Long non-coding RNAs PTENP1, GNG12-AS1, MAGI2-AS3 and MEG3 as tumor suppressors in breast cancer and their associations with clinicopathological parameters

. 2024 ; 40 (1) : 61-78.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38277283

BACKGROUND: Breast cancer is the most commonly occurring cancer worldwide and is the main cause of death from cancer in women. Novel biomarkers are highly warranted for this disease. OBJECTIVE: Evaluation of novel long non-coding RNAs biomarkers for breast cancer. METHODS: The study comprised the analysis of the expression of 71 candidate lncRNAs via screening, six of which (four underexpressed, two overexpressed) were validated and analyzed by qPCR in tumor tissues associated with NST breast carcinomas, compared with the benign samples and with respect to their clinicopathological characteristics. RESULTS: The results indicated the tumor suppressor roles of PTENP1, GNG12-AS1, MEG3 and MAGI2-AS3. Low levels of both PTENP1 and GNG12-AS1 were associated with worsened progression-free and overall survival rates. The reduced expression of GNG12-AS1 was linked to the advanced stage. A higher grade was associated with the lower expression of PTENP1, GNG12-AS1 and MAGI2-AS3. Reduced levels of both MEG3 and PTENP1 were linked to Ki-67 positivity. The NRSN2-AS1 and UCA1 lncRNAs were overexpressed; higher levels of UCA1 were associated with multifocality. CONCLUSIONS: The results suggest that the investigated lncRNAs may play important roles in breast cancer and comprise a potential factor that should be further evaluated in clinical studies.

Zobrazit více v PubMed

Sung H., Ferlay J., Siegel R.L., Laversanne M., Soerjomataram I. et al., Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries, Ca-Cancer J Clin 71 (2021), 209–249. doi: 10.3322/caac.21660. PubMed DOI

Xing J.A., Liu H.Z., Jiang W. and Wang L.H., LncRNA-Encoded Peptide: Functions and Predicting Methods, Front Oncol 10 (2021). doi: 10.3389/fonc.2020.622294. PubMed DOI PMC

Chi Y.J., Wang D., Wang J.P., Yu W.D. and Yang J.C., Long Non-Coding RNA in the Pathogenesis of Cancers, Cells 8 (2019). Article Number 1015. doi: 10.3390/cells8091015. PubMed DOI PMC

Jin H., Du W., Huang W.T., Yan J.J., Tang Q., Chen Y.B., Zou Z.Z., LncRNA and Breast Cancer: Progress From Identifying Mechanisms to Challenges and Opportunities of Clinical Treatment, Mol Ther-Nucleic Acids 25 (2021), 613–637. doi: 10.1016/j.omtn.2021.08.005. PubMed DOI PMC

He J.Y., Zhu S.M., Liang X., Zhang Q.X., Luo X.H., Liu C. and Song L.J., LncRNA As a Multifunctional Regulator in Cancer Multi-Drug Resistance, Mol Biol Rep 48 (2021), 6151–6165. doi: 10.1007/s11033-021-06603-7. PubMed DOI

Aprile M., Costa V., Cimmino A. and Calin G.A., Emerging Role of Oncogenic Long Noncoding RNA As Cancer Biomarkers, Int J Cancer 152 (2023), 822–834. doi: 10.1002/ijc.34282. PubMed DOI

Xu N., Chen F., Wang F.L., Lu X., Wang X., Lv M.M. and Lu C., Clinical Significance of High Expression of Circulating Serum LncRNA RP11-445H22.4 in Breast Cancer Patients: a Chinese Population-Based Study, Tumor Biol 36 (2015), 7659–7665. doi: 10.1007/s13277-015-3469-0. PubMed DOI

Jiao Z.Y., Tian Q., Li N., Wang H.B. and Li K.Z., Plasma Long Non-Coding RNAs LncRNAs Serve As Potential Biomarkers for Predicting Breast Cancer, Eur Rev Med Pharmacol Sci 22 (2018), 1994–1999. PubMed

