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Review

The regulation of microRNAs on chemoresistance in triple-negative breast cancer: a recent update

ORCID Icon, ORCID Icon & ORCID Icon
Pages 571-587 | Received 05 Dec 2023, Accepted 07 Mar 2024, Published online: 19 Apr 2024

References

  • Goldhirsch A, Winer EP, Coates AS et al. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann. Oncol. 24(9), 2206–2223 (2013).
  • Vallejos CS, Gómez HL, Cruz WR et al. Breast cancer classification according to immunohistochemistry markers: subtypes and association with clinicopathologic variables in a peruvian hospital database. Clin. Breast Cancer 10(4), 294–300 (2010).
  • Arnedos M, Bihan C, Delaloge S et al. Triple-negative breast cancer: are we making headway at least? Ther. Adv. Med. Oncol. 4(4), 195–210 (2012).
  • Mayer IA, Abramson VG, Lehmann BD et al. New strategies for triple-negative breast cancer–deciphering the heterogeneity. Clin. Cancer Res. 20(4), 782–790 (2014).
  • Bergin ART, Loi S. Triple-negative breast cancer: recent treatment advances. F1000Res 8, 1342 (2019).
  • Romano G, Veneziano D, Acunzo M et al. Small non-coding RNA and cancer. Carcinogenesis 38(5), 485–491 (2017).
  • Chang S, Johnston RJ Jr, Frøkjaer-Jensen C et al. MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode. Nature 430(7001), 785–789 (2004).
  • Davis BN, Hilyard AC, Nguyen PH et al. Smad proteins bind a conserved RNA sequence to promote microRNA maturation by Drosha. Mol. Cell 39(3), 373–384 (2010).
  • Lee Y, Ahn C, Han J et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956), 415–419 (2003).
  • Blahna MT, Hata A. Regulation of miRNA biogenesis as an integrated component of growth factor signaling. Curr. Opin. Cell Biol. 25(2), 233–240 (2013).
  • Ding HX, Lv Z, Yuan Y et al. MiRNA polymorphisms and cancer prognosis: a systematic review and meta-analysis. Front Oncol. 8, 596 (2018).
  • Bach DH, Hong JY, Park HJ et al. The role of exosomes and miRNAs in drug-resistance of cancer cells. Int. J. Cancer 141(2), 220–230 (2017).
  • Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2), 281–297 (2004).
  • Gebert LFR, Macrae IJ. Regulation of microRNA function in animals. Nat. Rev. Mol. Cell Biol. 20(1), 21–37 (2019).
  • Ma J, Dong C, Ji C. MicroRNA and drug resistance. Cancer Gene Ther. 17(8), 523–531 (2010).
  • Amawi H, Sim HM, Tiwari AK et al. ABC transporter-mediated multidrug-resistant cancer. Adv. Exp. Med. Biol. 1141, 549–580 (2019).
  • Sharom FJ. The P-glycoprotein efflux pump: how does it transport drugs? J. Membr. Biol. 160(3), 161–175 (1997).
  • Ford RC, Beis K. Learning the ABCs one at a time: structure and mechanism of ABC transporters. Biochem. Soc. Trans. 47(1), 23–36 (2019).
  • Vasiliou V, Vasiliou K, Nebert DW. Human ATP-binding cassette (ABC) transporter family. Hum. Genom. 3(3), 281–290 (2009).
  • Ozben T. Mechanisms and strategies to overcome multiple drug resistance in cancer. FEBS Lett. 580(12), 2903–2909 (2006).
  • Chen Z, Shi T, Zhang L et al. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family in multidrug resistance: a review of the past decade. Cancer Lett. 370(1), 153–164 (2016).
  • Yamada A, Ishikawa T, Ota I et al. High expression of ATP-binding cassette transporter ABCC11 in breast tumors is associated with aggressive subtypes and low disease-free survival. Breast Cancer Res. Treat. 137(3), 773–782 (2013).
  • Guestini F, Ono K, Miyashita M et al. Impact of Topoisomerase IIα, PTEN, ABCC1/MRP1, and KI67 on triple-negative breast cancer patients treated with neoadjuvant chemotherapy. Breast Cancer Res. Treat. 173(2), 275–288 (2019).
