A Gene Regulatory Network Balances Neural and Mesoderm Specification during Vertebrate Trunk Development
Transcriptional networks, regulated by extracellular signals, control cell fate decisions and determine the size and composition of developing tissues. One example is the network controlling bipotent neuromesodermal progenitors (NMPs) that fuel embryo elongation by generating spinal cord and trunk m...
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| Published in | Developmental cell Vol. 41; no. 3; pp. 243 - 261.e7 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
08.05.2017
Cell Press |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1534-5807 1878-1551 1878-1551 |
| DOI | 10.1016/j.devcel.2017.04.002 |
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| Abstract | Transcriptional networks, regulated by extracellular signals, control cell fate decisions and determine the size and composition of developing tissues. One example is the network controlling bipotent neuromesodermal progenitors (NMPs) that fuel embryo elongation by generating spinal cord and trunk mesoderm tissue. Here, we use single-cell transcriptomics to identify the molecular signature of NMPs and reverse engineer the mechanism that regulates their differentiation. Together with genetic perturbations, this reveals a transcriptional network that integrates opposing retinoic acid (RA) and Wnt signals to determine the rate at which cells enter and exit the NMP state. RA, produced by newly generated mesodermal cells, provides feedback that initiates NMP generation and induces neural differentiation, thereby coordinating the production of neural and mesodermal tissue. Together, the data define a regulatory network architecture that balances the generation of different cell types from bipotential progenitors in order to facilitate orderly axis elongation.
[Display omitted]
•Single-cell RNA-seq reveals a signature of neuromesodermal progenitors•In vitro NMPs resemble and differentiate similar to their in vivo counterparts•Dual role for retinoic acid signaling in NMP induction and neural differentiation•A transcriptional network regulates neural versus mesodermal allocation
Neuromesodermal progenitors (NMPs) generate cells of the spinal cord and somites. Gouti et al. demonstrate that in vitro NMPs resemble in vivo counterparts at the single-cell level and define a regulatory network that balances the generation of neural and mesodermal tissue to facilitate orderly extension of the embryonic axis. |
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| AbstractList | Transcriptional networks, regulated by extracellular signals, control cell fate decisions and determine the size and composition of developing tissues. One example is the network controlling bipotent neuromesodermal progenitors (NMPs) that fuel embryo elongation by generating spinal cord and trunk mesoderm tissue. Here, we use single-cell transcriptomics to identify the molecular signature of NMPs and reverse engineer the mechanism that regulates their differentiation. Together with genetic perturbations, this reveals a transcriptional network that integrates opposing retinoic acid (RA) and Wnt signals to determine the rate at which cells enter and exit the NMP state. RA, produced by newly generated mesodermal cells, provides feedback that initiates NMP generation and induces neural differentiation, thereby coordinating the production of neural and mesodermal tissue. Together, the data define a regulatory network architecture that balances the generation of different cell types from bipotential progenitors in order to facilitate orderly axis elongation. Transcriptional networks, regulated by extracellular signals, control cell fate decisions and determine the size and composition of developing tissues. One example is the network controlling bipotent neuromesodermal progenitors (NMPs) that fuel embryo elongation by generating spinal cord and trunk mesoderm tissue. Here, we use single-cell transcriptomics to identify the molecular signature of NMPs and reverse engineer the mechanism that regulates their differentiation. Together with genetic perturbations, this reveals a transcriptional network that integrates opposing retinoic acid (RA) and Wnt signals to determine the rate at which cells enter and exit the NMP state. RA, produced by newly generated mesodermal cells, provides feedback that initiates NMP generation and induces neural differentiation, thereby coordinating the production of neural and mesodermal tissue. Together, the data define a regulatory network architecture that balances the generation of different cell types from bipotential progenitors in order to facilitate orderly axis elongation.Transcriptional networks, regulated by extracellular signals, control cell fate decisions and determine the size and composition of developing tissues. One example is the network controlling bipotent neuromesodermal progenitors (NMPs) that fuel embryo elongation by generating spinal cord and trunk mesoderm tissue. Here, we use single-cell transcriptomics to identify the molecular signature of NMPs and reverse engineer the mechanism that regulates their differentiation. Together with genetic perturbations, this reveals a transcriptional network that integrates opposing retinoic acid (RA) and Wnt signals to determine the rate at which cells enter and exit the NMP state. RA, produced by newly generated mesodermal cells, provides feedback that initiates NMP generation and induces neural differentiation, thereby coordinating the production of neural and mesodermal tissue. Together, the data define a regulatory network architecture that balances the generation of different cell types from bipotential progenitors in order to facilitate orderly axis elongation. Transcriptional networks, regulated by extracellular signals, control cell fate decisions and determine the size and composition of developing tissues. One example is the network controlling bipotent neuromesodermal progenitors (NMPs) that fuel embryo elongation by generating spinal cord and trunk mesoderm tissue. Here, we use single-cell transcriptomics to identify the molecular signature of NMPs and reverse engineer the mechanism that regulates their differentiation. Together with genetic perturbations, this reveals a transcriptional network that integrates opposing retinoic acid (RA) and Wnt signals to determine the rate at which cells enter and exit the NMP state. RA, produced by newly generated mesodermal cells, provides feedback that initiates NMP generation and induces neural differentiation, thereby coordinating the production