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Long noncoding RNA LINC01296 regulates the cell proliferation, migration and invasion in neuroblastoma

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Abstract

Neuroblastoma (NB) is a childhood cancer that often occurs in the sympathetic nervous system. Previous reports showed that long non-coding RNAs (lncRNAs) could affect the progress of NB, but the mechanism is still indistinct. In this study, we unfolded the roles of LINC01296 in NB tissues and cells. The level of LINC01296, microRNA-584-5p (miR-584-5p), miR-34a-5p and mRNA of tripartite motif-containing 59 (TRIM59) were indicated by quantitative real-time polymerase chain reaction (qRT-PCR) in NB tissues. The capacities of NB cells were validated by MTT assay, Edu assay, transwell assay and flow cytometry analysis. The interplay between miR-584-5p/miR-34a-5p and LINC01296 or TRIM59 were detected by dual-luciferase reporter assay. Finally, the in vivo experiment was implemented to verify the effect of LINC01296 in vivo. The level of LINC01296 and TRIM59 were increased, whereas miR-584-5p and miR-34a-5p levels were reduced in NB tissues in contrast to that in normal tissues. For functional analysis, LINC01296 deficiency inhibited the cell vitality, cell proliferation, migration and invasion in NB cells, whereas promoted cell apoptosis. Moreover, miR-584-5p and miR-34a-5p were validated to act as a tumor repressive effect in NB cells by restraining TRIM59. The results also showed that LINC01296 could regulate the development of NB. In mechanism, LINC01296 acted as a miR-584-5p and miR-34a-5p sponge to modulate TRIM59 expression. In addition, LINC01296 knockdown also attenuated tumor growth in vivo. LINC01296 promotes the progression of NB by increasing TRIM59 expression via regulating miR-584-5p and miR-34a-5p, which also offered an underlying targeted therapy for NB treatment.

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Data availability

The data used to support the findings of this study are available from the corresponding author upon request.

References

  • Ambros V (2004) The functions of animal microRNAs. Nature 431(7006):350–355

    Article  CAS  Google Scholar 

  • Braekeveldt N, Bexell D (2018) Patient-derived xenografts as preclinical neuroblastoma models. Cell Tissue Res 372(2):233–243

    Article  Google Scholar 

  • Chen L, Chen DT, Kurtyka C, Rawal B, Fulp WJ, Haura EB et al (2012) Tripartite motif containing 28 (Trim28) can regulate cell proliferation by bridging HDAC1/E2F interactions. J Biol Chem 287(48):40106–40118

    Article  CAS  Google Scholar 

  • Eames HL, Saliba DG, Krausgruber T, Lanfrancotti A, Ryzhakov G, Udalova IA (2012) KAP1/TRIM28: an inhibitor of IRF5 function in inflammatory macrophages. Immunobiology 217(12):1315–1324

    Article  CAS  Google Scholar 

  • Garzon R, Marcucci G, Croce CM (2010) Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov 9(10):775–789

    Article  CAS  Google Scholar 

  • Guo T, Zheng C, Wang Z, Zheng X (2019) miR5845p regulates migration and invasion in nonsmall cell lung cancer cell lines through regulation of MMP14. Mol Med Rep 19(3):1747–1752

    CAS  PubMed  Google Scholar 

  • Gurney JG, Ross JA, Wall DA, Bleyer WA, Severson RK, Robison LL (1997) Infant cancer in the U.S.: Histology-specific incidence and trends, 1973 to 1992. J Pediatr Hematol Oncol 19(5):428–432

    Article  CAS  Google Scholar 

  • Levy D, Aerts I, Michon J, Lumbroso-Le Rouic L, Cellier C, Orbach D (2014) Childhood cancer: progress but prognosis still very unequal. Example of retinoblastoma and high-risk neuroblastoma. Bull Cancer 101(3):250–257

    Article  Google Scholar 

  • Li YY, Tao YW, Gao S, Li P, Zheng JM, Zhang SE et al (2018) Cancer-associated fibroblasts contribute to oral cancer cells proliferation and metastasis via exosome-mediated paracrine miR-34a-5p. EBioMedicine 36:209–220

