Generic placeholder image

Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Review Article

MicroRNAs as Biomarker for Breast Cancer

Author(s): Taru Aggarwal, Ridhima Wadhwa, Riya Gupta, Keshav Raj Paudel, Trudi Collet, Dinesh Kumar Chellappan, Gaurav Gupta, Haribalan Perumalsamy, Meenu Mehta, Saurabh Satija*, Philip M. Hansbro, Kamal Dua and Pawan Kumar Maurya*

Volume 20, Issue 10, 2020

Page: [1597 - 1610] Pages: 14

DOI: 10.2174/1871530320666200428113051

Price: $65

Abstract

Regardless of advances in detection and treatment, breast cancer affects about 1.5 million women all over the world. Since the last decade, genome-wide association studies (GWAS) have been extensively conducted for breast cancer to define the role of miRNA as a tool for diagnosis, prognosis and therapeutics. MicroRNAs are small, non-coding RNAs that are associated with the regulation of key cellular processes such as cell multiplication, differentiation, and death. They cause a disturbance in the cell physiology by interfering directly with the translation and stability of a targeted gene transcript. MicroRNAs (miRNAs) constitute a large family of non-coding RNAs, which regulate target gene expression and protein levels that affect several human diseases and are suggested as the novel markers or therapeutic targets, including breast cancer. MicroRNA (miRNA) alterations are not only associated with metastasis, tumor genesis but also used as biomarkers for breast cancer diagnosis or prognosis. These are explained in detail in the following review. This review will also provide an impetus to study the role of microRNAs in breast cancer.

Keywords: micro-RNA, breast cancer, oncomirs, oncosuppressormir, drug targeting, drug resistance.

Graphical Abstract

[1]
Gulati, M.; Mulvagh, S.L. The connection between the breast and heart in a woman: Breast cancer and cardiovascular disease. Clin. Cardiol., 2018, 41(2), 253-257.
[http://dx.doi.org/10.1002/clc.22886] [PMID: 29446841]
[2]
DeSantis, C.E.; Fedewa, S.A.; Goding Sauer, A.; Kramer, J.L.; Smith, R.A.; Jemal, A. Breast cancer statistics, 2015: Convergence of incidence rates between black and white women. CA Cancer J. Clin., 2016, 66(1), 31-42.
[http://dx.doi.org/10.3322/caac.21320] [PMID: 26513636]
[3]
Chang, J.T.; Wang, F.; Chapin, W.; Huang, R.S. Identification of MicroRNAs as breast cancer prognosis markers through the cancer genome atlas. PLoS One, 2016, 11(12)e0168284
[http://dx.doi.org/10.1371/journal.pone.0168284] [PMID: 27959953]
[4]
Iorio, M.V.; Casalini, P.; Piovan, C.; Braccioli, L.; Tagliabue, E. Breast cancer and microRNAs: therapeutic impact. Breast, 2011, 20(Suppl. 3), S63-S70.
[http://dx.doi.org/10.1016/S0960-9776(11)70297-1] [PMID: 22015296]
[5]
Siegel, R.; Naishadham, D.; Jemal, A. Cancer statistics, 2013. CA Cancer J. Clin., 2013, 63(1), 11-30.
[http://dx.doi.org/10.3322/caac.21166] [PMID: 23335087]
[6]
Bosch, A.; Eroles, P.; Zaragoza, R.; Viña, J.R.; Lluch, A. Triple-negative breast cancer: Molecular features, pathogenesis, treatment and current lines of research. Cancer Treat. Rev., 2010, 36(3), 206-215.
[http://dx.doi.org/10.1016/j.ctrv.2009.12.002] [PMID: 20060649]
[7]
Bartel, D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2), 281-297.
[http://dx.doi.org/10.1016/S0092-8674(04)00045-5] [PMID: 14744438]
[8]
Gibb, E.A.; Brown, C.J.; Lam, W.L. The functional role of long non-coding RNA in human carcinomas. Mol. Cancer, 2011, 10(1), 38.
[http://dx.doi.org/10.1186/1476-4598-10-38] [PMID: 21489289]
[9]
Zaleska, K. miRNA-Therapeutic tool in breast cancer? Where are we now? Rep. Pract. Oncol. Radiother., 2014, 20(2), 79-86.
[http://dx.doi.org/10.1016/j.rpor.2014.10.009] [PMID: 25859396]
[10]
Jackson, R.J.; Standart, N. How do microRNAs regulate gene expression? Sci. STKE, 2007, 2007(367), re1.
[http://dx.doi.org/10.1126/stke.3672007re1 ] [PMID: 17200520]
[11]
Nikitina, E.G.; Urazova, L.N.; Stegny, V.N. MicroRNAs and human cancer. Exp. Oncol., 2012, 34(1), 2-8.
[PMID: 22453141]
[12]
Lee, Y.M.; Lee, J.Y.; Ho, C.C.; Hong, Q.S.; Yu, S.L.; Tzeng, C.R.; Yang, P.C.; Chen, H.W. miRNA-34b as a tumor suppressor in estrogen-dependent growth of breast cancer cells. Breast Cancer Res., 2011, 13(6), R116.
[http://dx.doi.org/10.1186/bcr3059] [PMID: 22113133]
[13]
Lin, P.Y.; Yu, S.L.; Yang, P.C. MicroRNA in lung cancer. Br. J. Cancer, 2010, 103(8), 1144-1148.