Zhang L., Zhao F.Q., Li W.F., Song G.B., Kasim V. and Wu S.R., The Biological Roles and Molecular Mechanisms of Long Non-Coding RNA MEG3 in the Hallmarks of Cancer, Cancers 14 (2022). Article Number 6032. doi: 10.3390/cancers14246032. PubMed DOI PMC

Hu X., Zhang Q., Xing W.Y. and Wang W., Role of MicroRNA/LncRNA Intertwined With the Wnt/Beta-Catenin Axis in Regulating the Pathogenesis of Triple-Negative Breast Cancer, Front Pharmacol. 13 (2022). Article Number 814971. doi: 10.3389/fphar.2022.814971. PubMed DOI PMC

The Cancer Genome Atlas Program (TCGA). https://www.cancer.gov/tcga.

Edgar R., Domrachev M. and Lash A.E., Gene Expression Omnibus: NCBI gene expression and hybridization array data repository, Nucleic Acids Res 30 (2002), 207–10. doi: 10.1093/nar/30.1.207. PubMed DOI PMC

GEO DataSets. https://www.ncbi.nlm.nih.gov/gds.

Goldman M.J., Craft B., Hastie M., Repecka K., McDade F. et al. Visualizing and interpreting cancer genomics data via the Xena platform, Nat Biotechnol 38 (2020), 675–678. doi: 10.1038/s41587-020-0546-8. PubMed DOI PMC

UCSC Xena. https://xena.ucsc.edu/.

Hellemans J., Mortier G., De Paepe A., Speleman F. and Vandesompele J., qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data, Genome Biol. 8 (2007). Article number: R19. doi: 10.1186/gb-2007-8-2-r19. PubMed DOI PMC

Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A. and Speleman F., Accurate normalization of realtime quantitative RT-PCR data by geometric averaging of multiple internal control genes, Genome Biol 3 (2002). Article number: research0034.1. doi: 10.1186/gb-2002-3-7-research0034. PubMed DOI PMC

Parker J.S., Mullins M., Cheang M.C.U. et al. Supervised Risk Predictor of Breast Cancer Based on Intrinsic Subtypes, J Clin Oncol 27 (2009), 1160–1167. PubMed PMC

Zavesky L., Jandakova E., Weinberger V., Minar L., Hanzikova V. et al., Small Non-Coding RNA Profiling in Breast Cancer: Plasma U6 SnRNA, MiR-451a and MiR-548b-5p As Novel Diagnostic and Prognostic Biomarkers, Mol Biol Rep 49 (2022), 1955–1971. doi: 10.1007/s11033-021-07010-8. PubMed DOI

Yndestad S., Austreid E., Skaftnesmo K.O., Lonning P.E. and Eikesdal H.P., Divergent Activity of the Pseudogene PTENP1 in ER-Positive and Negative Breast Cancer, Mol Cancer Res 16 (2018), 78–89. doi: 10.1158/1541-7786.MCR-17-0207. PubMed DOI

Yi C., Li G., Wang W., Sun Y. et al. Disruption of YY1-EZH2 Interaction Using Synthetic Peptides Inhibits Breast Cancer Development, Cancers (Basel) 13 (2021), 2402. PubMed PMC

Shi X.B., Tang X.Q. and Su L., Overexpression of Long Noncoding RNA PTENP1 Inhibits Cell Proliferation and Migration Via Suppression of MiR-19b in Breast Cancer Cells, Oncol Res 26 (2018), 869–878. doi: 10.3727/096504017X15123838050075. PubMed DOI PMC

Gao X., Qin T., Mao J., Zhang J., Fan S.J. et al., PTENP1/MiR-20a/PTEN Axis Contributes to Breast Cancer Progression by Regulating PTEN Via PI3K/AKT Pathway, J Exp Clin Cancer Res 38 (2019). doi: 10.1186/s13046-019-1260-6. PubMed DOI PMC

