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Widespread and Functional RNA Circularization in Localized Prostate Cancer
Open accessAbstract
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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Metadata
- 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)
- 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
- 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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