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Cited by 127Genomics and Chromatin DynamicsGenomics and Phylogenetic StudiesRNA Research and Splicing

Dynamic regulation of the transcription initiation landscape at single nucleotide resolution during vertebrate embryogenesis

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Nepal, Chirag, Hadzhiev, Yavor, Previti, Christopher, Haberle, Vanja, Li, Nan, Takahashi, Hazuki, Suzuki, Ana Maria M., Sheng, Ying +15 more·2013·Genome Research
DOI 10.1101/gr.153692.112PMC PMC3814893
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Abstract

Spatiotemporal control of gene expression is central to animal development. Core promoters represent a previously unanticipated regulatory level by interacting with cis-regulatory elements and transcription initiation in different physiological and developmental contexts. Here, we provide a first and comprehensive description of the core promoter repertoire and its dynamic use during the development of a vertebrate embryo. By using cap analysis of gene expression (CAGE), we mapped transcription initiation events at single nucleotide resolution across 12 stages of zebrafish development. These CAGE-based transcriptome maps reveal genome-wide rules of core promoter usage, structure, and dynamics, key to understanding the control of gene regulation during vertebrate ontogeny. They revealed the existence of multiple classes of pervasive intra- and intergenic post-transcriptionally processed RNA products and their developmental dynamics. Among these RNAs, we report splice donor site-associated intronic RNA (sRNA) to be specific to genes of the splicing machinery. For the identification of conserved features, we compared the zebrafish data sets to the first CAGE promoter map of Tetraodon and the existing human CAGE data. We show that a number of features, such as promoter type, newly discovered promoter properties such as a specialized purine-rich initiator motif, as well as sRNAs and the genes in which they are detected, are conserved in mammalian and Tetraodon CAGE-defined promoter maps. The zebrafish developmental promoterome represents a powerful resource for studying developmental gene regulation and revealing promoter features shared across vertebrates.

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Authors
Nepal, C., Hadzhiev, Y., Previti, C., Haberle, V., Li, N., Takahashi, H., Suzuki, A. M. M., Sheng, Y., Abdelhamid, R. F., Anand, S., Gehrig, J., Akalin, A., Kockx, C. E. M., van der Sloot, A. A. J., van IJcken, W. F. J., Armant, O., Rastegar, S., Watson, C., Strähle, U., Stupka, E., Carninci, P., Lenhard, B., & Müller, F.
Affiliations
  • University of Bergen (NO)
  • University of Birmingham (GB)
  • Queen Mary University of London (GB)
  • Erasmus MC (NL)
  • Karlsruhe Institute of Technology (DE)
  • University of Florida (US)
  • Hammersmith Hospital (GB)
Corresponding author
  • Carninci, Piero
  • Lenhard, Boris
  • Müller, Ferenc
ORCID
Venue
Genome Research
Publisher
Cold Spring Harbor Laboratory
Published
2013-09-03
Volume
23
Issue
11
Pages
1938-1950
ISSN
1088-9051 (ISSN-L)
DOI
10.1101/gr.153692.112
PMC
PMC3814893
OpenAlex
W2040891939
Cited by
127
References
2
Citations by year
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Type
posted content
Language
en
Open access
Licence
other-oa
Locations
  • Genome Research (publishedVersion, other-oa)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • EUR Research Repository (Erasmus University Rotterdam) (publishedVersion, other-oa)
  • EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
  • RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
  • NORA - Norwegian Open Research Archives (submittedVersion, cc-by-nc)
  • University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
Funders
  • Ministry of Education, Culture, Sports, Science and Technology
  • RIKEN
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords
core promoter, transcription initiation, vertebrate embryonic development, zebrafish development, CAGE, splicing machinery, cis-regulatory elements, developmental gene regulation
MeSH terms
Animals, Genes, Phylogeny, Promoter Regions, Genetic, Purines, RNA, RNA Caps, RNA Splicing, Vertebrates, Zebrafish, Genome, Gene Expression Regulation, Developmental, Evolution, Molecular, Gene Expression Profiling, Transcription Initiation Site, Embryonic Development, Transcriptome

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