RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions

Alessandro Bonetti; Federico Agostini; Ana Maria Suzuki; Kosuke Hashimoto; Giovanni Pascarella; Juliette Gimenez; Leonie Roos; Alex J. Nash; Marco Ghilotti; Christopher J.F. Cameron; Matthew Valentine; Yulia A. Medvedeva; Shuhei Noguchi; Eneritz Agirre; Kaori Kashi; Samudyata; Joachim Luginbühl; Riccardo Cazzoli; Saumya Agrawal; Nicholas M. Luscombe; Mathieu Blanchette; Takeya Kasukawa; Michiel de Hoon; Erik Arner; Boris Lenhard; Charles Plessy; Gonçalo Castelo-Branco; Valerio Orlando; Piero Carninci

doi:10.1038/s41467-020-14337-6

RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions

Alessandro Bonetti, Federico Agostini, Ana Maria Suzuki, Kosuke Hashimoto, Giovanni Pascarella, Juliette Gimenez, Leonie Roos, Alex J. Nash, Marco Ghilotti, Christopher J.F. Cameron, Matthew Valentine, Yulia A. Medvedeva, Shuhei Noguchi, Eneritz Agirre, Kaori Kashi, Samudyata, Joachim Luginbühl, Riccardo Cazzoli, Saumya Agrawal, Nicholas M. LuscombeMathieu Blanchette, Takeya Kasukawa, Michiel de Hoon, Erik Arner, Boris Lenhard, Charles Plessy, Gonçalo Castelo-Branco, Valerio Orlando, Piero Carninci

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

96 Scopus citations

Abstract

Mammalian genomes encode tens of thousands of noncoding RNAs. Most noncoding transcripts exhibit nuclear localization and several have been shown to play a role in the regulation of gene expression and chromatin remodeling. To investigate the function of such RNAs, methods to massively map the genomic interacting sites of multiple transcripts have been developed; however, these methods have some limitations. Here, we introduce RNA And DNA Interacting Complexes Ligated and sequenced (RADICL-seq), a technology that maps genome-wide RNA–chromatin interactions in intact nuclei. RADICL-seq is a proximity ligation-based methodology that reduces the bias for nascent transcription, while increasing genomic coverage and unique mapping rate efficiency compared with existing methods. RADICL-seq identifies distinct patterns of genome occupancy for different classes of transcripts as well as cell type–specific RNA-chromatin interactions, and highlights the role of transcription in the establishment of chromatin structure.

Original language	English (US)
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-14337-6
State	Published - Feb 24 2020

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: This work was funded by a Research Grant from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, to the RIKEN Center for Life Science Technologies (http://www.mext.go.jp/en/). This work was also supported by the Francis Crick Institute, UK, which receives its core funding from Cancer Research UK (FC010110), the UK Medical Research Council (FC010110), and the Wellcome Trust (FC010110). N.M.L. is a Winton Group Leader in recognition of the Winton Charitable Foundation’s support towards the establishment of the Francis Crick Institute. N.M.L. isadditionally funded by a Wellcome Trust Joint Investigator Award (103760/Z/14/Z) and
the MRC eMedLab Medical Bioinformatics Infrastructure Award (MR/L016311/1). Work in G.C.-B.’s laboratory was supported by the European Union (Horizon 2020 European Research Council Consolidator Grant EPIScOPE), Swedish Research Council (no. 2015-03558), Swedish Brain Foundation (no. FO2017-0075), and Ming Wai Lau Centre for Reparative Medicine, Hong Kong. E.A. was supported by European Union, Horizon 2020, Marie-Skłodowska Curie Actions, grant SOLO no. 794689. Y.A.M. was partially supported by RSF grant 18-14-00240 and the Russian Ministry for Science and Higher Education. Work in V.O.’s laboratory (J.G. and V.O.) was supported by grants
from the European Union FP7 (InteGeR Marie Curie Initial Training Network and MODHEP), the Italian Ministry of Education, University and Research MIUR and the National Research Center CNR (Epigen), and grant from KAUST BAS01-01-37. Open access funding provided by Karolinska Institute.

