoblast Research, University of Cambridge
– sequence: 2
  givenname: Lucy
  surname: Gardner
  fullname: Gardner, Lucy
  organization: Department of Pathology, University of Cambridge, Centre for Trophoblast Research, University of Cambridge
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  givenname: Richard G.
  surname: Kay
  fullname: Kay, Richard G.
  organization: Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Wellcome Trust-MRC Institute of Metabolic Science, Addenbrooke’s Hospital
– sequence: 4
  givenname: Russell S.
  surname: Hamilton
  fullname: Hamilton, Russell S.
  organization: Department of Physiology, Development and Neuroscience, University of Cambridge, Centre for Trophoblast Research, University of Cambridge
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  surname: Prater
  fullname: Prater, Malwina
  organization: Department of Physiology, Development and Neuroscience, University of Cambridge, Centre for Trophoblast Research, University of Cambridge
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  surname: Hollinshead
  fullname: Hollinshead, Michael S.
  organization: Department of Pathology, University of Cambridge
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  surname: McWhinnie
  fullname: McWhinnie, Alasdair
  organization: Anthony Nolan Research Institute, Royal Free Hospital
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  surname: Esposito
  fullname: Esposito, Laura
  organization: Department of Pathology, University of Cambridge
– sequence: 9
  givenname: Ridma
  surname: Fernando
  fullname: Fernando, Ridma
  organization: Department of Physiology, Development and Neuroscience, University of Cambridge, Centre for Trophoblast Research, University of Cambridge
– sequence: 10
  givenname: Helen
  surname: Skelton
  fullname: Skelton, Helen
  organization: Department of Pathology, University of Cambridge
– sequence: 11
  givenname: Frank
  surname: Reimann
  fullname: Reimann, Frank
  organization: Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Wellcome Trust-MRC Institute of Metabolic Science, Addenbrooke’s Hospital
– sequence: 12
  givenname: Fiona M.
  surname: Gribble
  fullname: Gribble, Fiona M.
  organization: Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Wellcome Trust-MRC Institute of Metabolic Science, Addenbrooke’s Hospital
– sequence: 13
  givenname: Andrew
  surname: Sharkey
  fullname: Sharkey, Andrew
  organization: Department of Pathology, University of Cambridge, Centre for Trophoblast Research, University of Cambridge
– sequence: 14
  givenname: Steven G. E.
  surname: Marsh
  fullname: Marsh, Steven G. E.
  organization: Anthony Nolan Research Institute, Royal Free Hospital, UCL Cancer Institute, Royal Free Campus
– sequence: 15
  givenname: Stephen
  surname: O’Rahilly
  fullname: O’Rahilly, Stephen
  organization: Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Wellcome Trust-MRC Institute of Metabolic Science, Addenbrooke’s Hospital
– sequence: 16
  givenname: Myriam
  surname: Hemberger
  fullname: Hemberger, Myriam
  organization: Centre for Trophoblast Research, University of Cambridge, Epigenetics Programme, The Babraham Institute
– sequence: 17
  givenname: Graham J.
  surname: Burton
  fullname: Burton, Graham J.
  email: gjb2@cam.ac.uk
  organization: Department of Physiology, Development and Neuroscience, University of Cambridge, Centre for Trophoblast Research, University of Cambridge
– sequence: 18
  givenname: Ashley
  surname: Moffett
  fullname: Moffett, Ashley
  email: am485@cam.ac.uk
  organization: Department of Pathology, University of Cambridge, Centre for Trophoblast Research, University of Cambridge
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30487605$$D View this record in MEDLINE/PubMed
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Snippet The placenta is the extraembryonic organ that supports the fetus during intrauterine life. Although placental dysfunction results in major disorders of...
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StartPage 263
SubjectTerms 13
14
38
631/136
631/1647
Analysis
Antigens
Bioinformatics
Cell Differentiation
Cell Movement
Chorionic gonadotropin
Chorionic Gonadotropin - metabolism
Chorionic gonadotropins
Decidua
Decidua - cytology
Deoxyribonucleic acid
DNA
DNA Methylation
Epithelium
Female
Fetuses
Glycoproteins
Gonadotropins
Growth Differentiation Factor 15 - metabolism
Histocompatibility antigen HLA
HLA antigens
HLA Antigens - metabolism
Hormones
Humanities and Social Sciences
Humans
Implantation
Letter
Leukocytes
Mass spectrometry
Mass spectroscopy
Maternal-fetal exchange
Maternal-Fetal Relations
Models, Biological
multidisciplinary
Organoids
Organoids - cytology
Organoids - metabolism
Organoids - physiology
Peptides
Physiological aspects
Physiological research
Pituitary (anterior)
Placenta
Placental hormones
Placentation
Pregnancy
Pregnancy-Specific beta 1-Glycoproteins - metabolism
Principal components analysis
Science
Science (multidisciplinary)
Scientific imaging
Secretion
Spectroscopy
Stem cells
Surgical implants
Three dimensional analysis
Tissue Culture Techniques
Tissue typing
Transcriptome - genetics
Transplants & implants
Trophectoderm
Trophoblasts
Trophoblasts - cytology
Trophoblasts - metabolism
Trophoblasts - physiology
Title Trophoblast organoids as a model for maternal–fetal interactions during human placentation
URI https://link.springer.com/article/10.1038/s41586-018-0753-3
https://www.ncbi.nlm.nih.gov/pubmed/30487605
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https://pubmed.ncbi.nlm.nih.gov/PMC7220805
Volume 564
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