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BMC Cancer

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Open Access 01-12-2021 | Research

LINC00958 promotes bladder cancer carcinogenesis by targeting miR-490-3p and AURKA

Authors: Hongtao Zhen, Peng Du, Qiang Yi, Xiaolong Tang, Tongqing Wang

Published in: BMC Cancer | Issue 1/2021

Abstract

Background

Bladder cancer is a prevalent malignancy of the urinary system, in which long non-coding RNAs (lncRNAs) are highly associated. We aimed to elucidate the role of LINC00958 in bladder cancer.

Methods

LINC00958 expression levels were measured using qRT-PCR. The interaction of LINC00958-miR-490-3p-AURKA was analyzed by luciferase, RIP, and RNA pull-down assays. The biological roles of LINC00958, miR-490-3p, and AURKA in bladder cancer cells were analyzed using CCK8, BrdU, and transwell assays.

Results

Increased expression of LINC00958 and AURKA was observed in bladder cancer tissues and cell lines. Decreased LINC00958 expression repressed bladder cancer progression and downregulation of miR-490-3p accelerated bladder cancer cell progression. Moreover, LINC00958 sponges miR-490-3p to upregulate AURKA expression, thereby promoting carcinogenesis in bladder cancer cells.

Conclusions

Our study revealed that LINC00958 facilitated cell proliferation and invasion, and suppressed cell apoptosis by sponging miR-490-3p and upregulating AURKA, thus inspiring a new treatment method for bladder cancer.

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Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. https://doi.org/10.3322/caac.21492.CrossRefPubMed

Baughan DM, White-Baughan J, Pickwell S, Bartlome J, Wong S. Primary care needs of Cambodian refugees. J Fam Pract. 1990;30(5):565–8.PubMed

DeGeorge KC, Holt HR, Hodges SC. Bladder Cancer: diagnosis and treatment. Am Fam Physician. 2017;96(8):507–14.PubMed

Yao M, Shi X, Li Y, Xiao Y, Butler W, Huang Y, et al. LINC00675 activates androgen receptor axis signaling pathway to promote castration-resistant prostate cancer progression. Cell Death Dis. 2020;11(8):638. https://doi.org/10.1038/s41419-020-02856-5.CrossRefPubMedPubMedCentral

Gong X, Dong T, Niu M, Liang X, Sun S, Zhang Y, et al. lncRNA LCPAT1 upregulation promotes breast Cancer progression via enhancing MFAP2 transcription. Mol Ther Nucleic Acids. 2020;21:804–13. https://doi.org/10.1016/j.omtn.2020.07.015.CrossRefPubMedPubMedCentral

Shu J, Wang D. Functional characterization of the long noncoding RNA MIR22HG as a tumour suppressor in cervical cancer by targeting IGF2BP2. Eur Rev Med Pharmacol Sci. 2020;24(15):7953–62. https://doi.org/10.26355/eurrev_202008_22478.CrossRefPubMed

Ma L, Cao J, Liu L, Du Q, Li Z, Zou D, et al. LncBook: a curated knowledgebase of human long non-coding RNAs. Nucleic Acids Res. 2019;47(D1):D128–d134. https://doi.org/10.1093/nar/gky960.CrossRefPubMed

Wang X, Chen Q, Wang X, Li W, Yu G, Zhu Z, et al. ZEB1 activated-VPS9D1-AS1 promotes the tumorigenesis and progression of prostate cancer by sponging miR-4739 to upregulate MEF2D. Biomed Pharmacother. 2020;122:109557. https://doi.org/10.1016/j.biopha.2019.109557.CrossRefPubMed

Yao L, Chen L, Zhou H, Duan F, Wang L, Zhang Y. Long noncoding RNA NEAT1 promotes the progression of breast Cancer by regulating miR-138-5p/ZFX Axis. Cancer Biother Radiopharm. 2020. https://doi.org/10.1089/cbr.2019.3515.

10.

