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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Circular RNA circPOLR2A promotes clear cell renal cell carcinoma progression by facilitating the UBE3C-induced ubiquitination of PEBP1 and, thereby, activating the ERK signaling pathway
Xu, Z., Chen, S., Liu, R., Chen, H., Xu, B., Xu, W., & Chen, M. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01607-8 · Cited by 75
Self-citation
CircHERC1 promotes non-small cell lung cancer cell progression by sequestering FOXO1 in the cytoplasm and regulating the miR-142-3p-HMGB1 axis
Cui, Y., Wu, X., Jin, J., Man, W., Li, J., Li, X., Li, Y., He, Y., Liu, M., Zhong, R., et al. (2023) · Molecular Cancer · doi:10.1186/s12943-023-01888-7 · Cited by 76
“The landscape and action of circRNAs have been widely reported in various types of cancer [10], suggesting that circRNAs may be potential biomarkers or therapeutic targets [5, 11].”
BackgroundSelf-citation
The Circular RNA circHUWE1 Sponges the miR-29b-AKT3 Axis to Regulate Myoblast Development
Yue, B., Wang, J., Ru, W., Wu, J., Cao, X., Yang, H., Huang, Y., Lan, X., Lei, C., Huang, B., et al. (2020) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2019.12.039 · Cited by 71
“Among potential functions of circRNA, ceRNA effects, by which circRNA sponges miRNAs to alleviate degradation or translation repression of target mRNAs, have been increasingly described, especially in processes related to oncology.(22) Many studies showed that ceRNA crosstalk could be related to processes of myogenesi…”
Background
Circular RNAs drive oncogenic chromosomal translocations within the MLL recombinome in leukemia
Conn, V. M., Gabryelska, M., Toubia, J., Kirk, K., Gantley, L., Powell, J. A., Cildir, G., Marri, S., Liu, R., Stringer, B. W., et al. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.05.002 · Cited by 75
circPDE5A regulates prostate cancer metastasis via controlling WTAP-dependent N6-methyladenisine methylation of EIF3C mRNA
Ding, L., Wang, R., Zheng, Q., Shen, D., Wang, H., Lu, Z., Luo, W., Xie, H., Ren, L., Jiang, M., et al. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02391-5 · Cited by 70
Identification of CircRNA signature associated with tumor immune infiltration to predict therapeutic efficacy of immunotherapy
Dong, Y., Gao, Q., Chen, Y., Zhang, Z., Du, Y., Liu, Y., Zhang, G., Li, S., Wang, G., Chen, X., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38232-y · Cited by 71
“We performed overlap analyses among the two cohorts in this study, circAtlas 61 , and the MiOncoCirc 62,63 database.”
The influence of BRCA2 mutation on localized prostate cancer
Taylor, R. A., Fraser, M. E., Rebello, R. J., Boutros, P. C., Murphy, D. G., Bristow, R. G., & Risbridger, G. P. (2019) · Nature Reviews Urology · doi:10.1038/s41585-019-0164-8 · Cited by 68
Self-citation
A Multi-Omics Perspective of Quantitative Trait Loci in Precision Medicine
Ye, Y., Zhang, Z., Liu, Y., Diao, L., & Han, L. (2020) · Trends in Genetics · doi:10.1016/j.tig.2020.01.009 · Cited by 68
CRISPRi screens reveal a DNA methylation-mediated 3D genome dependent causal mechanism in prostate cancer
Ahmed, M., Soares, F., Xia, J., Yang, Y., Li, J., Guo, H., Su, P., Tian, Y., Lee, H. J., Wang, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21867-0 · Cited by 61
Self-citation
Sensitive, reliable and robust circRNA detection from RNA-seq with CirComPara2
Gaffo, E., Buratin, A., Molin, A. D., & Bortoluzzi, S. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab418 · Cited by 62
“GSE113120 (24 samples) 22Rv1, 42D, PC3, V16, LNCaP [48]”
Gastric cancer derived exosomes mediate the delivery of circRNA to promote angiogenesis by targeting miR-29a/VEGF axis in endothelial cells
Li, S., Li, J., Zhang, H., Zhang, Y., Wang, X., Yang, H., Zhou, Z., Hao, X., Ying, G., & Ba, Y. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.04.099 · Cited by 61
Self-citation
A urine extracellular vesicle circRNA classifier for detection of high-grade prostate cancer in patients with prostate-specific antigen 2–10 ng/mL at initial biopsy
He, Y., Tao, W., He, T., Wang, B.-Y., Tang, X., Zhang, L., Zhenquan, W., Deng, W., Zhang, L.-X., Shao, C., et al. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01388-6 · Cited by 60
The cell-free DNA methylome captures distinctions between localized and metastatic prostate tumors
Chen, S., Petricca, J., Ye, W., Guan, J., Zeng, Y., Cheng, N., Gong, L., Shen, S. Y., Hua, J. T., Crumbaker, M., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34012-2 · Cited by 66
Self-citation
ScRNA-seq revealed an immunosuppression state and tumor microenvironment heterogeneity related to lymph node metastasis in prostate cancer
Xin, S., Liu, X., Li, Z., Sun, X., Wang, R., Zhang, Z., Feng, X., Jin, L., Li, W., Tang, C., et al. (2023) · Experimental Hematology and Oncology · doi:10.1186/s40164-023-00407-0 · Cited by 62
“PCa is a malignant tumor with significant heterogeneity, including inter-tumor, intratumor, and clinical heterogeneity, which is manifested by spatial and clonal genomic diversity [9].”
