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Article Open Access

circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression

  • Authors:
    • Yunzhe Mi
    • Xinle Wang
    • Han Song
    • Zhenyu Wu
    • Sainan Li
    • Fei Liu
    • Wei Liu
    • Meixiang Sang
    • Cuizhi Geng

  • View Affiliations / Copyright

    Affiliations: Breast Center, The Fourth Hospital of Hebei Medical University, Hebei Medical University, Shijiazhuang, Hebei 050017, P.R. China, Core Facilities and Centers, Institute of Medical and Health Science, Hebei Medical University, Shijiazhuang, Hebei 050017, P.R. China, Department of General Surgery, Hebei Key Laboratory of Colorectal Cancer Precision Diagnosis and Treatment, The First Hospital of Hebei Medical University, Shijiazhuang, Hebei 050031, P.R. China, Breast Center, The Fourth Hospital of Hebei Medical University, Hebei Medical University, Shijiazhuang, Hebei 050017, P.R. China, Research Center, The Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei 050017, P.R. China, Department of Breast Surgery, The Fourth Hospital of Shijiazhuang City, Shijiazhuang, Hebei 050000, P.R. China, Research Center, The Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei 050017, P.R. China
    Copyright: © Mi et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 446
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    Published online on: July 17, 2025
       https://doi.org/10.3892/ol.2025.15192
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Abstract

Circular (circ)RNA, a type of non‑coding RNA, serves a critical role in several diseases, including cancer. The present study aimed to elucidate the involvement of hsa_circ_0006522 (circEFR3A) in the advancement of breast cancer (BC) and uncover the molecular mechanisms behind its function. Fluorescence in situ hybridization (FISH) was performed on a tissue microarray to assess the expression and intracellular localization of circEFR3A. Kaplan‑Meier analysis and Cox proportional hazards model were utilized to evaluate the potential prognostic significance of circEFR3A in relation to the overall survival of patients with BC. The biological function was assessed through gain‑ and loss‑of‑function experiments. In addition, dual luciferase reporter assays, RNA immunoprecipitation, FISH and western blotting were performed to identify the interaction between circEFR3A, microRNA (miR)‑590‑3p and androgen receptors (ARs). Rescue experiments were performed to identify the hypothetical regulatory role of circEFR3A on BC progression in vivo and in vitro. The results of the present study demonstrated that circEFR3A was significantly upregulated in BC tissues and was associated with a poor prognosis in patients. Findings from the Cell Counting Kit‑8, colony formation and Transwell assays revealed that increased circEFR3A expression notably promoted BC cell proliferation, invasion and migration, as well as tumor growth in vivo. Mechanistically, circEFR3A was demonstrated to act as a molecular sponge for miR‑590‑3p in vitro and in vivo, thereby regulating AR expression and functioning as an oncogene. In summary, the findings of the present study indicate that circEFR3A acts as a novel oncogene in BC by sponging miR‑590‑3p, leading to the upregulation of AR expression and consequently driving BC progression.
View Figures

Figure 1

Characterization of circEFR3A in breast cancer cells. (A) Splicing site sequence and circularization schematic of circEFR3A. Divergent primers successfully amplified the circular RNA transcript circEFR3A in cDNA but not in gDNA. By contrast, convergent primers amplified the linear RNA transcript circEFR3A in both cDNA and gDNA. GAPDH served as an internal control. (B) Expression level of circEFR3A in SK-BR-3, MCF7, BT-549 and MDA-MB-453 cells compared with MDA-MB-231 cells. (C) Relative expression levels of circEFR3A and linear EFR3A mRNA were assessed using RT-qPCR following Actinomycin treatment in MDA-MB-231 and MDA-MB-453 cells at the indicated time points. (D) mRNA expression of circEFR3A and linear EFR3A in RNase R-treated breast cancer cells, assessed using RT-qPCR. (E) Subcellular localization of circEFR3A was determined using fluorescence in situ hybridization. Scale bar, 10 µm. *P<0.05; **P<0.01; ***P<0.001 vs. MDA-MB-231 cells or as indicated. Circ, circular; cDNA, complementary DNA; gDNA, genomic DNA; RT-qPCR, reverse transcription-quantitative PCR; ns, not significant; bp, base pairs.