Wang S, Cheng Y, Yang P, Qin G. Silencing of long noncoding RNA LINC00324 interacts with MicroRNA-3200-5p to attenuate the tumorigenesis of gastric Cancer via regulating BCAT1. Gastroenterol Res Pract. 2020;2020:4159298–12. https://doi.org/10.1155/2020/4159298.CrossRefPubMedPubMedCentral

11.

Zhao H, Zheng GH, Li GC, Xin L, Wang YS, Chen Y, et al. Long noncoding RNA LINC00958 regulates cell sensitivity to radiotherapy through RRM2 by binding to microRNA-5095 in cervical cancer. J Cell Physiol. 2019;234(12):23349–59. https://doi.org/10.1002/jcp.28902.CrossRefPubMed

12.

Luo Z, Han Z, Shou F, Li Y, Chen Y. LINC00958 accelerates cell proliferation and migration in non-small cell lung Cancer through JNK/c-JUN signaling. Hum Gene Ther Methods. 2019;30(6):226–34. https://doi.org/10.1089/hgtb.2019.115.CrossRefPubMed

13.

Wang W, Song ZJ, Wang Y, Zhong WF, Kang P, Yang Y. Elevated long non-coding RNA LINC00958 was associated with metastasis and unfavorable prognosis in gastric cancer. Eur Rev Med Pharmacol Sci. 2019;23(2):598–603. https://doi.org/10.26355/eurrev_201901_16872.CrossRefPubMed

14.

Cui Y, Xie M, Zhang Z. LINC00958 involves in bladder Cancer through sponging miR-378a-3p to elevate IGF1R. Cancer Biother Radiopharm. 2020;35(10):776–88. https://doi.org/10.1089/cbr.2019.3300.CrossRefPubMed

15.

Di Leva G, Garofalo M, Croce CM. MicroRNAs in cancer. Annu Rev Pathol. 2014;9(1):287–314. https://doi.org/10.1146/annurev-pathol-012513-104715.CrossRefPubMed

16.

Wang M, Yang M, Deng B. miR-548a-3p weakens the tumorigenesis of Colon Cancer through targeting TPX2. Cancer Biother Radiopharm. 2020. https://doi.org/10.1089/cbr.2020.3767.

17.

Li H, Xu Y, Zhao D. MicroRNA-193b regulates human ovarian cancer cell growth via targeting STMN1. Exp Ther Med. 2020;20(4):3310–5. https://doi.org/10.3892/etm.2020.9033.CrossRefPubMedPubMedCentral

18.

Zhou JS, Yang ZS, Cheng SY, Yu JH, Huang CJ, Feng Q. miRNA-425-5p enhances lung cancer growth via the PTEN/PI3K/AKT signaling axis. BMC Pulm Med. 2020;20(1):223. https://doi.org/10.1186/s12890-020-01261-0.CrossRefPubMedPubMedCentral

19.

Wang H, Yang G, Yu Y, Gu P. MicroRNA-490-3p suppresses the proliferation and invasion of hepatocellular carcinoma cells via targeting TMOD3. Oncol Lett. 2020;20(4):95. https://doi.org/10.3892/ol.2020.11956.CrossRefPubMedPubMedCentral

20.

Liu W, Yin C, Liu Y. Circular RNA circ_0091579 promotes hepatocellular carcinoma proliferation, migration, invasion, and glycolysis through miR-490-5p/CASC3 Axis. Cancer Biother Radiopharm. 2020. https://doi.org/10.1089/cbr.2019.3472.

21.

Fan H. Zhang YS: miR-490-3p modulates the progression of prostate cancer through regulating histone deacetylase 2. Eur Rev Med Pharmacol Sci. 2019;23(2):539–46. https://doi.org/10.26355/eurrev_201901_16866.CrossRefPubMed

22.

Pan Z, Lin J, Wu D, He X, Wang W, Hu X, et al. Hsa_circ_0006948 enhances cancer progression and epithelial-mesenchymal transition through the miR-490-3p/HMGA2 axis in esophageal squamous cell carcinoma. Aging. 2019;11(24):11937–54. https://doi.org/10.18632/aging.102519.CrossRefPubMedPubMedCentral

23.

