Neural tube-associated boundary caps are a major source of mural cells in the skin
In addition to their roles in protecting nerves and increasing conduction velocity, peripheral glia plays key functions in blood vessel development by secreting molecules governing arteries alignment and maturation with nerves. Here, we show in mice that a specific, nerve-attached cell population, d...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2023-12-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/69413 |
| _version_ | 1797356572740943872 |
|---|---|
| author | Gaspard Gerschenfeld Fanny Coulpier Aurélie Gresset Pernelle Pulh Bastien Job Thomas Topilko Julie Siegenthaler Maria Eleni Kastriti Isabelle Brunet Patrick Charnay Piotr Topilko |
| author_facet | Gaspard Gerschenfeld Fanny Coulpier Aurélie Gresset Pernelle Pulh Bastien Job Thomas Topilko Julie Siegenthaler Maria Eleni Kastriti Isabelle Brunet Patrick Charnay Piotr Topilko |
| author_sort | Gaspard Gerschenfeld |
| collection | DOAJ |
| description | In addition to their roles in protecting nerves and increasing conduction velocity, peripheral glia plays key functions in blood vessel development by secreting molecules governing arteries alignment and maturation with nerves. Here, we show in mice that a specific, nerve-attached cell population, derived from boundary caps (BCs), constitutes a major source of mural cells for the developing skin vasculature. Using Cre-based reporter cell tracing and single-cell transcriptomics, we show that BC derivatives migrate into the skin along the nerves, detach from them, and differentiate into pericytes and vascular smooth muscle cells. Genetic ablation of this population affects the organization of the skin vascular network. Our results reveal the heterogeneity and extended potential of the BC population in mice, which gives rise to mural cells, in addition to previously described neurons, Schwann cells, and melanocytes. Finally, our results suggest that mural specification of BC derivatives takes place before their migration along nerves to the mouse skin. |
| first_indexed | 2024-03-08T14:29:38Z |
| format | Article |
| id | doaj.art-f791afb5a092412fabba20cf586ad994 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-08T14:29:38Z |
| publishDate | 2023-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-f791afb5a092412fabba20cf586ad9942024-01-12T15:07:34ZengeLife Sciences Publications LtdeLife2050-084X2023-12-011210.7554/eLife.69413Neural tube-associated boundary caps are a major source of mural cells in the skinGaspard Gerschenfeld0https://orcid.org/0000-0002-2456-704XFanny Coulpier1https://orcid.org/0009-0007-7638-3676Aurélie Gresset2Pernelle Pulh3Bastien Job4Thomas Topilko5Julie Siegenthaler6Maria Eleni Kastriti7Isabelle Brunet8https://orcid.org/0000-0002-5490-2937Patrick Charnay9Piotr Topilko10https://orcid.org/0000-0001-7381-6770Institut de Biologie de l'Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, France; Sorbonne Université, Collège Doctoral, Paris, FranceInstitut de Biologie de l'Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, France; nstitut Mondor de Recherche Biomédicale, Inserm U955-Team 9, Créteil, France; Genomic facility, Ecole normale supérieure, PSL Research University, CNRS, Inserm, Institut de Biologie de l'Ecole normale supérieure (IBENS), Paris, FranceInstitut de Biologie de l'Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, FranceInstitut de Biologie de l'Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, France; nstitut Mondor de Recherche Biomédicale, Inserm U955-Team 9, Créteil, FranceInserm US23, AMMICA, Institut Gustave Roussy, Villejuif, FranceLaboratoire de Plasticité Structurale, Sorbonne Université, ICM Institut du Cerveau et de la Moelle Epinière, Inserm U1127, CNRS UMR7225, Paris, FranceDepartment of Pediatrics Section of Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United StatesDepartment of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden; Department of Neuroimmunology, Center for Brain Research, Medical University Vienna, Vienna, AustriaInserm U1050, Centre Interdisciplinaire de Recherche en Biologie (CIRB), Collège de France, Paris, FranceInstitut de Biologie de l'Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, FranceInstitut de Biologie de l'Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, France; nstitut Mondor de Recherche Biomédicale, Inserm U955-Team 9, Créteil, FranceIn addition to their roles in protecting nerves and increasing conduction velocity, peripheral glia plays key functions in blood vessel development by secreting molecules governing arteries alignment and maturation with nerves. Here, we show in mice that a specific, nerve-attached cell population, derived from boundary caps (BCs), constitutes a major source of mural cells for the developing skin vasculature. Using Cre-based reporter cell tracing and single-cell transcriptomics, we show that BC derivatives migrate into the skin along the nerves, detach from them, and differentiate into pericytes and vascular smooth muscle cells. Genetic ablation of this population affects the organization of the skin vascular network. Our results reveal the heterogeneity and extended potential of the BC population in mice, which gives rise to mural cells, in addition to previously described neurons, Schwann cells, and melanocytes. Finally, our results suggest that mural specification of BC derivatives takes place before their migration along nerves to the mouse skin.https://elifesciences.org/articles/69413Schwann cell precursorsmural cellsboundary capsneural crestmeninges |
| spellingShingle | Gaspard Gerschenfeld Fanny Coulpier Aurélie Gresset Pernelle Pulh Bastien Job Thomas Topilko Julie Siegenthaler Maria Eleni Kastriti Isabelle Brunet Patrick Charnay Piotr Topilko Neural tube-associated boundary caps are a major source of mural cells in the skin eLife Schwann cell precursors mural cells boundary caps neural crest meninges |
| title | Neural tube-associated boundary caps are a major source of mural cells in the skin |
| title_full | Neural tube-associated boundary caps are a major source of mural cells in the skin |
| title_fullStr | Neural tube-associated boundary caps are a major source of mural cells in the skin |
| title_full_unstemmed | Neural tube-associated boundary caps are a major source of mural cells in the skin |
| title_short | Neural tube-associated boundary caps are a major source of mural cells in the skin |
| title_sort | neural tube associated boundary caps are a major source of mural cells in the skin |
| topic | Schwann cell precursors mural cells boundary caps neural crest meninges |
| url | https://elifesciences.org/articles/69413 |
| work_keys_str_mv | AT gaspardgerschenfeld neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT fannycoulpier neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT aureliegresset neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT pernellepulh neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT bastienjob neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT thomastopilko neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT juliesiegenthaler neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT mariaelenikastriti neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT isabellebrunet neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT patrickcharnay neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin AT piotrtopilko neuraltubeassociatedboundarycapsareamajorsourceofmuralcellsintheskin |