Clinical Application of MicroRNAs in Breast Cancer Treatment
Abstract
Background: Recurrence of breast cancer remains a critical problem. Therefore, it is imperative to identify biomarkers that accurately reflect disease state and develop novel drug therapies that are effective even after recurrence. MicroRNAs (miRNAs) are involved in the malignant transformation of various tumors. Circulating miRNAs are promising biomarkers for the diagnosis and treatment of cancers. Additionally, miRNAs are regarded as next-generation drug targets. Currently, various clinical trials are being conducted for anti-cancer drugs using miRNAs. In this review, we summarized recent studies on miRNA functions and circulating miRNAs in breast cancer, and discussed the status of miRNAs as drug discovery candidates. We also discussed the role of extracellular vesicles (EVs) in the clinical application of miRNAs.
Methods: Relevant articles published from 2002 to 2021 were acquired from PubMed database using the following key words: “miRNA” and “breast neoplasia”. Clinical trial data were retrieved from the database, ClinicalTrials.gov.
Results: Regulating these miRNAs may provide a new therapeutic strategy. Furthermore, miRNAs may be useful diagnostic and prognostic biomarkers for breast cancer. In addition, miRNAs have potential as anti-cancer agents, and may also be used in combination with other therapies to enhance the efficacies of other drugs.
Conclusion: In summary, miRNAs have shown promise as biomarkers and therapeutic targets. In addition, EVs will be the key to expanding the applications of miRNAs.
Full text article
References
Sung H, Ferlay J, Siegel RL. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. 2021;71(3):209-49. doi: 10.3322/caac.21660.
Burstein HJ, Curigliano G, Loibl S, Dubsky P, Gnant M, Poortmans P, et al. Estimating the benefits of therapy for early-stage breast cancer: the St. Gallen International Consensus Guidelines for the primary therapy of early breast cancer 2019. Annals of oncology : official journal of the European Society for Medical Oncology. 2019;30(10):1541-57. doi: 10.1093/annonc/mdz235.
Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-97. doi: 10.1016/s0092-8674(04)00045-5.
Gu W, Xu Y, Xie X, Wang T, Ko JH, Zhou T. The role of RNA structure at 5' untranslated region in microRNA-mediated gene regulation. RNA (New York, NY). 2014;20(9):1369-75. doi: 10.1261/rna.044792.114.
Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(24):15524-9. doi: https://doi.org/10.1073/pnas.242606799.
Kozomara A, Birgaoanu M, Griffiths-Jones S. miRBase: from microRNA sequences to function. Nucleic acids research. 2019;47(D1):D155-d62. doi: https://doi.org/10.1093/nar/gky1141.
Lakshmi S, Hughes TA, Priya S. Exosomes and exosomal RNAs in breast cancer: A status update. European journal of cancer (Oxford, England : 1990). 2021;144:252-68. doi: 10.1016/j.ejca.2020.11.033.
Wang H, Wei H, Wang J, Li L, Chen A, Li Z. MicroRNA-181d-5p-Containing Exosomes Derived from CAFs Promote EMT by Regulating CDX2/HOXA5 in Breast Cancer. Molecular therapy Nucleic acids. 2020;19:654-67. doi: 10.1016/j.omtn.2019.11.024.
Shen M, Dong C, Ruan X, Yan W, Cao M, Pizzo D, et al. Chemotherapy-Induced Extracellular Vesicle miRNAs Promote Breast Cancer Stemness by Targeting ONECUT2. Cancer research. 2019;79(14):3608-21. doi: 10.1158/0008-5472.can-18-4055.
Cornell L, Wander SA, Visal T, Wagle N, Shapiro GI. MicroRNA-Mediated Suppression of the TGF-β Pathway Confers Transmissible and Reversible CDK4/6 Inhibitor Resistance. Cell reports. 2019;26(10):2667-80.e7. doi: 10.1016/j.celrep.2019.02.023.
van Niel G, D'Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nature reviews Molecular cell biology. 2018;19(4):213-28. doi:10.1038/nrm.2017.125.