Fan H, Yuan J, Li X, Ma Y, Wang X, Xu B, et al. LncRNA LINC00173 enhances triple-negative breast cancer progression by suppressing miR-490-3p expression. Biomed Pharmacother. 2020;125:109987.CrossRefPubMed

24.

Li S, Xu X, Xu X, Hu Z, Wu J, Zhu Y, et al. MicroRNA-490-5p inhibits proliferation of bladder cancer by targeting c-Fos. Biochem Biophys Res Commun. 2013;441(4):976–81. https://doi.org/10.1016/j.bbrc.2013.11.006.CrossRefPubMed

25.

Wu L, Zhang M, Qi L, Zu X, Li Y, Liu L, et al. ERα-mediated alterations in circ_0023642 and miR-490-5p signaling suppress bladder cancer invasion. Cell Death Dis. 2019;10(9):635. https://doi.org/10.1038/s41419-019-1827-3.CrossRefPubMedPubMedCentral

26.

Lan G, Yang L, Xie X, Peng L, Wang Y. MicroRNA-490-5p is a novel tumor suppressor targeting c-FOS in human bladder cancer. Arch Med Sci. 2015;11(3):561–9. https://doi.org/10.5114/aoms.2015.52359.CrossRefPubMedPubMedCentral

27.

Ommer J, Selfe JL, Wachtel M, O'Brien EM, Laubscher D, Roemmele M, et al. Aurora a kinase inhibition destabilizes PAX3-FOXO1 and MYCN and synergizes with Navitoclax to induce rhabdomyosarcoma cell death. Cancer Res. 2020;80(4):832–42. https://doi.org/10.1158/0008-5472.CAN-19-1479.CrossRefPubMed

28.

Bertolin G, Tramier M. Insights into the non-mitotic functions of Aurora kinase a: more than just cell division. Cell Mol Life Sci. 2020;77(6):1031–47. https://doi.org/10.1007/s00018-019-03310-2.CrossRefPubMed

29.

Zhou W, Wu J, Liu X, Ni M, Meng Z, Liu S, et al. Identification of crucial genes correlated with esophageal cancer by integrated high-throughput data analysis. Medicine. 2020;99(20):e20340. https://doi.org/10.1097/MD.0000000000020340.CrossRefPubMedPubMedCentral

30.

Nieto-Jimenez C, Galan-Moya EM, Corrales-Sanchez V, Noblejas-Lopez MDM, Burgos M, Domingo B, et al. Inhibition of the mitotic kinase PLK1 overcomes therapeutic resistance to BET inhibitors in triple negative breast cancer. Cancer Lett. 2020;491:50–9. https://doi.org/10.1016/j.canlet.2020.06.020.CrossRefPubMed

31.

Thaiparambil J, Dong L, Jasso D, Huang JA, El-Zein RA. Mitotic Spindle Apparatus Abnormalities in Chronic Obstructive Pulmonary Disease Cells: A Potential Pathway to Lung Cancer. Cancer Prev Res (Philadelphia, Pa). 2020;13(11):923–34.CrossRef

32.

Burgess EF, Livasy C, Trufan S, Hartman A, Guerreri R, Naso C, et al. High aurora kinase expression identifies patients with muscle-invasive bladder cancer who have poor survival after neoadjuvant chemotherapy. Urol Oncol. 2019;37(12):900–6. https://doi.org/10.1016/j.urolonc.2019.09.009.CrossRefPubMed

33.

Guo M, Lu S, Huang H, Wang Y, Yang MQ, Yang Y, et al. Increased AURKA promotes cell proliferation and predicts poor prognosis in bladder cancer. BMC Syst Biol. 2018;12(Suppl 7):118. https://doi.org/10.1186/s12918-018-0634-2.CrossRefPubMedPubMedCentral

34.

Mobley A, Zhang S, Bondaruk J, Wang Y, Majewski T, Caraway NP, et al. Aurora kinase a is a biomarker for bladder Cancer detection and contributes to its aggressive behavior. Sci Rep. 2017;7(1):40714. https://doi.org/10.1038/srep40714.CrossRefPubMedPubMedCentral

35.

