An integrated expression atlas of miRNAs and their promoters in human and mouse

Derek De Rie; Imad Abugessaisa; Tanvir Alam; Erik Arner; Peter Arner; Haitham Ashoor; Gaby Åström; Magda Babina; Nicolas Bertin; A. Maxwell Burroughs; Ailsa J. Carlisle; Carsten O. Daub; Michael Detmar; Ruslan Deviatiiarov; Alexandre Fort; Claudia Gebhard; Daniel Goldowitz; Sven Guhl; Thomas J. Ha; Jayson Harshbarger; Akira Hasegawa; Kosuke Hashimoto; Meenhard Herlyn; Peter Heutink; Kelly J. Hitchens; Chung Chau Hon; Edward Huang; Yuri Ishizu; Chieko Kai; Takeya Kasukawa; Peter Klinken; Timo Lassmann; Charles Henri Lecellier; Weonju Lee; Marina Lizio; Vsevolod Makeev; Anthony Mathelier; Yulia A. Medvedeva; Niklas Mejhert; Christopher J. Mungall; Shohei Noma; Mitsuhiro Ohshima; Mariko Okada-Hatakeyama; Helena Persson; Patrizia Rizzu; Filip Roudnicky; Pål Sætrom; Hiroki Sato; Jessica Severin; Jay W. Shin; Rolf K. Swoboda; Hiroshi Tarui; Hiroo Toyoda; Kristoffer Vitting-Seerup; Louise Winteringham; Yoko Yamaguchi; Kayoko Yasuzawa; Misako Yoneda; Noriko Yumoto; Susan Zabierowski; Peter G. Zhang; Christine A. Wells; Kim M. Summers; Hideya Kawaji; Albin Sandelin; Michael Rehli; Yoshihide Hayashizaki; Piero Carninci; Alistair R.R. Forrest; Michiel J.L. De Hoon

doi:10.1038/nbt.3947

An integrated expression atlas of miRNAs and their promoters in human and mouse

Derek De Rie
, Imad Abugessaisa
, Tanvir Alam
, Erik Arner
, Peter Arner
, Haitham Ashoor
, Gaby Åström
, Magda Babina
, Nicolas Bertin
, A. Maxwell Burroughs
, Ailsa J. Carlisle
, Carsten O. Daub
, Michael Detmar
, Ruslan Deviatiiarov
, Alexandre Fort
, Claudia Gebhard
, Daniel Goldowitz
, Sven Guhl
, Thomas J. Ha
, Jayson Harshbarger

Akira Hasegawa, Kosuke Hashimoto, Meenhard Herlyn, Peter Heutink, Kelly J. Hitchens, Chung Chau Hon, Edward Huang, Yuri Ishizu, Chieko Kai, Takeya Kasukawa, Peter Klinken, Timo Lassmann, Charles Henri Lecellier, Weonju Lee, Marina Lizio, Vsevolod Makeev, Anthony Mathelier, Yulia A. Medvedeva, Niklas Mejhert, Christopher J. Mungall, Shohei Noma, Mitsuhiro Ohshima, Mariko Okada-Hatakeyama, Helena Persson, Patrizia Rizzu, Filip Roudnicky, Pål Sætrom, Hiroki Sato, Jessica Severin, Jay W. Shin, Rolf K. Swoboda, Hiroshi Tarui, Hiroo Toyoda, Kristoffer Vitting-Seerup, Louise Winteringham, Yoko Yamaguchi, Kayoko Yasuzawa, Misako Yoneda, Noriko Yumoto, Susan Zabierowski, Peter G. Zhang, Christine A. Wells, Kim M. Summers, Hideya Kawaji, Albin Sandelin, Michael Rehli, Yoshihide Hayashizaki, Piero Carninci, Alistair R.R. Forrest, Michiel J.L. De Hoon^*

