Gene Regulatory Networks of Epidermal and Neural Fate Choice in a Chordate
Abstract Neurons are a highly specialized cell type only found in metazoans. They can be scattered throughout the body or grouped together, forming ganglia or nerve cords. During embryogenesis, centralized nervous systems develop from the ectoderm, which also forms the epidermis. How pluripotent ect...
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creator | Leon, Anthony Subirana, Lucie Magre, Kevin Cases, Ildefonso Tena, Juan J. Irimia, Manuel Gomez-Skarmeta, Jose Luis Escriva, Hector Bertrand, Stéphanie |
description | Abstract
Neurons are a highly specialized cell type only found in metazoans. They can be scattered throughout the body or grouped together, forming ganglia or nerve cords. During embryogenesis, centralized nervous systems develop from the ectoderm, which also forms the epidermis. How pluripotent ectodermal cells are directed toward neural or epidermal fates, and to which extent this process is shared among different animal lineages, are still open questions. Here, by using micromere explants, we were able to define in silico the putative gene regulatory networks (GRNs) underlying the first steps of the epidermis and the central nervous system formation in the cephalochordate amphioxus. We propose that although the signal triggering neural induction in amphioxus (i.e., Nodal) is different from vertebrates, the main transcription factors implicated in this process are conserved. Moreover, our data reveal that transcription factors of the neural program seem to not only activate neural genes but also to potentially have direct inputs into the epidermal GRN, suggesting that the Nodal signal might also contribute to neural fate commitment by repressing the epidermal program. Our functional data on whole embryos support this result and highlight the complex interactions among the transcription factors activated by the signaling pathways that drive ectodermal cell fate choice in chordates. |
doi_str_mv | 10.1093/molbev/msac055 |
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Neurons are a highly specialized cell type only found in metazoans. They can be scattered throughout the body or grouped together, forming ganglia or nerve cords. During embryogenesis, centralized nervous systems develop from the ectoderm, which also forms the epidermis. How pluripotent ectodermal cells are directed toward neural or epidermal fates, and to which extent this process is shared among different animal lineages, are still open questions. Here, by using micromere explants, we were able to define in silico the putative gene regulatory networks (GRNs) underlying the first steps of the epidermis and the central nervous system formation in the cephalochordate amphioxus. We propose that although the signal triggering neural induction in amphioxus (i.e., Nodal) is different from vertebrates, the main transcription factors implicated in this process are conserved. Moreover, our data reveal that transcription factors of the neural program seem to not only activate neural genes but also to potentially have direct inputs into the epidermal GRN, suggesting that the Nodal signal might also contribute to neural fate commitment by repressing the epidermal program. Our functional data on whole embryos support this result and highlight the complex interactions among the transcription factors activated by the signaling pathways that drive ectodermal cell fate choice in chordates.</description><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msac055</identifier><identifier>PMID: 35276009</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Animals ; Development Biology ; Discoveries ; DNA binding proteins ; Embryology and Organogenesis ; Embryonic development ; Epidermis - metabolism ; Gene Expression Regulation, Developmental ; Gene Regulatory Networks ; Genes ; Genetic transcription ; Lancelets ; Life Sciences ; Nervous System - metabolism ; Neurobiology ; Neurons ; Neurons and Cognition ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Molecular biology and evolution, 2022-04, Vol.39 (4)</ispartof><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. 2022</rights><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.