Yuan Q, Sun T, Ye F, Kong W, Jin H. MicroRNA-124-3p affects proliferation, migration and apoptosis of bladder cancer cells through targeting AURKA. Cancer Biomark. 2017;19(1):93–101. https://doi.org/10.3233/CBM-160427.CrossRefPubMed

36.

Chen M, Xu Z, Zhang Y, Zhang X. LINC00958 promotes the malignancy of nasopharyngeal carcinoma by sponging microRNA-625 and thus upregulating NUAK1. OncoTargets Ther. 2019;12:9277–90. https://doi.org/10.2147/OTT.S216342.CrossRef

37.

Huang S, Zhan Z, Li L, Guo H, Yao Y, Feng M, et al. LINC00958-MYC positive feedback loop modulates resistance of head and neck squamous cell carcinoma cells to chemo- and radiotherapy in vitro. OncoTargets Ther. 2019;12:5989–6000. https://doi.org/10.2147/OTT.S208318.CrossRef

38.

Chen F, Liu M, Yu Y, Sun Y, Li J, Hu W, et al. LINC00958 regulated miR-627-5p/YBX2 axis to facilitate cell proliferation and migration in oral squamous cell carcinoma. Cancer Biol Ther. 2019;20(9):1270–80. https://doi.org/10.1080/15384047.2019.1617571.CrossRefPubMedPubMedCentral

39.

Wang L, Zhong Y, Yang B, Zhu Y, Zhu X, Xia Z, et al. LINC00958 facilitates cervical cancer cell proliferation and metastasis by sponging miR-625-5p to upregulate LRRC8E expression. J Cell Biochem. 2020;121(3):2500–9. https://doi.org/10.1002/jcb.29472.CrossRefPubMed

40.

Seitz AK, Christensen LL, Christensen E, Faarkrog K, Ostenfeld MS, Hedegaard J, et al. Profiling of long non-coding RNAs identifies LINC00958 and LINC01296 as candidate oncogenes in bladder cancer. Sci Rep. 2017;7(1):395. https://doi.org/10.1038/s41598-017-00327-0.CrossRefPubMedPubMedCentral

41.

Yazarlou F, Modarressi MH, Mowla SJ, Oskooei VK, Motevaseli E, Tooli LF, et al. Urinary exosomal expression of long non-coding RNAs as diagnostic marker in bladder cancer. Cancer Manag Res. 2018;10:6357–65. https://doi.org/10.2147/CMAR.S186108.CrossRefPubMedPubMedCentral

42.

He W, Zhong G, Jiang N, Wang B, Fan X, Chen C, et al. Long noncoding RNA BLACAT2 promotes bladder cancer-associated lymphangiogenesis and lymphatic metastasis. J Clin Invest. 2018;128(2):861–75. https://doi.org/10.1172/JCI96218.CrossRefPubMedPubMedCentral

43.

Kang NN, Ge SL, Zhang RQ, Huang YL, Liu SD, Wu KM. MiR-490-3p inhibited the proliferation and metastasis of esophageal squamous cell carcinoma by targeting HMGA2. Eur Rev Med Pharmacol Sci. 2018;22(23):8298–305. https://doi.org/10.26355/eurrev_201812_16527.CrossRefPubMed

44.

Liu X, He B, Xu T, Pan Y, Hu X, Chen X, et al. MiR-490-3p functions as a tumor suppressor by inhibiting oncogene VDAC1 expression in colorectal Cancer. J Cancer. 2018;9(7):1218–30. https://doi.org/10.7150/jca.23662.CrossRefPubMedPubMedCentral

45.

Zhang F, Wu A, Wang Y, Liu J. miR-490-3p functions as a tumor suppressor in glioma by inhibiting high-mobility group AT-hook 2 expression. Exp Ther Med. 2019;18(1):664–70. https://doi.org/10.3892/etm.2019.7606.CrossRefPubMedPubMedCentral

46.

Zabihula B, Yiliyasi M, Lu Y, Salai A. MicroRNA-490-3p inhibits proliferation and stimulates apoptosis of ESCC cells via MAPK1 downregulation. Oncol Lett. 2019;18(3):3170–6. https://doi.org/10.3892/ol.2019.10636.CrossRefPubMedPubMedCentral

47.

