Single-Cell Expression Profiling Reveals a Dynamic State of Cardiac Precursor Cells in the Early Mouse Embryo.
In the early vertebrate embryo, cardiac progenitor/precursor cells (CPs) give rise to cardiac structures. Better understanding their biological character is critical to understand the heart development and to apply CPs for the clinical arena. However, our knowledge remains incomplete. With the use o...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2015-01-01
|
| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0140831 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850162301620977664 |
|---|---|
| author | Ioannis Kokkinopoulos Hidekazu Ishida Rie Saba Prashant Ruchaya Claudia Cabrera Monika Struebig Michael Barnes Anna Terry Masahiro Kaneko Yasunori Shintani Steven Coppen Hidetaka Shiratori Torath Ameen Charles Mein Hiroshi Hamada Ken Suzuki Kenta Yashiro |
| author_facet | Ioannis Kokkinopoulos Hidekazu Ishida Rie Saba Prashant Ruchaya Claudia Cabrera Monika Struebig Michael Barnes Anna Terry Masahiro Kaneko Yasunori Shintani Steven Coppen Hidetaka Shiratori Torath Ameen Charles Mein Hiroshi Hamada Ken Suzuki Kenta Yashiro |
| author_sort | Ioannis Kokkinopoulos |
| collection | DOAJ |
| description | In the early vertebrate embryo, cardiac progenitor/precursor cells (CPs) give rise to cardiac structures. Better understanding their biological character is critical to understand the heart development and to apply CPs for the clinical arena. However, our knowledge remains incomplete. With the use of single-cell expression profiling, we have now revealed rapid and dynamic changes in gene expression profiles of the embryonic CPs during the early phase after their segregation from the cardiac mesoderm. Progressively, the nascent mesodermal gene Mesp1 terminated, and Nkx2-5+/Tbx5+ population rapidly replaced the Tbx5low+ population as the expression of the cardiac genes Tbx5 and Nkx2-5 increased. At the Early Headfold stage, Tbx5-expressing CPs gradually showed a unique molecular signature with signs of cardiomyocyte differentiation. Lineage-tracing revealed a developmentally distinct characteristic of this population. They underwent progressive differentiation only towards the cardiomyocyte lineage corresponding to the first heart field rather than being maintained as a progenitor pool. More importantly, Tbx5 likely plays an important role in a transcriptional network to regulate the distinct character of the FHF via a positive feedback loop to activate the robust expression of Tbx5 in CPs. These data expands our knowledge on the behavior of CPs during the early phase of cardiac development, subsequently providing a platform for further study. |
| format | Article |
| id | doaj-art-68625e7bac9c4986b217e49e1b2d98f6 |
| institution | OA Journals |
| issn | 1932-6203 |
| language | English |
| publishDate | 2015-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj-art-68625e7bac9c4986b217e49e1b2d98f62025-08-20T02:22:37ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-011010e014083110.1371/journal.pone.0140831Single-Cell Expression Profiling Reveals a Dynamic State of Cardiac Precursor Cells in the Early Mouse Embryo.Ioannis KokkinopoulosHidekazu IshidaRie SabaPrashant RuchayaClaudia CabreraMonika StruebigMichael BarnesAnna TerryMasahiro KanekoYasunori ShintaniSteven CoppenHidetaka ShiratoriTorath AmeenCharles MeinHiroshi HamadaKen SuzukiKenta YashiroIn the early vertebrate embryo, cardiac progenitor/precursor cells (CPs) give rise to cardiac structures. Better understanding their biological character is critical to understand the heart development and to apply CPs for the clinical arena. However, our knowledge remains incomplete. With the use of single-cell expression profiling, we have now revealed rapid and dynamic changes in gene expression profiles of the embryonic CPs during the early phase after their segregation from the cardiac mesoderm. Progressively, the nascent mesodermal gene Mesp1 terminated, and Nkx2-5+/Tbx5+ population rapidly replaced the Tbx5low+ population as the expression of the cardiac genes Tbx5 and Nkx2-5 increased. At the Early Headfold stage, Tbx5-expressing CPs gradually showed a unique molecular signature with signs of cardiomyocyte differentiation. Lineage-tracing revealed a developmentally distinct characteristic of this population. They underwent progressive differentiation only towards the cardiomyocyte lineage corresponding to the first heart field rather than being maintained as a progenitor pool. More importantly, Tbx5 likely plays an important role in a transcriptional network to regulate the distinct character of the FHF via a positive feedback loop to activate the robust expression of Tbx5 in CPs. These data expands our knowledge on the behavior of CPs during the early phase of cardiac development, subsequently providing a platform for further study.https://doi.org/10.1371/journal.pone.0140831 |
| spellingShingle | Ioannis Kokkinopoulos Hidekazu Ishida Rie Saba Prashant Ruchaya Claudia Cabrera Monika Struebig Michael Barnes Anna Terry Masahiro Kaneko Yasunori Shintani Steven Coppen Hidetaka Shiratori Torath Ameen Charles Mein Hiroshi Hamada Ken Suzuki Kenta Yashiro Single-Cell Expression Profiling Reveals a Dynamic State of Cardiac Precursor Cells in the Early Mouse Embryo. PLoS ONE |
| title | Single-Cell Expression Profiling Reveals a Dynamic State of Cardiac Precursor Cells in the Early Mouse Embryo. |
| title_full | Single-Cell Expression Profiling Reveals a Dynamic State of Cardiac Precursor Cells in the Early Mouse Embryo. |
| title_fullStr | Single-Cell Expression Profiling Reveals a Dynamic State of Cardiac Precursor Cells in the Early Mouse Embryo. |
| title_full_unstemmed | Single-Cell Expression Profiling Reveals a Dynamic State of Cardiac Precursor Cells in the Early Mouse Embryo. |
| title_short | Single-Cell Expression Profiling Reveals a Dynamic State of Cardiac Precursor Cells in the Early Mouse Embryo. |
| title_sort | single cell expression profiling reveals a dynamic state of cardiac precursor cells in the early mouse embryo |
| url | https://doi.org/10.1371/journal.pone.0140831 |
| work_keys_str_mv | AT ioanniskokkinopoulos singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT hidekazuishida singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT riesaba singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT prashantruchaya singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT claudiacabrera singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT monikastruebig singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT michaelbarnes singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT annaterry singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT masahirokaneko singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT yasunorishintani singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT stevencoppen singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT hidetakashiratori singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT torathameen singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT charlesmein singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT hiroshihamada singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT kensuzuki singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo AT kentayashiro singlecellexpressionprofilingrevealsadynamicstateofcardiacprecursorcellsintheearlymouseembryo |