Dysregulation of microRNAs in breast cancer and their potential role as prognostic and predictive biomarkers in patient management

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  van Schooneveld, Eleni ^a   Wildiers, Hans ^a   Vergote, Ignace ^a   Vermeulen, Peter B ^b   Dirix, Luc Y ^b   Van Laere, Steven J ^a,b  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 107; MICRORNA 10B; MICRORNA 133A; MICRORNA 133B; MICRORNA 143; MICRORNA 145; MICRORNA 146B; MICRORNA 155; MICRORNA 15A; MICRORNA 16; MICRORNA 17 92; MICRORNA 181A; MICRORNA 18A; MICRORNA 206; MICRORNA 21; MICRORNA 210; MICRORNA 221; MICRORNA 335; MICRORNA 342; MICRORNA 365; MICRORNA 373; MICRORNA 375; MICRORNA 376C; MICRORNA 451; MICRORNA 520C; MICRORNA 801; MICRORNA 92A; RNA; UNCLASSIFIED DRUG; TUMOR MARKER;

BIOGENESIS; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER DIAGNOSIS; CANCER HORMONE THERAPY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; DRUG SENSITIVITY; FLOW CYTOMETRY; HUMAN; IN SITU HYBRIDIZATION; MEDLINE; METASTASIS; MICROARRAY ANALYSIS; NEXT GENERATION SEQUENCING; NORTHERN BLOTTING; PATHOGENESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SYSTEMATIC REVIEW; TREATMENT RESPONSE; BREAST NEOPLASMS; DISEASE MANAGEMENT; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; META ANALYSIS; MORTALITY; PROGNOSIS;

BIOMARKERS, TUMOR; BREAST NEOPLASMS; DISEASE MANAGEMENT; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MICRORNAS; NEOPLASM METASTASIS; PROGNOSIS;

EID: 84924235379     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0526-y     Document Type: Review

References (133)

1. Bombonati A, Sgroi DC. The molecular pathology of breast cancer progression. J Pathol. 2011;223:308-18.
2. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature. 2012;486:346-52.
3. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 2004;5:522-31.
4. Dvinge H, Git A, Gräf S, Salmon-Divon M, Curtis C, Sottoriva A, et al. The shaping and functional consequences of the microRNA landscape in breast cancer. Nature. 2013;497:378-82.
5. Pillai RS. MicroRNA function: multiple mechanisms for a tiny RNA? RNA. 2005;11:1753-61.
6. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435:834-8.
7. Volinia S, Calin GA, Liu C-G, Ambs S, Cimmino A, Petrocca F, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A. 2006;103:2257-61.
8. Tang J, Ahmad A, Sarkar FH. The role of microRNAs in breast cancer migration, invasion and metastasis. Int J Mol Sci. 2012;13:13414-37.
9. 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. 2014;13:52.
10. Ahmad A, Aboukameel A, Kong D, Wang Z, Sethi S, Chen W, et al. Phosphoglucose isomerase/autocrine motility factor mediates epithelial-mesenchymal transition regulated by miR-200 in breast cancer cells. Cancer Res. 2011;71:3400-9.
11. Baffa R, Fassan M, Volinia S, OHara B, Liu C, Palazzo JP, et al. MicroRNA expression profiling of human metastatic cancers identifies cancer gene targets. J Pathol. 2009;219:214-21.
12. O'Day E, Lal A. MicroRNAs and their target gene networks in breast cancer. Breast Cancer Res. 2010;12:201.
13. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A. 2004;101(9):2999-3004.
14. Iorio MV, Casalini P, Piovan C, Braccioli L, Tagliabue E. Breast cancer and microRNAs: therapeutic impact. Breast. 2011;20:S63-70.
15. Corcoran C, Friel AM, Duffy MJ, Crown J, O'Driscoll L. Intracellular and extracellular microRNAs in breast cancer. Clin Chem. 2011;57:18-32.
16. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449:682-8.
17. Gabriely G, Teplyuk NM, Krichevsky AM. Context effect: microRNA-10b in cancer cell proliferation, spread and death. Autophagy. 2011;7:1384-6.
18. Huang TH, Wu F, Loeb GB, Hsu R, Heidersbach A, Brincat A, et al. Up-regulation of miR-21 by HER2/neu signaling promotes cell invasion. J Biol Chem. 2009;284:18515-24.
19. Han M, Wang Y, Liu M, Bi X, Bao J, Zeng N, et al. MiR-21 regulates epithelial-mesenchymal transition phenotype and hypoxia-inducible factor-1α expression in third-sphere forming breast cancer stem cell-like cells. Cancer Sci. 2012;103:1058-64.
