Antisense-oligonucleotide-mediated perturbation of long non-coding RNA reveals functional features in stem cells and across cell types

Chi Wai Yip; Chung-Chau Hon; Kayoko Yasuzawa; Divya M. Sivaraman; Jordan A. Ramilowski; Youtaro Shibayama; Saumya Agrawal; Anika V Prabhu; Callum Parr; Jessica Severin; Yan Jun Lan; Josée Dostie; Andreas Petri; Hiromi Nishiyori-Sueki; Michihira Tagami; Masayoshi Itoh; Fernando López-Redondo; Tsukasa Kouno; Jen-Chien Chang; Joachim Luginbühl; Masaki Kato; Mitsuyoshi Murata; Wing Hin Yip; Xufeng Shu; Imad Abugessaisa; Akira Hasegawa; Harukazu Suzuki; Sakari Kauppinen; Ken Yagi; Yasushi Okazaki; Takeya Kasukawa; Michiel de Hoon; Piero Carninci; Jay W. Shin

doi:10.1016/j.celrep.2022.111893

Antisense-oligonucleotide-mediated perturbation of long non-coding RNA reveals functional features in stem cells and across cell types

Chi Wai Yip, Chung-Chau Hon, Kayoko Yasuzawa, Divya M. Sivaraman, Jordan A. Ramilowski, Youtaro Shibayama, Saumya Agrawal, Anika V Prabhu, Callum Parr, Jessica Severin, Yan Jun Lan, Josée Dostie, Andreas Petri, Hiromi Nishiyori-Sueki, Michihira Tagami, Masayoshi Itoh, Fernando López-Redondo, Tsukasa Kouno, Jen-Chien Chang, Joachim LuginbühlMasaki Kato, Mitsuyoshi Murata, Wing Hin Yip, Xufeng Shu, Imad Abugessaisa, Akira Hasegawa, Harukazu Suzuki, Sakari Kauppinen, Ken Yagi, Yasushi Okazaki, Takeya Kasukawa, Michiel de Hoon, Piero Carninci, Jay W. Shin^*

^*Kontaktforfatter

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

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Abstract

Within the scope of the FANTOM6 consortium, we perform a large-scale knockdown of 200 long non-coding RNAs (lncRNAs) in human induced pluripotent stem cells (iPSCs) and systematically characterize their roles in self-renewal and pluripotency. We find 36 lncRNAs (18%) exhibiting cell growth inhibition. From the knockdown of 123 lncRNAs with transcriptome profiling, 36 lncRNAs (29.3%) show molecular phenotypes. Integrating the molecular phenotypes with chromatin-interaction assays further reveals cis- and trans-interacting partners as potential primary targets. Additionally, cell-type enrichment analysis identifies lncRNAs associated with pluripotency, while the knockdown of LINC02595, CATG00000090305.1, and RP11-148B6.2 modulates colony formation of iPSCs. We compare our results with previously published fibroblasts phenotyping data and find that 2.9% of the lncRNAs exhibit a consistent cell growth phenotype, whereas we observe 58.3% agreement in molecular phenotypes. This highlights that molecular phenotyping is more comprehensive in revealing affected pathways.

Originalsprog	Engelsk
Artikelnummer	111893
Tidsskrift	Cell reports
Vol/bind	41
Udgave nummer	13
ISSN	2211-1247
DOI	https://doi.org/10.1016/j.celrep.2022.111893
Status	Udgivet - 27 dec. 2022

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10.1016/j.celrep.2022.111893Licens: CC BY-NC-ND 4.0

Yip et al. (2022). Antisense-oligonucleotide-mediated perturbation of long non-coding RNA reveals functional features in stem cells and across cell typesForlagets udgivne version, 7,01 MBLicens: CC BY-NC-ND 4.0

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Yip, C. W., Hon, C.-C., Yasuzawa, K., Sivaraman, D. M., Ramilowski, J. A., Shibayama, Y., Agrawal, S., Prabhu, A. V., Parr, C., Severin, J., Lan, Y. J., Dostie, J., Petri, A., Nishiyori-Sueki, H., Tagami, M., Itoh, M., López-Redondo, F., Kouno, T., Chang, J.-C., ... Shin, J. W. (2022). Antisense-oligonucleotide-mediated perturbation of long non-coding RNA reveals functional features in stem cells and across cell types. Cell reports, 41(13), Artikel 111893. https://doi.org/10.1016/j.celrep.2022.111893