Li R.K., Gao J., Guo L.H., Huang G.Q. and Luo W.H., PTENP1 Acts As a CeRNA to Regulate PTEN by Sponging MiR-19b and Explores the Biological Role of PTENP1 in Breast Cancer, Cancer Gene Ther 24 (2017), 309–315. doi: 10.1038/cgt.2017.29. PubMed DOI

Yndestad S., Austreid E., Knappskog S., Chrisanthar R., Lilleng P.K. et al., High PTEN Gene Expression Is a Negative Prognostic Marker in Human Primary Breast Cancers With Preserved P53 Function, Breast Cancer Res Treat 163 (2017), 177–190. doi: 10.1007/s10549-017-4160-5. PubMed DOI PMC

Dong L., Qi P., Xu M.D., Ni S.J., Huang D., Xu Q.H. et al., Circulating CUDR, LSINCT-5 and PTENP1 Long Noncoding RNAs in Sera Distinguish Patients With Gastric Cancer From Healthy Controls, Int J Cancer 137 (2015), 1128–1135. doi: 10.1002/ijc.29484. PubMed DOI

Yan B., Wubuli A., Liu Y.D. and Wang X., Long Non-Coding RNA Phosphatase and Tensin Homolog Pseudogene 1 Sup-presses Osteosarcoma Cell Growth Via the Phosphoinositide 3-Kinase/Protein Kinase B Signaling Pathway, Exp Ther Med 15 (2018), 4829–4837. doi: 10.3892/etm.2018.6021. PubMed DOI PMC

Niemczyk M., Ito Y., Huddleston J., Git A., Abu-Amero S., Caldas C., Moore G.E., Stojic L. and Murre A., Imprinted Chromatin Around DIRAS3 Regulates Alternative Splicing of GNG12-AS1, a Long Noncoding RNA, Am J Hum Genet 93 (2013), 224–235. doi: 10.1016/j.ajhg.2013.06.010. PubMed DOI PMC

Stojic L., Niemczyk M., Orjalo A., Ito Y., Ruijter A.E.M. et al., Transcriptional Silencing of Long Noncoding RNA GNG12-AS1 Uncouples Its Transcriptional and Product-Related Functions, Nat Commun 7 (2016). Article Number 10406. doi: 10.1038/ncomms10406. PubMed DOI PMC

Zhang C.Y., Yu M.S., Li X., Zhang Z., Han C.R. and Yan B., Overexpression of Long Non-Coding RNA MEG3 Suppresses Breast Cancer Cell Proliferation, Invasion, and Angiogenesis Through AKT Pathway. Tumor Biol 39 (2017). doi: 10.1177/1010428317701311. PubMed DOI

Zhu M.Z., Wang X.C., Gu Y.T., Wang F., Li L. and Qiu X.G., MEG3 Overexpression Inhibits the Tumorigenesis of Breast Cancer by Downregulating MiR-21 Through the PI3K/Akt Pathway, Arch Biochem Biophys 661 (2019), 22–30. doi: 10.1016/j.abb.2018.10.021. PubMed DOI

Zhu X.T., Lv L., Wang M.Z., Fan C., Lu X.F. et al., DNMT1 Facilitates Growth of Breast Cancer by Inducing MEG3 Hyper-Methylation, Cancer Cell Int 22 (2022). doi: 10.1186/s12935-022-02463-8. PubMed DOI PMC

Pan T., Ding H., Jin L., Yhang S., Wu D. et al., DNMT1-mediated demethylation of lncRNA MEG3 promoter suppressed breast cancer progression by repressing Notch1 signaling pathway, Cell Cycle 21 (2022), 2323–2337. doi: 10.1080/15384101.2022.2094662. PubMed DOI PMC

Cui X.R., Yi Q., Jing X., Huang Y., Tian J., et al., Mining Prognostic Significance of MEG3 in Human Breast Cancer Using Bioinformatics Analysis, Cell Physiol Biochem 50 (2018), 41–51. doi: 10.1159/000493956. PubMed DOI

