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...

Full description

Saved in:
Bibliographic Details
Main Authors: Kenzo Ivanovitch, Pablo Soro-Barrio, Probir Chakravarty, Rebecca A Jones, Donald M Bell, S Neda Mousavy Gharavy, Despina Stamataki, Julien Delile, James C Smith, James Briscoe
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-05-01
Series:PLoS Biology
Online Access:https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001200&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850129729514897408
author Kenzo Ivanovitch
Pablo Soro-Barrio
Probir Chakravarty
Rebecca A Jones
Donald M Bell
S Neda Mousavy Gharavy
Despina Stamataki
Julien Delile
James C Smith
James Briscoe
author_facet Kenzo Ivanovitch
Pablo Soro-Barrio
Probir Chakravarty
Rebecca A Jones
Donald M Bell
S Neda Mousavy Gharavy
Despina Stamataki
Julien Delile
James C Smith
James Briscoe
author_sort Kenzo Ivanovitch
collection DOAJ
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.
format Article
id doaj-art-a5429e0ee4a848d2b0cec818d86e57c3
institution OA Journals
issn 1544-9173
1545-7885
language English
publishDate 2021-05-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj-art-a5429e0ee4a848d2b0cec818d86e57c32025-08-20T02:32:53ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852021-05-01195e300120010.1371/journal.pbio.3001200Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak.Kenzo IvanovitchPablo Soro-BarrioProbir ChakravartyRebecca A JonesDonald M BellS Neda Mousavy GharavyDespina StamatakiJulien DelileJames C SmithJames BriscoeThe 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.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001200&type=printable
spellingShingle Kenzo Ivanovitch
Pablo Soro-Barrio
Probir Chakravarty
Rebecca A Jones
Donald M Bell
S Neda Mousavy Gharavy
Despina Stamataki
Julien Delile
James C Smith
James Briscoe
Ventricular, atrial, and outflow tract heart progenitors arise from spatially and molecularly distinct regions of the primitive streak.
PLoS Biology
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
url https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001200&type=printable
work_keys_str_mv AT kenzoivanovitch ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT pablosorobarrio ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT probirchakravarty ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT rebeccaajones ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT donaldmbell ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT snedamousavygharavy ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT despinastamataki ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT juliendelile ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT jamescsmith ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak
AT jamesbriscoe ventricularatrialandoutflowtractheartprogenitorsarisefromspatiallyandmolecularlydistinctregionsoftheprimitivestreak