A distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero-posterior patterning of esophagus striated muscle

In most vertebrates, the upper digestive tract is composed of muscularized jaws linked to the esophagus that permits food ingestion and swallowing. Masticatory and esophagus striated muscles (ESM) share a common cardiopharyngeal mesoderm (CPM) origin, however ESM are unusual among striated muscles a...

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Main Authors: Glenda Comai, Eglantine Heude, Sebastian Mella, Sylvain Paisant, Francesca Pala, Mirialys Gallardo, Francina Langa, Gabrielle Kardon, Swetha Gopalakrishnan, Shahragim Tajbakhsh
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/47460
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author Glenda Comai
Eglantine Heude
Sebastian Mella
Sylvain Paisant
Francesca Pala
Mirialys Gallardo
Francina Langa
Gabrielle Kardon
Swetha Gopalakrishnan
Shahragim Tajbakhsh
author_facet Glenda Comai
Eglantine Heude
Sebastian Mella
Sylvain Paisant
Francesca Pala
Mirialys Gallardo
Francina Langa
Gabrielle Kardon
Swetha Gopalakrishnan
Shahragim Tajbakhsh
author_sort Glenda Comai
collection DOAJ
description In most vertebrates, the upper digestive tract is composed of muscularized jaws linked to the esophagus that permits food ingestion and swallowing. Masticatory and esophagus striated muscles (ESM) share a common cardiopharyngeal mesoderm (CPM) origin, however ESM are unusual among striated muscles as they are established in the absence of a primary skeletal muscle scaffold. Using mouse chimeras, we show that the transcription factors Tbx1 and Isl1 are required cell-autonomously for myogenic specification of ESM progenitors. Further, genetic loss-of-function and pharmacological studies point to MET/HGF signaling for antero-posterior migration of esophagus muscle progenitors, where Hgf ligand is expressed in adjacent smooth muscle cells. These observations highlight the functional relevance of a smooth and striated muscle progenitor dialogue for ESM patterning. Our findings establish a Tbx1-Isl1-Met genetic hierarchy that uniquely regulates esophagus myogenesis and identify distinct genetic signatures that can be used as framework to interpret pathologies arising within CPM derivatives.
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spelling doaj.art-e962c6ba7715450ba0c62e09611db8092022-12-22T03:52:59ZengeLife Sciences Publications LtdeLife2050-084X2019-09-01810.7554/eLife.47460A distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero-posterior patterning of esophagus striated muscleGlenda Comai0https://orcid.org/0000-0003-3244-3378Eglantine Heude1https://orcid.org/0000-0003-0563-9607Sebastian Mella2Sylvain Paisant3Francesca Pala4Mirialys Gallardo5Francina Langa6Gabrielle Kardon7https://orcid.org/0000-0003-2144-4463Swetha Gopalakrishnan8Shahragim Tajbakhsh9https://orcid.org/0000-0003-1809-7202Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France; CNRS UMR 3738, Paris, FranceDepartment of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France; CNRS UMR 3738, Paris, France; Department Adaptation du Vivant, CNRS/MNHN UMR 7221, Muséum national d’Histoire naturelle, Paris, FranceDepartment of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France; CNRS UMR 3738, Paris, FranceDepartment of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France; CNRS UMR 3738, Paris, FranceDepartment of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France; CNRS UMR 3738, Paris, France; Laboratory of Clinical Immunology and Microbiology (LCIM), National Institutes of Health, Bethesda, United StatesDepartment of Human Genetics, University of Utah, Salt Lake City, United StatesMouse Genetics Engineering Center, Institut Pasteur, Paris, FranceDepartment of Human Genetics, University of Utah, Salt Lake City, United StatesDepartment of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France; CNRS UMR 3738, Paris, France; Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, FinlandDepartment of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France; CNRS UMR 3738, Paris, FranceIn most vertebrates, the upper digestive tract is composed of muscularized jaws linked to the esophagus that permits food ingestion and swallowing. Masticatory and esophagus striated muscles (ESM) share a common cardiopharyngeal mesoderm (CPM) origin, however ESM are unusual among striated muscles as they are established in the absence of a primary skeletal muscle scaffold. Using mouse chimeras, we show that the transcription factors Tbx1 and Isl1 are required cell-autonomously for myogenic specification of ESM progenitors. Further, genetic loss-of-function and pharmacological studies point to MET/HGF signaling for antero-posterior migration of esophagus muscle progenitors, where Hgf ligand is expressed in adjacent smooth muscle cells. These observations highlight the functional relevance of a smooth and striated muscle progenitor dialogue for ESM patterning. Our findings establish a Tbx1-Isl1-Met genetic hierarchy that uniquely regulates esophagus myogenesis and identify distinct genetic signatures that can be used as framework to interpret pathologies arising within CPM derivatives.https://elifesciences.org/articles/47460cardiopharyngeal mesodermesophagus striated musclesTbx1-Isl1-Met/HGFmyogenic migrationantero-posterior patterning
spellingShingle Glenda Comai
Eglantine Heude
Sebastian Mella
Sylvain Paisant
Francesca Pala
Mirialys Gallardo
Francina Langa
Gabrielle Kardon
Swetha Gopalakrishnan
Shahragim Tajbakhsh
A distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero-posterior patterning of esophagus striated muscle
eLife
cardiopharyngeal mesoderm
esophagus striated muscles
Tbx1-Isl1-Met/HGF
myogenic migration
antero-posterior patterning
title A distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero-posterior patterning of esophagus striated muscle
title_full A distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero-posterior patterning of esophagus striated muscle
title_fullStr A distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero-posterior patterning of esophagus striated muscle
title_full_unstemmed A distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero-posterior patterning of esophagus striated muscle
title_short A distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero-posterior patterning of esophagus striated muscle
title_sort distinct cardiopharyngeal mesoderm genetic hierarchy establishes antero posterior patterning of esophagus striated muscle
topic cardiopharyngeal mesoderm
esophagus striated muscles
Tbx1-Isl1-Met/HGF
myogenic migration
antero-posterior patterning
url https://elifesciences.org/articles/47460
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