Zhang J.J., Guo S.H. and Jia B.Q., Down-Regulation of Long Non-Coding RNA MEG3 Serves As an Unfavorable Risk Factor for Survival of Patients With Breast Cancer, Eur Rev Med Pharmacol Sci 20 (2016), 5143–5147. PubMed

Deocesano-Pereira C., Machado R.A.C., De Jesus-Ferreira H.C., Marchini T., Pereira T.F. et al., Functional Impact of the Long Non-Coding RNA MEG3 Deletion by CRISPR/Cas9 in the Human Triple Negative Metastatic Hs578T Cancer Cell Line, Oncol Lett 18 (2019), 5941–5951. doi: 10.3892/ol.2019.10969. PubMed DOI PMC

Sun L., Li Y. and Yang B.X., Downregulated Long Non-Coding RNA MEG3 in Breast Cancer Regulates Proliferation, Migration and Invasion by Depending on P53’s Transcriptional Activity, Biochem Biophys Res Commun 478 (2016), 323–329. doi: 10.1016/j.bbrc.2016.05.031. PubMed DOI

Wang X.X., Guo G.C., Qian X.K., Dou D.W. and Zhang Z. et al., MiR-506 Attenuates Methylation of LncRNA MEG3 to Inhibit Migration and Invasion of Breast Cancer Cell Lines Via Targeting SP1 and SP3, Cancer Cell Int 18 (2018). doi: 10.1186/s12935-018-0642-8. PubMed DOI PMC

Zhang Y., Wu J., Jing H., Huang G., Sun Z.L. and Xu S.M., Long Noncoding RNA MEG3 Inhibits Breast Cancer Growth Via Upregulating Endoplasmic Reticulum Stress and Activating NF-Kappa B and P53, J Cell Biochem 120 (2019), 6789–6797. doi: 10.1002/jcb.27982. PubMed DOI

Zhu M.Z., Wang F., Mi H.L., Li L., Wang J., Han M.L. and Gu Y.T., Long Noncoding RNA MEG3 Suppresses Cell Prolifer-ation, Migration and Invasion, Induces Apoptosis and Paclitaxel-Resistance Via MiR-4513/PBLD Axis in Breast Cancer Cells, Cell Cycle 19 (2020), 3277–3288. doi: 10.1080/15384101.2020.1839700. PubMed DOI PMC

Ren G.Y., Han G.L., Song Z.Z., Zang A.M., Liu B. et al., LncRNA MCM3AP-AS1 Downregulates LncRNA MEG3 in Triple Negative Breast Cancer to Inhibit the Proliferation of Cancer Cells, Crit Rev Eukaryotic Gene Expression 31 (2021), 81–87. doi: 10.1615/CritRevEukaryotGeneExpr.2021038296. PubMed DOI

Xu J., Wang X., Zhu C.M. and Wang K.F., A Review of Current Evidence About LncRNA MEG3: A Tumor Suppressor in Multiple Cancers, Front Cell Dev Biol 10 (2022). Article Number 997633. doi: 10.3389/fcell.2022.997633. PubMed DOI PMC

Yang Y., Yang H., Xu M. and Zhang H.B., Sun M.T. et al., Long Non-Coding RNA LncRNA MAGI2-AS3 Inhibits Breast Cancer Cell Growth by Targeting the Fas/FasL Signalling Pathway, Hum Cell 31 (2018), 232–241. doi: 10.1007/s13577-018-0206-1. PubMed DOI

Du S.M., Hu W., Zhao Y., Zhou H.Z. and Wen W. et al., Long Non-Coding RNA MAGI2-AS3 Inhibits Breast Cancer Cell Migration and Invasion Via Sponging MicroRNA-374a, Cancer Biomarkers 24 (2019), 269–277. doi: 10.3233/CBM-182216. PubMed DOI

