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Occupancies of tissue-specific cis-regulatory modules by Spemann-Mangold organizer-specific transcription factors for embryonic head specification

ABSTRACT: Spemann-Mangold organizer-specific transcription factors (TFs), Otx2, Lim1/Lhx1, and Gsc, are essential for embryonic head specification. However, the molecular mechanisms by which those TFs interact with the genome to direct head formation are largely unknown. Here we employed ChIP-seq and RNA-seq approaches in Xenopus tropicalis gastrulae and found that occupancy of the corepressor, TLE/Groucho, is a better indicator of tissue-specific cis-regulatory modules (CRMs) than the coactivator p300, during early embryonic stages. On the basis of TLE binding and comprehensive CRM profiling, we defined two distinct types of Otx2- and TLE-occupied CRMs. Using these devices, Otx2 and Lim1/Lhx1 (activator) or Goosecoid (repressor) are able to upregulate or downregulate a large battery of target genes in the head organizer. An underlying principle is that Otx marks target genes for head specification to be regulated positively or negatively by partner TFs through specific types of CRMs.

ORGANISM(S): Xenopus tropicalis

PROVIDER: GSE172076 | GEO | 2021/04/15

REPOSITORIES: GEO

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Project description:Background: The Spemann/Mangold organizer is a transient tissue critical for patterning the gastrula stage vertebrate embryo and formation of the three germ layers. Despite its important role during development, there are still relatively few genes with specific expression in the organizer and its derivatives. Foxa2 is a forkhead transcription factor that is absolutely required for formation of the mammalian equivalent of the organizer, the node, the axial mesoderm and the definitive endoderm (DE). However, the targets of Foxa2 during embryogenesis, and the molecular impact of organizer loss on the gastrula embryo, have not been well defined. Results: To identify genes specific to the Spemann/Mangold organizer, we performed a microarray-based screen that compared wild-type and Foxa2 mutant embryos at late gastrulation stage (E7.5). We could detect genes that were consistently down-regulated in replicate pools of mutant embryos versus wild-type, and these included a number of known node and DE markers. We selected 314 genes without previously published data at E7.5 and screened for expression by whole mount in situ hybridization. We identified 10 novel expression patterns in the node and 5 in the definitive endoderm. We also found significant reduction of markers expressed in secondary tissues that require interaction with the organizer and its derivatives, such as cardiac mesoderm, vasculature, primitive streak, and anterior neuroectoderm. Conclusions: The genes identified in this screen represent novel Spemann/Mangold organizer genes as well as potential Foxa2 targets. Further investigation will be needed to define these genes as novel developmental regulatory factors involved in organizer formation and function. We have placed these genes in a Foxa2-dependent genetic regulatory network and we hypothesize how Foxa2 may regulate a molecular program of Spemann/Mangold organizer development. We have also shown how early loss of the organizer and its inductive properties in an otherwise normal embryo, impacts on the molecular profile of surrounding tissues.

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Occupancies of tissue-specific cis-regulatory modules by Spemann-Mangold organizer-specific transcription factors for embryonic head specification

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