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Research Articles

Identification of miRNAs and related hub genes associated with the triple negative breast cancer using integrated bioinformatics analysis and in vitro approach

, , , , &
Pages 11676-11690 | Received 30 May 2021, Accepted 24 Jul 2021, Published online: 13 Aug 2021

References

  • Alarmo, E. L., Kuukasjärvi, T., Karhu, R., & Kallioniemi, A. (2007). A comprehensive expression survey of bone morphogenetic proteins in breast cancer highlights the importance of BMP4 and BMP7. Breast Cancer Research & Treatment, 103(2), 239–246. https://doi.org/10.1007/s10549-006-9362-1
  • Altomare, D. A., & Testa, J. R. (2005). Perturbations of the AKT signaling pathway in human cancer. Oncogene, 24(50), 7455–7464. https://doi.org/10.1038/sj.onc.1209085
  • Avery-Kiejda, K. A., Braye, S. G., Mathe, A., Forbes, J. F., & Scott, R. J. (2014). Decreased expression of key tumour suppressor microRNAs is associated with lymph node metastases in triple negative breast cancer. BMC Cancer, 14, 51. https://doi.org/10.1186/1471-2407-14-51
  • Bai, Y., Kinne, J., Ding, L., Rath, E. C., Cox, A., & Naidu, S. D. (2017). Identification of genome-wide non-canonical spliced regions and analysis of biological functions for spliced sequences using Read-Split-Fly. BMC Bioinformatics, 18(Suppl 11), 382h. https://doi.org/10.1186/s12859-017-1801-y
  • Barrett, T., Wilhite, S. E., Ledoux, P., Evangelista, C., Kim, I. F., Tomashevsky, M., Marshall, K. A., Phillippy, K. H., Sherman, P. M., Holko, M., Yefanov, A., Lee, H., Zhang, N., Robertson, C. L., Serova, N., Davis, S., & Soboleva, A. (2013). NCBI GEO: Archive for functional genomics data sets-update. Nucleic Acids Research, 41(Database issue), D991–D995. https://doi.org/10.1093/nar/gks1193
  • Cao, F. Y., Zheng, Y. B., Yang, C., Huang, S. Y., He, X. B., & Tong, S. L. (2020). miR-635 targets KIFC1 to inhibit the progression of gastric cancer. Journal of Investigative Medicine: The Official Publication of the American Federation for Clinical Research, 68(8), 1357–1363. https://doi.org/10.1136/jim-2020-001438
  • Castronovo, V., Kusaka, M., Chariot, A., Gielen, J., & Sobel, M. (1994). Homeobox genes: Potential candidates for the transcriptional control of the transformed and invasive phenotype. Biochemical Pharmacology, 47(1), 137–143. https://doi.org/10.1016/0006-2952(94)90447-2
  • Cheung, S. Y., Boey, Y. J., Koh, V. C., Thike, A. A., Lim, J. C., Iqbal, J., & Tan, P. H. (2015). Role of epithelial-mesenchymal transition markers in triple-negative breast cancer. Breast Cancer Research & Treatment, 152(3), 489–498. https://doi.org/10.1007/s10549-015-3485-1
  • Chin, C. H., Chen, S. H., Wu, H. H., Ho, C. W., Ko, M. T., & Lin, C. Y. (2014). cytoHubba: Identifying hub objects and sub-networks from complex interactome. BMC Systems Biology, 8 Suppl 4(4), S11–S17. https://doi.org/10.1186/1752-0509-8-S4-S11
  • Dawson, S. J., Provenzano, E., & Caldas, C. (2009). Triple negative breast cancers: Clinical and prognostic implications. European Journal of Cancer, 45(1), 27–40. https://doi.org/10.1016/S0959-8049(09)70013-9
  • Dvinge, H., Git, A., Gräf, S., Salmon-Divon, M., Curtis, C., Sottoriva, A., Zhao, Y., Hirst, M., Armisen, J., Miska, E. A., Chin, S. F., Provenzano, E., Turashvili, G., Green, A., Ellis, I., Aparicio, S., & Caldas, C. (2013). The shaping and functional consequences of the microRNA landscape in breast cancer. Nature, 497(7449), 378–382. https://doi.org/10.1038/nature12108
