Cited by 765Circular RNAs in diseasesRNA Research and SplicingCancer-related molecular mechanisms research

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Circular RNAs are long-lived and display only minimal early alterations in response to a growth factor

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Enuka, Yehoshua, Lauriola, Mattia, Feldman, Morris E., Sas-Chen, Aldema, Ulitsky, Igor, Yarden, Yosef·2016·Nucleic Acids Research

DOI 10.1093/nar/gkv1367PMC PMC4756822

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Abstract

Circular RNAs (circRNAs) are widespread circles of non-coding RNAs with largely unknown function. Because stimulation of mammary cells with the epidermal growth factor (EGF) leads to dynamic changes in the abundance of coding and non-coding RNA molecules, and culminates in the acquisition of a robust migratory phenotype, this cellular model might disclose functions of circRNAs. Here we show that circRNAs of EGF-stimulated mammary cells are stably expressed, while mRNAs and microRNAs change within minutes. In general, the circRNAs we detected are relatively long-lived and weakly expressed. Interestingly, they are almost ubiquitously co-expressed with the corresponding linear transcripts, and the respective, shared promoter regions are more active compared to genes producing linear isoforms with no detectable circRNAs. These findings imply that altered abundance of circRNAs, unlike changes in the levels of other RNAs, might not play critical roles in signaling cascades and downstream transcriptional networks that rapidly commit cells to specific outcomes.

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Additional file 2 of The circular RNA circZFR phosphorylates Rb promoting cervical cancer progression by regulating the SSBP1/CDK2/cyclin E1 complex
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Additional file 3 of Circular RNA EPHA3 suppresses progression and metastasis in prostate cancer through the miR-513a-3p/BMP2 axis
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Additional file 3 of The circular RNA circCPE regulates myoblast development by sponging miR-138
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Additional file 9 of CircFAM73A promotes the cancer stem cell-like properties of gastric cancer through the miR-490-3p/HMGA2 positive feedback loop and HNRNPK-mediated β-catenin stabilization
Xia, Y., Lv, J., Jiang, T., Li, B., Li, Y., He, Z., Xuan, Z., Sun, G., Wang, S., Li, Z., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14234983
Additional file 4 of Islet-expressed circular RNAs are associated with type 2 diabetes status in human primary islets and in peripheral blood
Haque, S., Ames, R. M., Moore, K., Lee, B. P., Jeffery, N. M., & Harries, L. W. (2020) · Figshare · doi:10.6084/m9.figshare.12160503
Additional file 5 of The circular RNA circZFR phosphorylates Rb promoting cervical cancer progression by regulating the SSBP1/CDK2/cyclin E1 complex
Zhou, M., Yang, Z., 王丹波, Chen, P., & Zhang, Y. (2021) · Figshare · doi:10.6084/m9.figshare.13669320
Additional file 3 of As a biomarker for gastric cancer, circPTPN22 regulates the progression of gastric cancer through the EMT pathway
Ma, S., Kong, S., Gu, X., Xu, Y., Tao, M., Shen, L., Shen, X., & Ju, S. (2021) · Figshare · doi:10.6084/m9.figshare.13558311
Additional file 4 of The circular RNA circCPE regulates myoblast development by sponging miR-138
Ru, W., Qi, A., Shen, X., Yue, B., Zhang, X., Wang, J., Cao, H., & Chen, H. (2021) · Figshare · doi:10.6084/m9.figshare.16584674
Additional file 8 of Islet-expressed circular RNAs are associated with type 2 diabetes status in human primary islets and in peripheral blood
Haque, S., Ames, R. M., Moore, K., Lee, B. P., Jeffery, N. M., & Harries, L. W. (2020) · Figshare · doi:10.6084/m9.figshare.12160539
Additional file 5 of The circular RNA circCPE regulates myoblast development by sponging miR-138
Ru, W., Qi, A., Shen, X., Yue, B., Zhang, X., Wang, J., Cao, H., & Chen, H. (2021) · Figshare · doi:10.6084/m9.figshare.16584677
Additional file 1 of Blood RNA-Seq profiling reveals a set of circular RNAs differentially expressed in frail individuals
Iparraguirre, L., Alberro, A., Iñiguez, S. G., Muñoz‐Culla, M., Vergara, I., Matheu, A., & Otaegui, D. (2024) · Figshare · doi:10.6084/m9.figshare.26603491
Additional file 5 of Circular RNA EPHA3 suppresses progression and metastasis in prostate cancer through the miR-513a-3p/BMP2 axis
Feng, H., Deng, Z., Peng, W., Wei, X. W., Liu, J., & Wang, T. (2023) · Figshare · doi:10.6084/m9.figshare.22721341
Additional file 1 of The circular RNA circCPE regulates myoblast development by sponging miR-138
Ru, W., Qi, A., Shen, X., Yue, B., Zhang, X., Wang, J., Cao, H., & Chen, H. (2021) · Figshare · doi:10.6084/m9.figshare.16584665
Additional file 2 of Circular RNA EPHA3 suppresses progression and metastasis in prostate cancer through the miR-513a-3p/BMP2 axis
Feng, H., Deng, Z., Peng, W., Wei, X., Liu, J., & Wang, T. (2023) · Figshare · doi:10.6084/m9.figshare.22721332
Additional file 8 of Circular RNA EPHA3 suppresses progression and metastasis in prostate cancer through the miR-513a-3p/BMP2 axis
Feng, H., Deng, Z., Peng, W., Wei, X., Liu, J., & Wang, T. (2023) · Figshare · doi:10.6084/m9.figshare.22721350
Additional file 5 of Blood RNA-Seq profiling reveals a set of circular RNAs differentially expressed in frail individuals
Iparraguirre, L., Alberro, A., Iñiguez, S. G., Muñoz‐Culla, M., Vergara, I., Matheu, A., & Otaegui, D. (2024) · Figshare · doi:10.6084/m9.figshare.26603503
Additional file 6 of CircFAM73A promotes the cancer stem cell-like properties of gastric cancer through the miR-490-3p/HMGA2 positive feedback loop and HNRNPK-mediated β-catenin stabilization
Xia, Y., Lv, J., Jiang, T., Li, B., Li, Y., He, Z., Xuan, Z., Sun, G., Wang, S., Li, Z., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14234974
Additional file 7 of CircFAM73A promotes the cancer stem cell-like properties of gastric cancer through the miR-490-3p/HMGA2 positive feedback loop and HNRNPK-mediated β-catenin stabilization
Xia, Y., Lv, J., Jiang, T., Li, B., Li, Y., He, Z., Xuan, Z., Sun, G., Wang, S., Li, Z., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14234977
Additional file 7 of Blood RNA-Seq profiling reveals a set of circular RNAs differentially expressed in frail individuals
Iparraguirre, L., Alberro, A., Iñiguez, S. G., Muñoz‐Culla, M., Vergara, I., Matheu, A., & Otaegui, D. (2024) · Figshare · doi:10.6084/m9.figshare.26603509
Additional file 12 of CircFAM73A promotes the cancer stem cell-like properties of gastric cancer through the miR-490-3p/HMGA2 positive feedback loop and HNRNPK-mediated β-catenin stabilization
Xia, Y., Lv, J., Jiang, T., Li, B., Li, Y., He, Z., Xuan, Z., Sun, G., Wang, S., Li, Z., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14234953
Additional file 3 of CircFAM73A promotes the cancer stem cell-like properties of gastric cancer through the miR-490-3p/HMGA2 positive feedback loop and HNRNPK-mediated β-catenin stabilization
Xia, Y., Lv, J., Jiang, T., Li, B., Li, Y., He, Z., Xuan, Z., Sun, G., Wang, S., Li, Z., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14234965
Additional file 8 of CircFAM73A promotes the cancer stem cell-like properties of gastric cancer through the miR-490-3p/HMGA2 positive feedback loop and HNRNPK-mediated β-catenin stabilization
Xia, Y., Lv, J., Jiang, T., Li, B., Li, Y., He, Z., Xuan, Z., Sun, G., Wang, S., Li, Z., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14234980