20. Qi L, Bart J, Tan LP, Platteel I, Sluis T, Huitema S, et al. Expression of miR-21 and its targets (PTEN, PDCD4, TM1) in flat epithelial atypia of the breast in relation to ductal carcinoma in situ and invasive carcinoma. BMC Cancer. 2009;9:163.
21. Song B, Wang C, Liu J, Wang X, Lv L, Wei L, et al. MicroRNA-21 regulates breast cancer invasion partly by targeting tissue inhibitor of metalloproteinase 3 expression. J Exp Clin Cancer Res. 2010;29:29.
22. Lu Z, Liu M, Stribinskis V, Klinge CM, Ramos KS, Colburn NH, et al. MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene. 2008;27:4373-9.
23. Jiang S, Zhang HW, Lu MH, He XH, Li Y, Gu H, et al. MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res. 2010;70:3119-27.
24. Zhang CM, Zhao J, Deng HY. MiR-155 promotes proliferation of human breast cancer MCF-7 cells through targeting tumor protein 53-induced nuclear protein 1. J Biomed Sci. 2013;20:79.
25. Kong W, He L, Coppola M, Guo J, Esposito NN, Coppola D, et al. MicroRNA-155 regulates cell survival, growth, and chemosensitivity by targeting FOXO3a in breast cancer. J Biol Chem. 2010;285:17869-79.
26. Huang GQ, Gumireddy K, Schrier M, le Sage C, Nagel R, Coukos G, et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol. 2008;10:202-10.
27. Yan GR, Xu SH, Tan ZL, Liu L, He QY. Global identification of miR-373-regulated genes in breast cancer by quantitative proteomics. Proteomics. 2011;11:912-20.
28. Zhang B, Pan X, Cobb GP, Anderson TA. microRNAs as oncogenes and tumor suppressors. Dev Biol. 2007;302:1-12.
29. Ferracin M, Bassi C, Pedriali M, Pagotto S, D'Abundo L, Zagatti B, et al. miR-125b targets erythropoietin and its receptor and their expression correlates with metastatic potential and ERBB2/HER2 expression. Mol Cancer. 2013;12:130.
30. Feliciano A, Castellvi J, Artero-Castro A, Leal JA, Romagosa C, Hernández-Losa J, et al. miR-125b acts as a tumor suppressor in breast tumorigenesis via its novel direct targets ENPEP, CK2-α, CCNJ, and MEGF9. PLoS One. 2013;8:e76247.
31. Scott GK, Goga A, Bhaumik D, Berger CE, Sullivan CS, Benz CC. Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem. 2007;282:1479-86.
32. Liu J, Mao Q, Liu Y, Hao X, Zhang S, Zhang J. Analysis of miR-205 and miR-155 expression in the blood of breast cancer patients. Chin J Cancer Res. 2013;25:46-54.
33. Elgamal OA, Park JK, Gusev Y, Azevedo-Pouly AC, Jiang J, Roopra A, et al. Tumor suppressive function of mir-205 in breast cancer is linked to HMGB3 regulation. PLoS One. 2013;8:e76402.
34. Jiang H, Wang P, Li X, Wang Q, Deng ZB, Zhuang X, et al. Restoration of miR17/20a in solid tumor cells enhances the natural killer cell antitumor activity by targeting Mekk2. Cancer Immunol Res. 2014;2:789-99.
35. Fan M, Sethuraman A, Brown M, Sun W, Pfeffer LM. Systematic analysis of metastasis-associated genes identifies miR-17-5p as a metastatic suppressor of basal-like breast cancer. Breast Cancer Res Treat. 2014;146:487-502.
36. Li Y, Hong F, Yu Z. Decreased expression of microRNA-206 in breast cancer and its association with disease characteristics and patient survival. J Int Med Res. 2013;41:596-602.
37. Fu Y, Jiang BQ, Wu Y, Li ZD, Zhuang ZG. Hsa-miR-206 inhibits the migration and invasion of breast cancer by targeting Cx43. Zhonghua Yi XueZaZhi. 2013;93:2890-4.
38. Zhang HF, Xu LY, Li E. A family of pleiotropically acting microRNAs in cancer progression, miR-200: potential cancer therapeutic targets. Curr Pharm Des. 2014;20:1896-903.
39. Roy SS, Gonugunta VK, Bandyopadhyay A, Rao MK, Goodall GJ, Sun LZ, et al. Significance of PELP1/HDAC2/miR-200 regulatory network in EMT and metastasis of breast cancer. Oncogene. 2014;33:3707-16.