Hoshino A, Kim HS, Bojmar L, Gyan KE, Cioffi M, Hernandez J, et al. Extracellular Vesicle and Particle Biomarkers Define Multiple Human Cancers. Cell. 2020;182(4):1044-61.e18. doi: https://doi.org/10.1016/j.cell.2020.07.009.
Špilak A, Brachner A, Kegler U, Neuhaus W, Noehammer C. Implications and pitfalls for cancer diagnostics exploiting extracellular vesicles. Advanced drug delivery reviews. 2021;175:113819. doi: 10.1016/j.addr.2021.05.029.
Bose RJC, Uday Kumar S, Zeng Y, Afjei R, Robinson E, Lau K, et al. Tumor Cell-Derived Extracellular Vesicle-Coated Nanocarriers: An Efficient Theranostic Platform for the Cancer-Specific Delivery of Anti-miR-21 and Imaging Agents. ACS Nano. 2018;12(11):10817-32. doi: 10.1021/acsnano.8b02587.
Rupaimoole R, Slack FJ. MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nature reviews Drug discovery. 2017;16(3):203-22. doi: 10.1038/nrd.2016.246.
Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(30):10513-8. doi: 10.1073/pnas.0804549105.
Bottani M, Banfi G, Lombardi G. Circulating miRNAs as Diagnostic and Prognostic Biomarkers in Common Solid Tumors: Focus on Lung, Breast, Prostate Cancers, and Osteosarcoma. J Clin Med. 2019;8(10). doi: 10.3390/jcm8101661.
Di Cosimo S, Appierto V, Pizzamiglio S, de la Peña L, Izquierdo M, Huober J, et al. Plasma miRNA Levels for Predicting Therapeutic Response to Neoadjuvant Treatment in HER2-positive Breast Cancer: Results from the NeoALTTO Trial. Clinical cancer research : an official journal of the American Association for Cancer Research. 2019;25(13):3887-95. doi: 10.1158/1078-0432.ccr-18-2507
Lin HM, Mahon KL, Spielman C, Gurney H, Mallesara G, Stockler MR, et al. Phase 2 study of circulating microRNA biomarkers in castration-resistant prostate cancer. British journal of cancer. 2017;116(8):1002-11. doi: 10.1038/bjc.2017.50.
Svoronos AA, Engelman DM, Slack FJ. OncomiR or Tumor Suppressor? The Duplicity of MicroRNAs in Cancer. Cancer research. 2016;76(13):3666-70. doi: 10.1158/0008-5472.can-16-0359.
Perez-Añorve IX, Gonzalez-De la Rosa CH, Soto-Reyes E, Beltran-Anaya FO, Del Moral-Hernandez O, Salgado-Albarran M, et al. New insights into radioresistance in breast cancer identify a dual function of miR-122 as a tumor suppressor and oncomiR. Molecular oncology. 2019;13(5):1249-67. doi: 10.1002/1878-0261.12483.
Gorur A, Bayraktar R, Ivan C, Mokhlis HA, Bayraktar E, Kahraman N, et al. ncRNA therapy with miRNA-22-3p suppresses the growth of triple-negative breast cancer. Molecular therapy Nucleic acids. 2021;23:930-43. doi: 10.1016/j.omtn.2021.01.016.
Bao C, Chen J, Chen D, Lu Y, Lou W, Ding B, et al. MiR-93 suppresses tumorigenesis and enhances chemosensitivity of breast cancer via dual targeting E2F1 and CCND1. Cell death & disease. 2020;11(8):618. doi: 10.1038/s41419-020-02855-6.
Pandey AK, Zhang Y, Zhang S, Li Y, Tucker-Kellogg G, Yang H, et al. TIP60-miR-22 axis as a prognostic marker of breast cancer progression. Oncotarget. 2015;6(38):41290-306. doi: 10.18632/oncotarget.5636.
Li N, Miao Y, Shan Y, Liu B, Li Y, Zhao L, et al. MiR-106b and miR-93 regulate cell progression by suppression of PTEN via PI3K/Akt pathway in breast cancer. Cell Death Dis. 2017;8(5):e2796. doi: 10.1038/cddis.2017.119.
Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449(7163):682-8. doi: 10.1038/nature06174.