[http://dx.doi.org/10.1038/sj.bjc.6605901] [PMID: 20859290]
[14]
Rahimian, A.; Soleimani, M.; Kaviani, S.; Aghaee-Bakhtiari, S.H.; Atashi, A.; Arefian, E.; Nikougoftar, M. Bypassing the maturation arrest in myeloid cell line U937 by over-expression of microRNA-424. Hematology, 2011, 16(5), 298-302.
[http://dx.doi.org/10.1179/102453311X13085644680140] [PMID: 21902894]
[15]
Lee, Y.; Ahn, C.; Han, J.; Choi, H.; Kim, J.; Yim, J.; Lee, J.; Provost, P.; Rådmark, O.; Kim, S.; Kim, V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature, 2003, 425(6956), 415-419.
[http://dx.doi.org/10.1038/nature01957] [PMID: 14508493]
[16]
Lee, Y.; Kim, M.; Han, J.; Yeom, K.H.; Lee, S.; Baek, S.H.; Kim, V.N. MicroRNA genes are transcribed by RNA polymerase II. EMBO J., 2004, 23(20), 4051-4060.
[http://dx.doi.org/10.1038/sj.emboj.7600385] [PMID: 15372072]
[17]
Awasthi, R.; Roseblade, A.; Hansbro, P.M.; Rathbone, M.J.; Dua, K.; Bebawy, M. Nanoparticles in cancer treatment: Opportunities and obstacles. Curr. Drug Targets, 2018, 19(14), 1696-1709.
[http://dx.doi.org/10.2174/1389450119666180326122831] [PMID: 29577855]
[18]
Awasthi, R.; Rathbone, M.J.; Hansbro, P.M.; Bebawy, M.; Dua, K. Therapeutic prospects of microRNAs in cancer treatment through nanotechnology. Drug Deliv. Transl. Res., 2018, 8(1), 97-110.
[http://dx.doi.org/10.1007/s13346-017-0440-1] [PMID: 29185148]
[19]
Dua, K.; Hansbro, N.G.; Foster, P.S.; Hansbro, P.M. MicroRNAs as therapeutics for future drug delivery systems in treatment of lung diseases. Drug Deliv. Transl. Res., 2017, 7(1), 168-178.
[http://dx.doi.org/10.1007/s13346-016-0343-6] [PMID: 27848224]
[20]
Diederichs, S.; Haber, D.A. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell, 2007, 131(6), 1097-1108.
[http://dx.doi.org/10.1016/j.cell.2007.10.032] [PMID: 18083100]
[21]
Scott, M.S.; Ono, M. From snoRNA to miRNA: Dual function regulatory non-coding RNAs. Biochimie, 2011, 93(11), 1987-1992.
[http://dx.doi.org/10.1016/j.biochi.2011.05.026] [PMID: 21664409]
[22]
Melo, S.A.; Esteller, M. Dysregulation of microRNAs in cancer: playing with fire. FEBS Lett., 2011, 585(13), 2087-2099.
[http://dx.doi.org/10.1016/j.febslet.2010.08.009] [PMID: 20708002]
[23]
Li, H.; Bian, C.; Liao, L.; Li, J.; Zhao, R.C. miR-17-5p promotes human breast cancer cell migration and invasion through suppression of HBP1. Breast Cancer Res. Treat., 2011, 126(3), 565-575.
[http://dx.doi.org/10.1007/s10549-010-0954-4] [PMID: 20505989]
[24]
Liu, S.; Goldstein, R.H.; Scepansky, E.M.; Rosenblatt, M. Inhibition of rho-associated kinase signaling prevents breast cancer metastasis to human bone. Cancer Res., 2009, 69(22), 8742-8751.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-1541] [PMID: 19887617]
[25]
Kim, K.; Chadalapaka, G.; Lee, S.O.; Yamada, D.; Sastre-Garau, X.; Defossez, P-A.; Park, Y-Y.; Lee, J-S.; Safe, S. Identification of oncogenic microRNA-17-92/ZBTB4/specificity protein axis in breast cancer. Oncogene, 2012, 31(8), 1034-1044.
[http://dx.doi.org/10.1038/onc.2011.296] [PMID: 21765466]
[26]
Rippe, V.; Dittberner, L.; Lorenz, V.N.; Drieschner, N.; Nimzyk, R.; Sendt, W.; Junker, K.; Belge, G.; Bullerdiek, J. The two stem cell microRNA gene clusters C19MC and miR-371-3 are activated by specific chromosomal rearrangements in a subgroup of thyroid adenomas. PLoS One, 2010, 5(3)e9485
[http://dx.doi.org/10.1371/journal.pone.0009485] [PMID: 20209130]
[27]
Mochizuki, K.; Gorovsky, M.A. A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev., 2005, 19(1), 77-89.
[http://dx.doi.org/10.1101/gad.1265105] [PMID: 15598983]
[28]
Serpico, D.; Molino, L.; Di Cosimo, S. microRNAs in breast cancer development and treatment. Cancer Treat. Rev., 2014, 40(5), 595-604.
[http://dx.doi.org/10.1016/j.ctrv.2013.11.002] [PMID: 24286642]
[29]
White, N.M.; Fatoohi, E.; Metias, M.; Jung, K.; Stephan, C.; Yousef, G.M. Metastamirs: a stepping stone towards improved cancer management. Nat. Rev. Clin. Oncol., 2011, 8(2), 75-84.
