Transcriptome analysis of the response to thyroid hormone in Xenopus neural stem and progenitor cells

Background The thyroid hormones—thyroxine (T4) and 3,5,3′triiodothyronine (T3)—regulate the development of the central nervous system (CNS) in vertebrates by acting in different cell types. Although several T3 target genes have been identified in the brain, the changes in the transcriptome in respon...

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Veröffentlicht in:Developmental dynamics 2023-02, Vol.252 (2), p.294-304
Hauptverfasser: Cordero‐Véliz, Camila, Larraín, Juan, Faunes, Fernando
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Larraín, Juan
Faunes, Fernando
description Background The thyroid hormones—thyroxine (T4) and 3,5,3′triiodothyronine (T3)—regulate the development of the central nervous system (CNS) in vertebrates by acting in different cell types. Although several T3 target genes have been identified in the brain, the changes in the transcriptome in response to T3 specifically in neural stem and progenitor cells (NSPCs) during the early steps of NSPCs activation and neurogenesis have not been studied in vivo. Here, we characterized the transcriptome of FACS‐sorted NSPCs in response to T3 during Xenopus laevis metamorphosis. Results We identified 1252 upregulated and 726 downregulated genes after 16 hours of T3 exposure. Gene ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that T3‐upregulated genes were significantly enriched in rRNA processing and maturation, protein folding, ribosome biogenesis, translation, mitochondrial function, and proteasome. These results suggest that NSPCs activation induced by T3 is characterized by an early proteome remodeling through the synthesis of the translation machinery and the degradation of proteins by the proteasome. Conclusion This work provides new insights into the dynamics of activation of NPSCs in vivo in response to T3 during a critical period of neurogenesis in the metamorphosis. Key Findings We characterized the transcriptome of Xenopus neural stem and progenitor cells (NSPCs) in response to 16 hours of T3 exposure. T3‐upregulated genes were significantly enriched in ribosome biogenesis, proteasome and mitochondrial function. Our results reveal new insights into the early dynamics of NSPCs activation during neurogenesis.
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Although several T3 target genes have been identified in the brain, the changes in the transcriptome in response to T3 specifically in neural stem and progenitor cells (NSPCs) during the early steps of NSPCs activation and neurogenesis have not been studied in vivo. Here, we characterized the transcriptome of FACS‐sorted NSPCs in response to T3 during Xenopus laevis metamorphosis. Results We identified 1252 upregulated and 726 downregulated genes after 16 hours of T3 exposure. Gene ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that T3‐upregulated genes were significantly enriched in rRNA processing and maturation, protein folding, ribosome biogenesis, translation, mitochondrial function, and proteasome. These results suggest that NSPCs activation induced by T3 is characterized by an early proteome remodeling through the synthesis of the translation machinery and the degradation of proteins by the proteasome. Conclusion This work provides new insights into the dynamics of activation of NPSCs in vivo in response to T3 during a critical period of neurogenesis in the metamorphosis. Key Findings We characterized the transcriptome of Xenopus neural stem and progenitor cells (NSPCs) in response to 16 hours of T3 exposure. T3‐upregulated genes were significantly enriched in ribosome biogenesis, proteasome and mitochondrial function. Our results reveal new insights into the early dynamics of NSPCs activation during neurogenesis.</description><identifier>ISSN: 1058-8388</identifier><identifier>EISSN: 1097-0177</identifier><identifier>DOI: 10.1002/dvdy.535</identifier><identifier>PMID: 36065982</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley &amp; Sons, Inc</publisher><subject>Animals ; Cells (biology) ; Central nervous system ; Critical period ; Encyclopedias ; Flow cytometry ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; Genes ; Genomes ; Hormones ; Metamorphosis ; Metamorphosis, Biological - genetics ; Mitochondria ; neural stem and progenitor cells ; Neural stem cells ; Neural Stem Cells - metabolism ; Neurogenesis ; Progenitor cells ; proteasome ; Proteasome Endopeptidase Complex - genetics ; Proteasomes ; Protein folding ; Proteins ; Proteomes ; ribosome biogenesis ; RNA processing ; rRNA ; Thyroid gland ; thyroid hormone ; Thyroid hormones ; Thyroid Hormones - metabolism ; Thyroxine ; Transcriptomes ; Translation ; Triiodothyronine ; Vertebrates ; Xenopus laevis</subject><ispartof>Developmental dynamics, 2023-02, Vol.252 (2), p.294-304</ispartof><rights>2022 American Association for Anatomy.