Background
hsa_circ_0007841: A Novel Potential Biomarker and Drug Resistance for Multiple Myeloma
Gao, M., Li, C., Xiao, H., Dong, H., Jiang, S., Fu, Y., & Gong, L. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.01261 · Cited by 59
“They reported that circCSNK1G3 competitively bind to miR-181b/d and exhibit fundamental function on four prostate cancer cells (22).”
Background
An antisense circular RNA circSCRIB enhances cancer progression by suppressing parental gene splicing and translation
Ma, J., Du, W. W., Zeng, K., Wu, N., Fang, L., Lyu, J., Yee, A., & Yang, B. B. (2021) · Molecular Therapy · doi:10.1016/j.ymthe.2021.08.002 · Cited by 59
Understanding aberrant RNA splicing to facilitate cancer diagnosis and therapy
Dong, X., & Chen, R. (2019) · Oncogene · doi:10.1038/s41388-019-1138-2 · Cited by 57
“Two recent studies reported widespread expression of circRNAs in prostate tumor tissue samples [110, 111], advocating efforts to search for PCa-specific circRNAs detectable in patient plasma or urine.”
Background
RNA Dysregulation: An Expanding Source of Cancer Immunotherapy Targets
Pan, Y., Kadash-Edmondson, K. E., Wang, R., Phillips, J., Liu, S., Ribas, A., Aplenc, R., Witte, O. N., & Xing, Y. (2021) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2021.01.006 · Cited by 59
“CircRNAs perform biological functions in normal cells but can be dysregulated in cancer cells, resulting in distinct circRNA expression profiles in tumor tissues [36, 37].”
BackgroundSelf-citation
HNRNPM controls circRNA biogenesis and splicing fidelity to sustain cancer cell fitness
Ho, J., Tullio, F. D., Schwarz, M. C., Low, D. H. P., Incarnato, D., Gay, F. P. H., Tabaglio, T., Zhang, J., Wollmann, H., Chen, L., et al. (2021) · eLife · doi:10.7554/elife.59654 · Cited by 60
“Data for circRNA in PCa patients was obtained from Chen et al., 2019 , NCBI GEO repository accession number: GSE113120.”
InfluentialSelf-citation
CircRNA–miRNA networks in regulating bone disease
Huang, W., Wu, Y., Qiao, M., Xie, Z., Cen, X. B., Huang, X., & Zhao, Z. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30625 · Cited by 56
“Nowadays, we find circRNAs play vital roles in many physiological or pathological processes, such as regulation of the immune system, proliferation of cancer cells, and neuronal functions, and so on (S. Chen et al., 2019; Gokool et al., 2020; Z. Liu et al., 2019).”
Background
The landscape of RNA polymerase II–associated chromatin interactions in prostate cancer
Ramanand, S. G., Chen, Y., Yuan, J., Daescu, K., Lambros, M. B. K., Houlahan, K. E., Carreira, S., Yuan, W., Baek, G., Sharp, A., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci134260 · Cited by 54
Self-citation
Circular RNA CircNOLC1, Upregulated by NF-KappaB, Promotes the Progression of Prostate Cancer via miR-647/PAQR4 Axis
Chen, W., Cen, S., Zhou, X., Yang, T., Wu, K., Zou, L., Luo, J., Li, C., Lv, D., & Mao, X. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.624764 · Cited by 59
CircRNF220, not its linear cognate gene RNF220, regulates cell growth and is associated with relapse in pediatric acute myeloid leukemia
Liu, X., Liu, X., Cai, M., Luo, A., He, Y., Liu, S., Zhang, X., Yang, X., Xu, L., & Jiang, H. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01395-7 · Cited by 56
“RNA pulldown assay A pulldown assay was performed as previously reported [27].”
