The Overexpressed MicroRNAs miRs-182, 155, 493, 454, and U6 snRNA and Underexpressed let-7c, miR-328, and miR-451a as Potential Biomarkers in Invasive Breast Cancer and Their Clinicopathological Significance

. 2025 ; 103 (2) : 112-127. [epub] 20240812

Jazyk angličtina Země Švýcarsko Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39134012

INTRODUCTION: Breast cancer comprises the leading cause of cancer-related death in women. MicroRNAs (miRNAs) have emerged as important factors with concern to carcinogenesis and have potential for use as biomarkers. METHODS: This study provides a comprehensive evaluation of the microRNA expression in invasive breast carcinoma of no special type tissues compared with benign tissues via large-scale screening and the candidate-specific validation of 15 miRNAs and U6 snRNA applying qPCR and the examination of clinicopathological data. RESULTS: Of the six downregulated miRNAs, let-7c was identified as the most promising miRNA biomarker and its lower expression was linked with Ki-67 positivity, luminal B versus luminal A samples, multifocality, lymph node metastasis, and inferior PFS. Of the 9 upregulated sncRNAs, the data on U6 snRNA, miR-493 and miR-454 highlighted their potential oncogenic functions. An elevated U6 snRNA expression was associated with the tumor grade, Ki-67 positivity, luminal B versus A samples, lymph node metastasis, and worsened PFS (and OS) outcomes. An elevated miR-454 expression was detected in higher grades, Ki-67 positive and luminal B versus A samples. Higher miR-493 levels were noted for the tumor stage (and grade) and worse patient outcomes (PFS, OS). The data also suggested that miR-451a and miR-328 may have tumor suppressor roles, and miR-182 and miR-200c pro-oncogenic functions, while the remaining sncRNAs did not evince any significant associations. CONCLUSION: We showed particular microRNAs and U6 snRNA as differentially expressed between tumors and benign tissues and associated with clinicopathological parameters, thus potentially corresponding with important roles in breast carcinogenesis. Their importance should be further investigated and evaluated in follow-up studies to reveal their potential in clinical practice. INTRODUCTION: Breast cancer comprises the leading cause of cancer-related death in women. MicroRNAs (miRNAs) have emerged as important factors with concern to carcinogenesis and have potential for use as biomarkers. METHODS: This study provides a comprehensive evaluation of the microRNA expression in invasive breast carcinoma of no special type tissues compared with benign tissues via large-scale screening and the candidate-specific validation of 15 miRNAs and U6 snRNA applying qPCR and the examination of clinicopathological data. RESULTS: Of the six downregulated miRNAs, let-7c was identified as the most promising miRNA biomarker and its lower expression was linked with Ki-67 positivity, luminal B versus luminal A samples, multifocality, lymph node metastasis, and inferior PFS. Of the 9 upregulated sncRNAs, the data on U6 snRNA, miR-493 and miR-454 highlighted their potential oncogenic functions. An elevated U6 snRNA expression was associated with the tumor grade, Ki-67 positivity, luminal B versus A samples, lymph node metastasis, and worsened PFS (and OS) outcomes. An elevated miR-454 expression was detected in higher grades, Ki-67 positive and luminal B versus A samples. Higher miR-493 levels were noted for the tumor stage (and grade) and worse patient outcomes (PFS, OS). The data also suggested that miR-451a and miR-328 may have tumor suppressor roles, and miR-182 and miR-200c pro-oncogenic functions, while the remaining sncRNAs did not evince any significant associations. CONCLUSION: We showed particular microRNAs and U6 snRNA as differentially expressed between tumors and benign tissues and associated with clinicopathological parameters, thus potentially corresponding with important roles in breast carcinogenesis. Their importance should be further investigated and evaluated in follow-up studies to reveal their potential in clinical practice.