Yan W, Wu X, Zhou W, Fong MY, Cao M, Liu J, et al. Cancer-cell-secreted exosomal miR-105 promotes tumour growth through the MYC-dependent metabolic reprogramming of stromal cells. Nat Cell Biol 2018;20(5):597-609. doi: 10.1038/s41556-018-0083-6.
Fong MY, Zhou W, Liu L, Alontaga AY, Chandra M, Ashby J, et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol. 2015;17(2):183-94. doi: 10.1038/ncb3094.
Lu JT, Tan CC, Wu XR, He R, Zhang X, Wang QS, et al. FOXF2 deficiency accelerates the visceral metastasis of basal-like breast cancer by unrestrictedly increasing TGF-β and miR-182-5p. Cell death and differentiation. 2020;27(10):2973-87. doi: 10.1038/s41418-020-0555-7.
Jiang CF, Shi ZM, Li DM, Qian YC, Ren Y, Bai XM, et al. Estrogen-induced miR-196a elevation promotes tumor growth and metastasis via targeting SPRED1 in breast cancer. Molecular cancer. 2018;17(1):83. doi: 10.1186/s12943-018-0830-0.
Cuiffo BG, Campagne A, Bell GW, Lembo A, Orso F, Lien EC, et al. MSC-regulated microRNAs converge on the transcription factor FOXP2 and promote breast cancer metastasis. Cell stem cell. 2014;15(6):762-74. doi: 10.1016/j.stem.2014.10.001.
Pfeffer SR, Yang CH, Pfeffer LM. The Role of miR-21 in Cancer. Drug development research. 2015;76(6):270-7. DOI: https://doi.org/10.1002/ddr.21257.
Chen H, Pan H, Qian Y, Zhou W, Liu X. MiR-25-3p promotes the proliferation of triple negative breast cancer by targeting BTG2. Molecular cancer. 2018;17(1):4. doi: 10.1186/s12943-017-0754-0.
Castellano L, Dabrowska A, Pellegrino L, Ottaviani S, Cathcart P, Frampton AE, et al. Sustained expression of miR-26a promotes chromosomal instability and tumorigenesis through regulation of CHFR. Nucleic acids research. 2017;45(8):4401-12. doi: 10.1093/nar/gkx022.
Eastlack SC, Dong S, Ivan C, Alahari SK. Suppression of PDHX by microRNA-27b deregulates cell metabolism and promotes growth in breast cancer. Molecular cancer. 2018;17(1):100. doi: 10.1186/s12943-018-0851-8.
Wu Y, Shi W, Tang T, Wang Y, Yin X, Chen Y, et al. miR-29a contributes to breast cancer cells epithelial-mesenchymal transition, migration, and invasion via down-regulating histone H4K20 trimethylation through directly targeting SUV420H2. Cell death & disease. 2019;10(3):176. doi: 10.1038/s41419-019-1437-0.
Lv C, Li F, Li X, Tian Y, Zhang Y, Sheng X, et al. MiR-31 promotes mammary stem cell expansion and breast tumorigenesis by suppressing Wnt signaling antagonists. Nat Commun 2017;8(1):1036. doi: 10.1038/s41467-017-01059-5.
Cai WL, Huang WD, Li B, Chen TR, Li ZX, Zhao CL, et al. microRNA-124 inhibits bone metastasis of breast cancer by repressing Interleukin-11. Mol Cancer 2018;17(1):9. doi: 10.1186/s12943-017-0746-0.
Maroni P, Bendinelli P, Matteucci E, Desiderio MA. The therapeutic effect of miR-125b is enhanced by the prostaglandin endoperoxide synthase 2/cyclooxygenase 2 blockade and hampers ETS1 in the context of the microenvironment of bone metastasis. Cell death & disease. 2018;9(5):472. doi: 10.1038/s41419-018-0499-8.
Yu Y, Luo W, Yang ZJ, Chi JR, Li YR, Ding Y, et al. miR-190 suppresses breast cancer metastasis by regulation of TGF-β-induced epithelial-mesenchymal transition. Mol Cancer 2018;17(1):70. doi: 10.1186/s12943-018-0818-9.