  • Britton KM, Eyre R, Harvey IJ et al. Breast cancer, side population cells and ABCG2 expression. Cancer Lett. 323(1), 97–105 (2012).
  • Sissung TM, Baum CE, Kirkland CT et al. Pharmacogenetics of membrane transporters: an update on current approaches. Mol. Biotechnol. 44(2), 152–167 (2010).
  • Oguri T, Bessho Y, Achiwa H et al. MRP8/ABCC11 directly confers resistance to 5-fluorouracil. Mol. Cancer Ther. 6(1), 122–127 (2007).
  • Fanini F, Fabbri M. MicroRNAs and cancer resistance: a new molecular plot. Clin. Pharmacol. Ther. 99(5), 485–493 (2016).
  • Yeh WL, Tsai CF, Chen DR. Peri-foci adipose-derived stem cells promote chemoresistance in breast cancer. Stem Cell Res. Ther. 8(1), 177 (2017).
  • Zuo J, Yu Y, Zhu M et al. Inhibition of miR-155, a therapeutic target for breast cancer, prevented in cancer stem cell formation. Cancer Biomark 21(2), 383–392 (2018).
  • O'brien C, Cavet G, Pandita A et al. Functional genomics identifies ABCC3 as a mediator of taxane resistance in HER2-amplified breast cancer. Cancer Res. 68(13), 5380–5389 (2008).
  • Zeng C, Fan D, Xu Y et al. Curcumol enhances the sensitivity of doxorubicin in triple-negative breast cancer via regulating the miR-181b-2-3p-ABCC3 axis. Biochem. Pharmacol. 174, 113795 (2020).
  • Bao L, Hazari S, Mehra S et al. Increased expression of P-glycoprotein and doxorubicin chemoresistance of metastatic breast cancer is regulated by miR-298. Am. J. Pathol. 180(6), 2490–2503 (2012).
  • Yi D, Xu L, Wang R et al. miR-381 overcomes cisplatin resistance in breast cancer by targeting MDR1. Cell Biol. Int. 43(1), 12–21 (2019).
  • Simões-Wüst AP, Schürpf T, Hall J et al. Bcl-2/bcl-xL bispecific antisense treatment sensitizes breast carcinoma cells to doxorubicin, paclitaxel and cyclophosphamide. Breast Cancer Res. Treat. 76(2), 157–166 (2002).
  • Campbell KJ, Dhayade S, Ferrari N et al. MCL-1 is a prognostic indicator and drug target in breast cancer. Cell Death Dis. 9(2), 19 (2018).
  • Ozretic P, Alvir I, Sarcevic B et al. Apoptosis regulator Bcl-2 is an independent prognostic marker for worse overall survival in triple-negative breast cancer patients. Int. J. Biol. Markers 33(1), 109–115 (2018).
  • Pan B, Yi J, Song H. MicroRNA-mediated autophagic signaling networks and cancer chemoresistance. Cancer Biother. Radiopharm. 28(8), 573–578 (2013).
  • Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9(1), 47–59 (2008).
  • Liu X, Tang H, Chen J et al. MicroRNA-101 inhibits cell progression and increases paclitaxel sensitivity by suppressing MCL-1 expression in human triple-negative breast cancer. Oncotarget 6(24), 20070–20083 (2015).
  • Hou X, Niu Z, Liu L et al. miR-1207-5p regulates the sensitivity of triple-negative breast cancer cells to Taxol treatment via the suppression of LZTS1 expression. Oncol. Lett. 17(1), 990–998 (2019).
  • Zhang Y, Wang Y, Wei Y et al. MiR-129-3p promotes docetaxel resistance of breast cancer cells via CP110 inhibition. Sci. Rep. 5, 15424 (2015).
  • Ouyang M, Li Y, Ye S et al. MicroRNA profiling implies new markers of chemoresistance of triple-negative breast cancer. PLOS ONE 9(5), e96228 (2014).
  • Perotti C, Liu R, Parusel CT et al. Heat shock protein-90-alpha, a prolactin-STAT5 target gene identified in breast cancer cells, is involved in apoptosis regulation. Breast Cancer Res. 10(6), R94 (2008).