Zobrazit více v PubMed

Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. . Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49. PubMed

Najjar S, Allison KH. Updates on breast biomarkers. Virchows Arch. 2022;480(1):163–76. PubMed

Ortiz MMO, Andrechek ER. Molecular characterization and landscape of breast cancer models from a multi-omics perspective. J Mammary Gland Biol Neoplasia. 2023;28(1):12. PubMed PMC

Beermann J, Piccoli MT, Viereck J, Thum T. Non-coding RNAs in development and disease: background, mechanisms, and therapeutic approaches. Physiol Rev. 2016;96(4):1297–325. PubMed

Romano G, Veneziano D, Acunzo M, Croce CM. Small non-coding RNA and cancer. Carcinogenesis. 2017;38(5):485–91. PubMed PMC

Di Leva G, Garofalo M, Croce CM. MicroRNAs in cancer. In: Abbas AK, Galli SJ, Howley PM, editors. Annu rev pathol. Mechanisms of disease; 2014. Vol. Vol. 9. p. 287–314. PubMed PMC

Bhan A, Soleimani M, Mandal SS. Long noncoding RNA and cancer: a new paradigm. Cancer Res. 2017;77(15):3965–81. PubMed PMC

Volovat SR, Volovat C, Hordila I, Hordila DA, Mirestean CC, Miron OT, et al. . MiRNA and LncRNA as potential biomarkers in triple-negative breast cancer: a review. Front Oncol. 2020;10:526850. PubMed PMC

Zavesky L, Jandakova E, Weinberger V, Minar L, Hanzikova V, Duskova D, 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. 2022;49(3):1955–71. PubMed

Zavesky L, Jandakova E, Weinberger V, Minar L, Kohoutova M, Slanar O. Long non-coding RNAs PTENP1, GNG12-AS1, MAGI2-AS3 and MEG3 as tumor suppressors in breast cancer and their associations with clinicopathological parameters. Cancer Biomark. 2024;40(1):61–78. PubMed PMC

Liang JN, Wen JY, Huang Z, Chen XP, Zhang BX, Chu L. Small nucleolar RNAs: insight into their function in cancer. Front Oncol. 2019;9:587. PubMed PMC

Dvinge H, Guenthoer J, Porter PL, Bradley RK. RNA components of the spliceosome regulate tissue-and cancer-specific alternative splicing. Genome Res. 2019;29(10):1591–604. PubMed PMC

Appaiah HN, Goswami CP, Mina LA, Badve S, Sledge GW, Liu YL, et al. . Persistent upregulation of U6:SNORD44 small RNA ratio in the serum of breast cancer patients. Breast Cancer Res. 2011;13(5):R86. PubMed PMC

Naeli P, Winter T, Hackett AP, Alboushi L, Jafarnejad SM. The intricate balance between microRNA-induced mRNA decay and translational repression. FEBS J. 2023;290(10):2508–24. PubMed

Si WG, Shen JY, Zheng HL, Fan WM. The role and mechanisms of action of microRNAs in cancer drug resistance. Clin Epigenetics. 2019;11(1):25. PubMed PMC

Bertoli G, Cava C, Castiglioni I. MicroRNAs: new biomarkers for diagnosis, prognosis, therapy prediction and therapeutic tools for breast cancer. Theranostics. 2015;5(10):1122–43. PubMed PMC

Zavesky L, Jandakova E, Weinberger V, Minar L, Kohoutova M, Slanar O. Human endogenous retroviruses in breast cancer: altered expression pattern implicates divergent roles in carcinogenesis. Oncology. 2024;2024:1–10. PubMed PMC

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. . Accurate normalization of realtime quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):RESEARCH0034. PubMed PMC

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

Avery-Kiejda KA, Braye SG, Mathe A, Forbes JF, Scott RJ. Decreased expression of key tumour suppressor microRNAs is associated with lymph node metastases in triple negative breast cancer. BMC Cancer. 2014;14:51. PubMed PMC

Li XX, Gao SY, Wang PY, Zhou X, Li YJ, Yu Y, et al. . Reduced expression levels of let-7c in human breast cancer patients. Oncol Lett. 2015;9(3):1207–12. PubMed PMC

Fu XN, Mao X, Wang YX, Ding XF, Li YF. Let-7c-5p inhibits cell proliferation and induces cell apoptosis by targeting ERCC6 in breast cancer. Oncol Rep. 2017;38(3):1851–6. PubMed

Sun X, Xu CW, Xiao GD, Meng JY, Wang JC, Tang SC, et al. . Breast cancer stem-like cells are sensitized to tamoxifen induction of self-renewal inhibition with enforced Let-7c dependent on Wnt blocking. Int J Mol Med. 2018;41(4):1967–75. PubMed PMC

Aksan H, Kundaktepe BP, Sayili U, Velidedeoglu M, Simsek G, Koksal S, et al. . Circulating miR-155, let-7c, miR-21, and PTEN levels in differential diagnosis and prognosis of idiopathic granulomatous mastitis and breast cancer. Biofactors. 2020;46(6):955–62. PubMed

