Genome-wide analysis of mammalian promoter architecture and evolution

Piero Carninci; Albin Sandelin; Boris Lenhard; Shintaro Katayama; Kazuro Shimokawa; Jasmina Ponjavic; Colin A.M. Semple; Martin S. Taylor; Pär G. Engström; Martin C. Frith; Alistair R.R. Forrest; Wynand B. Alkema; Sin Lam Tan; Charles Plessy; Rimantas Kodzius; Timothy Ravasi; Takeya Kasukawa; Shiro Fukuda; Mutsumi Kanamori-Katayama; Yayoi Kitazume; Hideya Kawaji; Chikatoshi Kai; Mari Nakamura; Hideaki Konno; Kenji Nakano; Salim Mottagui-Tabar; Peter Arner; Alessandra Chesi; Stefano Gustincich; Francesca Persichetti; Harukazu Suzuki; Sean M. Grimmond; Christine A. Wells; Valerio Orlando; Claes Wahlestedt; Edison T. Liu; Matthias Harbers; Jun Kawai; Vladimir B. Bajic; David A. Hume; Yoshihide Hayashizaki

doi:10.1038/ng1789

Genome-wide analysis of mammalian promoter architecture and evolution

Piero Carninci, Albin Sandelin, Boris Lenhard, Shintaro Katayama, Kazuro Shimokawa, Jasmina Ponjavic, Colin A.M. Semple, Martin S. Taylor, Pär G. Engström, Martin C. Frith, Alistair R.R. Forrest, Wynand B. Alkema, Sin Lam Tan, Charles Plessy, Rimantas Kodzius, Timothy Ravasi, Takeya Kasukawa, Shiro Fukuda, Mutsumi Kanamori-Katayama, Yayoi KitazumeHideya Kawaji, Chikatoshi Kai, Mari Nakamura, Hideaki Konno, Kenji Nakano, Salim Mottagui-Tabar, Peter Arner, Alessandra Chesi, Stefano Gustincich, Francesca Persichetti, Harukazu Suzuki, Sean M. Grimmond, Christine A. Wells, Valerio Orlando, Claes Wahlestedt, Edison T. Liu, Matthias Harbers, Jun Kawai, Vladimir B. Bajic, David A. Hume^*, Yoshihide Hayashizaki

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

1069 Scopus citations

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.

Original language	English (US)
Pages (from-to)	626-635
Number of pages	10
Journal	Nature Genetics
Volume	38
Issue number	6
DOIs	https://doi.org/10.1038/ng1789
State	Published - Jun 2006
Externally published	Yes

Bibliographical note

Funding Information:
We thank the following individuals for discussion, encouragement and technical assistance: H. Atsui, A. Hasegawa, K. Hayashida, H. Himei, F. Hori, C. Kawazu, M. Kojima, K. Waki, M. Aoki, K Murakami, M. Murata, M. Nishikawa, H. Nishiyori, K. Nomura, M. Ohno, H. Sato, Y. Shigemoto, N. Suzuki, Y. Takeda and K. Yoshida. We especially thank A. Wada, T. Ogawa, M. Muramatsu, A. Kira and all the members of RIKEN Yokohama Research Promotion Division for supporting and encouraging the project. We also thank the Laboratory of Genome Exploration Research Group for secretarial and technical assistance, and Yokohama City University, who provided human samples and computational resources of the RIKEN Super Combined Cluster (RSCC). This work was mainly supported by Research Grant for the Genome Network Project from the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT), the RIKEN Genome Exploration Research Project from the Japanese Ministry of Education, Culture, Sports, Science and Technology of the Japanese Government (to Y.H.), Advanced and Innovational Research Program in Life Science (to Y.H.), National Project on Protein Structural and Functional Analysis from MEXT (to Y.H.), Presidential Research Grant for Intersystem Collaboration of RIKEN (to P.C. and Y.H.) and a grant from the Six Framework Program from the European Commission (to P.C.).

ASJC Scopus subject areas

Genetics

Access to Document

10.1038/ng1789

Cite this

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., ... Hayashizaki, Y. (2006). Genome-wide analysis of mammalian promoter architecture and evolution. Nature Genetics, 38(6), 626-635. https://doi.org/10.1038/ng1789

@article{03f6cc7552fd41279d5ea6ec3984a442,

title = "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.",

author = "Piero Carninci and Albin Sandelin and Boris Lenhard and Shintaro Katayama and Kazuro Shimokawa and Jasmina Ponjavic and Semple, {Colin A.M.} and Taylor, {Martin S.} and Engstr{\"o}m, {P{\"a}r G.} and Frith, {Martin C.} and Forrest, {Alistair R.R.} and Alkema, {Wynand B.} and Tan, {Sin Lam} and Charles Plessy and Rimantas Kodzius and Timothy Ravasi and Takeya Kasukawa and Shiro Fukuda and Mutsumi Kanamori-Katayama and Yayoi Kitazume and Hideya Kawaji and Chikatoshi Kai and Mari Nakamura and Hideaki Konno and Kenji Nakano and Salim Mottagui-Tabar and Peter Arner and Alessandra Chesi and Stefano Gustincich and Francesca Persichetti and Harukazu Suzuki and Grimmond, {Sean M.} and Wells, {Christine A.} and Valerio Orlando and Claes Wahlestedt and Liu, {Edison T.} and Matthias Harbers and Jun Kawai and Bajic, {Vladimir B.} and Hume, {David A.} and Yoshihide Hayashizaki",

