Skip to main content
SpringerLink
Log in

Circular RNA circCCNB1 inhibits the migration and invasion of nasopharyngeal carcinoma through binding and stabilizing TJP1 mRNA

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Nasopharyngeal carcinoma (NPC) is a malignant tumor that usually occurs in people from Southeast Asia and Southern China. NPC is prone to migration and invasion, leading to poor prognosis. A large number of circular RNAs (circRNAs) exacerbate the process of metastasis in NPC; however, their underlying mechanisms remain unclear. We found that the circular RNA circCCNB1, encoded by the oncogene CCNB1, was downregulated in NPC biopsies and cell lines. In vitro assays show that circCCNB1 inhibits NPC cell migration and invasion. Moreover, circCCNB1 induces a protein, nuclear factor 90 (NF90), to bind and prolong the half-life of tight junction protein 1 (TJP1) mRNA. Upregulation of TJP1 enhances tight junctions between cancer cells and inhibits NPC cell migration and invasion. This study reveals a novel biological function of circCCNB1 in the migration and invasion of NPC by enhancing the tight junctions of cancer cells by binding to NF90 proteins and TJP1 mRNA, and may provide a potential therapeutic target for NPC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Availability of data and materials

All data that support the findings of this study are available from the corresponding authors upon reasonable request.

References

  • Ao, X., Li, X., Chen, Y., Zang, Z., Guo, W., and Liang, J. (2020). TMEM98 mRNA promotes proliferation and invasion of gastric cells by directly interacting with NF90 protein. Cell Biol Int 44, 1820–1830.

    Article  PubMed  CAS  Google Scholar 

  • Aussem, A., de Morais, S.R., and Corbex, M. (2012). Analysis of nasopharyngeal carcinoma risk factors with Bayesian networks. Artif Intell Med 54, 53–62.

    Article  PubMed  Google Scholar 

  • Chen, E.B., Qin, X., Peng, K., Li, Q., Tang, C., Wei, Y.C., Yu, S., Gan, L., and Liu, T.S. (2019). HnRNPR-CCNBl/CENPF axis contributes to gastric cancer proliferation and metastasis. Aging 11, 7473–7491.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ding, D., Huang, H., Li, Q., Yu, W., Wang, C., Ma, H., Wu, J., Dang, Y., Yu, L., and Jiang, W. (2020). NF90 stabilizes cyclin E1 mRNA through phosphorylation of NF90-Ser382 by CDK2. Cell Death Discov 6, 3.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ding, N.H., Zhang, L., Xiao, Z., Rong, Z.X., Li, Z., He, J., Chen, L., Ou, D. M., Liao, W.H., and Sun, L.Q. (2018). NEK4 kinase regulates EMT to promote lung cancer metastasis. J Cell Mol Med 22, 5877–5887.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fan, C., Wang, J., Tang, Y., Zhang, S., Xiong, F., Guo, C., Zhou, Y., Li, Z., Li, X., Li, Y., et al. (2020). Upregulation of long non-coding RNA LOC284454 may serve as a new serum diagnostic biomarker for head and neck cancers. BMC Cancer 20, 917.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fan, C., Qu, H., Xiong, F., Tang, Y., Tang, T., Zhang, L., Mo, Y., Li, X., Guo, C., Zhang, S., et al. (2021a). CircARHGAP12 promotes nasopharyngeal carcinoma migration and invasion via ezrin-mediated cytoskeletal remodeling. Cancer Lett 496, 41–56.

    Article  PubMed  CAS  Google Scholar 

  • Fan, C., Zhang, S., Gong, Z., Li, X., Xiang, B., Deng, H., Zhou, M., Li, G., Li, Y., Xiong, W., et al. (2021b). Emerging role of metabolic reprogramming in tumor immune evasion and immunotherapy. Sci China Life Sci 64, 534–547.