Chen DN, Bao C, Zhao F, Yu HG, Zhong GS, Xu L, et al. . Exploring specific miRNA-mRNA axes with relationship to taxanes-resistance in breast cancer. Front Oncol. 2020;10:1397. PubMed PMC

Bozgeyik E. Bioinformatic analysis and in vitro validation of let-7b and let-7c in breast cancer. Comput Biol Chem. 2020;84:107191. PubMed

Chen WJ, Wang HB, Shen YL, Wang SW, Liu D, Zhao HC, et al. . Let-7c-5p down-regulates immune-related CDCA8 to inhibit hepatocellular carcinoma. Funct Integr Genomics. 2023;23(1):56. PubMed

Ouyang M, Li YX, Ye S, Ma JY, Lu LM, Lv WM, et al. . MicroRNA profiling implies new markers of chemoresistance of triple-negative breast cancer. PLoS One. 2014;9(5):e96228. PubMed PMC

Liu ZR, Song Y, Wan LH, Zhang YY, Zhou LM. Over-expression of miR-451a can enhance the sensitivity of breast cancer cells to tamoxifen by regulating 14-3-3ζ, estrogen receptor α, and autophagy. Life Sci. 2016;149:104–13. PubMed

Dong Y, Wang GL. Knockdown of lncRNA SNHG12 suppresses cell proliferation, migration and invasion in breast cancer by sponging miR-451a. Int J Clin Exp Pathol. 2020;13(3):393–402. PubMed PMC

Zhang H, Chen P, Yang J. miR-451a suppresses the development of breast cancer via targeted inhibition of CCND2. Mol Cel Probes. 2020;54:101651. PubMed

Zhang XM, Cong L, Xu DF, Leng Q, Shi M, Zhou YH. AC092127.1-miR-451a-AE binding protein 2 signaling facilitates malignant properties of breast cancer. J Breast Cancer. 2021;24(4):389–401. PubMed PMC

Xing AY, Wang B, Li YH, Chen X, Wang YW, Liu HT, et al. . Identification of miRNA signature in breast cancer to predict neoadjuvant chemotherapy response. Pathol Oncol Res. 2021;27:1609753. PubMed PMC

Woo JW, Choi HY, Kim M, Chung YR, Park SY. miR-145, miR-205 and miR-451: potential tumor suppressors involved in the progression of in situ to invasive carcinoma of the breast. Breast Cancer. 2022;29(5):814–24. PubMed

Saeed H, Ejaz S. Down-regulation of miRNA 451a promotes many oncogenic signaling pathways in breast cancer patients. Indian J Biochem Biophys. 2023;60(6):467–77.

Chang CW, Wu HC, Terry MB, Santella RM. microRNA expression in prospectively collected blood as a potential biomarker of breast cancer risk in the BCFR. Anticancer Res. 2015;35(7):3969–77. PubMed PMC

Arabkari V, Clancy E, Dwyer RM, Kerin MJ, Kalinina O, Holian E, et al. . Relative and absolute expression analysis of MicroRNAs associated with luminal A breast cancer- A comparison. Pathol Oncol Res. 2020;26(2):833–44. PubMed

Pan YZ, Morris ME, Yu AM. MicroRNA-328 negatively regulates the expression of breast cancer resistance protein (BCRP/ABCG2) in human cancer cells. Mol Pharmacol. 2009;75(6):1374–9. PubMed PMC

Xiao B, Chen DX, Zhou Q, Hang JF, Zhang WY, Kuang ZZ, et al. . Glutamate metabotropic receptor 4 (GRM4) inhibits cell proliferation, migration and invasion in breast cancer and is regulated by miR-328-3p and miR-370-3p. BMC Cancer. 2019;19(1):891. PubMed PMC

Ma HM, Liu T, Xu YH, Wang XY, Wang J, Liu XK. MiR-519d and miR-328-3p combinatorially suppress breast cancer progression. Onco Targets Ther. 2020;13:12987–97. PubMed PMC

Escuin D, Lopez-Vilaro L, Mora J, Bell O, Moral A, Perez I, et al. . Circulating microRNAs in early breast cancer patients and its association with lymph node metastases. Front Oncol. 2021;11:627811. PubMed PMC