of neural and mesodermal tissue. Together, the data define a regulatory network architecture that balances the generation of different cell types from bipotential progenitors in order to facilitate orderly axis elongation. • Single-cell RNA-seq reveals a signature of neuromesodermal progenitors • In vitro NMPs resemble and differentiate similar to their in vivo counterparts • Dual role for retinoic acid signaling in NMP induction and neural differentiation • A transcriptional network regulates neural versus mesodermal allocation Neuromesodermal progenitors (NMPs) generate cells of the spinal cord and somites. Gouti et al. demonstrate that in vitro NMPs resemble in vivo counterparts at the single-cell level and define a regulatory network that balances the generation of neural and mesodermal tissue to facilitate orderly extension of the embryonic axis. Transcriptional networks, regulated by extracellular signals, control cell fate decisions and determine the size and composition of developing tissues. One example is the network controlling bipotent neuromesodermal progenitors (NMPs) that fuel embryo elongation by generating spinal cord and trunk mesoderm tissue. Here, we use single-cell transcriptomics to identify the molecular signature of NMPs and reverse engineer the mechanism that regulates their differentiation. Together with genetic perturbations, this reveals a transcriptional network that integrates opposing retinoic acid (RA) and Wnt signals to determine the rate at which cells enter and exit the NMP state. RA, produced by newly generated mesodermal cells, provides feedback that initiates NMP generation and induces neural differentiation, thereby coordinating the production of neural and mesodermal tissue. Together, the data define a regulatory network architecture that balances the generation of different cell types from bipotential progenitors in order to facilitate orderly axis elongation. [Display omitted] •Single-cell RNA-seq reveals a signature of neuromesodermal progenitors•In vitro NMPs resemble and differentiate similar to their in vivo counterparts•Dual role for retinoic acid signaling in NMP induction and neural differentiation•A transcriptional network regulates neural versus mesodermal allocation Neuromesodermal progenitors (NMPs) generate cells of the spinal cord and somites. Gouti et al. demonstrate that in vitro NMPs resemble in vivo counterparts at the single-cell level and define a regulatory network that balances the generation of neural and mesodermal tissue to facilitate orderly extension of the embryonic axis. |
| Author | Huang, Yali Wymeersch, Filip J. Wilson, Valerie Delile, Julien Briscoe, James Gouti, Mina Kleinjung, Jens Stamataki, Despina |
| AuthorAffiliation | 3 Max Delbrück Center for Molecular Medicine, Robert-Rössle-Strasse 10, 13125 Berlin, Germany 2 MRC Centre for Regenerative Medicine, Institute for Stem Cell Research, School of Biological Sciences, University of Edinburgh, 5 Little France Drive, Edinburgh EH16 4UU, UK 1 The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK |
| AuthorAffiliation_xml | – name: 1 The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK – name: 2 MRC Centre for Regenerative Medicine, Institute for Stem Cell Research, School of Biological Sciences, University of Edinburgh, 5 Little France Drive, Edinburgh EH16 4UU, UK – name: 3 Max Delbrück Center for Molecular Medicine, Robert-Rössle-Strasse 10, 13125 Berlin, Germany |
| Author_xml | – sequence: 1 givenname: Mina surname: Gouti fullname: Gouti, Mina email: mina.gouti@mdc-berlin.de organization: The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK – sequence: 2 givenname: Julien surname: Delile fullname: Delile, Julien organization: The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK – sequence: 3 givenname: Despina surname: Stamataki fullname: Stamataki, Despina organization: The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK – sequence: 4 givenname: Filip J. surname: Wymeersch fullname: Wymeersch, Filip J. organization: MRC Centre for Regenerative Medicine, Institute for Stem Cell Research, School of Biological Sciences, University of Edinburgh, 5 Little France Drive, Edinburgh EH16 4UU, UK – sequence: 5 givenname: Yali surname: Huang fullname: Huang, Yali organization: MRC Centre for Regenerative Medicine, Institute for Stem Cell Research, School of Biological Sciences, University of Edinburgh, 5 Little France Drive, Edinburgh EH16 4UU, UK – sequence: 6 givenname: Jens surname: Kleinjung fullname: Kleinjung, Jens organization: The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK – sequence: 7 givenname: Valerie surname: Wilson fullname: Wilson, Valerie organization: MRC Centre for Regenerative Medicine, Institute for Stem Cell Research, School of Biological Sciences, University of Edinburgh, 5 Little France Drive, Edinburgh EH16 4UU, UK – sequence: 8 givenname: James surname: Briscoe fullname: Briscoe, James email: james.briscoe@crick.ac.uk organization: The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28457792$$D View this record in MEDLINE/PubMed |
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| Keywords | single-cell transcriptome analysis retinoic acid gene regulatory networks neuromesodermal progenitors NMPs vertebrate development dynamical systems modeling |
| Language | English |
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| OpenAccessLink | https://www.sciencedirect.com/science/article/pii/S1534580717302952 |
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| PublicationDate | 2017-05-08 |
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| PublicationPlace | United States |
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| PublicationTitle | Developmental cell |
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| PublicationYear | 2017 |
| Publisher | Elsevier Inc Cell Press |
| Publisher_xml | – name: Elsevier Inc – name: Cell Press |
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| SubjectTerms | Animals Body Patterning - physiology Cell Differentiation - physiology Cell Lineage - physiology dynamical systems modeling Gene Expression Regulation, Developmental - physiology gene regulatory networks Gene Regulatory Networks - physiology Mesoderm - metabolism neuromesodermal progenitors NMPs retinoic acid single-cell transcriptome analysis Spinal Cord - cytology vertebrate development Vertebrates - embryology Wnt Signaling Pathway - physiology |
| Title | A Gene Regulatory Network Balances Neural and Mesoderm Specification during Vertebrate Trunk Development |
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