^*Corresponding author for this work

Division of Genomic Technologies
RIKEN
Centre for Integrative Bioinformatics
Vrije Universiteit Amsterdam
King Abdullah University of Science and Technology
Department of Medicine
Karolinska Institutet
Compl. Bioscience Research Center Computer Electrical and Mathematical Sciences and Engineering
Department of Dermatology and Allergy
Charité – Universitätsmedizin Berlin
National University of Singapore
National Institutes of Health
University of Edinburgh
Institute of Pharmaceutical Sciences
ETH Zurich—Institute for Particle Physics and Astrophysics (IPA)
Kazan Volga Region Federal University
Department of Internal Medicine III
University of Regensburg
Regensburg Centre for Interventional Immunology
Department of Medical Genetics
University of British Columbia
Melanoma Research Center
Wistar Institute
German Center for Neurodegenerative Diseases
University of Queensland
School of Biomedical Sciences
University of Melbourne
Walter and Eliza Hall Institute of Medical Research
Laboratory Animal Research Center
The University of Tokyo
University of Western Australia
Telethon Kids Institute
Institute of Molecular Genetics of Montpellier
Department of Dermatology
Kyungpook National University
Russian Academy of Sciences
RAS - Engelhardt Institute of Molecular Biology
Dolgoprudny
Moscow Institute of Physics and Technology
Institute of Predictive and Personalized Medicine of Cancer
IMPPC
Environmental Genomics and Systems Biology Division
Lawrence Berkeley National Laboratory
Department of Biochemistry
Ohu University
Laboratory of Cell Systems
The University of Osaka
Department of Clinical Sciences
Lund University
Department of Computer and Information Science
Norwegian University of Science and Technology
Department of Clinical Molecular Genetics
Tokyo University of Pharmacy and Life Sciences
Bioinformatics Centre
University of Copenhagen
Department of Biochemistry
Nihon University
SKI Stem Cell Research Facility
Memorial Sloan-Kettering Cancer Center
Preventive Medicine and Diagnosis Innovation Program

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

483 Citations (Scopus)

Abstract

MicroRNAs (miRNAs) are short non-coding RNAs with key roles in cellular regulation. As part of the fifth edition of the Functional Annotation of Mammalian Genome (FANTOM5) project, we created an integrated expression atlas of miRNAs and their promoters by deep-sequencing 492 short RNA (sRNA) libraries, with matching Cap Analysis Gene Expression (CAGE) data, from 396 human and 47 mouse RNA samples. Promoters were identified for 1,357 human and 804 mouse miRNAs and showed strong sequence conservation between species. We also found that primary and mature miRNA expression levels were correlated, allowing us to use the primary miRNA measurements as a proxy for mature miRNA levels in a total of 1,829 human and 1,029 mouse CAGE libraries. We thus provide a broad atlas of miRNA expression and promoters in primary mammalian cells, establishing a foundation for detailed analysis of miRNA expression patterns and transcriptional control regions.

Original language	English
Pages (from-to)	872-878
Number of pages	7
Journal	Nature Biotechnology
Volume	35
Issue number	9
DOIs	https://doi.org/10.1038/nbt.3947
Publication status	Published - 1 Sept 2017
Externally published	Yes

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De Rie, D., Abugessaisa, I., Alam, T., Arner, E., Arner, P., Ashoor, H., Åström, G., Babina, M., Bertin, N., Burroughs, A. M., Carlisle, A. J., Daub, C. O., Detmar, M., Deviatiiarov, R., Fort, A., Gebhard, C., Goldowitz, D., Guhl, S., Ha, T. J., ... De Hoon, M. J. L. (2017). An integrated expression atlas of miRNAs and their promoters in human and mouse. Nature Biotechnology, 35(9), 872-878. https://doi.org/10.1038/nbt.3947

@article{156193af4d3b4551b8270703f4a4de6c,

title = "An integrated expression atlas of miRNAs and their promoters in human and mouse",

abstract = "MicroRNAs (miRNAs) are short non-coding RNAs with key roles in cellular regulation. As part of the fifth edition of the Functional Annotation of Mammalian Genome (FANTOM5) project, we created an integrated expression atlas of miRNAs and their promoters by deep-sequencing 492 short RNA (sRNA) libraries, with matching Cap Analysis Gene Expression (CAGE) data, from 396 human and 47 mouse RNA samples. Promoters were identified for 1,357 human and 804 mouse miRNAs and showed strong sequence conservation between species. We also found that primary and mature miRNA expression levels were correlated, allowing us to use the primary miRNA measurements as a proxy for mature miRNA levels in a total of 1,829 human and 1,029 mouse CAGE libraries. We thus provide a broad atlas of miRNA expression and promoters in primary mammalian cells, establishing a foundation for detailed analysis of miRNA expression patterns and transcriptional control regions.",