Liu T, Ye P, Ye YY, Lu S, Han BS. Circular RNA hsa_circRNA_002178 silencing retards breast cancer progression via microRNA-328-3p-mediated inhibition of COL1A1. J Cel Mol Med. 2020;24(3):2189–201. PubMed PMC

Li J, Li YM, Cheng H. Circ-RPPH1 knockdown retards breast cancer progression via miR-328-3p-mediated suppression of HMGA2. Clin Breast Cancer. 2022;22(3):E286–95. PubMed

Yang F, Bian ZH, Xu PW, Sun SB, Huang ZH. MicroRNA-204-5p: a pivotal tumor suppressor. Cancer Med. 2023;12(3):3185–200. PubMed PMC

Cai KT, Liu AG, Wang ZF, Jiang HW, Zeng JJ, He RQ, et al. . Expression and potential molecular mechanisms of miR-204-5p in breast cancer, based on bioinformatics and a meta-analysis of 2,306 cases. Mol Med Rep. 2019;19(2):1168–84. PubMed PMC

Zhang W, Xu J, Wang K, Tang XJ, He JJ. miR-139-3p suppresses the invasion and migration properties of breast cancer cells by targeting RAB1A. Oncol Rep. 2019;42(5):1699–708. PubMed PMC

Xie FY, Hosany S, Zhong S, Jiang Y, Zhang F, Lin LL, et al. . MicroRNA-193a inhibits breast cancer proliferation and metastasis by downregulating WT1. PLoS One. 2017;12(10):e0185565. PubMed PMC

Khordadmehr M, Shahbazi R, Baradaran B, Sadreddini S, Shanehbandi D, Hajiasgharzadeh K, et al. . In vitro. Pharm Sci. 2020;26(4):448–53. PubMed PMC

Moskwa P, Buffa FM, Pan YF, Panchakshari R, Gottipati P, Muschel RJ, et al. . miR-182-Mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell. 2011;41(2):210–20. PubMed PMC

Chiang CH, Hou MF, Hung WC. Up-regulation of miR-182 by β-catenin in breast cancer increases tumorigenicity and invasiveness by targeting the matrix metalloproteinase inhibitor RECK. Biochim Biophys Acta. 2013;1830(4):3067–76. PubMed

Wang PY, Gong HT, Li BF, Lv CL, Wang HT, Zhou HH, et al. . Higher expression of circulating miR-182 as a novel biomarker for breast cancer. Oncol Lett. 2013;6(6):1681–6. PubMed PMC

Li P, Sheng C, Huang LL, Zhang H, Huang LH, Cheng ZN, et al. . MiR-183/-96/-182 cluster is up-regulated in most breast cancers and increases cell proliferation and migration. Breast Cancer Res. 2014;16(6):473. PubMed PMC

Song CL, Zhang LJ, Wang J, Huang ZY, Li X, Wu MQ, et al. . High expression of microRNA-183/182/96 cluster as a prognostic biomarker for breast cancer. Sci Rep. 2016;6:24502. PubMed PMC

Wan P, He XL, Han Y, Wang LL, Yuan ZG. Stat5 inhibits NLRP3-mediated pyroptosis to enhance chemoresistance of breast cancer cells via promoting miR-182 transcription. Chem Biol Drug Des. 2023;102(1):14–25. PubMed

Xiang MQ, Zeng Y, Yang RR, Xu HF, Chen Z, Zhong J, et al. . U6 is not a suitable endogenous control for the quantification of circulating microRNAs. Biochem Biophys Res Commun. 2014;454(1):210–4. PubMed

Lou G, Ma N, Xu Y, Jiang L, Yang J, Wang CX, et al. . Differential distribution of U6 (RNU6-1) expression in human carcinoma tissues demonstrates the requirement for caution in the internal control gene selection for microRNA quantification. Int J Mol Med. 2015;36(5):1400–8. PubMed

Tambe M, Pruikkonen S, Maki-Jouppila J, Chen P, Elgaaen BV, Straume AH, et al. . Novel Mad2-targeting miR-493-3p controls mitotic fidelity and cancer cells' sensitivity to paclitaxel. Oncotarget. 2016;7(11):12267–85. PubMed PMC

Lehmann U, Streichert T, Otto B, Albat C, Hasemeier B, Christgen H, et al. . Identification of differentially expressed microRNAs in human male breast cancer. BMC Cancer. 2010;10:109. PubMed PMC