MethodSelf-citation
Circular RNAs
Li, D., Yang, Y. X., Li, Z.-Q., Li, L.-C., & Zhu, X. (2019) · Chinese Medical Journal · doi:10.1097/cm9.0000000000000465 · Cited by 55
The role of noncoding RNAs in epithelial cancer
Agostini, M., Ganini, C., Candi, E., & Melino, G. (2020) · Cell Death Discovery · doi:10.1038/s41420-020-0247-6 · Cited by 56
Circular RNA circMBOAT2 promotes prostate cancer progression via a miR-1271-5p/mTOR axis
Shi, J., Liu, C., Chen, C., Guo, K., Tang, Z., Luo, Y., Chen, L., Su, Y., & Xu, K. (2020) · Aging · doi:10.18632/aging.103432 · Cited by 55
“A recent study has revealed widespread expression and significant involvement of circRNAs in PCa [11].”
Background
CircRHBDD1 promotes immune escape via IGF2BP2/PD-L1 signaling and acts as a nanotherapeutic target in gastric cancer
Li, Y., Wang, Z., Gao, P., Cao, D., Dong, R., Zhu, M., Fei, Y., Zuo, X., & Cai, J. (2024) · Journal of Translational Medicine · doi:10.1186/s12967-024-05498-9 · Cited by 55
“With advances in high-throughput sequencing technology, many novel circRNAs have been identified in various cancers [38].”
Background
Pan-cancer pervasive upregulation of 3′ UTR splicing drives tumourigenesis
Chan, J. J., Zhang, B., Chew, X. H., Salhi, A., Kwok, Z. H., Lim, C. Y., Desi, N., Subramaniam, N., Siemens, A., Kinanti, T., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00913-z · Cited by 56
Circular RNAs in cardiovascular diseases
Mei, X., & Chen, S. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107991 · Cited by 55
Self-citation
Potential miRNA Use as a Biomarker: From Breast Cancer Diagnosis to Metastasis
Jordan‐Alejandre, E., Campos-Parra, A. D., Castro-López, D. L., & Silva-Cázares, M. B. (2023) · Cells · doi:10.3390/cells12040525 · Cited by 54
CircPVT1 promotes progression in clear cell renal cell carcinoma by sponging miR‐145‐5p and regulating TBX15 expression
Zheng, Z., Chen, Z., Zhong, Q., Zhu, D., Xie, Y., Shangguan, W., & Xie, W. (2021) · Cancer Science · doi:10.1111/cas.14814 · Cited by 51
Circular RNA circZNF566 Promotes Hepatocellular Carcinoma Progression by Sponging miR-4738-3p and Regulating TDO2 Expression
Li, S., Weng, J., Song, F., Li, L., Xiao, C. W., Yang, W., Zhu, Z., & Xu, J. (2019) · Cell Death and Disease · doi:10.1038/s41419-020-2616-8 · Cited by 51
The transcriptional landscape and biomarker potential of circular RNAs in prostate cancer
Hansen, E. B., Fredsøe, J., Okholm, T. L. H., Ulhøi, B. P., Klingenberg, S., Jensen, J. B., Kjems, J., Bouchelouche, K., Borre, M., Damgaard, C. K., et al. (2022) · Genome Medicine · doi:10.1186/s13073-021-01009-3 · Cited by 50
“Two previous studies have characterized the landscape of circRNA in cancer [10] and in PC in particular [11], demonstrating that circRNA expression is dysregulated in several malignancies, including in PC.”
Background
The circSPON2/miR-331-3p axis regulates PRMT5, an epigenetic regulator of CAMK2N1 transcription and prostate cancer progression
Yao, B., Zhu, S., Wei, X., Chen, M., Feng, Y., Li, Z., Xu, X., Zhang, Y., Wang, Y., Zhou, J., et al. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01598-6 · Cited by 48
“For example, circCSNK1G3 has been shown to promote the progression of PCa by interacting with miR-181 [52].”
BackgroundSelf-citation
Potential circRNA-disease association prediction using DeepWalk and network consistency projection
Li, G., Luo, J., Wang, D., Liang, C., Xiao, Q., Ding, P., & Chen, H. (2020) · Journal of Biomedical Informatics · doi:10.1016/j.jbi.2020.103624 · Cited by 48
Novel insights into the interaction between N6-methyladenosine modification and circular RNA
Xu, T., He, B., Sun, H., Xiong, M., Nie, J., Wang, S., & Pan, Y. (2022) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2022.01.007 · Cited by 48
A New Era of Prostate Cancer Precision Medicine
Malik, A., Srinivasan, S., & Batra, J. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.01263 · Cited by 49

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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