Xiang W, Lyu L, Huang T, Zheng F, Yuan J, Zhang C, et al. The long non-coding RNA SNHG1 promotes bladder cancer progression by interacting with miR-143-3p and EZH2. J Cell Mol Med. 2020;24(20):11858–73. https://doi.org/10.1111/jcmm.15806.CrossRefPubMedPubMedCentral

48.

Wang H, Niu X, Jiang H, Mao F, Zhong B, Jiang X, et al. Long non-coding RNA DLX6-AS1 facilitates bladder cancer progression through modulating miR-195-5p/VEGFA signaling pathway. Aging. 2020;12(16):16021–34. https://doi.org/10.18632/aging.103374.CrossRefPubMedPubMedCentral

49.

Dai G, Huang C, Yang J, Jin L, Fu K, Yuan F, et al. LncRNA SNHG3 promotes bladder cancer proliferation and metastasis through miR-515-5p/GINS2 axis. J Cell Mol Med. 2020;24(16):9231–43. https://doi.org/10.1111/jcmm.15564.CrossRefPubMedPubMedCentral

50.

Yang L, Xu L, Wang Q, Wang M, An G. Dysregulation of long non-coding RNA profiles in human colorectal cancer and its association with overall survival. Oncol Lett. 2016;12(5):4068–74. https://doi.org/10.3892/ol.2016.5138.CrossRefPubMedPubMedCentral

51.

Zhang H, Bao J, Zhao S, Huo Z, Li B. MicroRNA-490-3p suppresses hepatocellular carcinoma cell proliferation and migration by targeting the aurora kinase a gene (AURKA). Arch Med Sci. 2020;16(2):395–406. https://doi.org/10.5114/aoms.2019.91351.CrossRefPubMed

52.

Luo M, Liang C. LncRNA LINC00483 promotes gastric cancer development through regulating MAPK1 expression by sponging miR-490-3p. Biol Res. 2020;53(1):14. https://doi.org/10.1186/s40659-020-00283-6.CrossRefPubMedPubMedCentral

53.

Gao X, Lai Y, Zhang Z, Ma Y, Luo Z, Li Y, et al. Long Non-coding RNA RP11-480I12.5 Promotes the Proliferation, Migration, and Invasion of Breast Cancer Cells Through the miR-490-3p-AURKA-Wnt/β-Catenin Axis. Front Oncol. 2020;10:948.CrossRefPubMedPubMedCentral

54.

Ma ZL, Zhang BJ, Wang DT, Li X, Wei JL, Zhao BT, et al. Tanshinones suppress AURKA through up-regulation of miR-32 expression in non-small cell lung cancer. Oncotarget. 2015;6(24):20111–20. https://doi.org/10.18632/oncotarget.3933.CrossRefPubMedPubMedCentral

55.

Shao S, Wang C, Wang S, Zhang H, Zhang Y. Hsa_circ_0075341 is up-regulated and exerts oncogenic properties by sponging miR-149-5p in cervical cancer. Biomed Pharmacother. 2020;121:109582. https://doi.org/10.1016/j.biopha.2019.109582.CrossRefPubMed

56.

Kulkarni P, Dasgupta P, Bhat NS, Shahryari V, Shiina M, Hashimoto Y, et al. Elevated miR-182-5p associates with renal Cancer cell mitotic arrest through diminished MALAT-1 expression. Mol Cancer Res. 2018;16(11):1750–60. https://doi.org/10.1158/1541-7786.MCR-17-0762.CrossRefPubMedPubMedCentral

Title: LINC00958 promotes bladder cancer carcinogenesis by targeting miR-490-3p and AURKA
Authors: Hongtao Zhen
Peng Du
Qiang Yi
Xiaolong Tang
Tongqing Wang
Publication date: 01-12-2021
Publisher: BioMed Central
Published in: BMC Cancer / Issue 1/2021
Electronic ISSN: 1471-2407
DOI: https://doi.org/10.1186/s12885-021-08882-6

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