    Article  PubMed  Google Scholar 

  • Fan, C.M., Wang, J.P., Tang, Y.Y., Zhao, J., He, S.Y., Xiong, F., Guo, C., Xiang, B., Zhou, M., Li, X.L., et al. (2019). circMAN1A2 could serve as a novel serum biomarker for malignant tumors. Cancer Sci 110, 2180–2188.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fang, L., Du, W.W., Lyu, J., Dong, J., Zhang, C., Yang, W., He, A., Kwok, Y.S.S., Ma, J., Wu, N., et al. (2018). Enhanced breast cancer progression by mutant p53 is inhibited by the circular RNA circ-Ccnb1. Cell Death Differ 25, 2195–2208.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fang, L., Du, W.W., Awan, F.M., Dong, J., and Yang, B.B. (2019). The circular RNA circ-Ccnb1 dissociates Ccnb1/Cdk1 complex suppressing cell invasion and tumorigenesis. Cancer Lett 459, 216–226.

    Article  PubMed  CAS  Google Scholar 

  • Gao, X., Xia, X., Li, F., Zhang, M., Zhou, H., Wu, X., Zhong, J., Zhao, Z., Zhao, K., Liu, D., et al. (2021). Circular RNA-encoded oncogenic Ecadherin variant promotes glioblastoma tumorigenicity through activation of EGFR-STAT3 signalling. Nat Cell Biol 23, 278–291.

    Article  PubMed  CAS  Google Scholar 

  • Ge, J., Wang, J., Xiong, F., Jiang, X., Zhu, K., Wang, Y., Mo, Y., Gong, Z., Zhang, S., He, Y., et al. (2021). Epstein-Barr virus-encoded circular RNA circBART2.2 promotes immune escape of nasopharyngeal carcinoma by regulating PD-L1. Cancer Res 81, 5074–5088.

    Article  PubMed  CAS  Google Scholar 

  • Hildesheim, A., and Wang, C.P. (2012). Genetic predisposition factors and nasopharyngeal carcinoma risk: a review of epidemiological association studies, 2000–2011. Semin Cancer Biol 22, 107–116.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jiang, W., Huang, H., Ding, L., Zhu, P., Saiyin, H., Ji, G., Zuo, J., Han, D., Pan, Y., Ding, D., et al. (2015). Regulation of cell cycle of hepatocellular carcinoma by NF90 through modulation of cyclin E1 mRNA stability. Oncogene 34, 4460–4470.

    Article  PubMed  CAS  Google Scholar 

  • Jiang, X., Deng, X., Wang, J., Mo, Y., Shi, L., Wei, F., Zhang, S., Gong, Z., He, Y., Xiong, F., et al. (2022). BPIFB1 inhibits vasculogenic mimicry via downregulation of GLUT1-mediated H3K27 acetylation in nasopharyngeal carcinoma. Oncogene 41, 233–245.

    Article  PubMed  Google Scholar 

  • Karthi, S., Rajeshwari, M., Francis, A., Saravanan, M., Varalakshmi, P., Houlden, H., Thangaraj, K., and Ashokkumar, B. (2017). 3′-UTR SNP rs2229611 in G6PC1 affects mRNA stability, expression and Glycogen Storage Disease type-Ia risk. Clin Chim Acta 471, 46–54.

    Article  PubMed  CAS  Google Scholar 

  • Ke, J., Shao, W., Jiang, Y., Xu, J., Li, F., and Qin, J. (2018). MicroRNA-103 regulates tumorigenesis in colorectal cancer by targeting ZO-1. Mol Med Report 17, 783–788.

    CAS  Google Scholar 

  • Kuwano, Y., Pullmann Jr., R., Marasa, B.S., Abdelmohsen, K., Lee, E.K., Yang, X., Martindale, J.L., Zhan, M., and Gorospe, M. (2010). NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif. Nucleic Acids Res 38, 225–238.