  • Workman P, Burrows F, Neckers L et al. Drugging the cancer chaperone HSP90: combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Ann. NY Acad Sci. 1113, 202–216 (2007).
  • O'brien K, Lowry MC, Corcoran C et al. miR-134 in extracellular vesicles reduces triple-negative breast cancer aggression and increases drug sensitivity. Oncotarget 6(32), 32774–32789 (2015).
  • Yao YS, Qiu WS, Yao RY et al. miR-141 confers docetaxel chemoresistance of breast cancer cells via regulation of EIF4E expression. Oncol. Rep. 33(5), 2504–2512 (2015).
  • Huang Z, Su GF, Hu WJ et al. The study on expression of CIAPIN1 interfering hepatocellular carcinoma cell proliferation and its mechanisms. Eur. Rev. Med. Pharmacol. Sci. 21(13), 3054–3060 (2017).
  • Zhang YF, Li XH, Shi YQ et al. CIAPIN1 confers multidrug resistance through up-regulation of MDR-1 and Bcl-L in LoVo/Adr cells and is independent of p53. Oncol. Rep. 25(4), 1091–1098 (2011).
  • Zhang XW, Liu L, Zhang XZ et al. Kanglaite inhibits the expression of drug resistance genes through suppressing PVT1 in cisplatin-resistant gastric cancer cells. Exp. Ther. Med. 14(2), 1789–1794 (2017).
  • Wang XM, Gao SJ, Guo XF et al. CIAPIN1 gene silencing enhances chemosensitivity in a drug-resistant animal model in vivo. Braz. J. Med. Biol. Res. 47(4), 273–278 (2014).
  • Deng YW, Hao WJ, Li YW et al. Hsa-miRNA-143-3p reverses multidrug resistance of triple-negative breast cancer by inhibiting the expression of its target protein cytokine-induced apoptosis inhibitor 1 in vivo. J. Breast Cancer 21(3), 251–258 (2018).
  • Chen J, Shi P, Zhang J et al. CircRNA_0044556 diminishes the sensitivity of triple-negative breast cancer cells to adriamycin by sponging miR-145 and regulating NRAS. Mol. Med. Rep. 25(2) (2022).
  • Tang X, Jin L, Cao P et al. MicroRNA-16 sensitizes breast cancer cells to paclitaxel through suppression of IKBKB expression. Oncotarget 7(17), 23668–23683 (2016).
  • Wang S, Oh DY, Leventaki V et al. MicroRNA-17 acts as a tumor chemosensitizer by targeting JAB1/CSN5 in triple-negative breast cancer. Cancer Lett. 465, 12–23 (2019).
  • Ao X, Nie P, Wu B et al. Decreased expression of microRNA-17 and microRNA-20b promotes breast cancer resistance to taxol therapy by upregulation of NCOA3. Cell Death Dis. 7(11), e2463 (2016).
  • Niu J, Xue A, Chi Y et al. Induction of miRNA-181a by genotoxic treatments promotes chemotherapeutic resistance and metastasis in breast cancer. Oncogene 35(10), 1302–1313 (2016).
  • Fang H, Xie J, Zhang M et al. miRNA-21 promotes proliferation and invasion of triple-negative breast cancer cells through targeting PTEN. Am. J. Transl. Res. 9(3), 953–961 (2017).
  • Chen L, Bourguignon LY. Hyaluronan-CD44 interaction promotes c-Jun signaling and miRNA21 expression leading to Bcl-2 expression and chemoresistance in breast cancer cells. Mol. Cancer 13, 52 (2014).
  • Luo LJ, Yang F, Ding JJ et al. MiR-31 inhibits migration and invasion by targeting SATB2 in triple-negative breast cancer. Gene 594(1), 47–58 (2016).
  • Körner C, Keklikoglou I, Bender C et al. MicroRNA-31 sensitizes human breast cells to apoptosis by direct targeting of protein kinase C epsilon (PKCepsilon). J. Biol. Chem. 288(12), 8750–8761 (2013).
  • Shen X, Lei J, Du L. miR-31-5p may enhance the efficacy of chemotherapy with Taxol and cisplatin in TNBC. Exp. Ther. Med. 19(1), 375–383 (2020).