Xu X.L., Yuan X.N., Ni J.L., Guo J., Gao Y. et al., MAGI2-AS3 Inhibits Breast Cancer by Downregulating DNA Methylation of MAGI2. J Cell Physiol 236 (2021), 1116–1130. doi: 10.1002/jcp.29922. PubMed DOI

Tian T., Gong Z.Q., Wang M., Hao R.H., Lin S. et al., Identification of Long Non-Coding RNA Signatures in Triple-Negative Breast Cancer, Cancer Cell Int 18 (2018). Article Number 103. doi: 10.1186/s12935-018-0598-8. PubMed DOI PMC

Zhang Z., Yi Y., Wai Z., Zhang H., Zhao Y. et al. LncRNA MAGI2-AS3-Encoded Polypeptide Restrains the Proliferation and Migration of Breast Cancer Cells, Molecular Biotechnology (2023). doi: 10.1007/s12033-023-00801-3. PubMed DOI

Li F., Hu Q., Pang Z.H. and Xu X.Q., LncRNA MAGI2-AS3 Upregulates Cytokine Signaling 1 by Sponging MiR-155 in Non-Small Cell Lung Cancer, Cancer Biother, Radiopharm 35 (2020), 72–76. doi: 10.1089/cbr.2019.2898. PubMed DOI

Yin Z., Ma T.T., Yan J.H., Shi N., Zhang C.Z. et al., LncRNA MAGI2-AS3 Inhibits Hepatocellular Carcinoma Cell Proliferation and Migration by Targeting the MiR-374b-5p/SMG1 Signaling Pathway, J Cell Physiol 234 (2019), 18825–18836. doi: 10.1002/jcp.28521. PubMed DOI

Chen X.D., Zhu M.X. and Wang S.J., Expression of Long Non-Coding RNA MAGI2-AS3 in Human Gliomas and Its Prognostic Significance, Eur Rev Med Pharmacol Sci 23 (2019), 3455–3460. PubMed

Cao C., Zhou S. and Hu J., Long Noncoding RNA MAGI2-AS3/MiR-218-5p/GDPD5/SEC61A1 Axis Drives Cellular Proliferation and Migration and Confers Cisplatin Resistance in Nasopharyngeal Carcinoma, Int Forum Allergy Rhinol 10 (2020), 1012–1023. doi: 10.1002/alr.22562. PubMed DOI

Liu Q.F., Liu S., Wang X.Y., Zhang J. and Liu K.R., LncRNA MAGI2-AS3 Is Involved in Cervical Squamous Cell Carcinoma Development Through CDK6 Up-Regulation, Infect Agents Cancer 14 (2019). Article Number 37. doi: 10.1186/s13027-019-0238-5. PubMed DOI PMC

Xu T.X., Yan Z.Y., Lu J.T., Chen L.Y., Li X.X. et al., Long Non-Coding RNA NRSN2-AS1, Transcribed by SOX2, Promotes Progression of Esophageal Squamous Cell Carcinoma by Regulating the Ubiquitin-Degradation of PGK1, Clin Exp Metastasis 39 (2022), 757–769. doi: 10.1007/s10585-022-10174-7. PubMed DOI

Chen Q., Xie J. and Yang Y.S., Long Non-Coding RNA NRSN2-AS1 Facilitates Tumorigenesis and Progression of Ovarian Cancer Via MiR-744-5p/PRKX Axis, Biol Reprod 106 (2021), 526–539. doi: 10.1093/biolre/ioab212. PubMed DOI

Chen G.Y. and Wang D., Prognostic Value of Macrophage-Associated Long Non-Coding RNA Expression for Hepatocellular Carcinoma, Cancer Manage Res 14 (2022), 215–224. doi: 10.2147/CMAR.S340574. PubMed DOI PMC