    Article  PubMed  CAS  Google Scholar 

  • Li, P., Zhu, K., Mo, Y., Deng, X., Jiang, X., Shi, L., Guo, C., Zhang, W., Zeng, Z., Li, G., et al. (2021). Research progress of circRNAs in head and neck cancers. Front Oncol 11, 616202.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang, W.C., Wong, C.W., Liang, P.P., Shi, M., Cao, Y., Rao, S.T., Tsui, S. K.W., Waye, M.M.Y., Zhang, Q., Fu, W.M., et al. (2019). Translation of the circular RNA circβ-catenin promotes liver cancer cell growth through activation of the Wnt pathway. Genome Biol 20, 84.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, Z., Zou, D., Yang, X., Xue, X., Zuo, L., Zhou, Q., Hu, R., and Wang, Y. (2017). Melatonin inhibits colon cancer RKO cell migration by downregulating Rho-associated protein kinase expression via the p38/MAPK signaling pathway. Mol Med Rep 16, 9383–9392.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mattern, J., Roghi, C.S., Hurtz, M., Knäuper, V., Edwards, D.R., and Poghosyan, Z. (2019). ADAM15 mediates upregulation of Claudin-1 expression in breast cancer cells. Sci Rep 9, 12540.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mo, Y., Wang, Y., Zhang, S., Xiong, F., Yan, Q., Jiang, X., Deng, X., Wang, Y., Fan, C., Tang, L., et al. (2021). Circular RNA circRNF13 inhibits proliferation and metastasis of nasopharyngeal carcinoma via SUMO2. Mol Cancer 20, 112.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ouhara, K., Munenaga, S., Kajiya, M., Takeda, K., Matsuda, S., Sato, Y., Hamamoto, Y., Iwata, T., Yamasaki, S., Akutagawa, K., et al. (2018). The induced RNA-binding protein, HuR, targets 3′-UTR region of IL-6 mRNA and enhances its stabilization in periodontitis. Clin Exp Immunol 192, 325–336.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ouyang, J., Zhang, Y., Xiong, F., Zhang, S., Gong, Z, Yan, Q, He, Y., Wei, F., Zhang, W., Zhou, M., et al. (2021a). The role of alternative splicing in human cancer progression. Am J Cancer Res 11, 4642–4667.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ouyang, J., Zhong, Y., Zhang, Y., Yang, L., Wu, P., Hou, X., Xiong, F., Li, X., Zhang, S., Gong, Z., et al. (2021b). Long non-coding RNAs are involved in alternative splicing and promote cancer progression. Br J Cancer doi:https://doi.org/10.1038/s41416-021-01600-w.

  • Qu, H., Fan, C., Chen, M., Zhang, X., Yan, Q., Wang, Y., Zhang, S., Gong, Z., Shi, L., Li, X., et al. (2021). Recent advances of fluorescent biosensors based on cyclic signal amplification technology in biomedical detection. J Nanobiotechnol 19, 403.

    Article  CAS  Google Scholar 

  • Qu, H., Chen, M., Ge, J., Zhang, X., He, S., Xiong, F., Yan, Q., Zhang, S., Gong, Z., Guo, C., et al. (2022). A fluorescence strategy for circRNA quantification in tumor cells based on T7 nuclease-assisted cycling enzymatic amplification. Anal Chim Acta 1189, 339210.

    Article  PubMed  CAS  Google Scholar 

  • Ren, D., Hua, Y., Yu, B., Ye, X., He, Z., Li, C., Wang, J., Mo, Y., Wei, X., Chen, Y., et al. (2020). Predictive biomarkers and mechanisms underlying resistance to PD1/PD-L1 blockade cancer immunotherapy. Mol Cancer 19, 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Runkle, E.A., and Mu, D. (2013). Tight junction proteins: from barrier to tumorigenesis. Cancer Lett 337, 41–48.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanger, H.L., Klotz, G., Riesner, D., Gross, H.J., and Kleinschmidt, A.K. (1976). Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci USA 73, 3852–3856.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saw, P.E., Xu, X., Chen, J., and Song, E.W. (2021). Non-coding RNAs: the new central dogma of cancer biology. Sci China Life Sci 64, 22–50.

