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Genome-wide analysis of mammalian promoter architecture and evolution
Piero Carninci 1, 2, 21, Albin Sandelin 1, 3, 21, Boris Lenhard 1, 3, 20, 21, Shintaro Katayama 1, Kazuro Shimokawa 1, Jasmina Ponjavic 1, 20, Colin A M Semple 1, 4, Martin S Taylor 1, 5, Pär G Engström 3, Martin C Frith 1, 6, Alistair R R Forrest 6, Wynand B Alkema 3, Sin Lam Tan 7, Charles Plessy 2, Rimantas Kodzius 1, 2, Timothy Ravasi 1, 6, 8, Takeya Kasukawa 1, 9, Shiro Fukuda 1, Mutsumi Kanamori-Katayama 1, Yayoi Kitazume 1, Hideya Kawaji 1, 9, Chikatoshi Kai 1, Mari Nakamura 1, Hideaki Konno 1, Kenji Nakano 1, 9, Salim Mottagui-Tabar 3, 20, Peter Arner 10, Alessandra Chesi 11, Stefano Gustincich 11, Francesca Persichetti 12, Harukazu Suzuki 1, Sean M Grimmond 6, Christine A Wells 19, Valerio Orlando 13, Claes Wahlestedt 3, 20, Edison T Liu 14, Matthias Harbers 15, Jun Kawai 1, 2, Vladimir B Bajic 1, 7, 16, David A Hume 1, 6, 21
& Yoshihide Hayashizaki 1, 2, 17, 181
Genome Exploration Research Group, RIKEN Genomic Sciences Center (GSC), RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan. 2
Genome Science Laboratory, Discovery Research Institute, RIKEN Wako Institute, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan. 3
Center for Genomics and Bioinformatics, Karolinska Institutet, Berzelius v. 35, S-171 77
Stockholm, Sweden. 4
UK Medical Research Council (MRC) Human Genetics Unit, Western General Hospital, Crewe Road, Edinburgh, EH4 2XU, UK. 5
University of Oxford, Roosevelt Drive, Oxford, OX3 7BN, UK. 6
Australian Research Council (ARC) Special Research Centre for Functional and Applied Genomics, Institute for Molecular Bioscience, The University of Queensland, Brisbane Qld, 4072, Australia. 7
Knowledge Extraction Laboratory, Institute for Infocomm Research, 21 Heng Mui Keng Terrace, 119613, Singapore. 8
Department of Bioengineering, University of California, San Diego, 9500 Gilman Drive, 0412
La Jolla, California
92093, USA. 9
Broadband Communication Service Business Unit, Network Service Solution Business Group, NTT Software Corporation, Teisan Kannai Bldg. 209, Yamashita-cho Naka-ku, Yokohama, Kanagawa, 231-8551, Japan. 10
Department of Medicine, Karolinska Institute, Huddinge University Hospital, S 141 86
Huddinge, Sweden. 11
The Giovanni Armenise–Harvard Foundation Laboratory, Sector of Neurobiology, International School for Advanced Studies-Scuola Internazionale Superiore Studi Avanzati (I.S.A.S.-S.I.S.S.A.), AREA Science Park, Padriciano 99, 34012
Trieste, Italy. 12
Sector of Neurobiology, I.S.A.S.-S.I.S.S.A., AREA Science Park, Padriciano 99, 34012
Trieste, Italy. 13
Dulbecco Telethon Institute, Institute of Genetics and Biophysics, Consiglio Nazionale delle Ricerche (IGB CNR), Epigenetics and Genome Reprogramming Laboratory, Pietro Castellino Street 111, Napoli, 80131, Italy. 14
Genome Institute of Singapore, 60 Biopolis Street #02-01, Singapore
138672. 15
Kabushiki Kaisha Dnaform, 1-3-35, Mita, Minato-ku, Tokyo, 108-0073, Japan. 16
South African National Bioinformatics Institute, University of the Western Cape, Private Bag X17, Bellville, South Africa. 17
Yokohama City University, 1-7-29 Suehiro-cho Tsurumi-ku
Yokohama
230-0045
Japan. 18
Graduate School of Comprehensive Human Science, University of Tsukuba, 1-1-1 Tennodai, Tsukuba-shi Ibaraki-ken, 305-8577, Japan. 19
The Eskitis Institute for Cell and Molecular Therapies, Griffith University, Nathan Campus, Kessels Road, Queensland
4111, Australia. 20
Present addresses: Bergen Center for Computational Science, Unifob AS, University of Bergen, Thormøhlensgate 55, N-5008 Bergen, Norway (B.L.), Scripps Florida, Jupiter, Florida
33458, USA (C.W.), Department of Molecular Medicine, National Public Health Instititute, Department of Medical Genetics, University of Helsinki, Biomedicum, FIN-00251 Helsinki, Finland (S.M.-T.) and MRC Functional Genetics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford
OX1 3QX, UK (J.P.). 21
These authors contributed equally to this work.
Correspondence should be addressed to David A Hume d.hume@imb.uq.edu.au or Yoshihide Hayashizaki yosihide@gsc.riken.jp
Published in Nature Genetics
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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