  • Fan, C., & Liu, N. (2019). Identification of dysregulated microRNAs associated with diagnosis and prognosis in triple-negative breast cancer: An in silico study. Oncology Reports, 41(6), 3313–3324. https://doi.org/10.3892/or.2019.7094
  • Fife, C. M., McCarroll, J. A., & Kavallaris, M. (2014). Movers and shakers: Cell cytoskeleton in cancer metastasis. British Journal of Pharmacology, 171(24), 5507–5523. https://doi.org/10.1111/bph.12704
  • Gao, J., Aksoy, B. A., Dogrusoz, U., Dresdner, G., Gross, B., Sumer, S. O., Sun, Y., Jacobsen, A., Sinha, R., Larsson, E., Cerami, E., Sander, C., & Schultz, N. (2013). Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Science Signaling, 6(269), pl1. https://doi.org/10.1126/scisignal.2004088
  • Huang, D., Sherman, B. T., & Lempicki, R. A. (2009). Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37(1), 1–13. https://doi.org/10.1093/nar/gkn923
  • Huang, D., Sherman, B. T., & Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4(1), 44–57. https://doi.org/10.1038/nprot.2008.211
  • Hussain, I., Bhan, A., Ansari, K. I., Deb, P., Bobzean, S. A., Perrotti, L. I., & Mandal, S. S. (2015). Bisphenol-A induces expression of HOXC6, an estrogen-regulated homeobox-containing gene associated with breast cancer. Biochimica et Biophysica Acta, 1849(6), 697–708. https://doi.org/10.1016/j.bbagrm.2015.02.003
  • Ishrat, R., Ahmed, M. M., Tazyeen, S., Alam, A., Farooqui, A., Ali, R., Imam, N., Tamkeen, N., Ali, S., Zubbair Malik, M., & Sultan, A. (2021). In silico integrative approach revealed key microRNAs and associated target genes in cardiorenal syndrome. Bioinformatics & Biology Insights, 15, 11779322211027396–11779322211027398. https://doi.org/10.1177/11779322211027396
  • Kanehisa, M. (2002). The KEGG database. Novartis Foundation Symposium, 247, 91–252.
  • Kumar, S., Kushwaha, P. P., & Gupta, S. (2019). Emerging targets in cancer drug resistance. Cancer Drug Resistance, 2(2), 161–177. https://doi.org/10.20517/cdr.2018.27
  • Kushwaha, P. P., Gupta, S., Singh, A. K., & Kumar, S. (2019a). Emerging role of migration and invasion enhancer 1 (MIEN1) in cancer progression and metastasis. Frontiers in Oncology, 9, 868. https://doi.org/10.3389/fonc.2019.00868
  • Kushwaha, P. P., Gupta, S., Singh, A. K., Prajapati, K. S., Shuaib, M., & Kumar, S. (2020a). MicroRNA targeting nicotinamide adenine dinucleotide phosphate oxidases in cancer. Antioxidants & Redox Signal, 32(5), 267–284. https://doi.org/10.1089/ars.2019.7918
  • Kushwaha, P. P., Singh, A. K., Prajapati, K. S., Shuaib, M., Fayez, S., Bringmann, G., & Kumar, S. (2020b). Induction of apoptosis in breast cancer cells by naphthylisoquinoline alkaloids. Toxicology & Applied Pharmacology, 409, 115297. https://doi.org/10.1016/j.taap.2020.115297
  • Kushwaha, P. P., Singh, A. K., Shuaib, M., Prajapati, K. S., Vardhan, P. S., Gupta, S., & Kumar, S. (2020c). 3-O-(E)-p-Coumaroyl betulinic acid possess anticancer activity and inhibit notch signaling pathway in breast cancer cells and mammosphere. Chemical Biology & Interaction, 328, 109200. https://doi.org/10.1016/j.cbi.2020.109200
  • Kushwaha, P. P., Vardhan, P. S., Kapewangolo, P., Shuaib, M., Prajapati, S. K., Singh, A. K., & Kumar, S. (2019b). Bulbine frutescens phytochemical inhibits notch signaling pathway and induces apoptosis in triple negative and luminal breast cancer cells. Life Science, 234, 116783. https://doi.org/10.1016/j.lfs.2019.116783
