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Systematic identification of cis-interacting lncRNAs and their targets

Saumya Agrawal, View ORCID ProfileIvan V. Kulakovskiy, Jessica Severin, Masaru Koido, View ORCID ProfileTanvir Alam, View ORCID ProfileImad Abugessaisa, Andrey Buyan, Howard Y. Chang, Josee Dostie, Masayoshi Itoh, Juha Kere, Naoto Kondo, Yunjing Li, View ORCID ProfileVsevolod J. Makeev, Mickaël Mendez, Yasushi Okazaki, Jordan A. Ramilowski, Andrey I. Sigorskikh, Lisa J. Strug, Ken Yagi, Kayoko Yasuzawa, View ORCID ProfileChi Wai Yip, Chung Chau Hon, View ORCID ProfileMichael M. Hoffman, View ORCID ProfileChikashi Terao, View ORCID ProfileTakeya Kasukawa, 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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Ivan V. Kulakovskiy
19autosome.org
20FANTOM Consortium
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Jessica Severin
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Masaru Koido
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
2Institute of Medical Science, The University of Tokyo, Tokyo, Japan
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Tanvir Alam
3College of Science and Engineering, Hamad Bin Khalifa University, Doha, Qatar
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Imad Abugessaisa
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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Andrey Buyan
19autosome.org
20FANTOM Consortium
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Howard Y. Chang
4Center for Personal Dynamic Regulome, Stanford University, Stanford, California, USA
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Josee Dostie
5Department 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
6RIKEN Preventive Medicine and Diagnosis Innovation Program, Wako, Japan
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Juha Kere
7Department of Biosciences and Nutrition, Karolinska Institutet, Huddinge, Sweden
8Stem Cells and Metabolism Research Program, University of Helsinki and Folkhälsan Research Center, Helsinki, Finland
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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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Vsevolod J. Makeev
20FANTOM Consortium
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Mickaël Mendez
11Department of Computer Science, University of Toronto, Toronto, Ontario, Canada
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Yasushi Okazaki
1RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
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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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Andrey I. Sigorskikh
20FANTOM Consortium
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Lisa J. Strug
10Division of Biostatistics, Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada
11Department of Computer Science, University of Toronto, Toronto, Ontario, Canada
13Division of Biostatistics, University of Toronto, Ontario, Canada
14The Centre for Applied Genomics and Program in Genetics and Genome Biology, The Hospital for Sick Children, Toronto, Ontario, Canada
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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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Chung Chau Hon
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
15Princess Margaret Cancer Centre, Toronto, Ontario, Canada
16Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada
17Vector Institute, Toronto, Ontario, Canada
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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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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
18Human Technopole, Milan, Italy
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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
  • For correspondence: michiel.dehoon@riken.jp
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Abstract

The human genome is pervasively transcribed and produces a wide variety of long non-coding RNAs (lncRNAs), constituting the majority of transcripts across human cell types. Studying 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. LncRNAs direct the regulatory factors in the locations that are in cis to their transcription sites. We designed a model to predict if an lncRNA acts in cis based on its features and trained it using RNA-chromatin interaction data. The trained model is cell type-independent and does not require RNA-chromatin data. Combining RNA-chromatin and Hi-C data, we showed that lncRNA-chromatin binding sites are determined by chromosome conformation. For each lncRNA, the spatially proximal genes were identified as their potential targets by combining Hi-C and Cap Analysis Gene Expression (CAGE) data in 18 human cell types. RNA-protein and RNA-chromatin interaction data suggested that lncRNAs act as scaffolds to recruit regulatory proteins to target promoters and enhancers. We provide the data through an interactive visualization web portal at https://fantom.gsc.riken.jp/zenbu/reports/#F6_3D_lncRNA.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The revised version includes a model to predict if an lncRNA acts in cis. The model was trained using RNA-chromatin interaction data.

  • https://fantom.gsc.riken.jp/zenbu/reports/#F6_3D_lncRNA

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 July 12, 2022.
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Systematic identification of cis-interacting lncRNAs and their targets
Saumya Agrawal, Ivan V. Kulakovskiy, Jessica Severin, Masaru Koido, Tanvir Alam, Imad Abugessaisa, Andrey Buyan, Howard Y. Chang, Josee Dostie, Masayoshi Itoh, Juha Kere, Naoto Kondo, Yunjing Li, Vsevolod J. Makeev, Mickaël Mendez, Yasushi Okazaki, Jordan A. Ramilowski, Andrey I. Sigorskikh, Lisa J. Strug, Ken Yagi, Kayoko Yasuzawa, Chi Wai Yip, Chung Chau Hon, Michael M. Hoffman, Chikashi Terao, Takeya Kasukawa, 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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Systematic identification of cis-interacting lncRNAs and their targets
Saumya Agrawal, Ivan V. Kulakovskiy, Jessica Severin, Masaru Koido, Tanvir Alam, Imad Abugessaisa, Andrey Buyan, Howard Y. Chang, Josee Dostie, Masayoshi Itoh, Juha Kere, Naoto Kondo, Yunjing Li, Vsevolod J. Makeev, Mickaël Mendez, Yasushi Okazaki, Jordan A. Ramilowski, Andrey I. Sigorskikh, Lisa J. Strug, Ken Yagi, Kayoko Yasuzawa, Chi Wai Yip, Chung Chau Hon, Michael M. Hoffman, Chikashi Terao, Takeya Kasukawa, 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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