  • Liu M, Gong C, Xu R et al. MicroRNA-5195-3p enhances the chemosensitivity of triple-negative breast cancer to paclitaxel by downregulating EIF4A2. Cell Mol. Biol. Lett. 24, 47 (2019).
  • Wu C, Zhao A, Tan T et al. Overexpression of microRNA-620 facilitates the resistance of triple-negative breast cancer cells to gemcitabine treatment by targeting DCTD. Exp. Ther. Med. 18(1), 550–558 (2019).
  • Xia H, Hui KM. MicroRNAs involved in regulating epithelial–mesenchymal transition and cancer stem cells as molecular targets for cancer therapeutics. Cancer Gene Ther. 19(11), 723–730 (2012).
  • Du C, Wang Y, Zhang Y et al. LncRNA DLX6-AS1 contributes to epithelial–mesenchymal transition and cisplatin resistance in triple-negative breast cancer via modulating Mir-199b-5p/paxillin axis. Cell Transplant. 29, 963689720929983 (2020).
  • Batlle E, Sancho E, Francí C et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2(2), 84–89 (2000).
  • Lin LF, Li YT, Han H et al. MicroRNA-205-5p targets the HOXD9-Snail1 axis to inhibit triple-negative breast cancer cell proliferation and chemoresistance. Aging (Albany NY) 13(3), 3945–3956 (2021).
  • Guan X, Gu S, Yuan M et al. MicroRNA-33a-5p overexpression sensitizes triple-negative breast cancer to doxorubicin by inhibiting eIF5A2 and epithelial–mesenchymal transition. Oncol. Lett. 18(6), 5986–5994 (2019).
  • Cui N, Hu M, Khalil RA. Biochemical and biological attributes of matrix metalloproteinases. Prog. Mol. Biol. Transl. Sci. 147, 1–73 (2017).
  • Guo J, Luo C, Yang Y et al. MiR-491-5p, as a tumor suppressor, prevents migration and invasion of breast cancer by targeting ZNF-703 to regulate AKT/mTOR pathway. Cancer Manag. Res. 13, 403–413 (2021).
  • Huang WC, Chi HC, Tung SL et al. Identification of the novel tumor suppressor role of FOCAD/miR-491-5p to inhibit cancer stemness, drug resistance and metastasis via regulating RABIF/MMP signaling in triple-negative breast cancer. Cells 10(10), 2524 (2021).
  • Bayraktar R, Pichler M, Kanlikilicer P et al. MicroRNA 603 acts as a tumor suppressor and inhibits triple-negative breast cancer tumorigenesis by targeting elongation factor 2 kinase. Oncotarget 8(7), 11641–11658 (2017).
  • Hamurcu Z, Ashour A, Kahraman N et al. FOXM1 regulates expression of eukaryotic elongation factor 2 kinase and promotes proliferation, invasion and tumorgenesis of human triple-negative breast cancer cells. Oncotarget 7(13), 16619–16635 (2016).
  • Tekedereli I, Alpay SN, Tavares CD et al. Targeted silencing of elongation factor 2 kinase suppresses growth and sensitizes tumors to doxorubicin in an orthotopic model of breast cancer. PLOS ONE 7(7), e41171 (2012).
  • Zhang P, Sun Y, Ma L. ZEB1: at the crossroads of epithelial–mesenchymal transition, metastasis and therapy resistance. Cell Cycle 14(4), 481–487 (2015).
  • Wang G, Dong Y, Liu H et al. Loss of miR-873 contributes to gemcitabine resistance in triple-negative breast cancer via targeting ZEB1. Oncol. Lett. 18(4), 3837–3844 (2019).
  • Pilié PG, Tang C, Mills GB et al. State-of-the-art strategies for targeting the DNA damage response in cancer. Nat. Rev. Clin. Oncol. 16(2), 81–104 (2019).
  • Ambrosio S, Majello B. Autophagy roles in genome maintenance. Cancers (Basel) 12(7), 1793 (2020).
  • Chen SM, Chou WC, Hu LY et al. The effect of MicroRNA-124 overexpression on anti-tumor drug sensitivity. PLOS ONE 10(6), e0128472 (2015).
