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MiR-29a-3p inhibits high-grade transformation and epithelial–mesenchymal transition of lacrimal gland adenoid cystic carcinoma by targeting Quaking

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Abstract

Background

Lacrimal adenoid cystic carcinoma (LACC) is the most common orbital malignant epithelial neoplasm. LACC with high-grade transformation (LACC-HGT) has higher rates of recurrence, metastasis, and mortality than LACC without HGT. This study investigated the effects of microRNA-29a-3p (miR-29a-3p) in the pathogenesis of LACC-HGT.

Methods

An Agilent human miRNA microarray was used to screen the differentially expressed miRNAs (DEMs) in LACC and LACC-HGT tumor tissues. Then, the primary cells obtained in previous studies were used to determine the effect of miR-29a-3p.

Results

The expression of miR-29a-3p was abnormally lower in LACC-HGT than in LACC. miR-29a-3p can specifically target the 3ʹ UTR of Quaking mRNA and down-regulate Quaking expression, thereby inhibiting the proliferation, migration, and epithelial–mesenchymal transition of LACC cells.

Conclusions

This study illustrated that miR-29a-3p functions as a tumor suppressor by down-regulating the expression of Quaking to inhibit the tumorigenesis of LACC cells. This study may also reveal the pathogenesis of HGT in LACC cells and provide a reference for LACC-HGT targeted diagnosis.

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Data availability

The datasets used during the study available from the corresponding author on reasonable request.

Abbreviations

DEMs:

The differentially-expressed miRNAs

LACC:

Lacrimal gland adenoid cystic carcinoma

LACC-HGT:

Lacrimal gland adenoid cystic carcinoma with high-grade transformation

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

miRNA:

Micro ribonucleic acid

IHC:

Immunohistochemistry

QKI:

KH domain containing RNA binding provided by HGNC

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Acknowledgements

This study was performed at the Tianjin Medical University Eye Hospital.

Funding

This work was supported by the National Natural Science Foundation of China (Grant 81570872), Tianjin Research Program of Application Foundation and Advanced Technology (Grant 15JCYBJC24900), Science and Technology Project of Tianjin Health Commission (Grant Numbers MS20025), Open Project of Tianjin Key Laboratory of Retinal Functions and Diseases (2021tjswmm001), and Tianjin Key Medical Discipline (Specialty) Construction Project (TJYXZDXK-037A).

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Author notes

  1. Fei Xu and Meixia Jiang made the equal contribution to the article.

Authors and Affiliations

  1. Tianjin Key Laboratory of Retinal Functions and Diseases, Tianjin Branch of National Clinical Research Center for Ocular Disease, Eye Institute and School of Optometry, Tianjin Medical University Eye Hospital, Tianjin, 300384, People’s Republic of China

    Fei Xu, Qin Tang, Jiaqi Lin, Xun Liu, Chuanli Zhang, Jinzhi Zhao, Yanjin He, Lijie Dong, Limin Zhu & Tingting Lin

  2. Beijing Tongren Eye Center, Beijing Tongren Hospital, Beijing Key Laboratory of Ophthalmology &Visual Sciences, Capital Medical University, Beijing, China

    Meixia Jiang

  3. Beijing Institute of Ophthalmology, Beijing, China

    Meixia Jiang

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  1. Fei Xu
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Contributions

MX-J and F-X conceived the project. F-X and MX-J performed most of the experiment, collected the data. F-X wrote the manuscript. Q-T and JQ-L collected and analyzed the data. YJ-H, TT-L, LM-Z and JZ-Z made the surgeries for these patients. Pathological diagnosis was made by X-L. TT-L and CL-Z contributed to the interpretation of the data. TT-L and LJ-D made contributions to conception and design, and correction of the manuscript. TT-L provided the funding for the study. All authors have reviewed and approved the final manuscript for submission.

Corresponding authors

Correspondence to Lijie Dong, Limin Zhu or Tingting Lin.

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All authors approved the manuscript for publication.

Ethical approval

Institutional of Human Research Ethics Committee of the Tianjin Medical University Eye Hospital approved this review [No. 2018KY(L)-02].

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Xu, F., Jiang, M., Tang, Q. et al. MiR-29a-3p inhibits high-grade transformation and epithelial–mesenchymal transition of lacrimal gland adenoid cystic carcinoma by targeting Quaking. Mol Biol Rep 50, 2305–2316 (2023). https://doi.org/10.1007/s11033-022-08150-1

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