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 Astrom; 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; Pal Saetrom; 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 Astrom, 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 HarshbargerAkira 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, Pal Saetrom, 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

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410 Scopus citations

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 (US)
Pages (from-to)	872-+
Number of pages	871
Journal	Nature Biotechnology
Volume	35
Issue number	9
DOIs	https://doi.org/10.1038/nbt.3947
State	Published - 2017

Bibliographical note

KAUST Repository Item: Exported on 2021-07-09
Acknowledgements: FANTOM5 was made possible by the following grants: Research Grant for RIKEN Omics Science Center from MEXT to Y.H.; Grant of the Innovative Cell Biology by Innovative Technology (Cell Innovation Program) from the MEXT to Y.H.; Research Grant from MEXT to the RIKEN Center for Life Science Technologies; Research Grant to RIKEN Preventive Medicine and Diagnosis Innovation Program from MEXT to Y.H. K.V.-S. and A.S. were supported by the Lundbeck and Novo Nordisk Foundations. A.R.R.F. is supported by a Senior Cancer Research Fellowship from the Cancer Research Trust, funds raised by the MACA Ride to Conquer Cancer, and the Australian Research Council’s Discovery Projects funding scheme (DP160101960). Y.A.M. was supported by the Russian Science Foundation, grant 15-14-30002. R.D. was supported by the Russian Science Foundation, grant 14-44-00022. We would like to thank L. Schwarzfischer for technical assistance and N. Eichner and G. Meister for sequencing RACE products. We would also like to thank GeNAS for data production.

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de Rie, D., Abugessaisa, I., Alam, T., Arner, E., Arner, P., Ashoor, H., Astrom, 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-+. https://doi.org/10.1038/nbt.3947

@article{364a303e54dd4c4c8556e047ea7c85c4,

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 Astrom 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 Charles-Henri Lecellier 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 Pal Saetrom 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 = "KAUST Repository Item: Exported on 2021-07-09 Acknowledgements: FANTOM5 was made possible by the following grants: Research Grant for RIKEN Omics Science Center from MEXT to Y.H.; Grant of the Innovative Cell Biology by Innovative Technology (Cell Innovation Program) from the MEXT to Y.H.; Research Grant from MEXT to the RIKEN Center for Life Science Technologies; Research Grant to RIKEN Preventive Medicine and Diagnosis Innovation Program from MEXT to Y.H. K.V.-S. and A.S. were supported by the Lundbeck and Novo Nordisk Foundations. A.R.R.F. is supported by a Senior Cancer Research Fellowship from the Cancer Research Trust, funds raised by the MACA Ride to Conquer Cancer, and the Australian Research Council{\textquoteright}s Discovery Projects funding scheme (DP160101960). Y.A.M. was supported by the Russian Science Foundation, grant 15-14-30002. R.D. was supported by the Russian Science Foundation, grant 14-44-00022. We would like to thank L. Schwarzfischer for technical assistance and N. Eichner and G. Meister for sequencing RACE products. We would also like to thank GeNAS for data production.",

year = "2017",

doi = "10.1038/nbt.3947",

language = "English (US)",

volume = "35",

pages = "872--+",

journal = "Nature Biotechnology",

issn = "1546-1696",

publisher = "Nature Research",

number = "9",

}

de Rie, D, Abugessaisa, I, Alam, T, Arner, E, Arner, P, Ashoor, H, Astrom, 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, C-H, 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, Saetrom, 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-+. 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 - Astrom, 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 - Saetrom, Pal

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.

N1 - KAUST Repository Item: Exported on 2021-07-09 Acknowledgements: FANTOM5 was made possible by the following grants: Research Grant for RIKEN Omics Science Center from MEXT to Y.H.; Grant of the Innovative Cell Biology by Innovative Technology (Cell Innovation Program) from the MEXT to Y.H.; Research Grant from MEXT to the RIKEN Center for Life Science Technologies; Research Grant to RIKEN Preventive Medicine and Diagnosis Innovation Program from MEXT to Y.H. K.V.-S. and A.S. were supported by the Lundbeck and Novo Nordisk Foundations. A.R.R.F. is supported by a Senior Cancer Research Fellowship from the Cancer Research Trust, funds raised by the MACA Ride to Conquer Cancer, and the Australian Research Council’s Discovery Projects funding scheme (DP160101960). Y.A.M. was supported by the Russian Science Foundation, grant 15-14-30002. R.D. was supported by the Russian Science Foundation, grant 14-44-00022. We would like to thank L. Schwarzfischer for technical assistance and N. Eichner and G. Meister for sequencing RACE products. We would also like to thank GeNAS for data production.

PY - 2017

Y1 - 2017

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 - http://hdl.handle.net/10754/670083

UR - http://www.nature.com/articles/nbt.3947

UR - http://www.scopus.com/inward/record.url?scp=85028474852&partnerID=8YFLogxK

U2 - 10.1038/nbt.3947

DO - 10.1038/nbt.3947

M3 - Article

C2 - 28829439

SN - 1546-1696

VL - 35

SP - 872-+

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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