40. Castilla MÁ, Díaz-Martín J, Sarrió D, Romero-Pérez L, López-García MÁ, Vieites B, et al. MicroRNA-200 family modulation in distinct breast cancer phenotypes. PLoS One. 2012;7:e47709.
41. Xiang M, Birkbak NJ, Vafaizadeh V, Walker SR, Yeh JE, Liu S, et al. STAT3 induction of miR-146b forms a feedback loop to inhibit the NF-κB to IL-6 signaling axis and STAT3-driven cancer phenotypes. Sci Signal. 2014;7:ra11.
42. Bhaumik D, Scott GK, Schokrpur S, Patil CK, Campisi J, Benz CC. Expression of microRNA-146 suppresses NF-κB activity with reduction of metastatic potential in breast cancer cells. Oncogene. 2008;27:5643-7.
43. Png KJ, Halberg N, Yoshida M, Tavazoie SF. A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature. 2012;481:190-4.
44. Tavazoie SF, Alarcón C, Oskarsson T, Padua D, Wang Q, Bos PD, et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature. 2008;451:147-52.
45. Zhang S, Kim K, Jin UH, Pfent C, Cao H, Amendt B, et al. Aryl hydrocarbon receptor agonists induce microRNA-335 expression and inhibit lung metastasis of estrogen receptor negative breast cancer cells. Mol Cancer Ther. 2012;11:108-18.
46. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szász AM, Wang ZC, et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell. 2009;137:1032-46.
47. Augoff K, McCue B, Plow EF, Sossey-Alaoui K. miR-31 and its host gene lncRNA LOC554202 are regulated by promoter hypermethylation in triple-negative breast cancer. Mol Cancer. 2012;11:5.
48. Sossey-Alaoui K, Downs-Kelly E, Das M, Izem L, Tubbs R, Plow EF. WAVE3, an actin remodeling protein, is regulated by the metastasis suppressor microRNA, miR-31, during the invasion-metastasis cascade. Int J Cancer. 2011;129:1331-43.
49. Kasinski AL, Slack FJ. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat Rev Cancer. 2011;11:849-64.
50. Garcia AI, Buisson M, Bertrand P, Rimokh R, Rouleau E, Lopez BS, et al. Down-regulation of BRCA1 expression by miR-146a and miR-146b-5p in triple negative sporadic breast cancers. EMBO Mol Med. 2011;3:279-90.
51. Jiang H, Zhang G, Wu JH, Jiang CP. Diverse roles of miR-29 in cancer (review). Oncol Rep. 2014;31:1509-16.
52. Keklikoglou I, Koerner C, Schmidt C, Zhang JD, Heckmann D, Shavinskaya A, et al. MicroRNA-520/373 family functions as a tumor suppressor in estrogen receptor negative breast cancer by targeting NF-kB and TGF-b signaling pathways. Oncogene. 2012;31:4150-63.
53. Várallyay É, Burgyan J, Havelda J. MicroRNA detection by northern blotting using locked nucleic acid probes. Nat Protoc. 2008;3:190-6.
54. Hammond SM. microRNA detection comes of age. Nat Methods. 2006;3:12-3.
55. Balcells I, Cirera S, Busk PK. Specific and sensitive quantitative RT-PCR of miRNAs with DNA primers. BMC Biotechnol. 2011;11:70.
56. Li W, Ruan K. MicroRNA detection by microarray. Anal Bioanal Chem. 2009;394:1117-24.
57. Wu X, Somlo G, Yu Y, Palomares MR, Li AX, Zhou W, et al. De novo sequencing of circulating miRNAs identifies novel markers predicting clinical outcome of locally advanced breast cancer. J Transl Med. 2012;10:42.
58. Creighton CJ, Reid JG, Gunaratne PH. Expression profiling of microRNAs by deep sequencing. Brief Bioinform. 2009;10:490-7.
59. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:1-12.
60. van Schooneveld E, Wouters MC, Van der Auwera I, Peeters DJ, Wildiers H, Van Dam PA, et al. Expression profiling of cancerous and normal breast tissues identifies microRNAs that are differentially expressed in serum from patients with (metastatic) breast cancer and healthy volunteers. Breast Cancer Res. 2012;14:R34.
61. Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, Speleman F, et al. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 2009;10:R64.
62. 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. Mol Oncol. 2014;8:874-83.