  • Lánczky, A., Nagy, Á., Bottai, G., Munkácsy, G., Szabó, A., Santarpia, L., & Győrffy, B. (2016). miRpower: A web-tool to validate survival-associated miRNAs utilizing expression data from 2178 breast cancer patients. Breast Cancer Research & Treatment, 160(3), 439–446. https://doi.org/10.1007/s10549-016-4013-7
  • Li, Y., Liu, X., Tang, H., Yang, H., & Meng, X. (2017). RNA sequencing uncovers molecular mechanisms underlying pathological complete response to chemotherapy in patients with operable breast cancer. Medical Science Monitor: International Medical Journal of Experimental & Clinical Research, 23, 4321–4327. https://doi.org/10.12659/msm.903272
  • Ling, H., Fabbri, M., & Calin, G. A. (2013). MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nature Reviews: Drug Discovery, 12(11), 847–865. https://doi.org/10.1038/nrd4140
  • Lu, F., Xu, F. L., Kuang, G., Dong, Z. M., Guo, Y. L., Shen, S. P., Liang, J., Lu, S., & Guo, W. (2012). Expressions of microRNA-1250 and its host gene AATK and AATK gene methylation status in human esophageal squamous cell carcinoma. Tumor, 37(5), 483–490. https://doi.org/10.3781/j.issn.1000-7431.2017.33.075
  • Lu, T. P., Lee, C. Y., Tsai, M. H., Chiu, Y. C., Hsiao, C. K., Lai, L. C., & Chuang, E. Y. (2012). miRSystem: An integrated system for characterizing enriched functions and pathways of microRNA targets. PloS One, 7(8), e42390. https://doi.org/10.1371/journal.pone.0042390
  • Melo, S. A., Sugimoto, H., O'Connell, J. T., Kato, N., Villanueva, A., Vidal, A., Qiu, L., Vitkin, E., Perelman, L. T., Melo, C. A., Lucci, A., Ivan, C., Calin, G. A., & Kalluri, R. (2014). Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell, 26(5), 707–721. https://doi.org/10.1016/j.ccell.2014.09.005
  • Munding, J. B., Adai, A. T., Maghnouj, A., Urbanik, A., Zöllner, H., Liffers, S. T., Chromik, A. M., Uhl, W., Szafranska-Schwarzbach, A. E., Tannapfel, A., & Hahn, S. A. (2012). Global microRNA expression profiling of microdissected tissues identifies miR-135b as a novel biomarker for pancreatic ductal adenocarcinoma. International Journal of Cancer, 131(2), E86–E95. https://doi.org/10.1002/ijc.26466
  • Nama, S., Muhuri, M., Di Pascale, F., Quah, S., Aswad, L., Fullwood, M., & Sampath, P. (2019). MicroRNA-138 is a prognostic biomarker for triple-negative breast cancer and promotes tumorigenesis via TUSC2 repression. Scientific Reports, 9(1), 12718. https://doi.org/10.1038/s41598-019-49155-4
  • Nedeljković, M., & Damjanović, A. (2019). Mechanisms of chemotherapy resistance in triple-negative breast cancer – How we can rise to the challenge. Cells, 8(9), 957. https://doi.org/10.3390/cells8090957
  • Nie, Y., Jiao, Y., Li, Y., & Li, W. (2019). Investigation of the clinical significance and prognostic value of the lncRNA ACVR2B-As1 in liver cancer. Biomedical Research International, 2019, 4602371. https://doi.org/10.1155/2019/4602371
  • Nissinen, T. A., Hentilä, J., Penna, F., Lampinen, A., Lautaoja, J. H., Fachada, V., Holopainen, T., Ritvos, O., Kivelä, R., & Hulmi, J. J. (2018). Treating cachexia using soluble ACVR2B improves survival, alters mTOR localization, and attenuates liver and spleen responses. Journal of Cachexia Sarcopenia Muscle, 9(3), 514–529. https://doi.org/10.1002/jcsm.12310
  • Nitulescu, G. M., Margina, D., Juzenas, P., Peng, Q., Olaru, O. T., Saloustros, E., Fenga, C., Spandidos, D. Α., Libra, M., & Tsatsakis, A. M. (2016). Akt inhibitors in cancer treatment: The long journey from drug discovery to clinical use (Review). International Journal of Oncology, 48(3), 869–885. https://doi.org/10.3892/ijo.2015.3306