Authors: Enuka, Y., Lauriola, M., Feldman, M. E., Sas-Chen, A., Ulitsky, I., & Yarden, Y.
Affiliations: Weizmann Institute of Science (IL)
Corresponding author: Yarden, Yosef
ORCID: Enuka, Yehoshua
Lauriola, Mattia
Ulitsky, Igor
Yarden, Yosef
Venue: Nucleic Acids Research
Publisher: Oxford University Press (OUP)
Published: 2015-12-10
Volume: 44
Issue: 3
Pages: 1370-1383
ISSN: 0305-1048 (ISSN-L)
1362-4962
DOI: 10.1093/nar/gkv1367
PMC: PMC4756822
OpenAlex: W2285247593
Cited by: 757
References: 64
Citations by year: 2026: 66 · 2025: 91 · 2024: 100 · 2023: 105 · 2022: 93 · 2021: 107 · 2020: 68 · 2019: 57 · 2018: 33 · 2017: 26 · 2016: 9
FWCI: 9.85
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc
creativecommons.org/licenses/by-nc/4.0/ (vor, 340 d)
Locations: Nucleic Acids Research (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, cc-by-nc)
HighWire Press Open Archive (submittedVersion)
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, epidermal growth factor, mammary epithelial cells, RNA stability, non-coding RNA, microRNA, cell migration, growth factor signaling
MeSH terms: RNA, Circular, Breast, Cell Line, Epidermal Growth Factor, Epithelial Cells, Humans, RNA, RNA, Messenger, Gene Expression, Transforming Growth Factor alpha, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, RNA Stability, MicroRNAs, Heparin-binding EGF-like Growth Factor

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Circular RNAs are long-lived and display only minimal early alterations in response to a growth factor

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