</rights><rights>COPYRIGHT 2022 Oxford University Press</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c497t-6b24114e8f969750dc6ed9201f2b6b4911676aa428efa9b45bfde764cd442b013</citedby><cites>FETCH-LOGICAL-c497t-6b24114e8f969750dc6ed9201f2b6b4911676aa428efa9b45bfde764cd442b013</cites><orcidid>0000-0002-0689-0126 ; 0000-0002-2179-2567 ; 0000-0001-7577-5028</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9004418/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9004418/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1604,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35276009$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.sorbonne-universite.fr/hal-03643321$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Liu, Li</contributor><creatorcontrib>Leon, Anthony</creatorcontrib><creatorcontrib>Subirana, Lucie</creatorcontrib><creatorcontrib>Magre, Kevin</creatorcontrib><creatorcontrib>Cases, Ildefonso</creatorcontrib><creatorcontrib>Tena, Juan J.</creatorcontrib><creatorcontrib>Irimia, Manuel</creatorcontrib><creatorcontrib>Gomez-Skarmeta, Jose Luis</creatorcontrib><creatorcontrib>Escriva, Hector</creatorcontrib><creatorcontrib>Bertrand, Stéphanie</creatorcontrib><title>Gene Regulatory Networks of Epidermal and Neural Fate Choice in a Chordate</title><title>Molecular biology and evolution</title><addtitle>Mol Biol Evol</addtitle><description>Abstract
Neurons are a highly specialized cell type only found in metazoans. They can be scattered throughout the body or grouped together, forming ganglia or nerve cords. During embryogenesis, centralized nervous systems develop from the ectoderm, which also forms the epidermis. How pluripotent ectodermal cells are directed toward neural or epidermal fates, and to which extent this process is shared among different animal lineages, are still open questions. Here, by using micromere explants, we were able to define in silico the putative gene regulatory networks (GRNs) underlying the first steps of the epidermis and the central nervous system formation in the cephalochordate amphioxus. We propose that although the signal triggering neural induction in amphioxus (i.e., Nodal) is different from vertebrates, the main transcription factors implicated in this process are conserved. Moreover, our data reveal that transcription factors of the neural program seem to not only activate neural genes but also to potentially have direct inputs into the epidermal GRN, suggesting that the Nodal signal might also contribute to neural fate commitment by repressing the epidermal program. Our functional data on whole embryos support this result and highlight the complex interactions among the transcription factors activated by the signaling pathways that drive ectodermal cell fate choice in chordates.</description><subject>Animals</subject><subject>Development Biology</subject><subject>Discoveries</subject><subject>DNA binding proteins</subject><subject>Embryology and Organogenesis</subject><subject>Embryonic development</subject><subject>Epidermis - metabolism</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Genetic transcription</subject><subject>Lancelets</subject><subject>Life Sciences</subject><subject>Nervous System - metabolism</subject><subject>Neurobiology</subject><subject>Neurons</subject><subject>Neurons and Cognition</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>0737-4038</issn><issn>1537-1719</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNqFUU1vEzEQtRCIpoUrR7RHekjrr7XXF6Qo6gcoolIFZ8trjxPD7jrYu0H99zhK2gIX5INHb968N6OH0DuCLwhW7LKPXQu7yz4bi-v6BZqRmsk5kUS9RDMsS80xa07Qac7fMSacC_EanbCaSoGxmqHPNzBAdQ_rqTNjTA_VFxh_xfQjV9FXV9vgIPWmq8zgSmdKpbw2I1TLTQwWqjBUZl8nV8A36JU3XYa3x_8Mfbu--rq8na_ubj4tF6u55UqOc9FSTgiHxiuhZI2dFeAUxcTTVrRcESKkMIbTBrxRLa9b70AKbh3ntMWEnaGPB93t1PbgLAxj2UtvU-hNetDRBP13ZwgbvY47rTDmnDRF4PwgsPln7Hax0nsMM8EZo2S3N_twNEvx5wR51H3IFrrODBCnrKlgjaQN46JQLw7UtelAh8HH4m7Lc9AHGwfwoeALKXkjFGHyecCmmHMC_7QMwXqfrj6kq4_ploH3f17-RH-M8_myOG3_J_YbGYGv4A</recordid><startdate>20220411</startdate><enddate>20220411</enddate><creator>Leon, Anthony</creator><creator>Subirana, Lucie</creator><creator>Magre, Kevin</creator><creator>Cases, Ildefonso</creator><creator>Tena, Juan J.