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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“18 Unlike linear mRNA, circular RNA does not require 5 ′ cap analogs, modified nucleotides such as N1-methyl-pseudouridine (m1 ψ ), 19 or a 3 ′ poly(A) tail for translation and stability.”
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Kang, E., Kang, D., Cho, Y. K., Shin, M., Boo, S. H., Chang, J., Kim, H., Jo, J. H., & Kim, Y. K. (2026) · Journal of Molecular Biology · doi:10.1016/j.jmb.2026.169828 · Cited by 2
In vitro transcribed circRNA as a therapeutic agent for cancer
Xu, S., Zhao, Y., Tang, Y., Fu, G., Qian, C., Li, F., Yang, Z., Cui, W., & Cai, W. (2026) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2026.04.019 · Cited by 3
Circular RNAs in animals: Biogenesis, function and cell fate control
Mohammad, R., Parfyonova, Y. V., & Сергеевич, С. Ю. (2026) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2026.195154 · Cited by 2
Circular RNA: the rings of power over cell
Gordiyuk, V. V., & Mankovska, O. S. (2020) · Biopolymers and Cell · doi:10.7124/bc.000a23 · Cited by 2
Loss of circIGF1R Suppresses Cardiomyocytes Proliferation by Sponging miR-362-5p
Zeng, J., Li, H.-J., Liu, K., Liang, C., Wu, H., Chen, W.-Y., Tang, M., Zhao, W., Cai, D., & Qi, X. (2023) · DNA and Cell Biology · doi:10.1089/dna.2022.0590 · Cited by 2
Comprehensive analysis of circular RNAs in nasopharyngeal cancer
Zhu, S., Wang, X., Xie, H., & Liu, L. (2023) · Genes & Genomics · doi:10.1007/s13258-023-01438-x · Cited by 2
Application of self-amplifying mRNA technology in the development of infectious disease vaccines
Li, X., Wang, X., & Zhang, B. (2023) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/tb-2023-0902 · Cited by 3
Screening radiation-differentially expressed circular RNAs and establishing dose classification models in the human lymphoblastoid cell line AHH-1
Tian, X.-L., Zhang, T., Cai, T.-J., Tian, M., & Liu, Q.-J. (2024) · International Journal of Radiation Biology · doi:10.1080/09553002.2024.2304850 · Cited by 2
“Several studies have corroborated that circRNAs possess longer half-lives than their corresponding linear RNAs (Jeck et al. 2013; Enuka et al. 2015).”
BackgroundInfluential
Integrative Analysis of Dog Serum‐Derived CircRNA Expression and Disease Severity, Inflammatory and Cardiac Damage Biomarkers Related to Canine Parvoviral Enteritis
Değirmençay, Ş., Özdemir, S., Küçükler, S., Bayat, R., & Kadak, M. (2025) · Veterinary Medicine and Science · doi:10.1002/vms3.70344 · Cited by 2
Biogenesis, function and role of circular RNA in Gall Bladder Carcinoma-A narrative review
Singh, A. K., Anand, N., & Srivastava, P. (2025) · Surgical and Experimental Pathology · doi:10.1186/s42047-025-00188-2 · Cited by 2
Non-coding RNAs in cardiac remodeling: diversity in composition and function
Chatterjee, E., & Das, S. (2022) · Current Opinion in Physiology · doi:10.1016/j.cophys.2022.100534 · Cited by 2
EcircPred: Sequence and secondary structural property based computational identification of exonic circular RNAs
Kumar, R., & Lahiri, T. (2018) · Computational Biology and Chemistry · doi:10.1016/j.compbiolchem.2018.08.002 · Cited by 2
Advances in studies of ncRNAs in the pathophysiology and treatment of spinal disease
Wang, J., Wei, W., Jia, Y., & Xi, Y. J. X. (2022) · General Physiology and Biophysics · doi:10.4149/gpb_2021039 · Cited by 2
CircRNA PDE3B regulates tumorigenicity via the miR-136-5p/MAP3K2 axis of esophageal squamous cell carcinoma.
Yue, W., Ye, Y., Chen, B., Wu, D., Wang, H., & Hui, G. (2023) · PubMed · doi:10.14670/hh-18-567 · Cited by 2
Changes in mRNA Degradation Efficiencies under Varying Conditions Are Regulated by Multiple Determinants in Arabidopsis thaliana
Ueno, D., Mikami, M., Yamasaki, S., Kaneko, M., Mukuta, T., Demura, T., & Kato, K. (2020) · Plant and Cell Physiology · doi:10.1093/pcp/pcaa147 · Cited by 3
Platelet-Derived circRNAs hsa_circ_0004771 and hsa_circ_0019120 Differentially Expressed in Colorectal Cancer and Polyps
Razzaghi, H., Heiat, M., Khoncheh, A., Abyazi, M. A., & Zaki‐Dizaji, M. (2024) · Reports of Biochemistry and Molecular Biology · doi:10.61186/rbmb.13.3.368 · Cited by 1
circRNA Vaccines
Saw, P. E., & Song, E. (2025) · Springer eBooks · doi:10.1007/978-981-96-3041-7_27 · Cited by 1
Pharmaceutical perspectives on oligonucleotide therapeutics and delivery systems
Staller, D. W., Gawargi, F. I., Panigrahi, S. S., Mishra, P. K., & Mahato, R. I. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100065 · Cited by 1
The Role of Long Non-Coding RNAs in Skeletal Muscle Pathophysiology: A Therapeutic Perspective
Scalabrin, S., Kavoosi, S., & Cagnin, S. (2025) · Genetics. · doi:10.5772/intechopen.1009960 · Cited by 1
CircRSF1: A potential diagnostic biomarker for primary Sjögren's syndrome
Wang, Y., Ma, H., Du, L., Chen, Q., Su, Y., Guan, C., & Wang, X. (2025) · Life Sciences · doi:10.1016/j.lfs.2025.123794 · Cited by 1
Circular RNAs as Biomarkers in the Diagnosis of Human Diseases
Özdemir, S. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-981-96-9428-0_14 · Cited by 1
The advantage of periodic over constant signalling in microRNA-mediated regulation
Ferro, E., Szischik, C. L., Ventura, A. C., & Bosia, C. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf867 · Cited by 2
“For instance, the half-lives of circRNAs were shown to be on average 2.5 times longer than those of mRNAs [ 70 ]— a difference compatible in our predictions with the possibility of exclusive regulation in frequency.”