Tang X, Hou Y, Yang G, Wang X, Tang S, Du YE, et al. Stromal miR-200s contribute to breast cancer cell invasion through CAF activation and ECM remodeling. Cell death and differentiation. 2016;23(1):132-45. doi: 10.1038/cdd.2015.78.
Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10(5):593-601. doi: 10.1038/ncb1722.
Samaeekia R, Adorno-Cruz V, Bockhorn J, Chang YF, Huang S, Prat A, et al. miR-206 Inhibits Stemness and Metastasis of Breast Cancer by Targeting MKL1/IL11 Pathway. Clinical cancer research : an official journal of the American Association for Cancer Research. 2017;23(4):1091-103. doi: 10.1158/1078-0432.ccr-16-0943.
Chen D, Si W, Shen J, Du C, Lou W, Bao C, et al. miR-27b-3p inhibits proliferation and potentially reverses multi-chemoresistance by targeting CBLB/GRB2 in breast cancer cells. Cell death & disease. 2018;9(2):188. doi: 10.1038/s41419-017-0211-4.
di Gennaro A, Damiano V, Brisotto G, Armellin M, Perin T, Zucchetto A, et al. A p53/miR-30a/ZEB2 axis controls triple negative breast cancer aggressiveness. 2018;25(12):2165-80. doi: 10.1038/s41418-018-0103-x.
Kong P, Chen L, Yu M, Tao J, Liu J, Wang Y, et al. miR-3178 inhibits cell proliferation and metastasis by targeting Notch1 in triple-negative breast cancer. Cell death & disease. 2018;9(11):1059. doi: 10.1038/s41419-018-1091-y.
Weng YS, Tseng HY, Chen YA, Shen PC, Al Haq AT, Chen LM, et al. MCT-1/miR-34a/IL-6/IL-6R signaling axis promotes EMT progression, cancer stemness and M2 macrophage polarization in triple-negative breast cancer. Molecular cancer. 2019;18(1):42. doi: 10.1186/s12943-019-0988-0.
Tang H, Huang X, Wang J, Yang L, Kong Y, Gao G, et al. circKIF4A acts as a prognostic factor and mediator to regulate the progression of triple-negative breast cancer. Molecular cancer. 2019;18(1):23. doi: 10.1186/s12943-019-0946-x.
Ward A, Balwierz A, Zhang JD, Küblbeck M, Pawitan Y, Hielscher T, et al. Re-expression of microRNA-375 reverses both tamoxifen resistance and accompanying EMT-like properties in breast cancer. Oncogene. 2013;32(9):1173-82. doi: 10.1038/onc.2012.128.
Wang W, Zhang L, Wang Y, Ding Y, Chen T, Wang Y, et al. Involvement of miR-451 in resistance to paclitaxel by regulating YWHAZ in breast cancer. Cell death & disease. 2017;8(10):e3071. doi: 10.1038/cddis.2017.460.
Li Y, Liang Y, Sang Y, Song X, Zhang H, Liu Y, et al. MiR-770 suppresses the chemo-resistance and metastasis of triple negative breast cancer via direct targeting of STMN1. Cell Death Dis. 2018;9(1):14. doi: 10.1038/s41419-017-0030-7.
Zhang N, Zhang H, Liu Y, Su P, Zhang J, Wang X, et al. SREBP1, targeted by miR-18a-5p, modulates epithelial-mesenchymal transition in breast cancer via forming a co-repressor complex with Snail and HDAC1/2. Cell Death Differ 2019;26(5):843-59. doi: 10.1038/s41418-018-0158-8.
Si W, Shen J, Du C, Chen D, Gu X, Li C, et al. A miR-20a/MAPK1/c-Myc regulatory feedback loop regulates breast carcinogenesis and chemoresistance. Cell death and differentiation. 2018;25(2):406-20. doi: 10.1038/cdd.2017.176.
Chatterjee A, Jana S, Chatterjee S, Wastall LM, Mandal G, Nargis N, et al. MicroRNA-222 reprogrammed cancer-associated fibroblasts enhance growth and metastasis of breast cancer. Br J Cancer. 2019;121(8):679-89. doi: 10.1038/s41416-019-0566-7.