[http://dx.doi.org/10.1038/nrclinonc.2010.173] [PMID: 21045789]
[30]
Toyota, M.; Suzuki, H.; Sasaki, Y.; Maruyama, R.; Imai, K.; Shinomura, Y.; Tokino, T. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res., 2008, 68(11), 4123-4132.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-0325] [PMID: 18519671]
[31]
Rokhlin, O.W.; Scheinker, V.S.; Taghiyev, A.F.; Bumcrot, D.; Glover, R.A.; Cohen, M.B. MicroRNA-34 mediates AR-dependent p53-induced apoptosis in prostate cancer. Cancer Biol. Ther., 2008, 7(8), 1288-1296.
[http://dx.doi.org/10.4161/cbt.7.8.6284] [PMID: 18497571]
[32]
Ji, Q.; Hao, X.; Meng, Y.; Zhang, M.; Desano, J.; Fan, D.; Xu, L. Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer, 2008, 8, 266.
[http://dx.doi.org/10.1186/1471-2407-8-266] [PMID: 18803879]
[33]
Osborne, C.K.; Bardou, V.; Hopp, T.A.; Chamness, G.C.; Hilsenbeck, S.G.; Fuqua, S.A.; Wong, J.; Allred, D.C.; Clark, G.M.; Schiff, R. Role of the estrogen receptor coactivator AIB1 (SRC-3) and HER-2/neu in tamoxifen resistance in breast cancer. J. Natl. Cancer Inst., 2003, 95(5), 353-361.
[http://dx.doi.org/10.1093/jnci/95.5.353] [PMID: 12618500]
[34]
Pan, X.; Wang, Z.X.; Wang, R. MicroRNA-21: a novel therapeutic target in human cancer. Cancer Biol. Ther., 2010, 10(12), 1224-1232.
[http://dx.doi.org/10.4161/cbt.10.12.14252] [PMID: 21139417]
[35]
Watanabe, S.; Ueda, Y.; Akaboshi, S.; Hino, Y.; Sekita, Y.; Nakao, M. HMGA2 maintains oncogenic RAS-induced epithelial-mesenchymal transition in human pancreatic cancer cells. Am. J. Pathol., 2009, 174(3), 854-868.
[http://dx.doi.org/10.2353/ajpath.2009.080523] [PMID: 19179606]
[36]
Helland, Å.; Anglesio, M.S.; George, J.; Cowin, P.A.; Johnstone, C.N.; House, C.M.; Sheppard, K.E.; Etemadmoghadam, D.; Melnyk, N.; Rustgi, A.K.; Phillips, W.A.; Johnsen, H.; Holm, R.; Kristensen, G.B.; Birrer, M.J.; Pearson, R.B.; Børresen-Dale, A.L.; Huntsman, D.G.; deFazio, A.; Creighton, C.J.; Smyth, G.K.; Bowtell, D.D. Australian Ovarian Cancer Study Group. Deregulation of MYCN, LIN28B and LET7 in a molecular subtype of aggressive high-grade serous ovarian cancers. PLoS One, 2011, 6(4)e18064
[http://dx.doi.org/10.1371/journal.pone.0018064] [PMID: 21533284]
[37]
Hossain, A.; Kuo, M.T.; Saunders, G.F. Mir-17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Mol. Cell. Biol., 2006, 26(21), 8191-8201.
[http://dx.doi.org/10.1128/MCB.00242-06] [PMID: 16940181]
[38]
Kondo, N.; Toyama, T.; Sugiura, H.; Fujii, Y.; Yamashita, H. miR-206 Expression is down-regulated in estrogen receptor α-positive human breast cancer. Cancer Res., 2008, 68(13), 5004-5008.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-0180] [PMID: 18593897]
[39]
Lim, Y.; Wright, J.A.; Attema, J.L.; Gregory, P.A.; Bert, A.G.; Smith, E.; Thomas, D.; Drew, P.A.; Khew-Goodall, Y.; Goodall, G.J. Epigenetic modulation of the miR-200 family is associated with transition to a breast cancer stem cell-like state. J. Cell Sci., 2013, 126, 2256-2266.
[http://dx.doi.org/10.1242/jcs.122275 ]
[40]
Li, X.; Lewis, M.T.; Huang, J.; Gutierrez, C.; Osborne, C.K.; Wu, M-F.; Hilsenbeck, S.G.; Pavlick, A.; Zhang, X.; Chamness, G.C.; Wong, H.; Rosen, J.; Chang, J.C. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J. Natl. Cancer Inst., 2008, 100(9), 672-679.
[http://dx.doi.org/10.1093/jnci/djn123] [PMID: 18445819]
[41]
Dykxhoorn, D.M.; Wu, Y.; Xie, H.; Yu, F.; Lal, A.; Petrocca, F.; Martinvalet, D.; Song, E.; Lim, B.; Lieberman, J. miR-200 enhances mouse breast cancer cell colonization to form distant metastases. PLoS One, 2009, 4(9)e7181
[http://dx.doi.org/10.1371/journal.pone.0007181] [PMID: 19787069]
[42]
Wang, H.; Shi, H.; Luo, J.; Yi, Y.; Yao, D.; Zhang, X.; Ma, G.; Loor, J.J. MiR-145 Regulates Lipogenesis in Goat Mammary Cells Via Targeting INSIG1 and Epigenetic Regulation of Lipid-Related Genes. J. Cell. Physiol., 2017, 232(5), 1030-1040.