    Article  PubMed  CAS  Google Scholar 

  • Song, D., Huang, H., Wang, J., Zhao, Y., Hu, X., He, F., Yu, L., and Wu, J. (2017). NF90 regulates PARP1 mRNA stability in hepatocellular carcinoma. Biochem Biophys Res Commun 488, 211–217.

    Article  PubMed  CAS  Google Scholar 

  • Tang, L., Xiong, W., Zhang, L., Wang, D., Wang, Y., Wu, Y., Wei, F., Mo, Y., Hou, X., Shi, L., et al. (2021). circSETD3 regulates MAPRE1 through miR-615–5p and miR-1538 sponges to promote migration and invasion in nasopharyngeal carcinoma. Oncogene 40, 307–321.

    Article  PubMed  CAS  Google Scholar 

  • Wang, J., Ge, J., Wang, Y., Xiong, F., Guo, J., Jiang, X., Zhang, L., Deng, X., Gong, Z., Zhang, S., et al. (2022a). EBV miRNAs BART11 and BART17–3p promote immune escape through the enhancer-mediated transcription of PD-L1. Nat Commun 13, 866.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Bao, Y., Zhang, S., and Wang, Z. (2020). Splicing dysregulation in cancer: from mechanistic understanding to a new class of therapeutic targets. Sci China Life Sci 63, 469–484.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Y., Mo, Y., Peng, M., Zhang, S., Gong, Z., Yan, Q., Tang, Y., He, Y., Liao, Q., Li, X., et al. (2022b). The influence of circular RNAs on autophagy and disease progression. Autophagy 18, 240–253.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Y., Yan, Q., Mo, Y., Liu, Y., Wang, Y., Zhang, S., Guo, C., Wang, F., Li, G., Zeng, Z., et al. (2022c). Splicing factor derived circular RNA circCAMSAP1 accelerates nasopharyngeal carcinoma tumorigenesis via a SERPINH1/c-Myc positive feedback loop. Mol Cancer 21, 62.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wen, X., Liu, X., Mao, Y.P., Yang, X.J., Wang, Y.Q., Zhang, P.P., Lei, Y., Hong, X.H., He, Q.M., Ma, J., et al. (2018). Long non-coding RNA DANCR stabilizes HIF-1α and promotes metastasis by interacting with NF90/NF45 complex in nasopharyngeal carcinoma. Theranostics 8, 5676–5689.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, J., Zhou, X.J., Sun, X., Xia, T.S., Li, X.X., Shi, L., Zhu, L., Zhou, W. B., Wei, J.F., and Ding, Q. (2017). RBM38 is involved in TGF-β-induced epithelial-to-mesenchymal transition by stabilising zonula occludens-1 mRNA in breast cancer. Br J Cancer 117, 675–684.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, P., Mo, Y., Peng, M., Tang, T., Zhong, Y., Deng, X., Xiong, F., Guo, C., Wu, X., Li, Y., et al. (2020a). Emerging role of tumor-related functional peptides encoded by lncRNA and circRNA. Mol Cancer 19, 22.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, T.H., Shi, L., Lowe, A.W., Nicolls, M.R., and Kao, P.N. (2019). Inducible expression of immediate early genes is regulated through dynamic chromatin association by NF45/ILF2 and NF90/NF110/ILF3. PLoS ONE 14, e0216042.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, Y., Wang, D., Wei, F., Xiong, F., Zhang, S., Gong, Z., Shi, L., Li, X., Xiang, B., Ma, J., et al. (2020b). EBV-miR-BART12 accelerates migration and invasion in EBV-associated cancer cells by targeting tubulin polymerization-promoting protein 1. FASEB J 34, 16205–16223.