  • Fan YX, Dai YZ, Wang XL et al. MiR-18a upregulation enhances autophagy in triple negative cancer cells via inhibiting mTOR signaling pathway. Eur. Rev. Med. Pharmacol. Sci. 20(11), 2194–2200 (2016).
  • Mullan PB, Quinn JE, Harkin DP. The role of BRCA1 in transcriptional regulation and cell cycle control. Oncogene 25(43), 5854–5863 (2006).
  • Wu J, Lu LY, Yu X. The role of BRCA1 in DNA damage response. Protein Cell 1(2), 117–123 (2010).
  • Ho JC, Chen J, Cheuk IW et al. MicroRNA-199a-3p promotes drug sensitivity in triple-negative breast cancer by down-regulation of BRCA1. Am. J. Transl. Res. 14(3), 2021–2036 (2022).
  • Tan X, Peng J, Fu Y et al. miR-638 mediated regulation of BRCA1 affects DNA repair and sensitivity to UV and cisplatin in triple-negative breast cancer. Breast Cancer Res. 16(5), 435 (2014).
  • Li PP, Li RG, Huang YQ et al. LncRNA OTUD6B-AS1 promotes paclitaxel resistance in triple-negative breast cancer by regulation of miR-26a-5p/MTDH pathway-mediated autophagy and genomic instability. Aging (Albany NY) 13(21), 24171–24191 (2021).
  • Cataldo A, Cheung DG, Balsari A et al. miR-302b enhances breast cancer cell sensitivity to cisplatin by regulating E2F1 and the cellular DNA damage response. Oncotarget 7(1), 786–797 (2016).
  • Zhong S, Ma T, Zhang X et al. MicroRNA expression profiling and bioinformatics analysis of dysregulated microRNAs in vinorelbine-resistant breast cancer cells. Gene 556(2), 113–118 (2015).
  • Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell 149(6), 1192–1205 (2012).
  • Xu J, Prosperi JR, Choudhury N et al. β-Catenin is required for the tumorigenic behavior of triple-negative breast cancer cells. PLOS ONE 10(2), e0117097 (2015).
  • Yin S, Xu L, Bonfil RD et al. Tumor-initiating cells and FZD8 play a major role in drug resistance in triple-negative breast cancer. Mol. Cancer Ther. 12(4), 491–498 (2013).
  • Li HY, Liang JL, Kuo YL et al. miR-105/93-3p promotes chemoresistance and circulating miR-105/93-3p acts as a diagnostic biomarker for triple-negative breast cancer. Breast Cancer Res. 19(1), 133 (2017).
  • Wu Y, Tao L, Liang J et al. miR-187-3p increases gemcitabine sensitivity in breast cancer cells by targeting FGF9 expression. Exp. Ther. Med. 20(2), 952–960 (2020).
  • Harrison H, Farnie G, Howell SJ et al. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res. 70(2), 709–718 (2010).
  • Kim B, Stephen SL, Hanby AM et al. Chemotherapy induces Notch1-dependent MRP1 up-regulation, inhibition of which sensitizes breast cancer cells to chemotherapy. BMC Cancer 15, 634 (2015).
  • Li ZL, Chen C, Yang Y et al. Gamma secretase inhibitor enhances sensitivity to doxorubicin in MDA-MB-231 cells. Int. J. Clin. Exp. Pathol. 8(5), 4378–4387 (2015).
  • Qiu M, Peng Q, Jiang I et al. Specific inhibition of Notch1 signaling enhances the antitumor efficacy of chemotherapy in triple-negative breast cancer through reduction of cancer stem cells. Cancer Lett. 328(2), 261–270 (2013).
  • Zhao M, Sun B, Wang Y et al. miR-27-3p enhances the sensitivity of triple-negative breast cancer cells to the antitumor agent olaparib by targeting PSEN-1, the Catalytic subunit of Γ-secretase. Front Oncol. 11, 694491 (2021).
  • Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature 490(7418), 61–70 (2012).
  • Steelman LS, Navolanic PM, Sokolosky ML et al. Suppression of PTEN function increases breast cancer chemotherapeutic drug resistance while conferring sensitivity to mTOR inhibitors. Oncogene 27(29), 4086–4095 (2008).