[http://dx.doi.org/10.1002/jcp.25499] [PMID: 27448180]
[43]
Hu, J.; Guo, H.; Li, H.; Liu, Y.; Liu, J.; Chen, L.; Zhang, J.; Zhang, N. MiR-145 regulates epithelial to mesenchymal transition of breast cancer cells by targeting Oct4. PLoS One, 2012, 7(9)e45965
[http://dx.doi.org/10.1371/journal.pone.0045965] [PMID: 23049906]
[44]
Radojicic, J.; Zaravinos, A.; Vrekoussis, T.; Kafousi, M.; Spandidos, D.A.; Stathopoulos, E.N. MicroRNA expression analysis in triple-negative (ER, PR and Her2/neu) breast cancer. Cell Cycle, 2011, 10(3), 507-517.
[http://dx.doi.org/10.4161/cc.10.3.14754] [PMID: 21270527]
[45]
Wang, S.; Huang, J.; Lyu, H.; Lee, C.K.; Tan, J.; Wang, J.; Liu, B. Functional cooperation of miR-125a, miR-125b, and miR-205 in entinostat-induced downregulation of erbB2/erbB3 and apoptosis in breast cancer cells. Cell Death Dis., 2013, 4(3)e556
[http://dx.doi.org/10.1038/cddis.2013.79] [PMID: 23519125]
[46]
Wang, W.; Luo, Y.P. MicroRNAs in breast cancer: oncogene and tumor suppressors with clinical potential. J. Zhejiang Univ. Sci. B, 2015, 16(1), 18-31.
[http://dx.doi.org/10.1631/jzus.B1400184] [PMID: 25559952]
[47]
Heyn, H.; Engelmann, M.; Schreek, S.; Ahrens, P.; Lehmann, U.; Kreipe, H.; Schlegelberger, B.; Beger, C. MicroRNA miR-335 is crucial for the BRCA1 regulatory cascade in breast cancer development. Int. J. Cancer, 2011, 129(12), 2797-2806.
[http://dx.doi.org/10.1002/ijc.25962] [PMID: 21618216]
[48]
Fan, Y.; Yin, S.; Hao, Y.; Yang, J.; Zhang, H.; Sun, C.; Ma, M.; Chang, Q.; Xi, J.J. miR-19b promotes tumor growth and metastasis via targeting TP53. RNA, 2014, 20(6), 765-772.
[http://dx.doi.org/10.1261/rna.043026.113] [PMID: 24742936]
[49]
Calin, G.A.; Dumitru, C.D.; Shimizu, M.; Bichi, R.; Zupo, S.; Noch, E.; Aldler, H.; Rattan, S.; Keating, M.; Rai, K.; Rassenti, L.; Kipps, T.; Negrini, M.; Bullrich, F.; Croce, C.M. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA, 2002, 99(24), 15524-15529.
[http://dx.doi.org/10.1073/pnas.242606799] [PMID: 12434020]
[50]
Zhou, F.; Zhu, H.; Luo, D.; Wang, M.; Dong, X.; Hong, Y.; Lu, B.; Zhou, Y.; Zhou, J.; Zhang, Z.; Gong, W. A functional polymorphism in Pre-miR-146a is associated with susceptibility to gastric cancer in a Chinese population. DNA Cell Biol., 2012, 31(7), 1290-1295.
[http://dx.doi.org/10.1089/dna.2011.1596] [PMID: 22455393]
[51]
Xu, X.; Chen, Z.; Zhao, X.; Wang, J.; Ding, D.; Wang, Z.; Tan, F.; Tan, X.; Zhou, F.; Sun, J.; Sun, N.; Gao, Y.; Shao, K.; Li, N.; Qiu, B.; He, J. MicroRNA-25 promotes cell migration and invasion in esophageal squamous cell carcinoma. Biochem. Biophys. Res. Commun., 2012, 421(4), 640-645.
[http://dx.doi.org/10.1016/j.bbrc.2012.03.048] [PMID: 22450326]
[52]
Puzey, J.R.; Karger, A.; Axtell, M.; Kramer, E.M. Deep annotation of Populus trichocarpa microRNAs from diverse tissue sets. PLoS One, 2012, 7(3)e33034
[http://dx.doi.org/10.1371/journal.pone.0033034] [PMID: 22442676]
[53]
Shi, M.; Guo, N. MicroRNA expression and its implications for the diagnosis and therapeutic strategies of breast cancer. Cancer Treat. Rev., 2009, 35(4), 328-334.
[http://dx.doi.org/10.1016/j.ctrv.2008.12.002] [PMID: 19171434]
[54]
Shi, M.; Liu, D.; Duan, H.; Shen, B.; Guo, N. Metastasis-related miRNAs, active players in breast cancer invasion, and metastasis. Cancer Metastasis Rev., 2010, 29(4), 785-799.
[http://dx.doi.org/10.1007/s10555-010-9265-9] [PMID: 20938719]
[55]
Castañeda, C.A.; Agullo-Ortuño, M.T.; Fresno Vara, J.A.; Cortes-Funes, H.; Gomez, H.L.; Ciruelos, E. Implication of miRNA in the diagnosis and treatment of breast cancer. Expert Rev. Anticancer Ther., 2011, 11(8), 1265-1275.
[http://dx.doi.org/10.1586/era.11.40] [PMID: 21916580]
[56]
Han, J-G.; Jiang, Y-D.; Zhang, C-H.; Yang, Y-M.; Pang, D.; Song, Y-N.; Zhang, G-Q. A novel panel of serum miR-21/miR-155/miR-365 as a potential diagnostic biomarker for breast cancer. Ann. Surg. Treat. Res., 2017, 92(2), 55-66.
