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circRNA_0067717 promotes paclitaxel resistance in nasopharyngeal carcinoma by acting as a scaffold for TRIM41 and p53

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Abstract

Purpose

Circular RNAs (circRNAs) play important roles in tumour progression. This study aimed to explore the mechanism of hsa_circ_0067717 (termed circRNA_0067717) promoting paclitaxel resistance in nasopharyngeal carcinoma (NPC).

Methods

We assayed CNE-1 and HNE-2 parental cell lines and the corresponding paclitaxel-resistant NPC cell lines using circRNA microarrays. RNA pull-down assay, RNA immunoprecipitation, and RNA fluorescence in situ hybridization were used to identify the molecular mechanisms.

Results

Here, we confirm that circRNA_0067717 is significantly upregulated in NPC paclitaxel-resistant cells and is associated with paclitaxel resistance in NPC. Mechanistically, circRNA_0067717 functions as a scaffold for TRIM41 protein (a ubiquitin E3 ligase) and p53 protein. In nasopharyngeal carcinoma paclitaxel-resistant cells, the highly expressed circRNA_0067717 can bind to more TRIM41 and p53 protein, promoting TRIM41-induced p53 ubiquitination and degradation, resulting in a decrease in p53 protein level. Moreover, the 1–176 nt area of circRNA_0067717 and the 301–425 nt region of circRNA_0067717 are the binding sites for p53 and TRIM41, respectively. The resistance of NPC cells to paclitaxel can be reduced by blocking these binding regions of circRNA_0067717.

Conclusion

We demonstrate that circRNA_0067717 acts as a scaffold for TRIM41 and p53, enhancing paclitaxel chemoresistance in NPC by promoting TRIM41-induced p53 degradation via ubiquitination.

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Data availability

The material supporting the conclusion of this study has been included within the article.

Abbreviations

NPC:

Nasopharyngeal carcinoma

circRNAs:

Circular RNAs

UPS:

Ubiquitin-Proteasome System

DUBs:

Deubiquitinating enzymes

RBP:

RNA Binding Protien

RIP:

RNA immunoprecipitation

FISH:

Fluorescence in situ hybridization

block-p53:

Blocking oligo for p53 binding site

block-TRIM41:

Blocking oligo for TRIM41 binding site

IC25 :

25% Inhibiting concentration

IC50 :

50% Inhibiting concentration

CHX:

Cycloheximide

MG132:

Proteasomal inhibitor

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Funding

This work was supported by the National Natural Science Foundation of China (81874137), Funds for International Cooperation and Exchange of the National Natural Science Foundation of China(GZ1699), key research and development projects in Hunan Province(2022SK2022), the science and technology innovation Program of Hunan Province (2020RC4011), the Hunan Province Science and Technology Talent Promotion Project (2019TJ-Q10), Scientific research project of Hunan Provincial Health Commission (202209034683),Young Scholars of "Furong Scholar Program" in Hunan Province, and the Wisdom Accumulation and Talent Cultivation Project of the Third xiangya hosipital of Central South University (BJ202001), and Hunan Provincial Innovation Foundation for Postgraduate (CX20190253).

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Authors and Affiliations

  1. Department of Oncology, Third Xiangya Hospital of Central South University, 138 Tongzipo Road, Changsha, 410013, China

    Yaxin Cheng, Yuxing Zhu, Mengqing Xiao, Yeyu Zhang, Zhanwang Wang, Haotian Chen & Ke Cao

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  1. Yaxin Cheng
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  2. Yuxing Zhu
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  3. Mengqing Xiao
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  4. Yeyu Zhang
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Contributions

Y.-X.C. and K.C. designed the study. Y.-X.C., Z.-W.W. and M.-Q.X. performed experiments. Y.-X.C. and Y.-X.Z. analyzed and interpreted the data. Y.-X.C. wrote this manuscript. Z.-W.W., Y.-Y.Z., H.-T.C.and K.C. edited and revised the manuscript. All authors have seen and approved the final version of the manuscript.

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Correspondence to Ke Cao.

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Cheng, Y., Zhu, Y., Xiao, M. et al. circRNA_0067717 promotes paclitaxel resistance in nasopharyngeal carcinoma by acting as a scaffold for TRIM41 and p53. Cell Oncol. 46, 677–695 (2023). https://doi.org/10.1007/s13402-023-00776-y

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