63. Wang F, Hou J, Jin W, Li J, Yue Y, Jin H, et al. Increased circulating microRNA-155 as a potential biomarker for breast cancer screening: a meta-analysis. Molecules. 2014;19:6282-93.
64. Chan M, Liaw CS, Ji SM, Tan HH, Wong CY, Thike AA, et al. Identification of circulating microRNA signatures for breast cancer detection. Clin Cancer Res. 2013;19:4477-87.
65. Cuk K, Zucknick M, Heil J, Madhavan D, Schott S, Turchinovich A, et al. Circulating microRNAs in plasma as early detection markers for breast cancer. Int J Cancer. 2013;132:1602-12.
66. Ng EK, Li R, Shin VY, Jin HC, Leung CP, Ma ES, et al. Circulating microRNAs as specific biomarkers for breast cancer detection. PLoS One. 2013;8:e53141.
67. Godfrey AC, Xu Z, Weinberg CR, Getts RC, Wade PA, DeRoo LA, et al. Serum microRNA expression as an early marker for breast cancer risk in prospectively collected samples from the Sister Study cohort. Breast Cancer Res. 2013;15:R42.
68. Van der Auwera I, Yu W, Suo L, Van Neste L, Van Dam P, Van Marck EA, et al. Array-based DNA methylation profiling for breast cancer subtype discrimination. PLoS One. 2010;5:e12616.
69. Blenkiron C, Goldstein LD, Thorne NP, Spiteri I, Chin S-F, Dunning MJ, et al. MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol. 2007;8:R214.
70. Serpico D, Molino L, Di Cosimo S. microRNAs in breast cancer development and treatment. Cancer Treat Rev. 2014;40:595-604.
71. de Rinaldis E, Gazinska P, Mera A, Modrusan Z, Fedorowicz GM, Burford B, et al. 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;14:643.
72. Lowery AJ, Miller N, Devaney A, McNeill RE, Davoren PA, Lemetre C, et al. MicroRNA signatures predict oestrogen receptor, progesterone receptor and HER2/neu receptor status in breast cancer. Breast Cancer Res. 2009;11:R27.
73. Crippa E, Lusa L, De Cecco L, Marchesi E, Calin GA, Radice P, et al. miR-342 regulates BRCA1 expression through modulation of ID4 in breast cancer. PLoS One. 2014;9:e87039.
74. He YJ, Wu JZ, Ji MH, Ma T, Qiao EQ, Ma R, et al. miR-342 is associated with estrogen receptor-α expression and response to tamoxifen in breast cancer. Exp Ther Med. 2013;5:813-8.
75. Volinia S, Galasso M, Sana ME, Wise TF, Palatini J, Huebner K, et al. Breast cancer signatures for invasiveness and prognosis defined by deep sequencing of microRNA. Proc Natl Acad Sci U S A. 2012;109:1-6.
76. Giricz O, Reynolds PA, Ramnauth A, Liu C, Wang T, Stead L, et al. Hsa-miR-375 is differentially expressed during breast lobular neoplasia and promotes loss of mammary acinar polarity. J Pathol. 2012;226:108-19.
77. 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;103:532-41.
78. Lerebours F, Cizeron-Clairac G, Susini A, Vacher S, Mouret-Fourme E, Belichard C, et al. miRNA expression profiling of inflammatory breast cancer identifies a 5-miRNA signature predictive of breast tumor aggressiveness. Int J Cancer. 2013;133:1614-23.
79. Masri S, Liu Z, Phung S, Wang E, Yuan YC, Chen S. The role of microRNA-128a in regulating TGFbeta signaling in letrozole-resistant breast cancer cells. Breast Cancer Res Treat. 2010;124:89-99.
80. 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;32:1173-82.
81. Cittelly DM, Das PM, Spoelstra NS, Edgerton SM, Richer JK, Thor AD, et al. Downregulation of miR-342 is associated with tamoxifen resistant breast tumors. Mol Cancer. 2010;9:317.
82. Zhao JJ, Lin J, Yang H, Kong W, He L, Ma X, et al. MicroRNA-221/222 negatively regulates estrogen receptor alpha and is associated with tamoxifen resistance in breast cancer. J Biol Chem. 2008;283:31079-86.
83. Wei Y, Lai X, Yu S, Chen S, Ma Y, Zhang Y, et al. Exosomal miR-221/222 enhances tamoxifen resistance in recipient ER-positive breast cancer cells. Breast Cancer Res Treat. 2014;147:423-31.