Meghani K, Fuchs W, Detappe A, Dranę P, Gogola E, Rottenberg S, et al. . Multifaceted impact of MicroRNA 493-5p on genome-stabilizing pathways induces platinum and PARP inhibitor resistance in BRCA2-mutated carcinomas. Cell Rep. 2018;23(1):100–11. PubMed PMC

Liu Y, Chen SM, Peng G, Liao YW, Fan XG, Zhang ZP, et al. . CircRNA NALCN acts as an miR-493-3p sponge to regulate PTEN expression and inhibit glioma progression. Cancer Cel Int. 2021;21(1):307. PubMed PMC

Gasparini P, Cascione L, Fassan M, Lovat F, Guler G, Balci S, et al. . microRNA expression profiling identifies a four microRNA signature as a novel diagnostic and prognostic biomarker in triple negative breast cancers. Oncotarget. 2014;5(5):1174–84. PubMed PMC

Yao L, Liu YR, Cao ZG, Li JJ, Huang YN, Hu X, et al. . MicroRNA-493 is a prognostic factor in triple-negative breast cancer. Cancer Sci. 2018;109(7):2294–301. PubMed PMC

Zhao LF, Feng XB, Song XB, Zhou HM, Zhao YF, Cheng L, et al. . miR-493-5p attenuates the invasiveness and tumorigenicity in human breast cancer by targeting FUT4. Oncol Rep. 2016;36(2):1007–15. PubMed

Mattiske S, Suetani RJ, Neilsen PM, Callen DF. The oncogenic role of miR-155 in breast cancer. Cancer Epidemiol Biomarkers Prev. 2012;21(8):1236–43. PubMed

Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, et al. . MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005;65(16):7065–70. PubMed

Wang JF, Wang QY, Guan YA, Sun YL, Wang XZ, Lively K, et al. . Breast cancer cell-derived microRNA-155 suppresses tumor progression via enhancing immune cell recruitment and antitumor function. J Clin Invest. 2022;132(19):e157248–JCI157248. PubMed PMC

He XH, Zhu W, Yuan P, Jiang S, Li D, Zhang HW, et al. . miR-155 downregulates ErbB2 and suppresses ErbB2-induced malignant transformation of breast epithelial cells. Oncogene. 2016;35(46):6015–25. PubMed

Turkoglu F, Calisir A, Ozturk B. Clinical importance of serum miRNA levels in breast cancer patients. Discov Oncol. 2024;15(1):19. PubMed PMC

Garrido-Palacios A, Rojas Carvajal AM, Nunez-Negrillo AM, Cortęs-Martin J, Sanchez-Garcia JC, Aguilar-Cordero MJ. MicroRNA dysregulation in early breast cancer diagnosis: a systematic review and meta-analysis. Int J Mol Sci. 2023;24(9):8270. PubMed PMC

Kong W, He L, Richards EJ, Challa S, Xu CX, Permuth-Wey J, et al. . Upregulation of miRNA-155 promotes tumour angiogenesis by targeting VHL and is associated with poor prognosis and triple-negative breast cancer. Oncogene. 2014;33(6):679–89. PubMed PMC

Chen J, Wang BC, Tang JH. Clinical significance of microRNA-155 expression in human breast cancer. J Surg Oncol. 2012;106(3):260–6. PubMed

Guo J, Jiang W, Xu XJ, Zheng XZ. Serum microRNA-155 in early diagnosis and prognosis of breast cancer. Int J Clin Exp Med. 2016;9(6):10289–96.

Zhang W, Chen CJ, Guo GL. MiR-155 promotes the proliferation and migration of breast cancer cells via targeting SOCS1 and MMP16. Eur Rev Med Pharmacol Sci. 2018;22(21):7323–32. PubMed

Yang LW, Wu XJ, Liang Y, Ye GQ, Che YC, Wu XZ, et al. . miR-155 increases stemness and decitabine resistance in triple-negative breast cancer cells by inhibiting TSPAN5. Mol Carcinog. 2020;59(4):447–61. PubMed

Li Q, Liu J, Meng XY, Pang RZ, Li J. MicroRNA-454 may function as an oncogene via targeting AKT in triple negative breast cancer. J Biol Res Thessal. 2017;24:10. PubMed PMC

Cao ZG, Li JJ, Yao L, Huang YN, Liu YR, Hu X, et al. . High expression of microRNA-454 is associated with poor prognosis in triple-negative breast cancer. Oncotarget. 2016;7(40):64900–9. PubMed PMC