Access to Document

10.1038/s41467-020-14337-6

https://repository.kaust.edu.sa/bitstream/10754/661945/1/s41467-020-14337-6.pdf

Cite this

Bonetti, A., Agostini, F., Suzuki, A. M., Hashimoto, K., Pascarella, G., Gimenez, J., Roos, L., Nash, A. J., Ghilotti, M., Cameron, C. J. F., Valentine, M., Medvedeva, Y. A., Noguchi, S., Agirre, E., Kashi, K., Samudyata, Luginbühl, J., Cazzoli, R., Agrawal, S., ... Carninci, P. (2020). RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions. Nature Communications, 11(1). https://doi.org/10.1038/s41467-020-14337-6

@article{ab1cf529a2ae4346ab8f8c663862a69e,

title = "RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions",

abstract = "Mammalian genomes encode tens of thousands of noncoding RNAs. Most noncoding transcripts exhibit nuclear localization and several have been shown to play a role in the regulation of gene expression and chromatin remodeling. To investigate the function of such RNAs, methods to massively map the genomic interacting sites of multiple transcripts have been developed; however, these methods have some limitations. Here, we introduce RNA And DNA Interacting Complexes Ligated and sequenced (RADICL-seq), a technology that maps genome-wide RNA–chromatin interactions in intact nuclei. RADICL-seq is a proximity ligation-based methodology that reduces the bias for nascent transcription, while increasing genomic coverage and unique mapping rate efficiency compared with existing methods. RADICL-seq identifies distinct patterns of genome occupancy for different classes of transcripts as well as cell type–specific RNA-chromatin interactions, and highlights the role of transcription in the establishment of chromatin structure.",

author = "Alessandro Bonetti and Federico Agostini and Suzuki, {Ana Maria} and Kosuke Hashimoto and Giovanni Pascarella and Juliette Gimenez and Leonie Roos and Nash, {Alex J.} and Marco Ghilotti and Cameron, {Christopher J.F.} and Matthew Valentine and Medvedeva, {Yulia A.} and Shuhei Noguchi and Eneritz Agirre and Kaori Kashi and Samudyata and Joachim Luginb{\"u}hl and Riccardo Cazzoli and Saumya Agrawal and Luscombe, {Nicholas M.} and Mathieu Blanchette and Takeya Kasukawa and Hoon, {Michiel de} and Erik Arner and Boris Lenhard and Charles Plessy and Gon{\c c}alo Castelo-Branco and Valerio Orlando and Piero Carninci",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: This work was funded by a Research Grant from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, to the RIKEN Center for Life Science Technologies (http://www.mext.go.jp/en/). This work was also supported by the Francis Crick Institute, UK, which receives its core funding from Cancer Research UK (FC010110), the UK Medical Research Council (FC010110), and the Wellcome Trust (FC010110). N.M.L. is a Winton Group Leader in recognition of the Winton Charitable Foundation{\textquoteright}s support towards the establishment of the Francis Crick Institute. N.M.L. isadditionally funded by a Wellcome Trust Joint Investigator Award (103760/Z/14/Z) and the MRC eMedLab Medical Bioinformatics Infrastructure Award (MR/L016311/1). Work in G.C.-B.{\textquoteright}s laboratory was supported by the European Union (Horizon 2020 European Research Council Consolidator Grant EPIScOPE), Swedish Research Council (no. 2015-03558), Swedish Brain Foundation (no. FO2017-0075), and Ming Wai Lau Centre for Reparative Medicine, Hong Kong. E.A. was supported by European Union, Horizon 2020, Marie-Sk{\l}odowska Curie Actions, grant SOLO no. 794689. Y.A.M. was partially supported by RSF grant 18-14-00240 and the Russian Ministry for Science and Higher Education. Work in V.O.{\textquoteright}s laboratory (J.G. and V.O.) was supported by grants from the European Union FP7 (InteGeR Marie Curie Initial Training Network and MODHEP), the Italian Ministry of Education, University and Research MIUR and the National Research Center CNR (Epigen), and grant from KAUST BAS01-01-37. Open access funding provided by Karolinska Institute.",

year = "2020",

month = feb,

day = "24",

doi = "10.1038/s41467-020-14337-6",

language = "English (US)",

volume = "11",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

}

Bonetti, A, Agostini, F, Suzuki, AM, Hashimoto, K, Pascarella, G, Gimenez, J, Roos, L, Nash, AJ, Ghilotti, M, Cameron, CJF, Valentine, M, Medvedeva, YA, Noguchi, S, Agirre, E, Kashi, K, Samudyata, Luginbühl, J, Cazzoli, R, Agrawal, S, Luscombe, NM, Blanchette, M, Kasukawa, T, Hoon, MD, Arner, E, Lenhard, B, Plessy, C, Castelo-Branco, G, Orlando, V & Carninci, P 2020, 'RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions', Nature Communications, vol. 11, no. 1. https://doi.org/10.1038/s41467-020-14337-6

TY - JOUR

T1 - RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions

AU - Bonetti, Alessandro

AU - Agostini, Federico

AU - Suzuki, Ana Maria

AU - Hashimoto, Kosuke

AU - Pascarella, Giovanni

AU - Gimenez, Juliette

AU - Roos, Leonie

AU - Nash, Alex J.

