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Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak

The heart develops from 2 sources of mesoderm progenitors, the first and second heart field (FHF and SHF). Using a single-cell transcriptomic assay combined with genetic lineage tracing and live imaging, we find the FHF and SHF are subdivided into distinct pools of progenitors in gastrulating mouse...

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Autores principales: Ivanovitch, Kenzo, Soro-Barrio, Pablo, Chakravarty, Probir, Jones, Rebecca A., Bell, Donald M., Mousavy Gharavy, S. Neda, Stamataki, Despina, Delile, Julien, Smith, James C., Briscoe, James
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8158918/
https://www.ncbi.nlm.nih.gov/pubmed/33999917
http://dx.doi.org/10.1371/journal.pbio.3001200
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author Ivanovitch, Kenzo
Soro-Barrio, Pablo
Chakravarty, Probir
Jones, Rebecca A.
Bell, Donald M.
Mousavy Gharavy, S. Neda
Stamataki, Despina
Delile, Julien
Smith, James C.
Briscoe, James
author_facet Ivanovitch, Kenzo
Soro-Barrio, Pablo
Chakravarty, Probir
Jones, Rebecca A.
Bell, Donald M.
Mousavy Gharavy, S. Neda
Stamataki, Despina
Delile, Julien
Smith, James C.
Briscoe, James
author_sort Ivanovitch, Kenzo
collection PubMed
description The heart develops from 2 sources of mesoderm progenitors, the first and second heart field (FHF and SHF). Using a single-cell transcriptomic assay combined with genetic lineage tracing and live imaging, we find the FHF and SHF are subdivided into distinct pools of progenitors in gastrulating mouse embryos at earlier stages than previously thought. Each subpopulation has a distinct origin in the primitive streak. The first progenitors to leave the primitive streak contribute to the left ventricle, shortly after right ventricle progenitor emigrate, followed by the outflow tract and atrial progenitors. Moreover, a subset of atrial progenitors are gradually incorporated in posterior locations of the FHF. Although cells allocated to the outflow tract and atrium leave the primitive streak at a similar stage, they arise from different regions. Outflow tract cells originate from distal locations in the primitive streak while atrial progenitors are positioned more proximally. Moreover, single-cell RNA sequencing demonstrates that the primitive streak cells contributing to the ventricles have a distinct molecular signature from those forming the outflow tract and atrium. We conclude that cardiac progenitors are prepatterned within the primitive streak and this prefigures their allocation to distinct anatomical structures of the heart. Together, our data provide a new molecular and spatial map of mammalian cardiac progenitors that will support future studies of heart development, function, and disease.
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spelling pubmed-81589182021-06-09 Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak Ivanovitch, Kenzo Soro-Barrio, Pablo Chakravarty, Probir Jones, Rebecca A. Bell, Donald M. Mousavy Gharavy, S. Neda Stamataki, Despina Delile, Julien Smith, James C. Briscoe, James PLoS Biol Research Article The heart develops from 2 sources of mesoderm progenitors, the first and second heart field (FHF and SHF). Using a single-cell transcriptomic assay combined with genetic lineage tracing and live imaging, we find the FHF and SHF are subdivided into distinct pools of progenitors in gastrulating mouse embryos at earlier stages than previously thought. Each subpopulation has a distinct origin in the primitive streak. The first progenitors to leave the primitive streak contribute to the left ventricle, shortly after right ventricle progenitor emigrate, followed by the outflow tract and atrial progenitors. Moreover, a subset of atrial progenitors are gradually incorporated in posterior locations of the FHF. Although cells allocated to the outflow tract and atrium leave the primitive streak at a similar stage, they arise from different regions. Outflow tract cells originate from distal locations in the primitive streak while atrial progenitors are positioned more proximally. Moreover, single-cell RNA sequencing demonstrates that the primitive streak cells contributing to the ventricles have a distinct molecular signature from those forming the outflow tract and atrium. We conclude that cardiac progenitors are prepatterned within the primitive streak and this prefigures their allocation to distinct anatomical structures of the heart. Together, our data provide a new molecular and spatial map of mammalian cardiac progenitors that will support future studies of heart development, function, and disease. Public Library of Science 2021-05-17 /pmc/articles/PMC8158918/ /pubmed/33999917 http://dx.doi.org/10.1371/journal.pbio.3001200 Text en © 2021 Ivanovitch et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ivanovitch, Kenzo
Soro-Barrio, Pablo
Chakravarty, Probir
Jones, Rebecca A.
Bell, Donald M.
Mousavy Gharavy, S. Neda
Stamataki, Despina
Delile, Julien
Smith, James C.
Briscoe, James
Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak
title Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak
title_full Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak
title_fullStr Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak
title_full_unstemmed Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak
title_short Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak
title_sort ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8158918/
https://www.ncbi.nlm.nih.gov/pubmed/33999917
http://dx.doi.org/10.1371/journal.pbio.3001200
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