note = "Funding Information: We thank the following individuals for discussion, encouragement and technical assistance: H. Atsui, A. Hasegawa, K. Hayashida, H. Himei, F. Hori, C. Kawazu, M. Kojima, K. Waki, M. Aoki, K Murakami, M. Murata, M. Nishikawa, H. Nishiyori, K. Nomura, M. Ohno, H. Sato, Y. Shigemoto, N. Suzuki, Y. Takeda and K. Yoshida. We especially thank A. Wada, T. Ogawa, M. Muramatsu, A. Kira and all the members of RIKEN Yokohama Research Promotion Division for supporting and encouraging the project. We also thank the Laboratory of Genome Exploration Research Group for secretarial and technical assistance, and Yokohama City University, who provided human samples and computational resources of the RIKEN Super Combined Cluster (RSCC). This work was mainly supported by Research Grant for the Genome Network Project from the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT), the RIKEN Genome Exploration Research Project from the Japanese Ministry of Education, Culture, Sports, Science and Technology of the Japanese Government (to Y.H.), Advanced and Innovational Research Program in Life Science (to Y.H.), National Project on Protein Structural and Functional Analysis from MEXT (to Y.H.), Presidential Research Grant for Intersystem Collaboration of RIKEN (to P.C. and Y.H.) and a grant from the Six Framework Program from the European Commission (to P.C.).",

year = "2006",

month = jun,

doi = "10.1038/ng1789",

language = "English (US)",

volume = "38",

pages = "626--635",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Research",

number = "6",

}

Carninci, P, Sandelin, A, Lenhard, B, Katayama, S, Shimokawa, K, Ponjavic, J, Semple, CAM, Taylor, MS, Engström, PG, Frith, MC, Forrest, ARR, Alkema, WB, Tan, SL, 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, SM, Wells, CA, Orlando, V, Wahlestedt, C, Liu, ET, Harbers, M, Kawai, J, Bajic, VB, Hume, DA & Hayashizaki, Y 2006, 'Genome-wide analysis of mammalian promoter architecture and evolution', Nature Genetics, vol. 38, no. 6, pp. 626-635. https://doi.org/10.1038/ng1789

TY - JOUR

T1 - Genome-wide analysis of mammalian promoter architecture and evolution

AU - Carninci, Piero

AU - Sandelin, Albin

AU - Lenhard, Boris

AU - Katayama, Shintaro

AU - Shimokawa, Kazuro

AU - Ponjavic, Jasmina

AU - Semple, Colin A.M.

AU - Taylor, Martin S.

AU - Engström, Pär G.

AU - Frith, Martin C.

AU - Forrest, Alistair R.R.

AU - Alkema, Wynand B.

AU - Tan, Sin Lam

AU - Plessy, Charles

AU - Kodzius, Rimantas

AU - Ravasi, Timothy

AU - Kasukawa, Takeya

AU - Fukuda, Shiro

AU - Kanamori-Katayama, Mutsumi

AU - Kitazume, Yayoi

AU - Kawaji, Hideya

AU - Kai, Chikatoshi

AU - Nakamura, Mari

AU - Konno, Hideaki

AU - Nakano, Kenji

AU - Mottagui-Tabar, Salim

AU - Arner, Peter

AU - Chesi, Alessandra

AU - Gustincich, Stefano

AU - Persichetti, Francesca

AU - Suzuki, Harukazu

AU - Grimmond, Sean M.

AU - Wells, Christine A.

AU - Orlando, Valerio

AU - Wahlestedt, Claes

AU - Liu, Edison T.

AU - Harbers, Matthias

AU - Kawai, Jun

AU - Bajic, Vladimir B.

AU - Hume, David A.

AU - Hayashizaki, Yoshihide

N1 - Funding Information: We thank the following individuals for discussion, encouragement and technical assistance: H. Atsui, A. Hasegawa, K. Hayashida, H. Himei, F. Hori, C. Kawazu, M. Kojima, K. Waki, M. Aoki, K Murakami, M. Murata, M. Nishikawa, H. Nishiyori, K. Nomura, M. Ohno, H. Sato, Y. Shigemoto, N. Suzuki, Y. Takeda and K. Yoshida. We especially thank A. Wada, T. Ogawa, M. Muramatsu, A. Kira and all the members of RIKEN Yokohama Research Promotion Division for supporting and encouraging the project. We also thank the Laboratory of Genome Exploration Research Group for secretarial and technical assistance, and Yokohama City University, who provided human samples and computational resources of the RIKEN Super Combined Cluster (RSCC). This work was mainly supported by Research Grant for the Genome Network Project from the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT), the RIKEN Genome Exploration Research Project from the Japanese Ministry of Education, Culture, Sports, Science and Technology of the Japanese Government (to Y.H.), Advanced and Innovational Research Program in Life Science (to Y.H.), National Project on Protein Structural and Functional Analysis from MEXT (to Y.H.), Presidential Research Grant for Intersystem Collaboration of RIKEN (to P.C. and Y.H.) and a grant from the Six Framework Program from the European Commission (to P.C.).

PY - 2006/6

Y1 - 2006/6

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=33744805985&partnerID=8YFLogxK

U2 - 10.1038/ng1789

DO - 10.1038/ng1789

M3 - Article

C2 - 16645617

AN - SCOPUS:33744805985

SN - 1061-4036

VL - 38

SP - 626

EP - 635

JO - Nature Genetics

JF - Nature Genetics

IS - 6

ER -

Genome-wide analysis of mammalian promoter architecture and evolution

Abstract

Bibliographical note

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this