Tuo Y.L., Li X.M. and Luo J., Long Noncoding RNA UCA1 Modulates Breast Cancer Cell Growth and Apoptosis Through Decreasing Tumor Suppressive MiR-143, Eur Rev Med Pharmacol Sci 19 (2015), 3403–3411. PubMed

Li Y., Zeng Q.G., Qiu J.L., Pang T., Xian J.Z. and Zhang X.X., Long Non-Coding RNA UCA1 Promotes Breast Cancer by Upregulating PTP1B Expression Via Inhibiting MiR-206, Cancer Cell Int 19 (2019). Article Number 275. doi: 10.1186/s12935-019-0958-z. PubMed DOI PMC

Xu C.G., Yang M.F., Ren Y.Q., Wu C.H. and Wang L.Q., Exosomes Mediated Transfer of IncRNA UCA1 Results in Increased Tamoxifen Resistance in Breast Cancer Cells, Eur Rev Med Pharmacol Sci 20 (2016), 4362–4368. PubMed

Li X.N., Wu Y.M., Liu A.H. and Tang X., Long Non-Coding RNA UCA1 Enhances Tamoxifen Resistance in Breast Cancer Cells Through a MiR-18a-HIF1 Alpha Feedback Regulatory Loop, Tumor Biol 37 (2016), 14733–14743. doi: 10.1007/s13277-016-5348-8. PubMed DOI

Liu C.H., Jiang F., Zhang X.Q. and Xu X.L., Long Non-Coding RNA UCA1 Modulates Paclitaxel Resistance in Breast Cancer Via MiR-613/CDK12 Axis, Cancer Manage Res 12 (2020), 2777–2788. doi: 10.2147/CMAR.S241969. PubMed DOI PMC

Wo L.K., Zhang B., You X.B., Hu Y.Y., Gu Z.Q. et al., Up-Regulation of LncRNA UCA1 by TGF-Beta Promotes Doxorubicin Resistance in Breast Cancer Cells, Immunopharmacol, Immunotoxicol 44 (2022), 492–499. doi: 10.1080/08923973.2022.2054428. PubMed DOI

Wang H.H., Guan Z.H., He K.F., Qian J., Cao J. and Teng L.S., LncRNA UCA1 in Anti-Cancer Drug Resistance, Oncotarget 8 (2017), 64638–64650. doi: 10.18632/oncotarget.18344. PubMed DOI PMC

Xiao C., Wu C.H. and Hu H.Z., LncRNA UCA1 Promotes Epithelial-Mesenchymal Transition EMT of Breast Cancer Cells Via Enhancing Wnt/Beta-Catenin Signaling Pathway, Eur Rev Med Pharmacol Sci 20 (2016), 2819–2824. PubMed

Tang L., Wang S., Wang Y.P., Li K. and Li Q., LncRNA-UCA1 Regulates Lung Adenocarcinoma Progression Through Competitive Binding to MiR-383, Cell Cycle 22 (2023), 213–228. doi: 10.1080/15384101.2022.2111929. PubMed DOI PMC

An M., Xing X.F. and Chen T.H., Long Non-Coding RNA UCA1 Enhances Cervical Cancer Cell Proliferation and Invasion by Regulating MicroRNA-299-3p Expression, Oncol Lett 22 (2021). Article Number 772. doi: 10.3892/ol.2021.13033. PubMed DOI PMC

Wambecke A., Ahmad M., Morice P.M., Lambert B., Weiswald L.B. et al., The LncRNA ‘UCA1’ Modulates the Response to Chemotherapy of Ovarian Cancer Through Direct Binding to MiR-27a-5p and Control of UBE2N Levels, Mol Oncol 15 (2021), 3659–3678. doi: 10.1002/1878-0261.13045. PubMed DOI PMC

Hosseini N.F., Manoochehri H., Khoei S.G. and Sheykhhasan M., The Functional Role of Long Non-Coding RNA UCA1 in Human Multiple Cancers: a Review Study, Curr Mol Med 21 (2021), 96–110. doi: 10.2174/1566524020666200619124543. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...