Notch signaling is a critical initiator of roof plate formation as revealed by the use of RNA profiling of the dorsal neural tube
Abstract Background The dorsal domain of the neural tube is an excellent model to investigate the generation of complexity during embryonic development. It is a highly dynamic and multifaceted region being first transiently populated by prospective neural crest (NC) cells that sequentially emigrate...
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| Format: | Article |
| Language: | English |
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BMC
2021-04-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-021-01014-3 |
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| author | Shai Ofek Sophie Wiszniak Sarah Kagan Markus Tondl Quenten Schwarz Chaya Kalcheim |
| author_facet | Shai Ofek Sophie Wiszniak Sarah Kagan Markus Tondl Quenten Schwarz Chaya Kalcheim |
| author_sort | Shai Ofek |
| collection | DOAJ |
| description | Abstract Background The dorsal domain of the neural tube is an excellent model to investigate the generation of complexity during embryonic development. It is a highly dynamic and multifaceted region being first transiently populated by prospective neural crest (NC) cells that sequentially emigrate to generate most of the peripheral nervous system. Subsequently, it becomes the definitive roof plate (RP) of the central nervous system. The RP, in turn, constitutes a patterning center for dorsal interneuron development. The factors underlying establishment of the definitive RP and its segregation from NC and dorsal interneurons are currently unknown. Results We performed a transcriptome analysis at trunk levels of quail embryos comparing the dorsal neural tube at premigratory NC and RP stages. This unraveled molecular heterogeneity between NC and RP stages, and within the RP itself. By implementing these genes, we asked whether Notch signaling is involved in RP development. First, we observed that Notch is active at the RP-interneuron interface. Furthermore, gain and loss of Notch function in quail and mouse embryos, respectively, revealed no effect on early NC behavior. Constitutive Notch activation caused a local downregulation of RP markers with a concomitant development of dI1 interneurons, as well as an ectopic upregulation of RP markers in the interneuron domain. Reciprocally, in mice lacking Notch activity, both the RP and dI1 interneurons failed to form and this was associated with expansion of the dI2 population. Conclusions Collectively, our results offer a new resource for defining specific cell types, and provide evidence that Notch is required to establish the definitive RP, and to determine the choice between RP and interneuron fates, but not the segregation of RP from NC. |
| first_indexed | 2024-12-14T03:11:02Z |
| format | Article |
| id | doaj.art-78c8712c7a0148929ad44274a98fb72c |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-14T03:11:02Z |
| publishDate | 2021-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-78c8712c7a0148929ad44274a98fb72c2022-12-21T23:19:16ZengBMCBMC Biology1741-70072021-04-0119112310.1186/s12915-021-01014-3Notch signaling is a critical initiator of roof plate formation as revealed by the use of RNA profiling of the dorsal neural tubeShai Ofek0Sophie Wiszniak1Sarah Kagan2Markus Tondl3Quenten Schwarz4Chaya Kalcheim5Department of Medical Neurobiology, Institute of Medical Research Israel-Canada (IMRIC) and the Edmond and Lily Safra Center for Brain Sciences (ELSC), Hebrew University of Jerusalem-Hadassah Medical SchoolCentre for Cancer Biology, University of South Australia and SA PathologyDepartment of Medical Neurobiology, Institute of Medical Research Israel-Canada (IMRIC) and the Edmond and Lily Safra Center for Brain Sciences (ELSC), Hebrew University of Jerusalem-Hadassah Medical SchoolCentre for Cancer Biology, University of South Australia and SA PathologyCentre for Cancer Biology, University of South Australia and SA PathologyDepartment of Medical Neurobiology, Institute of Medical Research Israel-Canada (IMRIC) and the Edmond and Lily Safra Center for Brain Sciences (ELSC), Hebrew University of Jerusalem-Hadassah Medical SchoolAbstract Background The dorsal domain of the neural tube is an excellent model to investigate the generation of complexity during embryonic development. It is a highly dynamic and multifaceted region being first transiently populated by prospective neural crest (NC) cells that sequentially emigrate to generate most of the peripheral nervous system. Subsequently, it becomes the definitive roof plate (RP) of the central nervous system. The RP, in turn, constitutes a patterning center for dorsal interneuron development. The factors underlying establishment of the definitive RP and its segregation from NC and dorsal interneurons are currently unknown. Results We performed a transcriptome analysis at trunk levels of quail embryos comparing the dorsal neural tube at premigratory NC and RP stages. This unraveled molecular heterogeneity between NC and RP stages, and within the RP itself. By implementing these genes, we asked whether Notch signaling is involved in RP development. First, we observed that Notch is active at the RP-interneuron interface. Furthermore, gain and loss of Notch function in quail and mouse embryos, respectively, revealed no effect on early NC behavior. Constitutive Notch activation caused a local downregulation of RP markers with a concomitant development of dI1 interneurons, as well as an ectopic upregulation of RP markers in the interneuron domain. Reciprocally, in mice lacking Notch activity, both the RP and dI1 interneurons failed to form and this was associated with expansion of the dI2 population. Conclusions Collectively, our results offer a new resource for defining specific cell types, and provide evidence that Notch is required to establish the definitive RP, and to determine the choice between RP and interneuron fates, but not the segregation of RP from NC.https://doi.org/10.1186/s12915-021-01014-3BMPQuail embryosdelta1Dorsal interneuronsFate segregationMib1 |
| spellingShingle | Shai Ofek Sophie Wiszniak Sarah Kagan Markus Tondl Quenten Schwarz Chaya Kalcheim Notch signaling is a critical initiator of roof plate formation as revealed by the use of RNA profiling of the dorsal neural tube BMC Biology BMP Quail embryos delta1 Dorsal interneurons Fate segregation Mib1 |
| title | Notch signaling is a critical initiator of roof plate formation as revealed by the use of RNA profiling of the dorsal neural tube |
| title_full | Notch signaling is a critical initiator of roof plate formation as revealed by the use of RNA profiling of the dorsal neural tube |
| title_fullStr | Notch signaling is a critical initiator of roof plate formation as revealed by the use of RNA profiling of the dorsal neural tube |
| title_full_unstemmed | Notch signaling is a critical initiator of roof plate formation as revealed by the use of RNA profiling of the dorsal neural tube |
| title_short | Notch signaling is a critical initiator of roof plate formation as revealed by the use of RNA profiling of the dorsal neural tube |
| title_sort | notch signaling is a critical initiator of roof plate formation as revealed by the use of rna profiling of the dorsal neural tube |
| topic | BMP Quail embryos delta1 Dorsal interneurons Fate segregation Mib1 |
| url | https://doi.org/10.1186/s12915-021-01014-3 |
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