Weidhaas JB, Babar I, Nallur SM, Trang P, Roush S, Boehm M, et al. MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer research. 2007;67(23):11111-6. doi: 10.1158/0008-5472.can-07-2858.
Zhang W, Wu M, Chong QY, Zhang M, Zhang X, Hu L, et al. Loss of Estrogen-Regulated MIR135A1 at 3p21.1 Promotes Tamoxifen Resistance in Breast Cancer. Cancer research. 2018;78(17):4915-28. doi: 10.1158/0008-5472.can-18-0069.
Gu J, Wang Y, Wang X, Zhou D, Shao C, Zhou M, et al. Downregulation of lncRNA GAS5 confers tamoxifen resistance by activating miR-222 in breast cancer. Cancer letters. 2018;434:1-10. doi: 10.1016/j.canlet.2018.06.039.
Liu SS, Li Y, Zhang H, Zhang D, Zhang XB, Wang X, et al. The ERα-miR-575-p27 feedback loop regulates tamoxifen sensitivity in ER-positive Breast Cancer. Theranostics. 2020;10(23):10729-42. doi: 10.7150/thno.46297.
Fu R, Tong JS. miR-126 reduces trastuzumab resistance by targeting PIK3R2 and regulating AKT/mTOR pathway in breast cancer cells. J Cell Mol Med. 2020;24(13):7600-8. doi: 10.1111/jcmm.15396.
Yue D, Qin X. miR-182 regulates trastuzumab resistance by targeting MET in breast cancer cells. Cancer gene therapy. 2019;26(1-2):1-10. doi: 10.1038/s41417-018-0031-4.
Han M, Hu J, Lu P, Cao H, Yu C, Li X, et al. Exosome-transmitted miR-567 reverses trastuzumab resistance by inhibiting ATG5 in breast cancer. Cell death & disease. 2020;11(1):43. doi: 10.1038/s41419-020-2250-5.
Gupta I, Rizeq B. Circulating miRNAs in HER2-Positive and Triple Negative Breast Cancers: Potential Biomarkers and Therapeutic Targets. 2020;21(18). doi: 10.3390/ijms21186750.
Cuk K, Zucknick M, Madhavan D, Schott S, Golatta M, Heil J, et al. Plasma microRNA panel for minimally invasive detection of breast cancer. PloS one. 2013;8(10):e76729. doi : 10.1371/journal.pone.0076729.
Chan M, Liaw CS, Ji SM, Tan HH, Wong CY, Thike AA, et al. Identification of circulating microRNA signatures for breast cancer detection. Clinical cancer research : an official journal of the American Association for Cancer Research. 2013;19(16):4477-87. doi: 10.1158/1078-0432.ccr-12-3401.
Shen J, Hu Q, Schrauder M, Yan L, Wang D, Medico L, et al. Circulating miR-148b and miR-133a as biomarkers for breast cancer detection. Oncotarget. 2014;5(14):5284-94. doi: 10.18632/oncotarget.2014.
Kodahl AR, Lyng MB, Binder H, Cold S, Gravgaard K, Knoop AS, et al. Novel circulating microRNA signature as a potential non-invasive multi-marker test in ER-positive early-stage breast cancer: a case control study. Molecular oncology. 2014;8(5):874-83. doi: 10.1016/j.molonc.2014.03.002.
Zearo S, Kim E, Zhu Y, Zhao JT, Sidhu SB, Robinson BG, et al. MicroRNA-484 is more highly expressed in serum of early breast cancer patients compared to healthy volunteers. BMC cancer. 2014;14:200. doi: 10.1186/1471-2407-14-200.
Matamala N, Vargas MT, González-Cámpora R, Miñambres R, Arias JI, Menéndez P, et al. Tumor microRNA expression profiling identifies circulating microRNAs for early breast cancer detection. Clinical chemistry. 2015;61(8):1098-106. doi: 10.1373/clinchem.2015.238691.
Shimomura A, Shiino S, Kawauchi J, Takizawa S, Sakamoto H, Matsuzaki J, et al. Novel combination of serum microRNA for detecting breast cancer in the early stage. Cancer science. 2016;107(3):326-34. doi: 10.1111/cas.12880.