  • Normanno, N., Bianco, C., Strizzi, L., Mancino, M., Maiello, M. R., De Luca, A., Caponigro, F., & Salomon, D. S. (2005). The ErbB receptors and their ligands in cancer: An overview. Current Drug Targets, 6(3), 243–257. https://doi.org/10.2174/1389450053765879
  • Oliveros, J. C. 2007–2015. Venny. An interactive tool for comparing lists with Venn’s diagram. https://bioinfogp.cnb.csic.es/tools/venny/
  • Paszek, S., Gabło, N., Barnaś, E., Szybka, M., Morawiec, J., Kołacińska, A., & Zawlik, I. (2017). Dysregulation of microRNAs in triple-negative breast cancer. Ginekologia Polska, 88(10), 530–536. https://doi.org/10.5603/GP.a2017.0097
  • Penrod, N. M., & Moore, J. H. (2013). Key genes for modulating information flow play a temporal role as breast tumor coexpression networks are dynamically rewired by letrozole. BMC Medical Genomics, 6(Suppl 2), S2. https://doi.org/10.1186/1755-8794-6-S2-S2
  • Qiu, Q., Liu, J., Shao, J., Lou, X., Chen, C., & Lin, B. (2015). Target-resequencing to identify microRNA-associated SNP and predict the effect of SNP on microRNA function in colorectal cancer patients. Chinese Journal Oncology, 37(10), 759–763.
  • Rehmsmeier, M., Steffen, P., Hochsmann, M., & Giegerich, R. (2004). Fast and effective prediction of microRNA/target duplexes. RNA (New York, NY), 10(10), 1507–1517. https://doi.org/10.1261/rna.5248604
  • Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003). Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Research, 13(11), 2498–2504. https://doi.org/10.1101/gr.1239303
  • Shao, F., Sun, H., & Deng, C. X. (2017). Potential therapeutic targets of triple-negative breast cancer based on its intrinsic subtype. Oncotarget, 8(42), 73329–73344. https://doi.org/10.18632/oncotarget.20274
  • Shenoy, A., & Blelloch, R. H. (2014). Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nature Reviews. Molecular Cell Biology, 15(9), 565–576. https://doi.org/10.1038/nrm3854
  • Shoubridge, C., Tarpey, P. S., Abidi, F., Ramsden, S. L., Rujirabanjerd, S., Murphy, J. A., Boyle, J., Shaw, M., Gardner, A., Proos, A., Puusepp, H., Raymond, F. L., Schwartz, C. E., Stevenson, R. E., Turner, G., Field, M., Walikonis, R. S., Harvey, R. J., Hackett, A., … Gécz, J. (2010). Mutations in the guanine nucleotide exchange factor gene IQSEC2 cause nonsyndromic intellectual disability. Nature Genetics, 42(6), 486–488. https://doi.org/10.1038/ng.588
  • Siegel, R. L., Miller, K. D., & Jemal, A. (2017). Cancer statistics, 2017. CA: A Cancer Journal for Clinicians, 67(1), 7–30. https://doi.org/10.3322/caac.21387
  • Stinson, S., Lackner, M. R., Adai, A. T., Yu, N., Kim, H.-J., O'Brien, C., Spoerke, J., Jhunjhunwala, S., Boyd, Z., Januario, T., Newman, R. J., Yue, P., Bourgon, R., Modrusan, Z., Stern, H. M., Warming, S., de Sauvage, F. J., Amler, L., Yeh, R.-F., & Dornan, D. (2011). TRPS1 targeting by miR-221/222 promotes the epithelial-to-mesenchymal transition in breast cancer. Science Signaling, 4(177), ra41. 10.1126/scisignal.2001538
  • Tang, Z., Li, C., Kang, B., Gao, G., Li, C., & Zhang, Z. (2017). GEPIA: A web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Research, 45(W1), W98–W102. https://doi.org/10.1093/nar/gkx247
  • Teplyuk, N. M., Uhlmann, E. J., Gabriely, G., Volfovsky, N., Wang, Y., Teng, J., Karmali, P., Marcusson, E., Peter, M., Mohan, A., Kraytsberg, Y., Cialic, R., Chiocca, E. A., Godlewski, J., Tannous, B., & Krichevsky, A. M. (2016). Therapeutic potential of targeting microRNA-10b in established intracranial glioblastoma: First steps toward the clinic. EMBO Molecular Medicine, 8(3), 268–287. https://doi.org/10.15252/emmm.201505495