Influential
circADAMTS12 Inhibits the Antitumor Activity of Microglia to Enable Metastatic Colonization in the Brain
Xia, Z., Liu, W., Guo, D., Chen, L., Zhao, Y., Zhao, Y., Zhang, J., Xia, L., Zou, Y., Sun, P., et al. (2025) · Cancer Research · doi:10.1158/0008-5472.can-25-0738 · Cited by 1
Non‑coding RNAs in epithelial‑mesenchymal transition of renal cell carcinoma (Review)
Liu, Z., Zhou, H., Shen, J., Qi, Y., Gong, X., & Zhang, C. L. (2025) · Molecular Medicine Reports · doi:10.3892/mmr.2025.13761 · Cited by 2
“…be regulated by other ncrnas, such as circrnas and lncrnas, these molecules can serve as natural inhibitors of oncogenic mirnas. compared with linear rnas, circrnas have a more stable molecular structure, making them less susceptible to degradation by rnases and prolonging their half‑life (147).”
Role of circular RNAs in regulating toxicity induced by cancer therapies
Xian, J., Qadir, J., Yang, B. B., & Ye, T. (2025) · Genes & Diseases · doi:10.1016/j.gendis.2025.101982 · Cited by 1
Circular RNA circHomer1 mediates hippocampal functions via ribonucleoprotein granule transport and dendritic targeting of synaptic RNAs
Cai, Y., Zheng, Z., Xu, H., Zhu, Y., Zepeda, J. C., Grueter, B. A., Wang, X., Ku, T., Duan, Y., Tsang, H. W. S., et al. (2026) · Science Advances · doi:10.1126/sciadv.ads7509 · Cited by 2
“Moreover, the enhanced stability of circHomer1 ( 18 , 77 ) suggests that potential molecular recycling could amplify its functional impact.”
A highly-efficient isothermal nano-detection platform coupling CRISPR/Cas technology for detection of circRNA
Sun, K., & Wu, H. (2026) · The Analyst · doi:10.1039/d6an00107f · Cited by 1
Circular RNAs: An Under-Recognized Part in Different Scenarios of Host–Parasite Interrelationships
Sharaf, M. S., Ashour, D. S., & Othman, A. A. (2026) · Pathogens · doi:10.3390/pathogens15030307 · Cited by 1
“Their defining feature, a stable closed-loop structure, imparts a significantly longer half-life and enhanced resistance to RNase degradation compared to linear RNAs [81].”
A conserved mammalian mecciRNA, mecciATP6, regulates mitochondrial homeostasis through interaction with HNRNPA3
Cao, X., Sui, J., Shan, G., & Liu, X. (2026) · Non-coding RNA Research · doi:10.1016/j.ncrna.2026.03.002 · Cited by 1
Delivery routes and circular mRNA vaccine architecture synergistically shape in vivo immune profiles
Shu, Y., Shen, T., Niu, Y., Xu, Y., Kong, X., Su, M., Yang, X., Yuan, L., Xie, S., Wang, J., et al. (2026) · Journal of Controlled Release · doi:10.1016/j.jconrel.2026.114912 · Cited by 1
The “cutting edge” of non-canonical RNA splicing
Guo, J. (2026) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2026.1719817 · Cited by 1
“…head-to-tail circular structure, circRNAs lack free 5 ′ and 3 ′ ends and canonical splice junctions, making them largely resistant to exonucleolytic degradation and thereby substantially more stable than their linear RNA counterparts (Jeck et al., 2013; Enuka et al., 2016; Kristensen et al., 2019).”
Circular RNAs in Intestinal Mucosal Homeostasis and Pathologies
Chung, H. K., Xiao, L., & Wang, J.-Y. (2026) · Non-Coding RNA · doi:10.3390/ncrna12030014 · Cited by 1
“Specific RBPs such as quaking can bind to motifs in flanking introns and function through protein–protein interactions, bridging distant splice sites [24,25].”
A circular RNA vaccine induces durable and cross-protective immunity against Neisseria meningitidis serogroup B in mice
Zhang, Q., Niu, D., Jia, Y., Lu, L., Qu, C., Qu, C., Sun, Z., Li, S., Liu, Z., Lv, J., et al. (2026) · PLoS Pathogens · doi:10.1371/journal.ppat.1013741 · Cited by 1
“Compared with linear mRNA counterparts, circular RNA exhibits significantly extended half-lives in mammalian cells [23].”

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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