Skip to main content
SpringerLink
Log in

Long Non-coding RNA LINC01426 Contributes to the Malignant Behaviors of NSCLC Via Acting As a Sponge for miR-143-3p

  • Original Article
  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Recently, long non-coding RNA (lncRNA) is proved to play critical roles in non-small cell lung cancer (NSCLC) progression. However, the detailed effects of LINC01426 in NSCLC and its functional mechanism remain unknown. The expression of LINC01426, microRNA-143-3p (miR-143-3p), and Ubiquitin-specific peptidase 28 (USP28) was assessed by quantitative real-time polymerase chain reaction (RT-qPCR). The colony-forming ability was determined by colony-forming assay. 5-ethynyl-2′-deoxyuridine (EdU) staining assay was performed to evaluate cell proliferation. The migrated and invaded abilities of cells were measured by transwell assays. Flow cytometry was used to examine cell apoptosis. The protein expression was analyzed by Western blot analysis. The glycolysis ability was analyzed by commercial kits. Dual-luciferase reporter assay, RNA immunoprecipitation (RIP) assay, and RNA pull-down assay were used to confirm relationship among LINC01426, miR-143-3p, and USP28. A xenograft experiment was conducted to explore the effects of LINC01426 inhibition in vivo. Our results confirmed that LINC01426 and USP28 expression were increased, while miR-143-3p expression was decreased in NSCLC tissues and cells. Further functional experiments demonstrated that LINC01426 inhibition markedly impaired cell proliferation, migration, invasion, autophagy, and glycolysis while induced apoptosis in NSCLC cells, and LINC01426 derived malignant behaviors of NSCLC cells by sponging miR-143-3p. Additionally, LINC01426 regulated USP28 expression by sponging miR-143-3p. USP28 overexpression partly overturned the inhibitory effect of miR-143-3p on NSCLC progression. Consistently, silencing of LINC01426 significantly inhibited the growth of NSCLC tumor in vivo. LINC01426 accelerated the malignant progression of NSCLC. Mechanistically, LINC01426 acted as a competing endogenous RNA (ceRNA) for miR-143-3p to upregulate USP28 expression.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

Please contact the correspondence author for the data request.

References

  • Akhade VS, Pal D, Kanduri C (2017) Long nonacoding RNA: genome organization and mechanism of action. Adv Exp Med Biol 1008:47–74

    Article  CAS  PubMed  Google Scholar 

  • Cao J, Tang Z, Su Z (2020) Long non-coding RNA LINC01426 facilitates glioblastoma progression via sponging miR-345-3p and upregulation of VAMP8. Cancer Cell Int 20:327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai J, Wang B, Zhao Y, Zuo X, Cui H, Chen X et al (2020) Long noncoding RNA LINC01426 sequesters microRNA-519d-5p to promote non-small cell lung cancer progression by increasing ETS1 expression. Cancer Manag Res 12:12697–12708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devrim T, Atac F, Devrim AK, Balci M (2020) The concomitant use of USP28 and p53 to predict the progression of urothelial carcinoma of the bladder. Pathol Res Pract 216:152774

    Article  CAS  PubMed  Google Scholar 

  • Diefenbacher ME, Popov N, Blake SM, Schulein-Volk C, Nye E, Spencer-Dene B et al (2014) The deubiquitinase USP28 controls intestinal homeostasis and promotes colorectal cancer. J Clin Invest 124:3407–3418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herbst RS, Morgensztern D, Boshoff C (2018) The biology and management of non-small cell lung cancer. Nature 553:446–454

    Article  CAS  PubMed  Google Scholar 

  • Hirsch FR, Scagliotti GV, Mulshine JL, Kwon R, Curran WJ Jr, Wu YL et al (2017) Lung cancer: current therapies and new targeted treatments. Lancet 389:299–311

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Zhang H, Li W, Yan Y, Yao X, Gu W (2021) LINC01426 contributes to clear cell renal cell carcinoma progression by modulating CTBP1/miR-423-5p/FOXM1 axis via interacting with IGF2BP1. J Cell Physiol 236:427–439

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wang J, Chen Y, Yang L, Chen S (2017) A prognostic 4-gene expression signature for squamous cell lung carcinoma. J Cell Physiol 232:3702–3713

    Article  CAS  PubMed  Google Scholar 

  • Li P, Huang Z, Wang J, Chen W, Huang J (2019a) Ubiquitin-specific peptidase 28 enhances STAT3 signaling and promotes cell growth in non-small-cell lung cancer. OncoTargets Ther 12:1603–1611

    Article  CAS  Google Scholar 

  • Li F, Han H, Sun Q, Liu K, Lin N, Xu C et al (2019b) USP28 regulates deubiquitination of histone H2A and cell proliferation. Exp Cell Res 379:11–18

    Article  CAS  PubMed  Google Scholar 

  • Nasim F, Sabath BF, Eapen GA (2019) Lung cancer. Med Clin North Am 103:463–473

    Article  PubMed  Google Scholar 

  • Peng WX, Koirala P, Mo YY (2017) LncRNA-mediated regulation of cell signaling in cancer. Oncogene 36:5661–5667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prieto-Garcia C, Hartmann O, Reissland M, Braun F, Fischer T, Walz S et al (2020) Maintaining protein stability of Np63 via USP28 is required by squamous cancer cells. EMBO Mol Med 12:e11101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pu M, Chen J, Tao Z, Miao L, Qi X, Wang Y et al (2019) Regulatory network of miRNA on its target: coordination between transcriptional and post-transcriptional regulation of gene expression. Cell Mol Life Sci 76:441–451