Lu LS, Mao XH, Shi PY, He BY, Xu K, Zhang SM, et al. . MicroRNAs in the prognosis of triple-negative breast cancer A systematic review and meta-analysis. Medicine. 2017;96(22):e7085. PubMed PMC

Ren LL, Chen H, Song JW, Chen XH, Lin C, Zhang XL, et al. . MiR-454-3p-Mediated wnt/β-catenin signaling antagonists suppression promotes breast cancer metastasis. Theranostics. 2019;9(2):449–65. PubMed PMC

Lou WY, Liu JX, Ding BS, Jin LQ, Xu L, Li X, et al. . Five miRNAs-mediated PIEZO2 downregulation, accompanied with activation of Hedgehog signaling pathway, predicts poor prognosis of breast cancer. Aging-US. 2019;11(9):2628–52. PubMed PMC

Song HM, Luo QF, Deng XC, Ji CL, Li DF, Munankarmy A, et al. . VGLL4 interacts with STAT3 to function as a tumor suppressor in triple-negative breast cancer. Exp Mol Med. 2019;51(11):1–13. PubMed PMC

Li XH, Hou LL, Yin L, Zhao S. LncRNA XIST interacts with miR-454 to inhibit cells proliferation, epithelial mesenchymal transition and induces apoptosis in triple-negative breast cancer. J Biosci. 2020;45(1):45. PubMed

Aarthy R, Rao AKDM, Patel K, Sridevi V, Rajkumar T, Gowda H, et al. . Alteration of miR-362-5p and miR-454-3p expression elicits diverse responses in breast cancer cell lines. Mol Biol Rep. 2022;49(1):821–6. PubMed

Antolin S, Calvo L, Blanco-Calvo M, Santiago MP, Lorenzo-Patiño MJ, Haz-Conde M, et al. . Circulating miR-200c and miR-141 and outcomes in patients with breast cancer. BMC Cancer. 2015;15:297. PubMed PMC

Tuomarila M, Luostari K, Soini Y, Kataja V, Kosma VM, Mannermaa A. Overexpression of MicroRNA-200c predicts poor outcome in patients with PR-negative breast cancer. PLoS One. 2014;9(10):e109508. PubMed PMC

Madhavan D, Zucknick M, Wallwiener M, Cuk K, Modugno C, Scharpff M, et al. . Circulating miRNAs as surrogate markers for circulating tumor cells and prognostic markers in metastatic breast cancer. Clin Cancer Res. 2012;18(21):5972–82. PubMed

Lv JX, Xia K, Xu PF, Sun EH, Ma JJ, Gao S, et al. . miRNA expression patterns in chemoresistant breast cancer tissues. Biomed Pharmacother. 2014;68(8):935–42. PubMed

Chen JQ, Tian W, Cai HK, He HF, Deng YC. Down-regulation of microRNA-200c is associated with drug resistance in human breast cancer. Med Oncol. 2012;29(4):2527–34. PubMed

Kopp F, Oak PS, Wagner E, Roidl A. miR-200c sensitizes breast cancer cells to doxorubicin treatment by decreasing TrkB and Bmi1 expression. PLoS One. 2012;7(11):e50469. PubMed PMC

Zhang M, Wang F, Xiang Z, Huang T, Zhou WB. LncRNA XIST promotes chemoresistance of breast cancer cells to doxorubicin by sponging miR-200c-3p to upregulate ANLN. Clin Exp Pharmacol Physiol. 2020;47(8):1464–72. PubMed

Chen JQ, Tian W, He HF, Chen F, Huang J, Wang XJ, et al. . Downregulation of miR-200c-3p contributes to the resistance of breast cancer cells to paclitaxel by targeting SOX2. Oncol Rep. 2018;40(6):3821–9. PubMed

Kawaguchi T, Yan L, Qi QY, Peng X, Gabriel EM, Young J, et al. . Overexpression of suppressive microRNAs, miR-30a and miR-200c are associated with improved survival of breast cancer patients. Sci Rep. 2017;7(1):15945. PubMed PMC

Navarro-Manzano E, Luengo-Gil G, Gonzalez-Conejero R, Garcia-Garre E, Garcia-Martinez E, Garcia-Torralba E, et al. . Prognostic and predictive effects of tumor and plasma miR-200c-3p in locally advanced and metastatic breast cancer. Cancers. 2022;14(10):2390. PubMed PMC