[http://dx.doi.org/10.4174/astr.2017.92.2.55] [PMID: 28203552]
[57]
Peña-Chilet, M.; Martínez, M.T.; Pérez-Fidalgo, J.A.; Peiró-Chova, L.; Oltra, S.S.; Tormo, E.; Alonso-Yuste, E.; Martinez-Delgado, B.; Eroles, P.; Climent, J.; Burgués, O.; Ferrer-Lozano, J.; Bosch, A.; Lluch, A.; Ribas, G. MicroRNA profile in very young women with breast cancer. BMC Cancer, 2014, 14(1), 529.
[http://dx.doi.org/10.1186/1471-2407-14-529] [PMID: 25047087]
[58]
de Rinaldis, E.; Gazinska, P.; Mera, A.; Modrusan, Z.; Fedorowicz, G.M.; Burford, B.; Gillett, C.; Marra, P.; Grigoriadis, A.; Dornan, D.; Holmberg, L.; Pinder, S.; Tutt, A. Integrated genomic analysis of triple-negative breast cancers reveals novel microRNAs associated with clinical and molecular phenotypes and sheds light on the pathways they control. BMC Genomics, 2013, 14(1), 643.
[http://dx.doi.org/10.1186/1471-2164-14-643] [PMID: 24059244]
[59]
Tsai, H-P.; Huang, S-F.; Li, C-F.; Chien, H-T.; Chen, S-C. Differential microRNA expression in breast cancer with different onset age. PLoS One, 2018, 13(1)e0191195
[http://dx.doi.org/10.1371/journal.pone.0191195] [PMID: 29324832]
[60]
Guttilla, I.K.; White, B.A. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J. Biol. Chem., 2009, 284, 23204-23216.
[http://dx.doi.org/10.1074/jbc.M109.031427]
[61]
Inns, J.; James, V. Circulating microRNAs for the prediction of metastasis in breast cancer patients diagnosed with early stage disease. Breast, 2015, 24(4), 364-369.
[http://dx.doi.org/10.1016/j.breast.2015.04.001] [PMID: 25957467]
[62]
Romero-Cordoba, S.; Rodriguez-Cuevas, S.; Rebollar-Vega, R.; Quintanar-Jurado, V.; Maffuz-Aziz, A.; Jimenez-Sanchez, G.; Bautista-Piña, V.; Arellano-Llamas, R.; Hidalgo-Miranda, A. Identification and pathway analysis of microRNAs with no previous involvement in breast cancer. PLoS One, 2012, 7(3)e31904
[http://dx.doi.org/10.1371/journal.pone.0031904] [PMID: 22438871]
[63]
Sempere, L.F.; Christensen, M.; Silahtaroglu, A.; Bak, M.; Heath, C.V.; Schwartz, G.; Wells, W.; Kauppinen, S.; Cole, C.N. Altered MicroRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res., 2007, 67(24), 11612-11620.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-5019] [PMID: 18089790]
[64]
Iorio, M.V.; Ferracin, M.; Liu, C.G.; Veronese, A.; Spizzo, R.; Sabbioni, S.; Magri, E.; Pedriali, M.; Fabbri, M.; Campiglio, M.; Ménard, S.; Palazzo, J.P.; Rosenberg, A.; Musiani, P.; Volinia, S.; Nenci, I.; Calin, G.A.; Querzoli, P.; Negrini, M.; Croce, C.M. MicroRNA gene expression deregulation in human breast cancer. Cancer Res., 2005, 65(16), 7065-7070.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-1783] [PMID: 16103053]
[65]
Yan, L.X.; Huang, X.F.; Shao, Q.; Huang, M.Y.; Deng, L.; Wu, Q.L.; Zeng, Y.X.; Shao, J.Y. MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA, 2008, 14(11), 2348-2360.
[http://dx.doi.org/10.1261/rna.1034808] [PMID: 18812439]
[66]
Schwab, L.P.; Peacock, D.L.; Majumdar, D.; Ingels, J.F.; Jensen, L.C.; Smith, K.D.; Cushing, R.C.; Seagroves, T.N. Hypoxia-inducible factor 1α promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res., 2012, 14(1), R6.
[http://dx.doi.org/10.1186/bcr3087] [PMID: 22225988]
[67]
Ireland, C.T: Circulating miRNAs. ICORG, V2., 10-11 Available at:, https://ClinicalTrials.gov/show/NCT017228512011 (Accessed on January 24, 2019).
[68]
Regaud, IC: Circulating miRNAs as Biomarkers of Hormone Sensitivity in Breast Cancer., https://clinicaltrials.gov/show/NCT016128712012 (Accessed on January 24, 2019).
[69]
Center, WPC; Szczecin, PMU: Circulating MicroRNA as Biomarker of Cardiotoxicity in Breast Cancer. Available at:, https://clinicaltrials.gov/show/NCT020659082014 (Accessed on January 24, 2019).
[70]
Krek, A.; Grün, D.; Poy, M.N.; Wolf, R.; Rosenberg, L.; Epstein, E.J.; MacMenamin, P.; da Piedade, I.; Gunsalus, K.C.; Stoffel, M.; Rajewsky, N. Combinatorial microRNA target predictions. Nat. Genet., 2005, 37(5), 495-500.
[http://dx.doi.org/10.1038/ng1536] [PMID: 15806104]
[71]
Xiao, J.; Yang, B.; Lin, H.; Lu, Y.; Luo, X.; Wang, Z. Novel approaches for gene-specific interference via manipulating actions of microRNAs: examination on the pacemaker channel genes HCN2 and HCN4. J. Cell. Physiol., 2007, 212(2), 285-292.