Figure 2

circEFR3A is associated with breast cancer progression and promotes breast cancer cell proliferation, migration and invasion. (A) Fluorescence in situ hybridization analysis revealed the expression level of circEFR3A in breast cancer tissue specimens. Scale bar, 50 µm. (B) Survival analysis demonstrated that patients with breast cancer with high circEFR3A expression had a worse prognosis compared with those with low expression. (C) Quantification of circEFR3A Levels in MDA-MB-231 cells following transfection with circEFR3A siRNA. (D) CCK-8 assay results demonstrated that reduced circEFR3A expression significantly inhibited the proliferation of MDA-MB-231 cells. (E) Colony formation assay results revealed a significant reduction in the number of cell colonies following circEFR3A knockdown in breast cancer cells. Scale bar, 250 µm. (F) Transwell assay results indicated that knockdown of circEFR3A expression suppressed migration and invasion in MDA-MB-231 cells. Scale bar, 100 µm. (G) Level of circEFR3A in MDA-MB-453 cells after transfection with circEFR3A, assessed using reverse transcription-quantitative PCR. (H) CCK-8 assay results demonstrated that circEFR3A overexpression significantly enhanced the proliferation of MDA-MB-453 cells. (I) Colony formation assay results indicated a significant increase in the number of cell colonies following circEFR3A overexpression in MDA-MB-453 cells. Scale bar, 250 µm. (J) Transwell assay results demonstrated that circEFR3A overexpression promoted the migration and invasion of MDA-MB-453 cells. Scale bar, 100 µm.**P<0.01; ***P<0.001. Circ, circular; si, small interfering; CCK-8, Cell Counting Kit-8; OS, overall survival; NC, negative control; OD, optical density.

Figure 3

circEFR3A serves as a miR-590-3p sponge in breast cancer cells. (A) Predicting miRNA that bind to circEFR3A based on the TargetScan and miRanda databases. (B) Minimum free energy secondary structure of circEFR3A was predicted using the RNAfold web server, highlighting the regions relevant for miR-590-3p binding. (C) Luciferase assay was performed to determine the luciferase activity of circEFR3A when co-transfected with wild-type or mutant luc-circEFR3A vector and miR-NC or miR-590-3p mimics in MDA-MB-231 cells. (D) RIP assay was performed to assess the binding between circEFR3A and miR-590-3p, confirming their interaction. Experiments were repeated three times. (E) MDA-MB-231 cells were transfected with si-NC or si-circEFR3A, followed by reverse transcription-quantitative PCR to assess the relative expression levels of circEFR3A and miR-590-3p. (F) Fluorescence in situ hybridization demonstrated that circEFR3A and miR-590-3p were co-localized in the cytoplasm of MDA-MB-453 cells. Scale bar, 10 µm. **P<0.01; ***P<0.001. Circ, circular; miR/miRNA, microRNA; NC, negative control; RIP, RNA immunoprecipitation; si, small interfering.

Figure 4

miR-590-3p inhibits the proliferation, migration and invasion of breast cancer cells. (A) Expression levels of miR-590-3p in MDA-MB-231 cells, assessed using RT-qPCR. (B) CCK-8 assay results revealed that miR-590-3p low expression significantly enhanced the proliferation of MDA-MB-231 cells. (C) Colony formation assay results revealed a significant increase in the number of cell colonies following miR-590-3p downregulation in MDA-MB-231 cells. Scale bar, 250 µm. (D) Transwell assay results demonstrated that low miR-590-3p expression was significantly associated with an increase in the migration and invasion of MDA-MB-231 cells. Scale bar, 100 µm. (E) Expression of miR-590-3p in MDA-MB-453 cells, assessed using RT-qPCR. (F) CCK-8 assays revealed that miR-590-3p overexpression significantly promoted the proliferation of MDA-MB-453 cells. (G) Colony formation assay results indicated a significant increase in cell colony formation after miR-590-3p upregulation in MDA-MB-453 cells. Scale bar, 250 µm. (H) Transwell assay analysis indicated that miR-590-3p overexpression reduced the migration and invasion of MDA-MB-453 cells. Scale bar, 100 µm. **P<0.01; ***P<0.001. miR, microRNA; RT-qPCR, reverse transcription-quantitative PCR; CCK-8, Cell Counting Kit-8; NC, negative control; OD, optical density.