Frères P, Wenric S, Boukerroucha M, Fasquelle C, Thiry J, Bovy N, et al. Circulating microRNA-based screening tool for breast cancer. Oncotarget. 2016;7(5):5416-28. doi: 10.18632/oncotarget.6786.
Huang SK, Luo Q, Peng H, Li J, Zhao M, Wang J, et al. A Panel of Serum Noncoding RNAs for the Diagnosis and Monitoring of Response to Therapy in Patients with Breast Cancer. Medical science monitor : international medical journal of experimental and clinical research. 2018;24:2476-88. doi: 10.12659/msm.909453.
Li M, Zou X, Xia T, Wang T, Liu P, Zhou X, et al. A five-miRNA panel in plasma was identified for breast cancer diagnosis. Cancer Med. 2019;8(16):7006-17. doi: 10.1002/cam4.2572.
Li M, Zhou Y, Xia T, Zhou X, Huang Z, Zhang H, et al. Circulating microRNAs from the miR-106a-363 cluster on chromosome X as novel diagnostic biomarkers for breast cancer. 2018;170(2):257-70. doi: 10.1007/s10549-018-4757-3.
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. Clinical cancer research : an official journal of the American Association for Cancer Research. 2012;18(21):5972-82. doi: 10.1158/1078-0432.ccr-12-1407.
Khodadadi-Jamayran A, Akgol-Oksuz B, Afanasyeva Y, Heguy A, Thompson M, Ray K, et al. Prognostic role of elevated mir-24-3p in breast cancer and its association with the metastatic process. Oncotarget. 2018;9(16):12868-78. doi: 10.18632/oncotarget.24403.
Kleivi Sahlberg K, Bottai G, Naume B, Burwinkel B, Calin GA, Børresen-Dale AL, et al. A serum microRNA signature predicts tumor relapse and survival in triple-negative breast cancer patients. Clinical cancer research : an official journal of the American Association for Cancer Research. 2015;21(5):1207-14. doi: 10.1158/1078-0432.ccr-14-2011.
Madhavan D, Peng C, Wallwiener M, Zucknick M, Nees J, Schott S, et al. Circulating miRNAs with prognostic value in metastatic breast cancer and for early detection of metastasis. Carcinogenesis. 2016;37(5):461-70. doi: 10.1093/carcin/bgw008.
Li H, Liu J, Chen J, Wang H, Yang L, Chen F, et al. A serum microRNA signature predicts trastuzumab benefit in HER2-positive metastatic breast cancer patients. Nat Commun. 2018;9(1):1614. doi: 10.1038/s41467-018-03537-w.
Wang Y, Yin W, Lin Y, Yin K, Zhou L, Du Y, et al. Downregulated circulating microRNAs after surgery: potential noninvasive biomarkers for diagnosis and prognosis of early breast cancer. Cell death discovery. 2018;4:21. doi: 10.1038/s41420-018-0089-7.
Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG, et al. Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nature biotechnology. 2010;28(4):341-7. doi: 10.1038/nbt.1618.
Yoo B, Kavishwar A, Wang P, Ross A, Pantazopoulos P, Dudley M, et al. Therapy targeted to the metastatic niche is effective in a model of stage IV breast cancer. Scientific reports. 2017;7:45060. doi: 10.1038/srep45060.
Yoo B, Ross A, Pantazopoulos P, Medarova Z. MiRNA10b-directed nanotherapy effectively targets brain metastases from breast cancer. Scientific reports. 2021;11(1):2844. doi: 10.1038/s41598-021-82528-2.
Gao L, Guo Q, Li X, Yang X, Ni H, Wang T, et al. MiR-873/PD-L1 axis regulates the stemness of breast cancer cells. EBioMedicine. 2019;41:395-407. doi: 10.1016/j.ebiom.2019.02.034.
Ninio-Many L, Hikri E, Burg-Golani T, Stemmer SM, Shalgi R, Ben-Aharon I. miR-125a Induces HER2 Expression and Sensitivity to Trastuzumab in Triple-Negative Breast Cancer Lines. Frontiers in oncology. 2020;10:191. doi: 10.3389/fonc.2020.00191.