</creator><creator>Irimia, Manuel</creator><creator>Gomez-Skarmeta, Jose Luis</creator><creator>Escriva, Hector</creator><creator>Bertrand, Stéphanie</creator><general>Oxford University Press</general><general>Oxford University Press (OUP)</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0689-0126</orcidid><orcidid>https://orcid.org/0000-0002-2179-2567</orcidid><orcidid>https://orcid.org/0000-0001-7577-5028</orcidid></search><sort><creationdate>20220411</creationdate><title>Gene Regulatory Networks of Epidermal and Neural Fate Choice in a Chordate</title><author>Leon, Anthony ; Subirana, Lucie ; Magre, Kevin ; Cases, Ildefonso ; Tena, Juan J. ; Irimia, Manuel ; Gomez-Skarmeta, Jose Luis ; Escriva, Hector ; Bertrand, Stéphanie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c497t-6b24114e8f969750dc6ed9201f2b6b4911676aa428efa9b45bfde764cd442b013</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Development Biology</topic><topic>Discoveries</topic><topic>DNA binding proteins</topic><topic>Embryology and Organogenesis</topic><topic>Embryonic development</topic><topic>Epidermis - metabolism</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Regulatory Networks</topic><topic>Genes</topic><topic>Genetic transcription</topic><topic>Lancelets</topic><topic>Life Sciences</topic><topic>Nervous System - metabolism</topic><topic>Neurobiology</topic><topic>Neurons</topic><topic>Neurons and Cognition</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Leon, Anthony</creatorcontrib><creatorcontrib>Subirana, Lucie</creatorcontrib><creatorcontrib>Magre, Kevin</creatorcontrib><creatorcontrib>Cases, Ildefonso</creatorcontrib><creatorcontrib>Tena, Juan J.</creatorcontrib><creatorcontrib>Irimia, Manuel</creatorcontrib><creatorcontrib>Gomez-Skarmeta, Jose Luis</creatorcontrib><creatorcontrib>Escriva, Hector</creatorcontrib><creatorcontrib>Bertrand, Stéphanie</creatorcontrib><collection>Open Access: Oxford University Press Open Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Leon, Anthony</au><au>Subirana, Lucie</au><au>Magre, Kevin</au><au>Cases, Ildefonso</au><au>Tena, Juan J.</au><au>Irimia, Manuel</au><au>Gomez-Skarmeta, Jose Luis</au><au>Escriva, Hector</au><au>Bertrand, Stéphanie</au><au>Liu, Li</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Gene Regulatory Networks of Epidermal and Neural Fate Choice in a Chordate</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2022-04-11</date><risdate>2022</risdate><volume>39</volume><issue>4</issue><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>Abstract
Neurons are a highly specialized cell type only found in metazoans. They can be scattered throughout the body or grouped together, forming ganglia or nerve cords. During embryogenesis, centralized nervous systems develop from the ectoderm, which also forms the epidermis. How pluripotent ectodermal cells are directed toward neural or epidermal fates, and to which extent this process is shared among different animal lineages, are still open questions. Here, by using micromere explants, we were able to define in silico the putative gene regulatory networks (GRNs) underlying the first steps of the epidermis and the central nervous system formation in the cephalochordate amphioxus. We propose that although the signal triggering neural induction in amphioxus (i.e., Nodal) is different from vertebrates, the main transcription factors implicated in this process are conserved. Moreover, our data reveal that transcription factors of the neural program seem to not only activate neural genes but also to potentially have direct inputs into the epidermal GRN, suggesting that the Nodal signal might also contribute to neural fate commitment by repressing the epidermal program. Our functional data on whole embryos support this result and highlight the complex interactions among the transcription factors activated by the signaling pathways that drive ectodermal cell fate choice in chordates.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>35276009</pmid><doi>10.1093/molbev/msac055</doi><orcidid>https://orcid.org/0000-0002-0689-0126</orcidid><orcidid>https://orcid.org/0000-0002-2179-2567</orcidid><orcidid>https://orcid.org/0000-0001-7577-5028</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Development Biology Discoveries DNA binding proteins Embryology and Organogenesis Embryonic development Epidermis - metabolism Gene Expression Regulation, Developmental Gene Regulatory Networks Genes Genetic transcription Lancelets Life Sciences Nervous System - metabolism Neurobiology Neurons Neurons and Cognition Transcription Factors - genetics Transcription Factors - metabolism |
title | Gene Regulatory Networks of Epidermal and Neural Fate Choice in a Chordate |
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