</rights><rights>2023 American Association for Anatomy</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c2795-e4fada3321fabac62b494f5cd6962e0de5f1648ac1e70f02f6fbd099f87a77893</citedby><cites>FETCH-LOGICAL-c2795-e4fada3321fabac62b494f5cd6962e0de5f1648ac1e70f02f6fbd099f87a77893</cites><orcidid>0000-0003-2657-2552</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fdvdy.535$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fdvdy.535$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36065982$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cordero‐Véliz, Camila</creatorcontrib><creatorcontrib>Larraín, Juan</creatorcontrib><creatorcontrib>Faunes, Fernando</creatorcontrib><title>Transcriptome analysis of the response to thyroid hormone in Xenopus neural stem and progenitor cells</title><title>Developmental dynamics</title><addtitle>Dev Dyn</addtitle><description>Background The thyroid hormones—thyroxine (T4) and 3,5,3′triiodothyronine (T3)—regulate the development of the central nervous system (CNS) in vertebrates by acting in different cell types. Although several T3 target genes have been identified in the brain, the changes in the transcriptome in response to T3 specifically in neural stem and progenitor cells (NSPCs) during the early steps of NSPCs activation and neurogenesis have not been studied in vivo. Here, we characterized the transcriptome of FACS‐sorted NSPCs in response to T3 during Xenopus laevis metamorphosis. Results We identified 1252 upregulated and 726 downregulated genes after 16 hours of T3 exposure. Gene ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that T3‐upregulated genes were significantly enriched in rRNA processing and maturation, protein folding, ribosome biogenesis, translation, mitochondrial function, and proteasome. These results suggest that NSPCs activation induced by T3 is characterized by an early proteome remodeling through the synthesis of the translation machinery and the degradation of proteins by the proteasome. Conclusion This work provides new insights into the dynamics of activation of NPSCs in vivo in response to T3 during a critical period of neurogenesis in the metamorphosis. Key Findings We characterized the transcriptome of Xenopus neural stem and progenitor cells (NSPCs) in response to 16 hours of T3 exposure. T3‐upregulated genes were significantly enriched in ribosome biogenesis, proteasome and mitochondrial function. 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Although several T3 target genes have been identified in the brain, the changes in the transcriptome in response to T3 specifically in neural stem and progenitor cells (NSPCs) during the early steps of NSPCs activation and neurogenesis have not been studied in vivo. Here, we characterized the transcriptome of FACS‐sorted NSPCs in response to T3 during Xenopus laevis metamorphosis. Results We identified 1252 upregulated and 726 downregulated genes after 16 hours of T3 exposure. Gene ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that T3‐upregulated genes were significantly enriched in rRNA processing and maturation, protein folding, ribosome biogenesis, translation, mitochondrial function, and proteasome. These results suggest that NSPCs activation induced by T3 is characterized by an early proteome remodeling through the synthesis of the translation machinery and the degradation of proteins by the proteasome. Conclusion This work provides new insights into the dynamics of activation of NPSCs in vivo in response to T3 during a critical period of neurogenesis in the metamorphosis. Key Findings We characterized the transcriptome of Xenopus neural stem and progenitor cells (NSPCs) in response to 16 hours of T3 exposure. T3‐upregulated genes were significantly enriched in ribosome biogenesis, proteasome and mitochondrial function. Our results reveal new insights into the early dynamics of NSPCs activation during neurogenesis.</abstract><cop>Hoboken, USA</cop><pub>John Wiley &amp; Sons, Inc</pub><pmid>36065982</pmid><doi>10.1002/dvdy.535</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-2657-2552</orcidid></addata></record>
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subjects Animals
Cells (biology)
Central nervous system
Critical period
Encyclopedias
Flow cytometry
Gene Expression Profiling
Gene Expression Regulation, Developmental
Genes
Genomes
Hormones
Metamorphosis
Metamorphosis, Biological - genetics
Mitochondria
neural stem and progenitor cells
Neural stem cells
Neural Stem Cells - metabolism
Neurogenesis
Progenitor cells
proteasome
Proteasome Endopeptidase Complex - genetics
Proteasomes
Protein folding
Proteins
Proteomes
ribosome biogenesis
RNA processing
rRNA
Thyroid gland
thyroid hormone
Thyroid hormones
Thyroid Hormones - metabolism
Thyroxine
Transcriptomes
Translation
Triiodothyronine
Vertebrates
Xenopus laevis
title Transcriptome analysis of the response to thyroid hormone in Xenopus neural stem and progenitor cells
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