  • Tian, L., Guo, Z., Wang, H., & Liu, X. (2017). MicroRNA-635 inhibits the malignancy of osteosarcoma by inducing apoptosis. Molecular Medicine Reports, 16(4), 4829–4834. https://doi.org/10.3892/mmr.2017.7127
  • Turashvili, G., Lightbody, E. D., Tyryshkin, K., SenGupta, S. K., Elliott, B. E., Madarnas, Y., Ghaffari, A., Day, A., & Nicol, C. (2018). Novel prognostic and predictive microRNA targets for triple-negative breast cancer. FASEB Journal. https://doi.org/10.1096/fj.201800120R
  • Vicier, C., Dieci, M. V., Arnedos, M., Delaloge, S., Viens, P., & Andre, F. (2014). Clinical development of mTOR inhibitors in breast cancer. Breast Cancer Research: BCR, 16(1), 203. https://doi.org/10.1186/bcr3618
  • Wang, D., Naydenov, N. G., Dozmorov, M. G., Koblinski, J. E., & Ivanov, A. I. (2020). Anillin regulates breast cancer cell migration, growth, and metastasis by non-canonical mechanisms involving control of cell stemness and differentiation. Breast Cancer Research, 22(1), 3. https://doi.org/10.1186/s13058-019-1241-x
  • Wang, L., Tang, H., Thayanithy, V., Subramanian, S., Oberg, A. L., Cunningham, J. M., Cerhan, J. R., Steer, C. J., & Thibodeau, S. N. (2009). Gene networks and microRNAs implicated in aggressive prostate cancer. Cancer Research, 69(24), 9490–9497. https://doi.org/10.1158/0008-5472.CAN-09-2183
  • Wang, X., Chen, T., Zhang, Y., Zhang, N., Li, C., Li, Y., Liu, Y., Zhang, H., Zhao, W., Chen, B., Wang, L., & Yang, Q. (2019). Long noncoding RNA Linc00339 promotes triple-negative breast cancer progression through miR-377-3p/HOXC6 signaling pathway. Journal of Cellular Physiology, 234(8), 13303–13317. https://doi.org/10.1002/jcp.28007
  • Waseem, M., Ahmad, M. K., Srivatava, V. K., Rastogi, N., Serajuddin, M., Kumar, S., Mishra, D. P., Sankhwar, S. N., & Mahdi, A. A. (2017). Evaluation of miR-711 as novel biomarker in prostate cancer progression. Asian Pacific Journal of Cancer Prevention: APJCP, 18(8), 2185–2191. https://doi.org/10.22034/APJCP.2017.18.8.2185
  • Wu, X., Ding, M., & Lin, J. (2019). Three-microRNA expression signature predicts survival in triple-negative breast cancer. Oncology Letters, 19(1), 301–308. https://doi.org/10.3892/ol.2019.11118
  • Yadi, W., Shurui, C., Tong, Z., Suxian, C., Qing, T., & Dongning, H. (2020). Bioinformatic analysis of peripheral blood miRNA of breast cancer patients in relation with anthracycline cardiotoxicity. BMC Cardiovascular Disorders, 20(1), 43. https://doi.org/10.1186/s12872-020-01346-y
  • Ye, Y., Zhang, F., Chen, Q., Huang, Z., & Li, M. (2019). LncRNA MALAT1 modified progression of clear cell kidney carcinoma (KIRC) by regulation of miR-194-5p/ACVR2B signaling. Molecular Carcinogenesis, 58(2), 279–292. https://doi.org/10.1002/mc.22926
  • Zhang, M. Y., Wang, L. Q., & Chim, C. S. (2021). miR-1250-5p is a novel tumor suppressive intronic miRNA hypermethylated in non-Hodgkin's lymphoma: Novel targets with impact on ERK signaling and cell migration. Cell Communication & Signaling, 19(1), 62. https://doi.org/10.1186/s12964-021-007070
  • Zhang, Y., Sun, Z., Zhang, Y., Fu, T., Liu, C., Liu, Y., & Lin, Y. (2016). The microRNA-635 suppresses tumorigenesis in non-small cell lung cancer. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie, 84, 1274–1281. https://doi.org/10.1016/j.biopha.2016.10.040

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