  • Pelicano H, Zhang W, Liu J et al. Mitochondrial dysfunction in some triple-negative breast cancer cell lines: role of mTOR pathway and therapeutic potential. Breast Cancer Res. 16(5), 434 (2014).
  • Paplomata E, O'regan R. The PI3K/AKT/mTOR pathway in breast cancer: targets, trials and biomarkers. Ther. Adv. Med. Oncol. 6(4), 154–166 (2014).
  • Zhang W, Gao Z, Guan M et al. ASF1B promotes oncogenesis in lung adenocarcinoma and other cancer types. Front Oncol. 11, 731547 (2021).
  • Wang L, Yang X, Zhou F et al. Circular RNA UBAP2 facilitates the cisplatin resistance of triple-negative breast cancer via microRNA-300/anti-silencing function 1B histone chaperone/PI3K/AKT/mTOR axis. Bioengineered 13(3), 7197–7208 (2022).
  • Liu MM, Li Z, Han XD et al. MiR-30e inhibits tumor growth and chemoresistance via targeting IRS1 in breast cancer. Sci. Rep. 7(1), 15929 (2017).
  • Dastmalchi N, Safaralizadeh R, Hosseinpourfeizi MA et al. MicroRNA-424-5p enhances chemosensitivity of breast cancer cells to Taxol and regulates cell cycle, apoptosis, and proliferation. Mol. Biol. Rep. 48(2), 1345–1357 (2021).
  • Kim EK, Choi EJ. Compromised MAPK signaling in human diseases: an update. Arch. Toxicol. 89(6), 867–882 (2015).
  • Fang JY, Richardson BC. The MAPK signalling pathways and colorectal cancer. Lancet Oncol. 6(5), 322–327 (2005).
  • Degirmenci U, Wang M, Hu J. Targeting aberrant RAS/RAF/MEK/ERK signaling for cancer therapy. Cells 9(1), 198 (2020).
  • Loi S, Dushyanthen S, Beavis PA et al. Correction: RAS/MAPK activation is associated with reduced tumor-infiltrating lymphocytes in triple-negative breast cancer: therapeutic cooperation between MEK and PD-1/PD-L1 immune checkpoint inhibitors. Clin. Cancer Res. 25(4), 1437 (2019).
  • Smith AL, Robin TP, Ford HL. Molecular pathways: targeting the TGF-β pathway for cancer therapy. Clin. Cancer Res. 18(17), 4514–4521 (2012).
  • Neuzillet C, Tijeras-Raballand A, Cohen R et al. Targeting the TGF-β pathway for cancer therapy. Pharmacol. Ther. 147, 22–31 (2015).
  • Xu X, Zhang L, He X et al. TGF-β plays a vital role in triple-negative breast cancer (TNBC) drug-resistance through regulating stemness, EMT and apoptosis. Biochem. Biophys. Res. Commun. 502(1), 160–165 (2018).
  • Bhola NE, Balko JM, Dugger TC et al. TGF-β inhibition enhances chemotherapy action against triple-negative breast cancer. J. Clin. Invest. 123(3), 1348–1358 (2013).
  • Kumar U, Hu Y, Masrour N et al. MicroRNA-495/TGF-β/FOXC1 axis regulates multidrug resistance in metaplastic breast cancer cells. Biochem. Pharmacol. 192, 114692 (2021).
  • Longley DB, Johnston PG. Molecular mechanisms of drug resistance. J. Pathol. 205(2), 275–292 (2005).
  • Shibata M, Hoque MO. Targeting cancer stem cells: a strategy for effective eradication of cancer. Cancers (Basel) 11(5), 732 (2019).
  • Creighton CJ, Li X, Landis M et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Natl Acad. Sci. USA 106(33), 13820–13825 (2009).
  • Lee HE, Kim JH, Kim YJ et al. An increase in cancer stem cell population after primary systemic therapy is a poor prognostic factor in breast cancer. Br. J. Cancer 104(11), 1730–1738 (2011).