[http://dx.doi.org/10.1002/jcp.21062] [PMID: 17516552]
[72]
Garofalo, M.; Condorelli, G.; Croce, C.M. MicroRNAs in diseases and drug response. Curr. Opin. Pharmacol., 2008, 8(5), 661-667.
[http://dx.doi.org/10.1016/j.coph.2008.06.005] [PMID: 18619557]
[73]
Yang, H.; Kong, W.; He, L.; Zhao, J.J.; O’Donnell, J.D.; Wang, J.; Wenham, R.M.; Coppola, D.; Kruk, P.A.; Nicosia, S.V.; Cheng, J.Q. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res., 2008, 68(2), 425-433.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-2488] [PMID: 18199536]
[74]
Chen, J.; Tian, W.; Cai, H.; He, H.; Deng, Y. Down-regulation of microRNA-200c is associated with drug resistance in human breast cancer. Med. Oncol., 2012, 29(4), 2527-2534.
[http://dx.doi.org/10.1007/s12032-011-0117-4] [PMID: 22101791]
[75]
Salter, K.H.; Acharya, C.R.; Walters, K.S.; Redman, R.; Anguiano, A.; Garman, K.S.; Anders, C.K.; Mukherjee, S.; Dressman, H.K.; Barry, W.T.; Marcom, K.P.; Olson, J.; Nevins, J.R.; Potti, A. An integrated approach to the prediction of chemotherapeutic response in patients with breast cancer. PLoS One, 2008, 3(4)e1908
[http://dx.doi.org/10.1371/journal.pone.0001908] [PMID: 18382681]
[76]
Blower, P.E.; Verducci, J.S.; Lin, S.; Zhou, J.; Chung, J.H.; Dai, Z.; Liu, C.G.; Reinhold, W.; Lorenzi, P.L.; Kaldjian, E.P.; Croce, C.M.; Weinstein, J.N.; Sadee, W. MicroRNA expression profiles for the NCI-60 cancer cell panel. Mol. Cancer Ther., 2007, 6(5), 1483-1491.
[http://dx.doi.org/10.1158/1535-7163.MCT-07-0009] [PMID: 17483436]
[77]
Kaboli, P.J.; Rahmat, A.; Ismail, P.; Ling, K-H. MicroRNA-based therapy and breast cancer: A comprehensive review of novel therapeutic strategies from diagnosis to treatment. Pharmacol. Res., 2015, 97, 104-121.
[http://dx.doi.org/10.1016/j.phrs.2015.04.015] [PMID: 25958353]
[78]
Leivonen, S-K.; Sahlberg, K.K.; Mäkelä, R.; Due, E.U.; Kallioniemi, O.; Børresen-Dale, A-L.; Perälä, M. High-throughput screens identify microRNAs essential for HER2 positive breast cancer cell growth. Mol. Oncol., 2014, 8(1), 93-104.
[http://dx.doi.org/10.1016/j.molonc.2013.10.001] [PMID: 24148764]
[79]
Kota, S.K.; Balasubramanian, S. Cancer therapy via modulation of micro RNA levels: A promising future. Drug Discov. Today, 2010, 15(17-18), 733-740.
[http://dx.doi.org/10.1016/j.drudis.2010.07.003] [PMID: 20692360]
[80]
Yan, L.X.; Wu, Q.N.; Zhang, Y.; Li, Y.Y.; Liao, D.Z.; Hou, J.H.; Fu, J.; Zeng, M.S.; Yun, J.P.; Wu, Q.L.; Zeng, Y.X.; Shao, J.Y. Knockdown of miR-21 in human breast cancer cell lines inhibits proliferation, in vitro migration and in vivo tumor growth. Breast Cancer Res., 2011, 13(1), R2.
[http://dx.doi.org/10.1186/bcr2803] [PMID: 21219636]
[81]
Ma, L.; Young, J.; Prabhala, H.; Pan, E.; Mestdagh, P.; Muth, D.; Teruya-Feldstein, J.; Reinhardt, F.; Onder, T.T.; Valastyan, S.; Westermann, F.; Speleman, F.; Vandesompele, J.; Weinberg, R.A. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol., 2010, 12(3), 247-256.
[http://dx.doi.org/10.1038/ncb2024] [PMID: 20173740]
[82]
Srivastava, S.P.; Koya, D.; Kanasaki, K. MicroRNAs in kidney fibrosis and diabetic nephropathy: Roles on EMT and EndMT. BioMed Res. Int., 2013, 2013125469
[http://dx.doi.org/10.1155/2013/125469]] [PMID: 24089659]
[83]
Ji, J.; Yamashita, T.; Budhu, A.; Forgues, M.; Jia, H.L.; Li, C.; Deng, C.; Wauthier, E.; Reid, L.M.; Ye, Q.H.; Qin, L.X.; Yang, W.; Wang, H.Y.; Tang, Z.Y.; Croce, C.M.; Wang, X.W. Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology, 2009, 50(2), 472-480.
[http://dx.doi.org/10.1002/hep.22989] [PMID: 19585654]
[84]
Suryawanshi, S.M.; Vlad, A.M.; Lin, H-M.; Smaldone, G.M.; Laskey, R.; Lee, M.; Lin, Y.; Donnellan, N.; Klein-Patel, M.; Lee, T. Plasma microRNAs as novel biomarkers for endometriosis and endometriosis-associated ovarian cancer. Clin. Cancer Res., 2013, 19(5), 1213-1224.
[85]
Rodrigues, A.S.; Dinis, J.; Gromicho, M.; Martins, C.; Laires, A.; Rueff, J. Genomics and Cancer Drug Resistance. Curr. Pharm. Biotechnol., 2011, 13(5), 651-673.
