Cited by 590Circular RNAs in diseasesRNA Research and SplicingCancer-related molecular mechanisms research

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Widespread and Functional RNA Circularization in Localized Prostate Cancer

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Chen, Sujun, Huang, Vincent, Xu, Xin, Livingstone, Julie, Soares, Fraser, Jeon, Jouhyun, Zeng, Yong, Hua, Junjie Tony, Petricca, Jessica, Guo, Haiyang, Wang, Miranda, Yousif, Fouad, Zhang, Yuzhe, Donmez, Nilgun, Ahmed, Musaddeque, Volik, Stas, Lapuk, Anna, Chua, Melvin L.K., Heisler, Lawrence E., Foucal, Adrien, Fox, Natalie S., Fraser, Michael, Bhandari, Vinayak, Shiah, Yu-Jia, Guan, Jiansheng, Li, Jixi, Orain, Michèle, Picard, Valérie, Hovington, Hélène, Bergeron, Alain, Lacombe, Louis, Fradet, Yves, Têtu, Bernard, Liu, Stanley, Feng, Felix, Wu, Xue, Shao, Yang W., Komor, Malgorzata A., Sahinalp, Cenk, Collins, Colin, Hoogstrate, Youri, de Jong, Mark, Fijneman, Remond J.A., Fei, Teng, Jenster, Guido, van der Kwast, Theodorus, Bristow, Robert G., Boutros, Paul C., He, Housheng Hansen·2019·Cell

DOI 10.1016/j.cell.2019.01.025

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Abstract

The cancer transcriptome is remarkably complex, including low-abundance transcripts, many not polyadenylated. To fully characterize the transcriptome of localized prostate cancer, we performed ultra-deep total RNA-seq on 144 tumors with rich clinical annotation. This revealed a linear transcriptomic subtype associated with the aggressive intraductal carcinoma sub-histology and a fusion profile that differentiates localized from metastatic disease. Analysis of back-splicing events showed widespread RNA circularization, with the average tumor expressing 7,232 circular RNAs (circRNAs). The degree of circRNA production was correlated to disease progression in multiple patient cohorts. Loss-of-function screening identified 11.3% of highly abundant circRNAs as essential for cell proliferation; for ∼90% of these, their parental linear transcripts were not essential. Individual circRNAs can have distinct functions, with circCSNK1G3 promoting cell growth by interacting with miR-181. These data advocate for adoption of ultra-deep RNA-seq without poly-A selection to interrogate both linear and circular transcriptomes.

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See all 590

Authors: Chen, S., Huang, V., Xu, X., Livingstone, J., Soares, F., Jeon, J., Zeng, Y., Hua, J. T., Petricca, J., Guo, H., Wang, M., Yousif, F., Zhang, Y., Donmez, N., Ahmed, M., Volik, S., Lapuk, A., Chua, M. L. K., Heisler, L. E., Foucal, A., Fox, N. S., Fraser, M., Bhandari, V., Shiah, Y.-J., Guan, J., Li, J., Orain, M., Picard, V., Hovington, H., Bergeron, A., Lacombe, L., Fradet, Y., Têtu, B., Liu, S., Feng, F., Wu, X., Shao, Y. W., Komor, M. A., Sahinalp, C., Collins, C., Hoogstrate, Y., de Jong, M., Fijneman, R. J. A., Fei, T., Jenster, G., van der Kwast, T., Bristow, R. G., Boutros, P. C., & He, H. H.
Affiliations: Ontario Institute for Cancer Research (CA)
University Health Network (CA)
Vancouver Prostate Centre (CA)
Fudan University (CN)
Centre de recherche du CHU de Québec-Université Laval (CA)
Sunnybrook Health Science Centre (CA)
University of California, San Francisco (US)
Nanjing Medical University (CN)
The Netherlands Cancer Institute (NL)
University of British Columbia (CA)
Erasmus MC (NL)
Northeastern University (CN)
Corresponding author: Boutros, Paul C.
He, Housheng Hansen
ORCID: Chen, Sujun
Huang, Vincent
Xu, Xin
Livingstone, Julie
Soares, Fraser
Jeon, Jouhyun
Zeng, Yong
Hua, Junjie Tony
Guo, Haiyang
Zhang, Yuzhe
Ahmed, Musaddeque
Lapuk, Anna
Chua, Melvin L.K.
Heisler, Lawrence E.
Foucal, Adrien
Fox, Natalie S.
Fraser, Michael
Bhandari, Vinayak
Shiah, Yu-Jia
Guan, Jiansheng
Li, Jixi
Orain, Michèle
Picard, Valérie
Hovington, Hélène
Bergeron, Alain
Lacombe, Louis
Fradet, Yves
Têtu, Bernard
Liu, Stanley
Feng, Felix
Wu, Xue
Shao, Yang W.
Komor, Malgorzata A.
Collins, Colin
Hoogstrate, Youri
Fijneman, Remond J.A.
Fei, Teng
Jenster, Guido
Bristow, Robert G.
Boutros, Paul C.
He, Housheng Hansen
Venue: Cell
Publisher: Elsevier BV
Published: 2019-02
Volume: 176
Issue: 4
Pages: 831-843.e22
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2019.01.025
OpenAlex: W2913336364
Cited by: 544
References: 91
Citations by year: 2026: 13 · 2025: 26 · 2024: 107 · 2023: 44 · 2022: 105 · 2021: 110 · 2020: 83 · 2019: 55
FWCI: 31.45
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 371 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Research Explorer (The University of Manchester) (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
Funders: Princess Margaret Cancer Foundation (886012001223)
Canada Foundation for Innovation and Ontario Research Fund (CFI32372)
NSERC (498706)
Canadian Cancer Society (705649, 703800)
Prostate Cancer Canada (RS2014-01, RS2016-1022)
CIHR (146586, 142246, 152863, 152864, 159567)
Ontario Institute for Cancer Research
TFRI
OMIR
Shanghai Committee of Science and Technology (18430711400)
University of Toronto
STARS21
CTMM (03O-402)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Circular RNAs in diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
Keywords: circular RNA, RNA circularization, localized prostate cancer, back-splicing, intraductal carcinoma, metastatic prostate cancer, miR-181, cell proliferation, transcriptomic subtypes
MeSH terms: Genetic Profile, RNA, Circular, Humans, Male, Prostate, Prostatic Neoplasms, RNA, RNA Splicing, Sequence Analysis, RNA, Gene Expression Profiling, RNA, Untranslated, MicroRNAs, HEK293 Cells, Transcriptome

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Widespread and Functional RNA Circularization in Localized Prostate Cancer

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