    Article  Google Scholar 

  • London WB, Castleberry RP, Matthay KK, Look AT, Seeger RC, Shimada H et al (2005) Evidence for an age cutoff greater than 365 days for neuroblastoma risk group stratification in the Children's oncology group. J Clin Oncol 23(27):6459–6465

    Article  CAS  Google Scholar 

  • Miller RW, Young JL Jr, Novakovic B (1995) Childhood cancer. Cancer 75(1 Suppl):395–405

    Article  CAS  Google Scholar 

  • Mitra S, Muralidharan SV, Marco MD, Juvvuna PK, Kosalai ST, Reischl S et al (2021) Subcellular distribution of p53 by the p53-responsive lncRNA NBAT1 determines chemotherapeutic response in neuroblastoma. Cancer Res 81(6):1457–1471

    Article  CAS  Google Scholar 

  • Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81:145–166

    Article  CAS  Google Scholar 

  • Sato T, Okumura F, Ariga T, Hatakeyama S (2012) TRIM6 interacts with Myc and maintains the pluripotency of mouse embryonic stem cells. J Cell Sci 125(Pt 6):1544–1555

    CAS  PubMed  Google Scholar 

  • Speleman F, Park JR, TO H (2016) Neuroblastoma: a tough nut to crack. Am Soc Clin Oncol Educ Book 35:e548–e557

    Article  Google Scholar 

  • Tan P, Ye Y, He L, Xie J, Jing J, Ma G et al (2018) TRIM59 promotes breast cancer motility by suppressing p62-selective autophagic degradation of PDCD10. PLoS Biol 16(11):e3000051

    Article  Google Scholar 

  • Tian F, Wang J, Zhang Z, Yang J (2020) LncRNA SNHG7/miR-34a-5p/SYVN1 axis plays a vital role in proliferation, apoptosis and autophagy in osteoarthritis. Biol Res 53(1):9

    Article  CAS  Google Scholar 

  • Versteeg GA, Benke S, Garcia-Sastre A, Rajsbaum R (2014) InTRIMsic immunity: positive and negative regulation of immune signaling by tripartite motif proteins. Cytokine Growth Factor Rev 25(5):563–576

    Article  CAS  Google Scholar 

  • Wang ZC, Yang S, Chen MQ, Wu SS, Lv HH, Jin WX (2019) LINC01296 promotes the proliferation and invasion by regulating microRNA-760 expression and predicts poor prognosis of hepatocellular carcinoma. Eur Rev Med Pharmacol Sci 23(22):9848–9856

    PubMed  Google Scholar 

  • Wang B, Xu L, Zhang J, Cheng X, Xu Q, Wang J et al (2020a) LncRNA NORAD accelerates the progression and doxorubicin resistance of neuroblastoma through up-regulating HDAC8 via sponging miR-144-3p. Biomed Pharmacother 129:110268

    Article  CAS  Google Scholar 

  • Wang SY, Wang X, Zhang CY (2020b) LncRNA SNHG7 enhances chemoresistance in neuroblastoma through cisplatin-induced autophagy by regulating miR-329-3p/MYO10 axis. Eur Rev Med Pharmacol Sci 24(7):3805–3817

    PubMed  Google Scholar 

  • Wei H, Wang J, Xu Z, Lu Y, Wu X, Zhuo C et al (2019) miR-584-5p regulates hepatocellular carcinoma cell migration and invasion through targeting KCNE2. Mol Genet Genomic Med 7(6):e702

    Article  Google Scholar 

  • Yang Z, Liu D, Wu D, Liu F, Liu C (2019) The biological function of long noncoding RNA FAL1 in oesophageal carcinoma cells. Artif Cells Nanomed Biotechnol 47(1):896–903

    Article  CAS  Google Scholar 

  • Yang H, Guo JF, Zhang ML, Li AM (2020) LncRNA SNHG4 promotes neuroblastoma proliferation, migration, and invasion by sponging miR-377-3p. Neoplasma 67(5):1054–1062