    Article  PubMed  CAS  Google Scholar 

  • Xia, X., Li, X., Li, F., Wu, X., Zhang, M., Zhou, H., Huang, N., Yang, X., Xiao, F., Liu, D., et al. (2019). A novel tumor suppressor protein encoded by circular AKT3 RNA inhibits glioblastoma tumorigenicity by competing with active phosphoinositide-dependent Kinase-1. Mol Cancer 18, 131.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie, B.S., Wang, Y.Q., Lin, Y., Zhao, C.C., Mao, Q., Feng, J.F., Cao, J.Y., Gao, G.Y., and Jiang, J.Y. (2018). Circular RNA expression profiles alter significantly after traumatic brain injury in rats. J Neurotrauma 35, 1659–1666.

    Article  PubMed  Google Scholar 

  • Xie, L., Shi, F., Li, Y., Li, W., Yu, X., Zhao, L., Zhou, M., Hu, J., Luo, X., Tang, M., et al. (2020). Drp1-dependent remodeling of mitochondrial morphology triggered by EBV-LMP1 increases cisplatin resistance. Sig Transduct Target Ther 5, 56.

    Article  CAS  Google Scholar 

  • Xiong, F., Zhu, K., Deng, S., Huang, H., Yang, L., Gong, Z., Shi, L., He, Y., Tang, Y., Liao, Q., et al. (2021). AFAP1-AS1: a rising star among oncogenic long non-coding RNAs. Sci China Life Sci 64, 1602–1611.

    Article  PubMed  CAS  Google Scholar 

  • Ye, J., Jin, H., Pankov, A., Song, J.S., and Blelloch, R. (2017). NF45 and NF90/NF110 coordinately regulate ESC pluripotency and differentiation. RNA 23, 1270–1284.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu, A.Q., Wang, Z.X., Wu, W., Chen, K.Y., Yan, S.R., and Mao, Z.B. (2019). Circular RNA CircCCNB1 sponges micro RNA-449a to inhibit cellular senescence by targeting CCNE2. Aging 11, 10220–10241.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zeng, Z.Y., Huang, H.B., Zhang, W.L., Xiang, B., Zhou, M., Zhou, Y.H., Ma, J., Yi, M., Li, X.Y., Li, X.L., et al. (2011). Nasopharyngeal carcinoma: advances in genomics and molecular genetics. Sci China Life Sci 54, 966–975.

    Article  PubMed  Google Scholar 

  • Zhang, L., Feng, T., and Spicer, L.J. (2018). The role of tight junction proteins in ovarian follicular development and ovarian cancer. Reproduction 155, R183–R198.

    Article  PubMed  CAS  Google Scholar 

  • Zhao, J., Guo, C., Xiong, F., Yu, J., Ge, J., Wang, H., Liao, Q., Zhou, Y., Gong, Q., Xiang, B., et al. (2020). Single cell RNA-seq reveals the landscape of tumor and infiltrating immune cells in nasopharyngeal carcinoma. Cancer Lett 477, 131–143.

    Article  PubMed  CAS  Google Scholar 

  • Zhong, Y., Du, Y., Yang, X., Mo, Y., Fan, C., Xiong, F., Ren, D., Ye, X., Li, C., Wang, Y., et al. (2018). Circular RNAs function as ceRNAs to regulate and control human cancer progression. Mol Cancer 17, 79.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, R., Wu, Y., Wang, W., Su, W., Liu, Y., Wang, Y., Fan, C., Li, X., Li, G., Li, Y., et al. (2018). Circular RNAs (circRNAs) in cancer. Cancer Lett 425, 134–142.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, K., Hu, X., Chen, H., Li, F., Yin, N., Liu, A.L., Shan, K., Qin, Y.W., Huang, X., Chang, Q., et al. (2019). Downregulation of circRNA DMNT3B contributes to diabetic retinal vascular dysfunction through targeting miR-20b-5p and BAMBI. Ebiomedicine 49, 341–353.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu, K., Ge, J., He, Y., Li, P., Jiang, X., Wang, J., Mo, Y., Huang, W., Gong, Z., Zeng, Z., et al. (2021). Bioinformatics analysis of the signaling pathways and genes of gossypol induce death of nasopharyngeal carcinoma cells. DNA Cell Biol 40, 1052–1063.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (82002239, 82072374 and 82073135), the Overseas Expertise Introduction Project for Discipline Innovation (111 Project, 111-2-12), the Natural Science Foundation of Hunan Province (2021JJ41043 and 2021JJ30897), Central South University Graduate Research and Innovation Project (2021zzts0310). We thank Prof. Li Yong for providing pcDNA3.1(+) CircRNA Mini Vectors.