Figure 5

circEFR3A promotes the proliferation, migration and invasion of breast cancer via miR-590-3p. (A) Cell Counting Kit-8 and (B) colony formation assays demonstrated that transfection with circEFR3A alone significantly enhanced the proliferation of MDA-MB-453 cells. Additionally, the pro-proliferative effects of circEFR3A were partially reversed by miR-590-3p mimics. Transwell assay results indicated that transfection with circEFR3A alone significantly increased the (C) migration and (D) invasion rates of MDA-MB-453 cells. However, co-transfection with miR-590-3p mimics partially counteracted these enhanced effects. Scale bar, 100 µm. (E) Schematic diagram of grouping for the xenotransplantation model. (F) In the xenograft tumor experiment, mice were injected with MDA-MB-453 cells stably transfected with either pLC5-ciR + miR-NC, circEFR3A + miR-NC or circEFR3A + miR-590-3p. (G) Tumor mass and (H) volume were evaluated. **P<0.01; ***P<0.001. circ, circular; miR, microRNA; NC, negative control.

Figure 6

AR is a target gene of miR-590-3p. (A) Downstream signaling pathway of miR-590-3p, predicted using the miRPathDB database. (B) Potential target genes of miR-590-3p, identified using the Targetscan and miRPathDB databases, cross-referenced with key breast cancer genes from the GeneCards database and genes involved in the post-translational protein modification pathway, with intersecting genes visualized in a Venn diagram. (C) Predicted miR-590-3p binding site in AR 3′UTR, along with a diagrammatic depiction of the AR 3′UTR wild-type or mutant reporter constructs. (D) A luciferase reporter assay was performed to measure the activity of the wild-type or mutant AR 3′UTR vector in MDA-MB-453 cells that were co-transfected with either miR-590-3p mimics or a negative control vector. (E) Expression of AR mRNA in 1,085 breast cancer specimens and 291 normal specimens, determined based on the Gene Expression Profiling Interactive Analysis database. (F) Mice were injected with MDA-MB-453 cells stably transfected with either pLC5-ciR + miR-NC, circEFR3A + miR-NC or circEFR3A + miR-590-3p. The mRNA expression levels of AR were measured in tissues from three groups of nude mice. *P<0.05; **P<0.01. AR protein expression in MDA-MB-453 cells transfected with (G) miR-590-3p or miR-NC and (H) miR-NC or miR-590-3p + circEFR3A or pLC5-ciR+miR-NC was assessed using western blotting. AR, androgen receptor; miR, microRNA; circ, circular; NC, negative control.
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Copy and paste a formatted citation
Spandidos Publications style
Mi Y, Wang X, Song H, Wu Z, Li S, Liu F, Liu W, Sang M and Geng C: circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression. Oncol Lett 30: 446, 2025.
APA
Mi, Y., Wang, X., Song, H., Wu, Z., Li, S., Liu, F. ... Geng, C. (2025). circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression. Oncology Letters, 30, 446. https://doi.org/10.3892/ol.2025.15192
MLA
Mi, Y., Wang, X., Song, H., Wu, Z., Li, S., Liu, F., Liu, W., Sang, M., Geng, C."circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression". Oncology Letters 30.3 (2025): 446.
Chicago
Mi, Y., Wang, X., Song, H., Wu, Z., Li, S., Liu, F., Liu, W., Sang, M., Geng, C."circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression". Oncology Letters 30, no. 3 (2025): 446. https://doi.org/10.3892/ol.2025.15192
Copy and paste a formatted citation
x
Spandidos Publications style
Mi Y, Wang X, Song H, Wu Z, Li S, Liu F, Liu W, Sang M and Geng C: circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression. Oncol Lett 30: 446, 2025.
APA
Mi, Y., Wang, X., Song, H., Wu, Z., Li, S., Liu, F. ... Geng, C. (2025). circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression. Oncology Letters, 30, 446. https://doi.org/10.3892/ol.2025.15192
MLA
Mi, Y., Wang, X., Song, H., Wu, Z., Li, S., Liu, F., Liu, W., Sang, M., Geng, C."circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression". Oncology Letters 30.3 (2025): 446.
Chicago
Mi, Y., Wang, X., Song, H., Wu, Z., Li, S., Liu, F., Liu, W., Sang, M., Geng, C."circEFR3A promotes breast cancer progression by sponging miR‑590‑3p to upregulate androgen receptor expression". Oncology Letters 30, no. 3 (2025): 446. https://doi.org/10.3892/ol.2025.15192
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