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A genome-wide assessment of the ancestral neural crest gene regulatory network

Hockman, Dorit and Chong-Morrison, Vanessa and Green, Stephen A. and Gavriouchkina, Daria and Candido-Ferreira, Ivan and Ling, Irving T. C. and Williams, Ruth M. and Amemiya, Chris T. and Smith, Jeramiah J. and Bronner, Marianne E. and Sauka-Spengler, Tatjana (2019) A genome-wide assessment of the ancestral neural crest gene regulatory network. Nature Communications, 10 . Art. No. 4689. ISSN 2041-1723. PMCID PMC6795873. https://resolver.caltech.edu/CaltechAUTHORS:20181026-140937942

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Abstract

The neural crest is an embryonic cell population that contributes to key vertebrate-specific features including the craniofacial skeleton and peripheral nervous system. Here we examine the transcriptional profiles and chromatin accessibility of neural crest cells in the basal sea lamprey, in order to gain insight into the ancestral state of the neural crest gene regulatory network (GRN) at the dawn of vertebrates. Transcriptome analyses reveal clusters of co-regulated genes during neural crest specification and migration that show high conservation across vertebrates for dynamic programmes like Wnt modulation during the epithelial to mesenchymal transition, but also reveal novel transcription factors and cell-adhesion molecules not previously implicated in neural crest migration. ATAC-seq analysis refines the location of known cis-regulatory elements at the Hox-α2 locus and uncovers novel cis-regulatory elements for Tfap2B and SoxE1. Moreover, cross-species deployment of lamprey elements in zebrafish reveals that the lamprey SoxE1 enhancer activity is deeply conserved, mediating homologous expression in jawed vertebrates. Together, our data provide new insight into the core elements of the GRN that are conserved to the base of the vertebrates, as well as expose elements that are unique to lampreys.


Item Type:Article
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https://doi.org/10.1038/s41467-019-12687-4DOIArticle
https://rdcu.be/bU5AxPublisherFree ReadCube access
https://doi.org/10.1101/275875DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE112072Related ItemData
https://github.com/tsslab/chick_NC-GRNRelated ItemCode
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6795873/PubMed CentralArticle
ORCID:
AuthorORCID
Hockman, Dorit0000-0003-2613-6216
Chong-Morrison, Vanessa0000-0002-2547-3694
Gavriouchkina, Daria0000-0002-7488-5898
Smith, Jeramiah J.0000-0001-5333-5531
Bronner, Marianne E.0000-0003-4274-1862
Sauka-Spengler, Tatjana0000-0001-9289-0263
Additional Information:© 2019 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 03 March 2018; Accepted 23 September 2019; Published 16 October 2019. Data availability: The authors declare that all data supporting the findings of this study are available within the article and its supplementary information files or from the corresponding author upon reasonable request. The data sets generated during and/or analysed during the current study have been deposited in the NCBI GEOarchive database under accession code: GSE112072 https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE112072. Code availability: The custom script used to calculate motif co-occurrences is available at https://github.com/tsslab/chick_NC-GRN. Details of software versions and parameters used, when different from default, are indicated in the Methods section. We thank Sebastian Shimeld for access to embryos and genomic DNA of the brook lamprey, Hugo Parker for the lamprey HLC vector, and Sally-Ann Clark at the WIMM FACS Core Facility for assistance with cell sorting. We thank Toros Tasgin and Sarah Meyes for cloning candidate genes for in situ and Justine Van Greenen for amplifying and analysing L. planeri genomic DNA sequences. This work was supported by a Leverhulme Research Grant to T.S.S. (RPG-2015–026), the National Institute of General Medical Sciences of the National Institutes of Health grants to J.J.S. (R01GM104123) and C.T.A. (R24GM095471), a Wellcome Trust Institutional Strategic Support Fund grant (H2RZKC00) to D.H. and T.S.S., a Junior Research Fellowship (Trinity College, Oxford), the Sydney Brenner Fellowship, a Company of Biologists Travelling Fellowship (DEVTF-150403) and an EMBO Short Term Fellowship to D.H., and a Clarendon Fund Fellowship to V.C.M. Author Contributions: D.H. and T.S.S. conceived this research programme. D.H. generated RNA-seq and ATAC-seq data, performed and analysed lamprey reporter expression assays and performed bioinformatics analysis. V.C.-M. performed zebrafish transgenesis, splinkerette assay, CRIPSR/Cas9 experiments and immunostaining. S.G. performed lamprey whole-mount in situ hybridisation. D.G. assisted in the analysis of RNA-seq and ATAC-seq data. I.C.F assisted in ATAC-seq data analysis. I.L. performed chicken embryo electroporations and imaging. R.W. performed in situ HCR and whole-mount in situ hybridisations. J.S. and C.T.A. provided access to the draft sea lamprey germline genome assembly. M.E.B. provided access to sea lamprey embryos. D.H. and T.S.S. discussed ideas and interpretations and wrote the manuscript. D.H., M.E.B., and T.S.S. edited the manuscript and all authors commented on it. T.S.S. supervised the study. Competing Interests: The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Leverhulme TrustRPG-2015-026
NIHR01GM104123
NIHR24GM095471
Wellcome TrustH2RZKC00
Trinity CollegeUNSPECIFIED
Sydney Brenner FellowshipUNSPECIFIED
Company of BiologistsDEVTF-150403
European Molecular Biology Organization (EMBO)UNSPECIFIED
Clarendon FundUNSPECIFIED
Subject Keywords:Epigenomics; Evolutionary developmental biology; Regulatory networks; Transcriptomics;
PubMed Central ID:PMC6795873
Record Number:CaltechAUTHORS:20181026-140937942
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20181026-140937942
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90438
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:26 Oct 2018 21:33
Last Modified:22 Oct 2019 21:24

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