Author information

Author notes

  1. Contributed equally to this work

Authors and Affiliations

  1. NHC Key Laboratory of Carcinogenesis, Hunan Cancer Hospital and the Affiliated Cancer Hospital of Xiangya School of Medicine, Central South University, Changsha, 410078, China

    Mengyao Zhao, Yian Wang, Qianjin Liao, Guiyuan Li, Zhaoyang Zeng & Wei Xiong

  2. Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Cancer Research Institute, Central South University, Changsha, 410083, China

    Mengyao Zhao, Yian Wang, Fenghua Tan, Xiangchan Hou, Chunmei Fan, Le Tang, Yongzhen Mo, Yumin Wang, Qijia Yan, Zheng Li, Can Guo, He Huang, Guiyuan Li, Zhaoyang Zeng, Wei Xiong & Fuyan Wang

  3. Cancer Research Institute, Hengyang Medical College, University of South China, Hengyang, 421009, China

    Lingyun Liu & Xi Zeng

  4. Department of Oral and Maxillofacial Surgery, the Second Xiangya Hospital, Central South University, Changsha, 410011, China

    Zhaojian Gong

  5. Hunan Key Laboratory of Nonresolving Inflammation and Cancer, Disease Genome Research Center, the Third Xiangya Hospital, Central South University, Changsha, 410013, China

    Guiyuan Li

Authors
  1. Mengyao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fenghua Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lingyun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiangchan Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chunmei Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Le Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yongzhen Mo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yumin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qijia Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Zhaojian Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Zheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Qianjin Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Can Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. He Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Xi Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Guiyuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Zhaoyang Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Wei Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Fuyan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wei Xiong or Fuyan Wang.

Ethics declarations

Compliance and ethics The author(s) declare that they have no conflict of interest. The present study was approved by the Ethics Committee of Central South University.

Supplementary Material/Additional Files

Supplementary material, approximately 30.5 KB.

Supplemental Table 1. sgRNA target sites, nicking sgRNA, RT template and PBS of ten target sites.

11427_2021_2089_MOESM3_ESM.pdf

Table S1. Clinicopathological data of 23 nasopharyngeal carcinoma (NPC) tissue samples and 10 non-neoplastic nasopharyngeal epithelial (NPE) tissue samples for RT-qPCR.

Table S2. Summary of the proteins differentially expressed in the HNE2 cells transfected with si-circCCNB1/circCCNB1.

Table S3. Mass spectrometry identification of proteins pulled down by the biotin-labeled circCCNB1 probe.

11427_2021_2089_MOESM6_ESM.pdf

Table S4. Probe for circRNA immunoprecipitation (circRIP), fluorescence in situ hybridization (FISH), RNA pull-down, small interfering RNAs (siRNAs), and primers for RT-qPCR.

11427_2021_2089_MOESM7_ESM.pdf

Table S5. List of antibodies for Western blotting, Immunofluorescence (IF), and RNA-binding protein immunoprecipitation (RIP).

Supplementary material, approximately 1.33 MB.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, M., Wang, Y., Tan, F. et al. Circular RNA circCCNB1 inhibits the migration and invasion of nasopharyngeal carcinoma through binding and stabilizing TJP1 mRNA. Sci. China Life Sci. 65, 2233–2247 (2022). https://doi.org/10.1007/s11427-021-2089-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-021-2089-8

Keywords

Search

Navigation