    Article  CAS  PubMed  Google Scholar 

  • Ren K, Li Y, Lu H, Li Z, Han X (2017) miR-3940-5p functions as a tumor suppressor in non-small cell lung cancer cells by targeting cyclin D1 and ubiquitin specific peptidase-28. Transl Oncol 10:80–89

    Article  PubMed  Google Scholar 

  • Sahami-Fard MH, Kheirandish S, Sheikhha MH (2019) Expression levels of miR-143-3p and -424-5p in colorectal cancer and their clinical significance. Cancer Biomark 24:291–297

    Article  CAS  PubMed  Google Scholar 

  • Saliminejad K, Khorram Khorshid HR, Soleymani Fard S, Ghaffari SH (2019) An overview of microRNAs: biology, functions, therapeutics, and analysis methods. J Cell Physiol 234:5451–5465

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Shen H, Xu J, Zhao S, Yao S, Jiang N (2018) MiR-143-3p suppresses the progression of ovarian cancer. Am J Transl Res 10:866–874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Siegel RL, Miller KD, Jemal A (2019) Cancer statistics, 2019. CA Cancer J Clin 69:7–34

    Article  PubMed  Google Scholar 

  • Sun W, Zu Y, Fu X, Deng Y (2017) Knockdown of lncRNA-XIST enhances the chemosensitivity of NSCLC cells via suppression of autophagy. Oncol Rep 38:3347–3354

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tian B, Han X, Li G, Jiang H, Qi J, Li J et al (2020) A long intergenic non-coding RNA, LINC01426, promotes cancer progression via AZGP1 and predicts poor prognosis in patients with LUAD. Mol Ther Methods Clin Dev 18:765–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SJ, Wang H, Zhao CD, Li R (2018a) Long noncoding RNA LINC01426 promotes glioma progression through PI3K/AKT signaling pathway and serves as a prognostic biomarker. Eur Rev Med Pharmacol Sci 22:6358–6368

    PubMed  Google Scholar 

  • Wang X, Liu Z, Zhang L, Yang Z, Chen X, Luo J et al (2018b) Targeting deubiquitinase USP28 for cancer therapy. Cell Death Dis 9:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weili Z, Zhikun L, Jianmin W, Qingbao T (2019) Knockdown of USP28 enhances the radiosensitivity of esophageal cancer cells via the c-Myc/hypoxia-inducible factor-1 alpha pathway. J Cell Biochem 120:201–212

    Article  PubMed  Google Scholar 

  • Xia C, Yang Y, Kong F, Kong Q, Shan C (2018) MiR-143-3p inhibits the proliferation, cell migration and invasion of human breast cancer cells by modulating the expression of MAPK7. Biochimie 147:98–104

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Wang J, Qiu M, Xu L, Li M, Jiang F et al (2015) Upregulation of the long noncoding RNA TUG1 promotes proliferation and migration of esophageal squamous cell carcinoma. Tumour Biol 36:1643–1651

    Article  CAS  PubMed  Google Scholar 

  • Yamanaka S, Sato Y, Oikawa D, Goto E, Fukai S, Tokunaga F et al (2020) Subquinocin, a small molecule inhibitor of CYLD and USP-family deubiquitinating enzymes, promotes NF-kappaB signaling. Biochem Biophys Res Commun 524:1–7

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Li S, Cao J, Li Y, Hu H, Wu Z (2019) RRM2 regulated by LINC00667/miR-143-3p signal is responsible for non-small cell lung cancer cell progression. OncoTargets Ther 12:9927–9939

    Article  CAS  Google Scholar 

  • Yang J, Jia Y, Wang B, Yang S, Du K, Luo Y et al (2020) Circular RNA TUBA1C accelerates the progression of non-small-cell lung cancer by sponging miR-143-3p. Cell Signal 74:109693

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Xu B, Qiang Y, Huang H, Wang C, Li D et al (2015) Overexpression of deubiquitinating enzyme USP28 promoted non-small cell lung cancer growth. J Cell Mol Med 19:799–805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao LJ, Zhang T, Feng XJ, Chang J, Suo FZ, Ma JL et al (2018) USP28 contributes to the proliferation and metastasis of gastric cancer. J Cell Biochem. https://doi.org/10.1002/jcb.28040

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

None.

Funding

None.

Author information

Authors and Affiliations

  1. Department of General Thoracic Surgery, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Shushan District, Hefei City, 230022, Anhui Province, People’s Republic of China

    Wei Liu, Panpan Si, Hanlin Fang, Guangyao Ning, Chen Lu & Yunlong Huang

Authors
  1. Wei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Panpan Si
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hanlin Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guangyao Ning
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chen Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yunlong Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

WL was responsible for drafting the manuscript. WL, PS, HF, and GN: Contributed to the analysis and interpretation of the data. WL, CL, and YH: Contributed in the data collection. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Wei Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no financial conflict of interest.

Ethical Approval

Written informed consent was obtained from patients with approval by the Institutional Review Board in The First Affiliated Hospital of Anhui Medical University (No. 202080584).

Consent for Publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, W., Si, P., Fang, H. et al. Long Non-coding RNA LINC01426 Contributes to the Malignant Behaviors of NSCLC Via Acting As a Sponge for miR-143-3p. Biochem Genet 60, 2570–2586 (2022). https://doi.org/10.1007/s10528-022-10234-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-022-10234-3

Keywords

Search

Navigation