@article{571001232566469a95340fbe9f544bdc,

title = "Antisense-oligonucleotide-mediated perturbation of long non-coding RNA reveals functional features in stem cells and across cell types",

abstract = "Within the scope of the FANTOM6 consortium, we perform a large-scale knockdown of 200 long non-coding RNAs (lncRNAs) in human induced pluripotent stem cells (iPSCs) and systematically characterize their roles in self-renewal and pluripotency. We find 36 lncRNAs (18%) exhibiting cell growth inhibition. From the knockdown of 123 lncRNAs with transcriptome profiling, 36 lncRNAs (29.3%) show molecular phenotypes. Integrating the molecular phenotypes with chromatin-interaction assays further reveals cis- and trans-interacting partners as potential primary targets. Additionally, cell-type enrichment analysis identifies lncRNAs associated with pluripotency, while the knockdown of LINC02595, CATG00000090305.1, and RP11-148B6.2 modulates colony formation of iPSCs. We compare our results with previously published fibroblasts phenotyping data and find that 2.9% of the lncRNAs exhibit a consistent cell growth phenotype, whereas we observe 58.3% agreement in molecular phenotypes. This highlights that molecular phenotyping is more comprehensive in revealing affected pathways.",

keywords = "Embryonic Stem Cells/metabolism, Gene Expression Profiling/methods, Humans, Induced Pluripotent Stem Cells/metabolism, Oligonucleotides, Antisense, RNA, Long Noncoding/genetics, CAGE, CP: Stem cell research, iPSC, functional annotation, gapmer ASO, CP: Molecular biology, long non-coding RNA",

author = "Yip, {Chi Wai} and Chung-Chau Hon and Kayoko Yasuzawa and Sivaraman, {Divya M.} and Ramilowski, {Jordan A.} and Youtaro Shibayama and Saumya Agrawal and Prabhu, {Anika V} and Callum Parr and Jessica Severin and Lan, {Yan Jun} and Jos{\'e}e Dostie and Andreas Petri and Hiromi Nishiyori-Sueki and Michihira Tagami and Masayoshi Itoh and Fernando L{\'o}pez-Redondo and Tsukasa Kouno and Jen-Chien Chang and Joachim Luginb{\"u}hl and Masaki Kato and Mitsuyoshi Murata and Yip, {Wing Hin} and Xufeng Shu and Imad Abugessaisa and Akira Hasegawa and Harukazu Suzuki and Sakari Kauppinen and Ken Yagi and Yasushi Okazaki and Takeya Kasukawa and {de Hoon}, Michiel and Piero Carninci and Shin, {Jay W.}",

year = "2022",

month = dec,

day = "27",

doi = "10.1016/j.celrep.2022.111893",

language = "English",

volume = "41",

journal = "Cell reports",

issn = "2211-1247",

publisher = "Cell Press",

number = "13",

}

Yip, CW, Hon, C-C, Yasuzawa, K, Sivaraman, DM, Ramilowski, JA, Shibayama, Y, Agrawal, S, Prabhu, AV, Parr, C, Severin, J, Lan, YJ, Dostie, J, Petri, A, Nishiyori-Sueki, H, Tagami, M, Itoh, M, López-Redondo, F, Kouno, T, Chang, J-C, Luginbühl, J, Kato, M, Murata, M, Yip, WH, Shu, X, Abugessaisa, I, Hasegawa, A, Suzuki, H, Kauppinen, S, Yagi, K, Okazaki, Y, Kasukawa, T, de Hoon, M, Carninci, P & Shin, JW 2022, 'Antisense-oligonucleotide-mediated perturbation of long non-coding RNA reveals functional features in stem cells and across cell types', Cell reports, bind 41, nr. 13, 111893. https://doi.org/10.1016/j.celrep.2022.111893

TY - JOUR

T1 - Antisense-oligonucleotide-mediated perturbation of long non-coding RNA reveals functional features in stem cells and across cell types

AU - Yip, Chi Wai

AU - Hon, Chung-Chau

AU - Yasuzawa, Kayoko

AU - Sivaraman, Divya M.

AU - Ramilowski, Jordan A.

AU - Shibayama, Youtaro

AU - Agrawal, Saumya

AU - Prabhu, Anika V

AU - Parr, Callum

AU - Severin, Jessica

AU - Lan, Yan Jun

AU - Dostie, Josée

AU - Petri, Andreas

AU - Nishiyori-Sueki, Hiromi

AU - Tagami, Michihira

AU - Itoh, Masayoshi

AU - López-Redondo, Fernando

AU - Kouno, Tsukasa

AU - Chang, Jen-Chien

AU - Luginbühl, Joachim

AU - Kato, Masaki

AU - Murata, Mitsuyoshi

AU - Yip, Wing Hin

AU - Shu, Xufeng

AU - Abugessaisa, Imad

AU - Hasegawa, Akira

AU - Suzuki, Harukazu

AU - Kauppinen, Sakari

AU - Yagi, Ken

AU - Okazaki, Yasushi

AU - Kasukawa, Takeya

AU - de Hoon, Michiel

AU - Carninci, Piero

AU - Shin, Jay W.

PY - 2022/12/27

Y1 - 2022/12/27

N2 - Within the scope of the FANTOM6 consortium, we perform a large-scale knockdown of 200 long non-coding RNAs (lncRNAs) in human induced pluripotent stem cells (iPSCs) and systematically characterize their roles in self-renewal and pluripotency. We find 36 lncRNAs (18%) exhibiting cell growth inhibition. From the knockdown of 123 lncRNAs with transcriptome profiling, 36 lncRNAs (29.3%) show molecular phenotypes. Integrating the molecular phenotypes with chromatin-interaction assays further reveals cis- and trans-interacting partners as potential primary targets. Additionally, cell-type enrichment analysis identifies lncRNAs associated with pluripotency, while the knockdown of LINC02595, CATG00000090305.1, and RP11-148B6.2 modulates colony formation of iPSCs. We compare our results with previously published fibroblasts phenotyping data and find that 2.9% of the lncRNAs exhibit a consistent cell growth phenotype, whereas we observe 58.3% agreement in molecular phenotypes. This highlights that molecular phenotyping is more comprehensive in revealing affected pathways.

AB - Within the scope of the FANTOM6 consortium, we perform a large-scale knockdown of 200 long non-coding RNAs (lncRNAs) in human induced pluripotent stem cells (iPSCs) and systematically characterize their roles in self-renewal and pluripotency. We find 36 lncRNAs (18%) exhibiting cell growth inhibition. From the knockdown of 123 lncRNAs with transcriptome profiling, 36 lncRNAs (29.3%) show molecular phenotypes. Integrating the molecular phenotypes with chromatin-interaction assays further reveals cis- and trans-interacting partners as potential primary targets. Additionally, cell-type enrichment analysis identifies lncRNAs associated with pluripotency, while the knockdown of LINC02595, CATG00000090305.1, and RP11-148B6.2 modulates colony formation of iPSCs. We compare our results with previously published fibroblasts phenotyping data and find that 2.9% of the lncRNAs exhibit a consistent cell growth phenotype, whereas we observe 58.3% agreement in molecular phenotypes. This highlights that molecular phenotyping is more comprehensive in revealing affected pathways.

KW - Embryonic Stem Cells/metabolism

KW - Gene Expression Profiling/methods

KW - Humans

KW - Induced Pluripotent Stem Cells/metabolism

KW - Oligonucleotides, Antisense

KW - RNA, Long Noncoding/genetics

KW - CAGE

KW - CP: Stem cell research

KW - iPSC

KW - functional annotation

KW - gapmer ASO

KW - CP: Molecular biology

KW - long non-coding RNA

UR - http://www.scopus.com/inward/record.url?scp=85144903471&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2022.111893

DO - 10.1016/j.celrep.2022.111893

M3 - Journal article

C2 - 36577377

SN - 2211-1247

VL - 41

JO - Cell reports

JF - Cell reports

IS - 13

M1 - 111893

ER -

Antisense-oligonucleotide-mediated perturbation of long non-coding RNA reveals functional features in stem cells and across cell types

Abstract

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