    Article  CAS  Google Scholar 

  • Yerukala Sathipati S, Sahu D, Huang HC, Lin Y, Ho SY (2019) Identification and characterization of the lncRNA signature associated with overall survival in patients with neuroblastoma. Sci Rep 9(1):5125

    Article  Google Scholar 

  • Ying H, Ji L, Xu Z, Fan X, Tong Y, Liu H et al (2020) TRIM59 promotes tumor growth in hepatocellular carcinoma and regulates the cell cycle by degradation of protein phosphatase 1B. Cancer Lett 473:13–24

    Article  CAS  Google Scholar 

  • Zaman MM, Nomura T, Takagi T, Okamura T, Jin W, Shinagawa T et al (2013) Ubiquitination-deubiquitination by the TRIM27-USP7 complex regulates tumor necrosis factor alpha-induced apoptosis. Mol Cell Biol 33(24):4971–4984

    Article  Google Scholar 

  • Zhang J, Li WY, Yang Y, Yan LZ, Zhang SY, He J et al (2019) LncRNA XIST facilitates cell growth, migration and invasion via modulating H3 histone methylation of DKK1 in neuroblastoma. Cell Cycle 18(16):1882–1892

    Article  Google Scholar 

  • Zheng F, Li J, Ma C, Tang X, Tang Q, Wu J et al (2020) Novel regulation of miR-34a-5p and HOTAIR by the combination of berberine and gefitinib leading to inhibition of EMT in human lung cancer. J Cell Mol Med 24(10):5578–5592

    Article  CAS  Google Scholar 

  • Zhu K, Wang L, Zhang X, Sun H, Chen T, Sun C et al (2020) LncRNA HCP5 promotes neuroblastoma proliferation by regulating miR-186-5p/MAP3K2 signal axis. J Pediatr Surg 56(4):778–787

    Article  Google Scholar 

  • Zuo Y, Zheng W, Liu J, Tang Q, Wang SS, Yang XS (2020) MiR-34a-5p/PD-L1 axis regulates cisplatin chemoresistance of ovarian cancer cells. Neoplasma 67(1):93–101

    Article  CAS  Google Scholar 

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Author notes

  1. Huiling Xiao and Yanhong Li contributed equally to this work.

Authors and Affiliations

  1. Department of Pediatrics, Xiangyang Central Hospital, Affiliated Hospital of Hubei University of Arts and Science, Xiangyang, 441000, China

    Huiling Xiao & Yanhong Li

  2. Department of Pediatrics, Xiangyang NO.1 People’s Hospital Affiliated Hospital of Hubei University of Medicine, No.15, Jiefang Road, Fancheng District, Xiangyang, 441000, China

    Ying Zhang

  3. Department of Neurosurgery, Xiangyang Central Hospital, Affiliated Hospital of Hubei University of Arts and Science, No.2, Chunyuandong Road, Fancheng District, Xiangyang, 441000, China

    Peng Wang

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  1. Huiling Xiao
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  2. Yanhong Li
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  3. Ying Zhang
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  4. Peng Wang
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Correspondence to Ying Zhang or Peng Wang.

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Supplementary Fig. 1

Expression of LINC01296 in NB with different malignant degrees. (A) QRT-PCR analysis of LINC01296 expression in NB tissues at advanced stages (III and IV) and early-stages (I, II, and IVs). (B) QRT-PCR analysis of LINC01296 expression in NB tissues with high-risk, intermediate-risk, and low-risk. *P < 0.05, ***P < 0.001 (PNG 40 kb)

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Xiao, H., Li, Y., Zhang, Y. et al. Long noncoding RNA LINC01296 regulates the cell proliferation, migration and invasion in neuroblastoma. Metab Brain Dis 37, 1247–1258 (2022). https://doi.org/10.1007/s11011-022-00935-4

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  • DOI: https://doi.org/10.1007/s11011-022-00935-4

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