AU - Ghilotti, Marco

AU - Cameron, Christopher J.F.

AU - Valentine, Matthew

AU - Medvedeva, Yulia A.

AU - Noguchi, Shuhei

AU - Agirre, Eneritz

AU - Kashi, Kaori

AU - Samudyata,

AU - Luginbühl, Joachim

AU - Cazzoli, Riccardo

AU - Agrawal, Saumya

AU - Luscombe, Nicholas M.

AU - Blanchette, Mathieu

AU - Kasukawa, Takeya

AU - Hoon, Michiel de

AU - Arner, Erik

AU - Lenhard, Boris

AU - Plessy, Charles

AU - Castelo-Branco, Gonçalo

AU - Orlando, Valerio

AU - Carninci, Piero

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: This work was funded by a Research Grant from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, to the RIKEN Center for Life Science Technologies (http://www.mext.go.jp/en/). This work was also supported by the Francis Crick Institute, UK, which receives its core funding from Cancer Research UK (FC010110), the UK Medical Research Council (FC010110), and the Wellcome Trust (FC010110). N.M.L. is a Winton Group Leader in recognition of the Winton Charitable Foundation’s support towards the establishment of the Francis Crick Institute. N.M.L. isadditionally funded by a Wellcome Trust Joint Investigator Award (103760/Z/14/Z) and the MRC eMedLab Medical Bioinformatics Infrastructure Award (MR/L016311/1). Work in G.C.-B.’s laboratory was supported by the European Union (Horizon 2020 European Research Council Consolidator Grant EPIScOPE), Swedish Research Council (no. 2015-03558), Swedish Brain Foundation (no. FO2017-0075), and Ming Wai Lau Centre for Reparative Medicine, Hong Kong. E.A. was supported by European Union, Horizon 2020, Marie-Skłodowska Curie Actions, grant SOLO no. 794689. Y.A.M. was partially supported by RSF grant 18-14-00240 and the Russian Ministry for Science and Higher Education. Work in V.O.’s laboratory (J.G. and V.O.) was supported by grants from the European Union FP7 (InteGeR Marie Curie Initial Training Network and MODHEP), the Italian Ministry of Education, University and Research MIUR and the National Research Center CNR (Epigen), and grant from KAUST BAS01-01-37. Open access funding provided by Karolinska Institute.

PY - 2020/2/24

Y1 - 2020/2/24

N2 - Mammalian genomes encode tens of thousands of noncoding RNAs. Most noncoding transcripts exhibit nuclear localization and several have been shown to play a role in the regulation of gene expression and chromatin remodeling. To investigate the function of such RNAs, methods to massively map the genomic interacting sites of multiple transcripts have been developed; however, these methods have some limitations. Here, we introduce RNA And DNA Interacting Complexes Ligated and sequenced (RADICL-seq), a technology that maps genome-wide RNA–chromatin interactions in intact nuclei. RADICL-seq is a proximity ligation-based methodology that reduces the bias for nascent transcription, while increasing genomic coverage and unique mapping rate efficiency compared with existing methods. RADICL-seq identifies distinct patterns of genome occupancy for different classes of transcripts as well as cell type–specific RNA-chromatin interactions, and highlights the role of transcription in the establishment of chromatin structure.

AB - Mammalian genomes encode tens of thousands of noncoding RNAs. Most noncoding transcripts exhibit nuclear localization and several have been shown to play a role in the regulation of gene expression and chromatin remodeling. To investigate the function of such RNAs, methods to massively map the genomic interacting sites of multiple transcripts have been developed; however, these methods have some limitations. Here, we introduce RNA And DNA Interacting Complexes Ligated and sequenced (RADICL-seq), a technology that maps genome-wide RNA–chromatin interactions in intact nuclei. RADICL-seq is a proximity ligation-based methodology that reduces the bias for nascent transcription, while increasing genomic coverage and unique mapping rate efficiency compared with existing methods. RADICL-seq identifies distinct patterns of genome occupancy for different classes of transcripts as well as cell type–specific RNA-chromatin interactions, and highlights the role of transcription in the establishment of chromatin structure.

UR - http://hdl.handle.net/10754/661945

UR - http://www.nature.com/articles/s41467-020-14337-6

UR - http://www.scopus.com/inward/record.url?scp=85079776808&partnerID=8YFLogxK

U2 - 10.1038/s41467-020-14337-6

DO - 10.1038/s41467-020-14337-6

M3 - Article

C2 - 32094342

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

ER -

RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions

Abstract

Bibliographical note

Access to Document

Other files and links

Fingerprint

Cite this