author = "\{De Rie\}, Derek and Imad Abugessaisa and Tanvir Alam and Erik Arner and Peter Arner and Haitham Ashoor and Gaby {\AA}str{\"o}m and Magda Babina and Nicolas Bertin and Burroughs, \{A. Maxwell\} and Carlisle, \{Ailsa J.\} and Daub, \{Carsten O.\} and Michael Detmar and Ruslan Deviatiiarov and Alexandre Fort and Claudia Gebhard and Daniel Goldowitz and Sven Guhl and Ha, \{Thomas J.\} and Jayson Harshbarger and Akira Hasegawa and Kosuke Hashimoto and Meenhard Herlyn and Peter Heutink and Hitchens, \{Kelly J.\} and Hon, \{Chung Chau\} and Edward Huang and Yuri Ishizu and Chieko Kai and Takeya Kasukawa and Peter Klinken and Timo Lassmann and Lecellier, \{Charles Henri\} and Weonju Lee and Marina Lizio and Vsevolod Makeev and Anthony Mathelier and Medvedeva, \{Yulia A.\} and Niklas Mejhert and Mungall, \{Christopher J.\} and Shohei Noma and Mitsuhiro Ohshima and Mariko Okada-Hatakeyama and Helena Persson and Patrizia Rizzu and Filip Roudnicky and P{\aa}l S{\ae}trom and Hiroki Sato and Jessica Severin and Shin, \{Jay W.\} and Swoboda, \{Rolf K.\} and Hiroshi Tarui and Hiroo Toyoda and Kristoffer Vitting-Seerup and Louise Winteringham and Yoko Yamaguchi and Kayoko Yasuzawa and Misako Yoneda and Noriko Yumoto and Susan Zabierowski and Zhang, \{Peter G.\} and Wells, \{Christine A.\} and Summers, \{Kim M.\} and Hideya Kawaji and Albin Sandelin and Michael Rehli and Yoshihide Hayashizaki and Piero Carninci and Forrest, \{Alistair R.R.\} and \{De Hoon\}, \{Michiel J.L.\}",

note = "Publisher Copyright: {\textcopyright} 2017 Nature America, Inc., part of Springer Nature.",

year = "2017",

month = sep,

day = "1",

doi = "10.1038/nbt.3947",

language = "English",

volume = "35",

pages = "872--878",

journal = "Nature Biotechnology",

issn = "1087-0156",

publisher = "Nature Research",

number = "9",

}

De Rie, D, Abugessaisa, I, Alam, T, Arner, E, Arner, P, Ashoor, H, Åström, G, Babina, M, Bertin, N, Burroughs, AM, Carlisle, AJ, Daub, CO, Detmar, M, Deviatiiarov, R, Fort, A, Gebhard, C, Goldowitz, D, Guhl, S, Ha, TJ, Harshbarger, J, Hasegawa, A, Hashimoto, K, Herlyn, M, Heutink, P, Hitchens, KJ, Hon, CC, Huang, E, Ishizu, Y, Kai, C, Kasukawa, T, Klinken, P, Lassmann, T, Lecellier, CH, Lee, W, Lizio, M, Makeev, V, Mathelier, A, Medvedeva, YA, Mejhert, N, Mungall, CJ, Noma, S, Ohshima, M, Okada-Hatakeyama, M, Persson, H, Rizzu, P, Roudnicky, F, Sætrom, P, Sato, H, Severin, J, Shin, JW, Swoboda, RK, Tarui, H, Toyoda, H, Vitting-Seerup, K, Winteringham, L, Yamaguchi, Y, Yasuzawa, K, Yoneda, M, Yumoto, N, Zabierowski, S, Zhang, PG, Wells, CA, Summers, KM, Kawaji, H, Sandelin, A, Rehli, M, Hayashizaki, Y, Carninci, P, Forrest, ARR & De Hoon, MJL 2017, 'An integrated expression atlas of miRNAs and their promoters in human and mouse', Nature Biotechnology, vol. 35, no. 9, pp. 872-878. https://doi.org/10.1038/nbt.3947

TY - JOUR

T1 - An integrated expression atlas of miRNAs and their promoters in human and mouse

AU - De Rie, Derek

AU - Abugessaisa, Imad

AU - Alam, Tanvir

AU - Arner, Erik

AU - Arner, Peter

AU - Ashoor, Haitham

AU - Åström, Gaby

AU - Babina, Magda

AU - Bertin, Nicolas

AU - Burroughs, A. Maxwell

AU - Carlisle, Ailsa J.