Huang GL, Sun JC, Lu Y, Liu YK, Cao HY, Zhang HY, et al. . MiR-200 family and cancer: from a meta-analysis view. Mol Aspects Med. 2019;70:57–71. PubMed

Zhang GX, Zhang W, Li BJ, Stringer-Reasor E, Chu CJ, Sun LY, et al. . MicroRNA-200c and microRNA-141 are regulated by a FOXP3-KAT2B axis and associated with tumor metastasis in breast cancer. Breast Cancer Res. 2017;19(1):73. PubMed PMC

Debeb BG, Lacerda L, Anfossi S, Diagaradjane P, Chu K, Bambhroliya A, et al. . miR-141-Mediated regulation of brain metastasis from breast cancer. J Natl Cancer Inst. 2016;108(8):djw026. PubMed PMC

Thi Chung Duong T, Nguyen THN, Thi Ngoc Nguyen T, Huynh LH, Ngo HP, Thi Nguyen H. Diagnostic and prognostic value of miR-200 family in breast cancer: a meta-analysis and systematic review. Cancer Epidemiol. 2022;77:102097. PubMed

Choi SK, Kim HS, Jin T, Hwang EH, Jung M, Moon WK. Overexpression of the miR-141/200c cluster promotes the migratory and invasive ability of triple-negative breast cancer cells through the activation of the FAK and PI3K/AKT signaling pathways by secreting VEGF-A. BMC Cancer. 2016;16:570. PubMed PMC

Han GD, Qiu N, Luo K, Liang HL, Li HS. Downregulation of miroRNA-141 mediates acquired resistance to trastuzumab and is associated with poor outcome in breast cancer by upregulating the expression of ERBB4. J Cel Biochem. 2019;120(7):11390–400. PubMed

Shi W, Bruce J, Lee M, Yue SJ, Rowe M, Pintilie M, et al. . MiR-449a promotes breast cancer progression by targeting CRIP2. Oncotarget. 2016;7(14):18906–18. PubMed PMC

Ramirez-Ardila DE, Ruigrok-Ritstier K, Helmijr JC, Look MP, van Laere S, Dirix L, et al. . LRG1 mRNA expression in breast cancer associates with PIK3CA genotype and with aromatase inhibitor therapy outcome. Mol Oncol. 2016;10(8):1363–73. PubMed PMC

Zhang ZL, Wang JW, Gao RF, Yang X, Zhang YF, Li J, et al. . Downregulation of MicroRNA-449 promotes migration and invasion of breast cancer cells by targeting tumor protein D52 (TPD52). Oncol Res. 2017;25(5):753–61. PubMed PMC

Tormo E, Pineda B, Serna E, Guijarro A, Ribas G, Fores J, et al. . MicroRNA profile in response to doxorubicin treatment in breast cancer. J Cel Biochem. 2015;116(9):2061–73. PubMed

Huang GC, Zhong XW, Yao LH, Ma Q, Liao HB, Xu L, et al. . MicroRNA-449a inhibits cell proliferation and migration by regulating mutant p53 in MDA-MB-468 cells. Exp Ther Med. 2021;22(3):1020. PubMed PMC

Van der Auwera I, Limame R, van Dam P, Vermeulen PB, Dirix LY, Van Laere SJ. Integrated miRNA and mRNA expression profiling of the inflammatory breast cancer subtype. Br J Cancer. 2010;103(4):532–41. PubMed PMC

Hamdi K, Goerlitz D, Stambouli N, Islam M, Baroudi O, Neili B, et al. . miRNAs in Sera of Tunisian patients discriminate between inflammatory breast cancer and non-inflammatory breast cancer. Springerplus. 2014;3:636. PubMed PMC

Romero-Cordoba SL, Rodriguez-Cuevas S, Bautista-Pina V, Maffuz-Aziz A, D’Ippolito E, Cosentino G, et al. . Loss of function of miR-342-3p results in MCT1 over-expression and contributes to oncogenic metabolic reprogramming in triple negative breast cancer. Sci Rep. 2018;8(1):12252. PubMed PMC

Martinez-Gutierrez AD, Catalan OM, Vazquez-Romo R, Porras Reyes FI, Alvarado-Miranda A, Lara Medina F, et al. . miRNA profile obtained by next-generation sequencing in metastatic breast cancer patients is able to predict the response to systemic treatments. Int J Mol Med. 2019;44(4):1267–80. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...