OVO-like 1 regulates progenitor cell fate in human trophoblast development
Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a specialized epithelium. This paradigm exists in human placenta, where cytotrophoblast cells either propagate or undergo a unique differentiation program: fusion into an ov...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 45; pp. E6175 - E6184 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
10.11.2015
National Acad Sciences |
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a specialized epithelium. This paradigm exists in human placenta, where cytotrophoblast cells either propagate or undergo a unique differentiation program: fusion into an overlying syncytiotrophoblast. Syncytiotrophoblast is the primary barrier regulating the exchange of nutrients and gases between maternal and fetal blood and is the principal site for synthesizing hormones vital for human pregnancy. How trophoblast cells regulate their differentiation into a syncytium is not well understood. In this study, we show that the transcription factor OVO-like 1 (OVOL1), a homolog ofDrosophilaovo, regulates the transition from progenitor to differentiated trophoblast cells. OVOL1 is expressed in human placenta and was robustly induced following stimulation of trophoblast differentiation. Disruption of OVOL1 abrogated cytotrophoblast fusion and inhibited the expression of a broad set of genes required for trophoblast cell fusion and hormonogenesis. OVOL1 was required to suppress genes that maintain cytotrophoblast cells in a progenitor state, includingMYC, ID1, TP63,andASCL2,and bound specifically to regions upstream of each of these genes. Our results reveal an important function of OVOL1 as a regulator of trophoblast progenitor cell fate during human trophoblast development. |
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| AbstractList | Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a functional epithelium. In the placenta, cytotrophoblast cells comprise this progenitor population, but the differentiation program they undertake is unlike any other in human tissues: acquisition of hormonogenesis and cell fusion to form a syncytialized (syncytio)trophoblast. Syncytiotrophoblast forms the primary epithelial barrier separating maternal and fetal tissue and performs functions vital for pregnancy. In the present study, we found that OVO-like 1 (OVOL1), a transcription factor homolog of Drosophila ovo, regulates the transition between progenitor and differentiated cytotrophoblast. It does so by repressing genes that maintain cytotrophoblast progenitor traits. This study provides insight into the role of OVOL1 in human trophoblast development.
Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a specialized epithelium. This paradigm exists in human placenta, where cytotrophoblast cells either propagate or undergo a unique differentiation program: fusion into an overlying syncytiotrophoblast. Syncytiotrophoblast is the primary barrier regulating the exchange of nutrients and gases between maternal and fetal blood and is the principal site for synthesizing hormones vital for human pregnancy. How trophoblast cells regulate their differentiation into a syncytium is not well understood. In this study, we show that the transcription factor OVO-like 1 (OVOL1), a homolog of
Drosophila
ovo, regulates the transition from progenitor to differentiated trophoblast cells. OVOL1 is expressed in human placenta and was robustly induced following stimulation of trophoblast differentiation. Disruption of OVOL1 abrogated cytotrophoblast fusion and inhibited the expression of a broad set of genes required for trophoblast cell fusion and hormonogenesis. OVOL1 was required to suppress genes that maintain cytotrophoblast cells in a progenitor state, including
MYC
,
ID1
,
TP63
, and
ASCL2
, and bound specifically to regions upstream of each of these genes. Our results reveal an important function of OVOL1 as a regulator of trophoblast progenitor cell fate during human trophoblast development. Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a specialized epithelium. This paradigm exists in human placenta, where cytotrophoblast cells either propagate or undergo a unique differentiation program: fusion into an overlying syncytiotrophoblast. Syncytiotrophoblast is the primary barrier regulating the exchange of nutrients and gases between maternal and fetal blood and is the principal site for synthesizing hormones vital for human pregnancy. How trophoblast cells regulate their differentiation into a syncytium is not well understood. In this study, we show that the transcription factor OVO-like 1 (OVOL1), a homolog of Drosophila ovo, regulates the transition from progenitor to differentiated trophoblast cells. OVOL1 is expressed in human placenta and was robustly induced following stimulation of trophoblast differentiation. Disruption of OVOL1 abrogated cytotrophoblast fusion and inhibited the expression of a broad set of genes required for trophoblast cell fusion and hormonogenesis. OVOL1 was required to suppress genes that maintain cytotrophoblast cells in a progenitor state, including MYC, ID1, TP63, and ASCL2, and bound specifically to regions upstream of each of these genes. Our results reveal an important function of OVOL1 as a regulator of trophoblast progenitor cell fate during human trophoblast development. Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a specialized epithelium. This paradigm exists in human placenta, where cytotrophoblast cells either propagate or undergo a unique differentiation program: fusion into an overlying syncytiotrophoblast. Syncytiotrophoblast is the primary barrier regulating the exchange of nutrients and gases between maternal and fetal blood and is the principal site for synthesizing hormones vital for human pregnancy. How trophoblast cells regulate their differentiation into a syncytium is not well understood. In this study, we show that the transcription factor OVO-like 1 (OVOL1), a homolog ofDrosophilaovo, regulates the transition from progenitor to differentiated trophoblast cells. OVOL1 is expressed in human placenta and was robustly induced following stimulation of trophoblast differentiation. Disruption of OVOL1 abrogated cytotrophoblast fusion and inhibited the expression of a broad set of genes required for trophoblast cell fusion and hormonogenesis. OVOL1 was required to suppress genes that maintain cytotrophoblast cells in a progenitor state, includingMYC, ID1, TP63,andASCL2,and bound specifically to regions upstream of each of these genes. Our results reveal an important function of OVOL1 as a regulator of trophoblast progenitor cell fate during human trophoblast development. |
| Author | Rumi, M. A. Karim Soares, Michael J. Mason, Clifford W. Vivian, Jay L. Renaud, Stephen J. Chakraborty, Damayanti |
| Author_xml | – sequence: 1 givenname: Stephen J. surname: Renaud fullname: Renaud, Stephen J. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 2 givenname: Damayanti surname: Chakraborty fullname: Chakraborty, Damayanti organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 3 givenname: Clifford W. surname: Mason fullname: Mason, Clifford W. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 4 givenname: M. A. Karim surname: Rumi fullname: Rumi, M. A. Karim organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 5 givenname: Jay L. surname: Vivian fullname: Vivian, Jay L. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 6 givenname: Michael J. surname: Soares fullname: Soares, Michael J. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26504231$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by R. Michael Roberts, University of Missouri-Columbia, Columbia, MO, and approved October 1, 2015 (received for review April 20, 2015) 1Present address: Department of Anatomy and Cell Biology, University of Western Ontario, London, ON, Canada N6A5C1. Author contributions: S.J.R. and M.J.S. designed research; S.J.R., D.C., and C.W.M. performed research; C.W.M., M.A.K.R., J.L.V., and M.J.S. contributed new reagents/analytic tools; S.J.R. and M.J.S. analyzed data; and S.J.R. and M.J.S. wrote the paper. |
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| Snippet | Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a specialized epithelium. This... Epithelial barrier integrity is dependent on progenitor cells that either divide to replenish themselves or differentiate into a functional epithelium. In the... |
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| SubjectTerms | Analysis of Variance Animals Base Sequence Biological Sciences Blotting, Western Cell Differentiation - physiology Cells Chromatin Immunoprecipitation DNA-Binding Proteins - metabolism Female Fluorescent Antibody Technique Gases Gene Expression Regulation, Developmental - physiology Genes Humans Immunohistochemistry In Situ Hybridization Mice Mice, Inbred C57BL Microarray Analysis Molecular Sequence Data Nutrients Placenta PNAS Plus Pregnancy Rats Rats, Sprague-Dawley Reverse Transcriptase Polymerase Chain Reaction RNA, Small Interfering - genetics Sequence Analysis, RNA Stem Cells - physiology Tissues Transcription Factors - metabolism Trophoblasts - cytology Trophoblasts - physiology |
| Title | OVO-like 1 regulates progenitor cell fate in human trophoblast development |
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