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Genome-wide analysis of mammalian promoter architecture and evolution
Abstract
Mammalian promoters can be separated into two classes, conserved TATA box-enriched promoters, which initiate at a well-defined site, and more plastic, broad and evolvable CpG-rich promoters. We have sequenced tags corresponding to several hundred thousand transcription start sites (TSSs) in the mouse and human genomes, allowing precise analysis of the sequence architecture and evolution of distinct promoter classes. Different tissues and families of genes differentially use distinct types of promoters. Our tagging methods allow quantitative analysis of promoter usage in different tissues and show that differentially regulated alternative TSSs are a common feature in protein-coding genes and commonly generate alternative N termini. Among the TSSs, we identified new start sites associated with the majority of exons and with 3' UTRs. These data permit genome-scale identification of tissue-specific promoters and analysis of the cis-acting elements associated with them.
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“Cap Analysis of Gene Expression Sequencing (CAGE-seq) determines the 5’-ends of TSSs at single nucleotide resolution11,12 and quantifies gene expression similar to RNA-seq13.”
From Alternative promoters in CpG depleted regions are prevalently associated with epigenetic misregulation of liver cancer transcriptomes (2023) · cites this paper as [11]
In the citing paper
“CAGE TCs overlapping reference promoters have significantly broader widths (Fig. 3e, f), which are termed broad promoters11”
From Alternative promoters in CpG depleted regions are prevalently associated with epigenetic misregulation of liver cancer transcriptomes (2023) · cites this paper as [11]
In the citing paper
“Contrary, CAGE TCs overlapping alternative promoters have narrow widths (Fig. 3e, f), which are termed sharp promoters11”
From Alternative promoters in CpG depleted regions are prevalently associated with epigenetic misregulation of liver cancer transcriptomes (2023) · cites this paper as [11]
In the citing paper
“Human promoters are mostly CG-rich35,62 and have distinct promoter architecture and regulation11 compared to CG-poor promoters which are mostly tissue-specific17”
From Alternative promoters in CpG depleted regions are prevalently associated with epigenetic misregulation of liver cancer transcriptomes (2023) · cites this paper as [11]
In the citing paper
“In addition, CGIs are often origins of replication31–33 and are generally associated with multiple TSSs dispersed over a 50–100 bp region.34,35”
From Adeno-Associated Virus Serotype-Specific Inverted Terminal Repeat Sequence Role in Vector Transgene Expression (2020) · cites this paper as [34]
In the citing paper
“This observation is further supported by the control of gene transcription largely through proximal promoters.64”
From Census and evaluation of p53 target genes (2017) · cites this paper as [64]
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Metadata
- Authors
- Carninci, P., Sandelin, A., Lenhard, B., Katayama, S., Shimokawa, K., Ponjavic, J., Semple, C. A. M., Taylor, M. S., Engström, P. G., Frith, M. C., Forrest, A. R. R., Alkema, W. B., Tan, S. L., Plessy, C., Kodzius, R., Ravasi, T., Kasukawa, T., Fukuda, S., Kanamori-Katayama, M., Kitazume, Y., Kawaji, H., Kai, C., Nakamura, M., Konno, H., Nakano, K., Mottagui-Tabar, S., Arner, P., Chesi, A., Gustincich, S., Persichetti, F., Suzuki, H., Grimmond, S. M., Wells, C. A., Orlando, V., Wahlestedt, C., Liu, E. T., Harbers, M., Kawai, J., Bajic, V. B., Hume, D. A., & Hayashizaki, Y.
- Affiliations
- RIKEN (JP)
- Karolinska Institutet (SE)
- University of Helsinki (FI)
- Western General Hospital (GB)
- University of Oxford (GB)
- Australian Research Council (AU)
- Institute for Infocomm Research (SG)
- NTT (Japan) (JP)
- Scuola Internazionale Superiore di Studi Avanzati (IT)
- Griffith University (AU)
- Dulbecco Telethon Institute (IT)
- Genome Institute of Singapore (SG)
- University of Tsukuba (JP)
- Corresponding author
- Hume, David A
- Hayashizaki, Yoshihide
- ORCID
- Carninci, Piero
- Sandelin, Albin
- Lenhard, Boris
- Katayama, Shintaro
- Shimokawa, Kazuro
- Semple, Colin A M
- Taylor, Martin S
- Engström, Pär G
- Frith, Martin C
- Forrest, Alistair R R
- Alkema, Wynand B
- Plessy, Charles
- Kodzius, Rimantas
- Ravasi, Timothy
- Kasukawa, Takeya
- Fukuda, Shiro
- Kawaji, Hideya
- Nakamura, Mari
- Arner, Peter
- Chesi, Alessandra
- Gustincich, Stefano
- Persichetti, Francesca
- Suzuki, Harukazu
- Grimmond, Sean M
- Wells, Christine A
- Orlando, Valerio
- Liu, Edison T
- Harbers, Matthias
- Kawai, Jun
- Hume, David A
- Hayashizaki, Yoshihide
- Venue
- Nature Genetics
- Published
- 2006-04-28
- Volume
- 38
- Issue
- 6
- Pages
- 626-635
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- OpenAlex
- W2057692691
- Cited by
- 1,350
- References
- 41
- Citations by year
- 2026: 25 · 2025: 36 · 2024: 52 · 2023: 46 · 2022: 53 · 2021: 54 · 2020: 60 · 2019: 73 · 2018: 46 · 2017: 56 · 2016: 58 · 2015: 63 · 2014: 81 · 2013: 72 · 2012: 66
- FWCI
- 42.97
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- SDL (submittedVersion)
- Griffith Research Online (submittedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/H531586/1, S17961)
- 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 › Epigenetics and DNA Methylation
- Keywords
- promoter architecture, transcription start sites, TATA box, promoter evolution, alternative promoters, tissue-specific promoters, cis-regulatory elements, gene expression regulation
- MeSH terms
- Animals, Base Sequence, DNA, Promoter Regions, Genetic, TATA Box, Genome, Evolution, Molecular, 3' Untranslated Regions, Proteome
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