[http://dx.doi.org/10.2174/138920112799857549.PMID: 22122479 ]
[86]
Majumder, S.; Jacob, S.T. Emerging role of microRNAs in drug-resistant breast cancer. Gene Expr., 2011, 15(3), 141-151.
[http://dx.doi.org/10.3727/105221611X13176664479287] [PMID: 22268296]
[87]
Tordonato, C.; Di Fiore, P.P.; Nicassio, F. The role of non-coding RNAs in the regulation of stem cells and progenitors in the normal mammary gland and in breast tumors. Front. Genet., 2015, 6, 72.
[http://dx.doi.org/10.3389/fgene.2015.00072] [PMID: 25774169]
[88]
Gangopadhyay, S.; Nandy, A.; Hor, P.; Mukhopadhyay, A. Breast cancer stem cells: A novel therapeutic target. Clin. Breast Cancer, 2013, 13(1), 7-15.
[http://dx.doi.org/10.1016/j.clbc.2012.09.017] [PMID: 23127340]
[89]
Taube, J.H.; Malouf, G.G.; Lu, E.; Sphyris, N.; Vijay, V.; Ramachandran, P.P.; Ueno, K.R.; Gaur, S.; Nicoloso, M.S.; Rossi, S.; Herschkowitz, J.I.; Rosen, J.M.; Issa, J.P.; Calin, G.A.; Chang, J.T.; Mani, S.A. Epigenetic silencing of microRNA-203 is required for EMT and cancer stem cell properties. Sci. Rep., 2013, 3, 2687.
[http://dx.doi.org/10.1038/srep02687] [PMID: 24045437]
[90]
Song, S.J.; Poliseno, L.; Song, M.S.; Ala, U.; Webster, K.; Ng, C.; Beringer, G.; Brikbak, N.J.; Yuan, X.; Cantley, L.C.; Richardson, A.L.; Pandolfi, P.P. MicroRNA-antagonism regulates breast cancer stemness and metastasis via TET-family-dependent chromatin remodeling. Cell, 2013, 154(2), 311-324.
[http://dx.doi.org/10.1016/j.cell.2013.06.026] [PMID: 23830207]
[91]
Guo, J.Y.; Xia, B.; White, E. Autophagy-mediated tumor promotion. Cell, 2013, 155(6), 1216-1219.
[http://dx.doi.org/10.1016/j.cell.2013.11.019] [PMID: 24315093]
[92]
Aceto, N.; Toner, M.; Maheswaran, S.; Haber, D.A. En route to metastasis: circulating tumor cell clusters and epithelial-to-mesenchymal transition. Trends Cancer, 2015, 1(1), 44-52.
[http://dx.doi.org/10.1016/j.trecan.2015.07.006] [PMID: 28741562]
[93]
Iliopoulos, D.; Hirsch, H.A.; Struhl, K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell, 2009, 139(4), 693-706.
[http://dx.doi.org/10.1016/j.cell.2009.10.014] [PMID: 19878981]
[94]
Gregory, P.A.; Bert, A.G.; Paterson, E.L.; Barry, S.C.; Tsykin, A.; Farshid, G.; Vadas, M.A.; Khew-Goodall, Y.; Goodall, G.J. 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.
[http://dx.doi.org/10.1038/ncb1722] [PMID: 18376396]
[95]
Chao, C-H.; Chang, C-C.; Wu, M-J.; Ko, H-W.; Wang, D.; Hung, M-C.; Yang, J-Y.; Chang, C-J. MicroRNA-205 signaling regulates mammary stem cell fate and tumorigenesis. J. Clin. Invest., 2014, 124(7), 3093-3106.
[http://dx.doi.org/10.1172/JCI73351] [PMID: 24911147]
[96]
Ichikawa, T.; Sato, F.; Terasawa, K.; Tsuchiya, S.; Toi, M.; Tsujimoto, G.; Shimizu, K. Trastuzumab produces therapeutic actions by upregulating miR-26a and miR-30b in breast cancer cells. PLoS One, 2012, 7(2)e31422
[http://dx.doi.org/10.1371/journal.pone.0031422] [PMID: 22384020]
[97]
Kurokawa, K.; Tanahashi, T.; Iima, T.; Yamamoto, Y.; Akaike, Y.; Nishida, K.; Masuda, K.; Kuwano, Y.; Murakami, Y.; Fukushima, M.; Rokutan, K. Role of miR-19b and its target mRNAs in 5-fluorouracil resistance in colon cancer cells. J. Gastroenterol., 2012, 47(8), 883-895.
[http://dx.doi.org/10.1007/s00535-012-0547-6] [PMID: 22382630]
[98]
Catuogno, S.; Cerchia, L.; Romano, G.; Pognonec, P.; Condorelli, G.; de Franciscis, V. miR-34c may protect lung cancer cells from paclitaxel-induced apoptosis. Oncogene, 2012.
[PMID: 22370637]
[99]
Underwood, J.C. Lymphoreticular infiltration in human tumours: prognostic and biological implications: a review. Br. J. Cancer, 1974, 30(6), 538-548.