Bouchie A. First microRNA mimic enters clinic. Nature biotechnology. 2013;31(7):577. doi: 10.1038/nbt0713-577.
Faraldi M, Gomarasca M, Banfi G, Lombardi G. Free Circulating miRNAs Measurement in Clinical Settings: The Still Unsolved Issue of the Normalization. Advances in clinical chemistry. 2018;87:113-39. doi: 10.1016/bs.acc.2018.07.003.
Krug AK, Enderle D, Karlovich C, Priewasser T, Bentink S, Spiel A, et al. Improved EGFR mutation detection using combined exosomal RNA and circulating tumor DNA in NSCLC patient plasma. Annals of oncology : official journal of the European Society for Medical Oncology. 2018;29(3):700-6. doi: 10.1093/annonc/mdx765.
Yoshikawa M, Iinuma H, Umemoto Y, Yanagisawa T, Matsumoto A, Jinno H. Exosome-encapsulated microRNA-223-3p as a minimally invasive biomarker for the early detection of invasive breast cancer. Oncology letters. 2018;15(6):9584-92. doi: 10.3892/ol.2018.8457.
Moloney BM, Gilligan KE, Joyce DP, O'Neill CP, O'Brien KP, Khan S, et al. Investigating the Potential and Pitfalls of EV-Encapsulated MicroRNAs as Circulating Biomarkers of Breast Cancer. Cells. 2020;9(1). doi: 10.3390/cells9010141.
Lujan H, Griffin WC, Taube JH, Sayes CM. Synthesis and characterization of nanometer-sized liposomes for encapsulation and microRNA transfer to breast cancer cells. International journal of nanomedicine. 2019;14:5159-73. doi: 10.2147/ijn.s203330.
Sharma S, Rajendran V, Kulshreshtha R, Ghosh PC. Enhanced efficacy of anti-miR-191 delivery through stearylamine liposome formulation for the treatment of breast cancer cells. International journal of pharmaceutics. 2017;530(1-2):387-400. doi: 10.1016/j.ijpharm.2017.07.079.
Yoo B, Kavishwar A, Ross A, Wang P, Tabassum DP, Polyak K, et al. Combining miR-10b-Targeted Nanotherapy with Low-Dose Doxorubicin Elicits Durable Regressions of Metastatic Breast Cancer. Cancer research. 2015;75(20):4407-15. doi: 10.1158/0008-5472.can-15-0888.
Yu Y, Yao Y, Yan H, Wang R, Zhang Z, Sun X, et al. A Tumor-specific MicroRNA Recognition System Facilitates the Accurate Targeting to Tumor Cells by Magnetic Nanoparticles. Molecular therapy Nucleic acids. 2016;5(5):e318. doi: 10.1038/mtna.2016.28.
Wagner MJ, Mitra R, McArthur MJ, Baze W, Barnhart K, Wu SY, et al. Preclinical Mammalian Safety Studies of EPHARNA (DOPC Nanoliposomal EphA2-Targeted siRNA). Molecular cancer therapeutics. 2017;16(6):1114-23. doi: 10.1158/1535-7163.mct-16-0541.
Yin H, Xiong G, Guo S, Xu C, Xu R, Guo P, et al. Delivery of Anti-miRNA for Triple-Negative Breast Cancer Therapy Using RNA Nanoparticles Targeting Stem Cell Marker CD133. Molecular therapy : the journal of the American Society of Gene Therapy. 2019;27(7):1252-61. doi: 10.1016/j.ymthe.2019.04.018.
Eichmüller SB, Osen W, Mandelboim O, Seliger B. Immune Modulatory microRNAs Involved in Tumor Attack and Tumor Immune Escape. Journal of the National Cancer Institute. 2017;109(10). doi: 10.1093/jnci/djx034.
Authors
Copyright (c) 2022 Archives of Breast Cancer
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Copyright©. This is an open-access article distributed under the terms of the Creative Commons Attribution-Non-Commercial 4.0 International License, which permits copy and redistribution of the material in any medium or format or adapt, remix, transform, and build upon the material for any purpose, except for commercial purposes.