AU - Daub, Carsten O.

AU - Detmar, Michael

AU - Deviatiiarov, Ruslan

AU - Fort, Alexandre

AU - Gebhard, Claudia

AU - Goldowitz, Daniel

AU - Guhl, Sven

AU - Ha, Thomas J.

AU - Harshbarger, Jayson

AU - Hasegawa, Akira

AU - Hashimoto, Kosuke

AU - Herlyn, Meenhard

AU - Heutink, Peter

AU - Hitchens, Kelly J.

AU - Hon, Chung Chau

AU - Huang, Edward

AU - Ishizu, Yuri

AU - Kai, Chieko

AU - Kasukawa, Takeya

AU - Klinken, Peter

AU - Lassmann, Timo

AU - Lecellier, Charles Henri

AU - Lee, Weonju

AU - Lizio, Marina

AU - Makeev, Vsevolod

AU - Mathelier, Anthony

AU - Medvedeva, Yulia A.

AU - Mejhert, Niklas

AU - Mungall, Christopher J.

AU - Noma, Shohei

AU - Ohshima, Mitsuhiro

AU - Okada-Hatakeyama, Mariko

AU - Persson, Helena

AU - Rizzu, Patrizia

AU - Roudnicky, Filip

AU - Sætrom, Pål

AU - Sato, Hiroki

AU - Severin, Jessica

AU - Shin, Jay W.

AU - Swoboda, Rolf K.

AU - Tarui, Hiroshi

AU - Toyoda, Hiroo

AU - Vitting-Seerup, Kristoffer

AU - Winteringham, Louise

AU - Yamaguchi, Yoko

AU - Yasuzawa, Kayoko

AU - Yoneda, Misako

AU - Yumoto, Noriko

AU - Zabierowski, Susan

AU - Zhang, Peter G.

AU - Wells, Christine A.

AU - Summers, Kim M.

AU - Kawaji, Hideya

AU - Sandelin, Albin

AU - Rehli, Michael

AU - Hayashizaki, Yoshihide

AU - Carninci, Piero

AU - Forrest, Alistair R.R.

AU - De Hoon, Michiel J.L.

PY - 2017/9/1

Y1 - 2017/9/1

N2 - MicroRNAs (miRNAs) are short non-coding RNAs with key roles in cellular regulation. As part of the fifth edition of the Functional Annotation of Mammalian Genome (FANTOM5) project, we created an integrated expression atlas of miRNAs and their promoters by deep-sequencing 492 short RNA (sRNA) libraries, with matching Cap Analysis Gene Expression (CAGE) data, from 396 human and 47 mouse RNA samples. Promoters were identified for 1,357 human and 804 mouse miRNAs and showed strong sequence conservation between species. We also found that primary and mature miRNA expression levels were correlated, allowing us to use the primary miRNA measurements as a proxy for mature miRNA levels in a total of 1,829 human and 1,029 mouse CAGE libraries. We thus provide a broad atlas of miRNA expression and promoters in primary mammalian cells, establishing a foundation for detailed analysis of miRNA expression patterns and transcriptional control regions.

AB - MicroRNAs (miRNAs) are short non-coding RNAs with key roles in cellular regulation. As part of the fifth edition of the Functional Annotation of Mammalian Genome (FANTOM5) project, we created an integrated expression atlas of miRNAs and their promoters by deep-sequencing 492 short RNA (sRNA) libraries, with matching Cap Analysis Gene Expression (CAGE) data, from 396 human and 47 mouse RNA samples. Promoters were identified for 1,357 human and 804 mouse miRNAs and showed strong sequence conservation between species. We also found that primary and mature miRNA expression levels were correlated, allowing us to use the primary miRNA measurements as a proxy for mature miRNA levels in a total of 1,829 human and 1,029 mouse CAGE libraries. We thus provide a broad atlas of miRNA expression and promoters in primary mammalian cells, establishing a foundation for detailed analysis of miRNA expression patterns and transcriptional control regions.

UR - https://www.scopus.com/pages/publications/85028474852

U2 - 10.1038/nbt.3947

DO - 10.1038/nbt.3947

M3 - Article

C2 - 28829439

AN - SCOPUS:85028474852

SN - 1087-0156

VL - 35

SP - 872

EP - 878

JO - Nature Biotechnology

JF - Nature Biotechnology

IS - 9

ER -

An integrated expression atlas of miRNAs and their promoters in human and mouse

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