[http://dx.doi.org/10.1038/bjc.1974.233] [PMID: 4614858]
[100]
Denkert, C.; von Minckwitz, G.; Darb-Esfahani, S.; Lederer, B.; Heppner, B.I.; Weber, K.E.; Budczies, J.; Huober, J.; Klauschen, F.; Furlanetto, J.; Schmitt, W.D.; Blohmer, J.U.; Karn, T.; Pfitzner, B.M.; Kümmel, S.; Engels, K.; Schneeweiss, A.; Hartmann, A.; Noske, A.; Fasching, P.A.; Jackisch, C.; van Mackelenbergh, M.; Sinn, P.; Schem, C.; Hanusch, C.; Untch, M.; Loibl, S. Tumour-infiltrating lymphocytes and prognosis in different subtypes of breast cancer: a pooled analysis of 3771 patients treated with neoadjuvant therapy. Lancet Oncol., 2018, 19(1), 40-50.
[http://dx.doi.org/10.1016/S1470-2045(17)30904-X] [PMID: 29233559]
[101]
O’Loughlin, M.; Andreu, X.; Bianchi, S.; Chemielik, E.; Cordoba, A.; Cserni, G.; Figueiredo, P.; Floris, G.; Foschini, M.P.; Heikkilä, P. Reproducibility and predictive value of scoring stromal tumour infiltrating lymphocytes in triple-negative breast cancer: A multi-institutional study; Springer, 2018.
[102]
Loi, S.; Sirtaine, N.; Piette, F.; Salgado, R.; Viale, G.; Van Eenoo, F.; Rouas, G.; Francis, P.; Crown, J.P.; Hitre, E.; de Azambuja, E.; Quinaux, E.; Di Leo, A.; Michiels, S.; Piccart, M.J.; Sotiriou, C. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J. Clin. Oncol., 2013, 31(7), 860-867.
[http://dx.doi.org/10.1200/JCO.2011.41.0902] [PMID: 23341518]
[103]
Jasinski-Bergner, S.; Mandelboim, O.; Seliger, B. The role of microRNAs in the control of innate immune response in cancer. J. Natl. Cancer Inst., 2014, 106(10)dju257
[http://dx.doi.org/10.1093/jnci/dju257] [PMID: 25217579]
[104]
Podshivalova, K.; Salomon, D.R. MicroRNA regulation of T-lymphocyte immunity: Modulation of molecular networks responsible for T-cell activation, differentiation, and development. Crit. Rev. Immunol., 2013, 33(5), 435-476.
[105]
Dieci, M.V.; Radosevic-Robin, N.; Fineberg, S.; van den Eynden, G.; Ternes, N.; Penault-Llorca, F.; Pruneri, G.; D’Alfonso, T.M.; Demaria, S.; Castaneda, C. Update on tumor-infiltrating lymphocytes (TILs) in breast cancer, including recommendations to assess TILs in residual disease after neoadjuvant therapy and in carcinoma in situ: A report of the International Immuno-Oncology Biomarker Working Group on Breast Cancer. In: Seminars in cancer biology: 2017;; Elsevier, 2017.
[106]
Rodriguez, A.; Vigorito, E.; Clare, S.; Warren, M.V.; Couttet, P.; Soond, D.R.; van Dongen, S.; Grocock, R.J.; Das, P.P.; Miska, E.A.; Vetrie, D.; Okkenhaug, K.; Enright, A.J.; Dougan, G.; Turner, M.; Bradley, A. Requirement of bic/microRNA-155 for normal immune function. Science, 2007, 316(5824), 608-611.
[http://dx.doi.org/10.1126/science.1139253] [PMID: 17463290]
[107]
Zonari, E.; Pucci, F.; Saini, M.; Mazzieri, R.; Politi, L.S.; Gentner, B.; Naldini, L. A role for miR-155 in enabling tumor-infiltrating innate immune cells to mount effective antitumor responses in mice. Blood, 2013, 122(2), 243-252.
[108]
Hamam, R.; Hamam, D.; Alsaleh, K.A.; Kassem, M.; Zaher, W.; Alfayez, M.; Aldahmash, A.; Alajez, N.M. Circulating microRNAs in breast cancer: novel diagnostic and prognostic biomarkers. Cell Death Dis., 2017, 8(9)e3045
[http://dx.doi.org/10.1038/cddis.2017.440] [PMID: 28880270]
[109]
Hamam, R.; Ali, A.M.; Alsaleh, K.A.; Kassem, M.; Alfayez, M.; Aldahmash, A.; Alajez, N.M. microRNA expression profiling on individual breast cancer patients identifies novel panel of circulating microRNA for early detection. Sci. Rep., 2016, 6, 25997.
[http://dx.doi.org/10.1038/srep25997] [PMID: 27180809]
[110]
Wang, K.; Yuan, Y.; Cho, J-H.; McClarty, S.; Baxter, D.; Galas, D.J. Comparing the MicroRNA spectrum between serum and plasma. PLoS One, 2012, 7(7)e41561
[http://dx.doi.org/10.1371/journal.pone.0041561] [PMID: 22859996]
[111]
Diener, Y.; Walenda, T.; Jost, E.; Brümmendorf, T.H.; Bosio, A.; Wagner, W.; Bissels, U. MicroRNA expression profiles of serum from patients before and after chemotherapy. Genom. Data, 2015, 6, 125-127.
[http://dx.doi.org/10.1016/j.gdata.2015.08.018] [PMID: 26697352]
[112]
Hansen, T.F.; Carlsen, A.L.; Heegaard, N.H.; Sørensen, F.B.; Jakobsen, A. Changes in circulating microRNA-126 during treatment with chemotherapy and bevacizumab predicts treatment response in patients with metastatic colorectal cancer. Br. J. Cancer, 2015, 112(4), 624-629.
[http://dx.doi.org/10.1038/bjc.2014.652] [PMID: 25584492]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy