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Functional annotation of human long noncoding RNAs using chromatin conformation data

Saumya Agrawal, Tanvir Alam, Masaru Koido, View ORCID ProfileIvan V. Kulakovskiy, Jessica Severin, Imad Abugessaisa, Andrey Buyan, Josee Dostie, Masayoshi Itoh, Naoto Kondo, Yunjing Li, Mickaël Mendez, Jordan A. Ramilowski, Ken Yagi, Kayoko Yasuzawa, Chi Wai Yip, Yasushi Okazaki, View ORCID ProfileMichael M. Hoffman, Lisa Strug, Chung Chau Hon, View ORCID ProfileChikashi Terao, View ORCID ProfileTakeya Kasukawa, Vsevolod J. Makeev, Jay W. Shin, View ORCID ProfilePiero Carninci, View ORCID ProfileMichiel JL de Hoon
doi: https://doi.org/10.1101/2021.01.13.426305
Saumya Agrawal
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Tanvir Alam
2College of Science and Engineering, Hamad Bin Khalifa University, Doha, Qatar
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Masaru Koido
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
3Institute of Medical Science, The University of Tokyo, Tokyo, Japan
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Ivan V. Kulakovskiy
4Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia
5Institute of Protein Research, Russian Academy of Sciences, Pushchino, Russia
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  • ORCID record for Ivan V. Kulakovskiy
Jessica Severin
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Imad Abugessaisa
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Andrey Buyan
5Institute of Protein Research, Russian Academy of Sciences, Pushchino, Russia
6Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, Russia
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Josee Dostie
7Department of Biochemistry, Rosalind and Morris Goodman Cancer Research Center, McGill University, Montréal, Québec, Canada
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Masayoshi Itoh
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
8RIKEN Preventive Medicine and Diagnosis Innovation Program, Wako, Japan
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Naoto Kondo
9RIKEN Center for Life Science Technologies, Yokohama, Japan
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Yunjing Li
10Division of Biostatistics, Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada
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Mickaël Mendez
11Department of Computer Science, University of Toronto, Toronto, Ontario, Canada
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Jordan A. Ramilowski
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
12Advanced Medical Research Center, Yokohama City University, Yokohama, Japan
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Ken Yagi
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Kayoko Yasuzawa
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Chi Wai Yip
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Yasushi Okazaki
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Michael M. Hoffman
11Department of Computer Science, University of Toronto, Toronto, Ontario, Canada
13Princess Margaret Cancer Centre, Toronto, Ontario, Canada
14Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada
15Vector Institute, Toronto, Ontario, Canada
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  • For correspondence: michiel.dehoon@riken.jp
Lisa Strug
10Division of Biostatistics, Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada
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Chung Chau Hon
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Chikashi Terao
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Takeya Kasukawa
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Vsevolod J. Makeev
4Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia
16Moscow Institute of Physics and Technology, Dolgoprudny, Russia
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Jay W. Shin
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Piero Carninci
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Michiel JL de Hoon
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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  • ORCID record for Michiel JL de Hoon
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Abstract

Transcription of the human genome yields mostly long non-coding RNAs (lncRNAs). Systematic functional annotation of lncRNAs is challenging due to their low expression level, cell type-specific occurrence, poor sequence conservation between orthologs, and lack of information about RNA domains. Currently, 95% of human lncRNAs have no functional characterization. Using chromatin conformation and Cap Analysis of Gene Expression (CAGE) data in 18 human cell types, we systematically located genomic regions in spatial proximity to lncRNA genes and identified functional clusters of interacting protein-coding genes, lncRNAs and enhancers. Using these clusters we provide a cell type-specific functional annotation for 7,651 out of 14,198 (53.88%) lncRNAs. LncRNAs tend to have specialized roles in the cell type in which it is first expressed, and to incorporate more general functions as its expression is acquired by multiple cell types during evolution. By analyzing RNA-binding protein and RNA-chromatin interaction data in the context of the spatial genomic interaction map, we explored mechanisms by which these lncRNAs can act.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://fantom.gsc.riken.jp/zenbu/reports/#FANTOM6_HiC

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted January 14, 2021.
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Functional annotation of human long noncoding RNAs using chromatin conformation data
Saumya Agrawal, Tanvir Alam, Masaru Koido, Ivan V. Kulakovskiy, Jessica Severin, Imad Abugessaisa, Andrey Buyan, Josee Dostie, Masayoshi Itoh, Naoto Kondo, Yunjing Li, Mickaël Mendez, Jordan A. Ramilowski, Ken Yagi, Kayoko Yasuzawa, Chi Wai Yip, Yasushi Okazaki, Michael M. Hoffman, Lisa Strug, Chung Chau Hon, Chikashi Terao, Takeya Kasukawa, Vsevolod J. Makeev, Jay W. Shin, Piero Carninci, Michiel JL de Hoon
bioRxiv 2021.01.13.426305; doi: https://doi.org/10.1101/2021.01.13.426305
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Functional annotation of human long noncoding RNAs using chromatin conformation data
Saumya Agrawal, Tanvir Alam, Masaru Koido, Ivan V. Kulakovskiy, Jessica Severin, Imad Abugessaisa, Andrey Buyan, Josee Dostie, Masayoshi Itoh, Naoto Kondo, Yunjing Li, Mickaël Mendez, Jordan A. Ramilowski, Ken Yagi, Kayoko Yasuzawa, Chi Wai Yip, Yasushi Okazaki, Michael M. Hoffman, Lisa Strug, Chung Chau Hon, Chikashi Terao, Takeya Kasukawa, Vsevolod J. Makeev, Jay W. Shin, Piero Carninci, Michiel JL de Hoon
bioRxiv 2021.01.13.426305; doi: https://doi.org/10.1101/2021.01.13.426305

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