  • He L, Wick N, Germans SK et al. The role of breast cancer stem cells in chemoresistance and metastasis in triple-negative breast cancer. Cancers (Basel) 13(24), 6209 (2021).
  • Sabatier R, Charafe-Jauffret E, Pierga JY et al. Stem cells inhibition by bevacizumab in combination with neoadjuvant chemotherapy for breast cancer. J. Clin. Med. 8(5), 612 (2019).
  • Nasr M, Farghaly M, Elsaba T et al. Resistance of primary breast cancer cells with enhanced pluripotency and stem cell activity to sex hormonal stimulation and suppression. Int. J. Biochem. Cell Biol. 105, 84–93 (2018).
  • Vaupel P. Hypoxia and aggressive tumor phenotype: implications for therapy and prognosis. Oncologist 13(Suppl. 3), 21–26 (2008).
  • Gerweck LE, Vijayappa S, Kozin S. Tumor pH controls the in vivo efficacy of weak acid and base chemotherapeutics. Mol. Cancer Ther. 5(5), 1275–1279 (2006).
  • Cosse JP, Michiels C. Tumour hypoxia affects the responsiveness of cancer cells to chemotherapy and promotes cancer progression. Anticancer Agents Med. Chem. 8(7), 790–797 (2008).
  • Kim H, Lin Q, Glazer PM et al. The hypoxic tumor microenvironment in vivo selects the cancer stem cell fate of breast cancer cells. Breast Cancer Res. 20(1), 16 (2018).
  • Chouaib S, Noman MZ, Kosmatopoulos K et al. Hypoxic stress: obstacles and opportunities for innovative immunotherapy of cancer. Oncogene 36(4), 439–445 (2017).
  • Skoda AM, Simovic D, Karin V et al. The role of the Hedgehog signaling pathway in cancer: a comprehensive review. Bosn J. Basic Med. Sci. 18(1), 8–20 (2018).
  • Harris LG, Pannell LK, Singh S et al. Increased vascularity and spontaneous metastasis of breast cancer by hedgehog signaling mediated upregulation of cyr61. Oncogene 31(28), 3370–3380 (2012).
  • Arnold KM, Pohlig RT, Sims-Mourtada J. Co-activation of Hedgehog and Wnt signaling pathways is associated with poor outcomes in triple-negative breast cancer. Oncol. Lett. 14(5), 5285–5292 (2017).
  • Sims-Mourtada J, Opdenaker LM, Davis J et al. Taxane-induced hedgehog signaling is linked to expansion of breast cancer stem-like populations after chemotherapy. Mol. Carcinog. 54(11), 1480–1493 (2015).
  • Slack FJ, Chinnaiyan AM. The role of non-coding RNAs in oncology. Cell 179(5), 1033–1055 (2019).
  • Pan Y, Liu G, Zhou F et al. DNA methylation profiles in cancer diagnosis and therapeutics. Clin. Exp. Med. 18(1), 1–14 (2018).
  • Xu Q, Jiang Y, Yin Y et al. A regulatory circuit of miR-148a/152 and DNMT1 in modulating cell transformation and tumor angiogenesis through IGF-IR and IRS1. J. Mol. Cell Biol. 5(1), 3–13 (2013).
  • Purwanto I, Heriyanto DS, Widodo I et al. MicroRNA-223 is associated with resistance towards platinum-based chemotherapy and worse prognosis in Indonesian triple-negative breast cancer patients. Breast Cancer (Dove Med. Press) 13, 1–7 (2021).
  • Rupaimoole R, Slack FJ. MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat. Rev. Drug Discov. 16(3), 203–222 (2017).
  • Abd-Aziz N, Kamaruzman NI, Poh CL. Development of MicroRNAs as potential therapeutics against cancer. J. Oncol. 2020, 8029721 (2020).
  • Lin S, Gregory RI. MicroRNA biogenesis pathways in cancer. Nat. Rev. Cancer 15(6), 321–333 (2015).
  • Seto AG, Beatty X, Lynch JM et al. Cobomarsen, an oligonucleotide inhibitor of miR-155, co-ordinately regulates multiple survival pathways to reduce cellular proliferation and survival in cutaneous T-cell lymphoma. Br. J. Haematol. 183(3), 428–444 (2018).

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