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Hauptverfasser: Bernadskaya, Yelena Y, Kuan, Ariel, Tjärnberg, Andreas, Brandenburg, Jonas, Zhang, Ping, Wiechecki, Keira, Kaplan, Nicole, Failla, Margaux, Bikou, Maria, Madilian, Oliver, Bruderer, Noah, Wang, Wei, Christiaen, Lionel
Format: Artículo científico
Sprache:en
Veröffentlicht: The EMBO journal 2025
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Online-Zugang:https://pubmed.ncbi.nlm.nih.gov/41184589/
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author Bernadskaya, Yelena Y
Kuan, Ariel
Tjärnberg, Andreas
Brandenburg, Jonas
Zhang, Ping
Wiechecki, Keira
Kaplan, Nicole
Failla, Margaux
Bikou, Maria
Madilian, Oliver
Bruderer, Noah
Wang, Wei
Christiaen, Lionel
author_facet Bernadskaya, Yelena Y
Kuan, Ariel
Tjärnberg, Andreas
Brandenburg, Jonas
Zhang, Ping
Wiechecki, Keira
Kaplan, Nicole
Failla, Margaux
Bikou, Maria
Madilian, Oliver
Bruderer, Noah
Wang, Wei
Christiaen, Lionel
Bernadskaya, Yelena Y
Kuan, Ariel
Tjärnberg, Andreas
Brandenburg, Jonas
Zhang, Ping
Wiechecki, Keira
Kaplan, Nicole
Failla, Margaux
Bikou, Maria
Madilian, Oliver
Bruderer, Noah
Wang, Wei
Christiaen, Lionel
collection PubMed - marine biology
contents Cell cycle-driven transcriptome maturation confers multilineage competence to cardiopharyngeal progenitors. Bernadskaya, Yelena Y Kuan, Ariel Tjärnberg, Andreas Brandenburg, Jonas Zhang, Ping Wiechecki, Keira Kaplan, Nicole Failla, Margaux Bikou, Maria Madilian, Oliver Bruderer, Noah Wang, Wei Christiaen, Lionel Animals Transcriptome Cell Lineage Cell Cycle Ciona intestinalis Pharynx Cell Differentiation Stem Cells T-Box Domain Proteins Gene Expression Regulation, Developmental During development, stem and progenitor cells divide and transition through multipotent states to generate the diverse cell types by undergoing defined changes in biomolecular composition, which underlie the progressive loss of potency and acquisition of lineage-specific characteristics. For example, the cardiac and pharyngeal muscle programs are jointly primed in multipotent cardiopharyngeal progenitors, and segregate in distinct daughter cells only after cell division. Here, using the tunicate Ciona, we showed that multipotent cardiopharyngeal progenitors acquire the competence to produce distinct Tbx1/10 (+) and (-) daughter cells shortly before mitosis, which is necessary for Tbx1/10 activation. By combining transgene-based sample barcoding with single-cell RNA-sequencing (scRNA-seq), we uncovered transcriptome-wide dynamics in migrating cardiopharyngeal progenitors as cells progress through G1, S, and G2 phases. We refer to this process as "transcriptome maturation", and identified candidate mature genes, including the Rho GAP-coding gene Depdc1b, which peaks in late G2. Functional assays indicated that transcriptome maturation fosters cardiopharyngeal competence, in part through multilineage priming and by enabling asymmetric cell division that influences subsequent fate decisions, illustrating the concept of "behavioral competence". We show that both classic regulatory circuits and coupling with the G1-S transition drive transcriptome maturation, ensuring the timely deployment of lineage-specific programs.
format Artículo científico
id pubmed_41184589
institution PubMed
language en
publishDate 2025
publisher The EMBO journal
record_format pubmed
spellingShingle Cell cycle-driven transcriptome maturation confers multilineage competence to cardiopharyngeal progenitors.
Bernadskaya, Yelena Y
Kuan, Ariel
Tjärnberg, Andreas
Brandenburg, Jonas
Zhang, Ping
Wiechecki, Keira
Kaplan, Nicole
Failla, Margaux
Bikou, Maria
Madilian, Oliver
Bruderer, Noah
Wang, Wei
Christiaen, Lionel
Animals
Transcriptome
Cell Lineage
Cell Cycle
Ciona intestinalis
Pharynx
Cell Differentiation
Stem Cells
T-Box Domain Proteins
Gene Expression Regulation, Developmental
Cell cycle-driven transcriptome maturation confers multilineage competence to cardiopharyngeal progenitors. Bernadskaya, Yelena Y Kuan, Ariel Tjärnberg, Andreas Brandenburg, Jonas Zhang, Ping Wiechecki, Keira Kaplan, Nicole Failla, Margaux Bikou, Maria Madilian, Oliver Bruderer, Noah Wang, Wei Christiaen, Lionel Animals Transcriptome Cell Lineage Cell Cycle Ciona intestinalis Pharynx Cell Differentiation Stem Cells T-Box Domain Proteins Gene Expression Regulation, Developmental During development, stem and progenitor cells divide and transition through multipotent states to generate the diverse cell types by undergoing defined changes in biomolecular composition, which underlie the progressive loss of potency and acquisition of lineage-specific characteristics. For example, the cardiac and pharyngeal muscle programs are jointly primed in multipotent cardiopharyngeal progenitors, and segregate in distinct daughter cells only after cell division. Here, using the tunicate Ciona, we showed that multipotent cardiopharyngeal progenitors acquire the competence to produce distinct Tbx1/10 (+) and (-) daughter cells shortly before mitosis, which is necessary for Tbx1/10 activation. By combining transgene-based sample barcoding with single-cell RNA-sequencing (scRNA-seq), we uncovered transcriptome-wide dynamics in migrating cardiopharyngeal progenitors as cells progress through G1, S, and G2 phases. We refer to this process as "transcriptome maturation", and identified candidate mature genes, including the Rho GAP-coding gene Depdc1b, which peaks in late G2. Functional assays indicated that transcriptome maturation fosters cardiopharyngeal competence, in part through multilineage priming and by enabling asymmetric cell division that influences subsequent fate decisions, illustrating the concept of "behavioral competence". We show that both classic regulatory circuits and coupling with the G1-S transition drive transcriptome maturation, ensuring the timely deployment of lineage-specific programs.
title Cell cycle-driven transcriptome maturation confers multilineage competence to cardiopharyngeal progenitors.
topic Animals
Transcriptome
Cell Lineage
Cell Cycle
Ciona intestinalis
Pharynx
Cell Differentiation
Stem Cells
T-Box Domain Proteins
Gene Expression Regulation, Developmental
url https://pubmed.ncbi.nlm.nih.gov/41184589/