84. Gan R, Yang Y, Yang X, Zhao L, Lu J, Meng QH. Downregulation of miR-221/222 enhances sensitivity of breast cancer cells to tamoxifen through upregulation of TIMP3. Cancer Gene Ther. 2014;21:290-6.
85. Rao X, Di Leva G, Li M, Fang F, Devlin C, Hartman-Frey C, et al. MicroRNA-221/222 confers breast cancer fulvestrant resistance by regulating multiple signaling pathways. Oncogene. 2011;30:1082-97.
86. Shibahara Y, Miki Y, Onodera Y, Hata S, Chan MS, Yiu CC, et al. Aromatase inhibitor treatment of breast cancer cells increases the expression of let-7f, a microRNA targeting CYP19A1. J Pathol. 2012;227:357-66.
87. Jung EJ, Santarpia L, Kim J, Esteva FJ, Moretti E, Buzdar AU, et al. Plasma microRNA 210 levels correlate with sensitivity to trastuzumab and tumor presence in breast cancer patients. Cancer. 2012;118:2603-14.
88. Zhou M, Liu Z, Zhao Y, Ding Y, Liu H, Xi Y, et al. MicroRNA-125b confers the resistance of breast cancer cells to paclitaxel through suppression of pro-apoptotic Bcl-2 antagonist killer 1 (Bak1) expression. J Biol Chem. 2010;285:21496-507.
89. Wang H, Tan G, Dong L, Cheng L, Li K, Wang Z, et al. Circulating MiR-125b as a marker predicting chemoresistance in breast cancer. PLoS One. 2012;7:e34210.
90. Climent J, Dimitrow P, Fridlyand J, Palacios J, Siebert R, Albertson DG, et al. Deletion of chromosome 11q predicts response to anthracycline-based chemotherapy in early breast cancer. Cancer Res. 2007;67:818-26.
91. Bockhorn J, Dalton R, Nwachukwu C, Huang S, Prat A, Yee K, et al. MicroRNA-30c inhibits human breast tumour chemotherapy resistance by regulating TWF1 and IL-11. Nat Commun. 2013;4:1393.
92. Fang Y, Shen H, Cao Y, Li H, Qin R, Chen Q, et al. Involvement of miR-30c in resistance to doxorubicin by regulating YWHAZ in breast cancer cells. Braz J Med Biol Res. 2014;47:60-9.
93. Mei M, Ren Y, Zhou X, Yuan XB, Han L, Wang GX, et al. Downregulation of miR-21 enhances chemotherapeutic effect of taxol in breast carcinoma cells. Technol Cancer Res Treat. 2010;9:77-86.
94. Dong J, Zhao YP, Zhou L, Zhang TP, Chen G. Bcl-2 upregulation induced by miR-21 via a direct interaction is associated with apoptosis and chemoresistance in MIA PaCa-2 pancreatic cancer cells. Arch Med Res. 2011;42:8-14.
95. Kato M, Paranjape T, Müller RU, Nallur S, Gillespie E, Keane K, et al. The mir-34 microRNA is required for the DNA damage response in vivo in C. elegans and in vitro in human breast cancer cells. Oncogene. 2009;28:2419-24.
96. Stankevicins L, da Silva AP A, Ventura Dos Passos F, Dos Santos Ferreira E, Menks Ribeiro MC, G David M, et al. MiR-34a is up-regulated in response to low dose, low energy X-ray induced DNA damage in breast cells. Radiat Oncol. 2013;8:231.
97. Quesne JL, Jones J, Warren J, Dawson S-J, Ali HR, Bardwell H, et al. Biological and prognostic associations of miR-205 and let-7b in breast cancer revealed by in situ hybridization analysis of micro-RNA expression in arrays of archival tumour tissue. J Pathol. 2012;227:306-14.
98. Sempere LF, Christensen M, Silahtaroglu A, Bak M, Heath CV, Schwartz G, et al. Altered microRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res. 2007;67:11612-20.
99. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, Hammond SM, et al. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J. 2009;28:347-58.
100. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 2007;131:1109-23.
101. Ma L, Li GZ, Wu ZS, Meng G. Prognostic significance of let-7b expression in breast cancer and correlation to its target gene of BSG expression. Med Oncol. 2014;31:1-5.
102. Markou A, Yousef GM, Stathopoulos E, Georgoulias V, Lianidou E. Prognostic significance of metastasis-related microRNAs in early breast cancer patients with a long follow-up. Clin Chem. 2014;60:197-205.
103. Xu Y, Jin J, Liu Y, Huang Z, Deng Y, You T, et al. Snail-regulated miR-375 inhibits migration and invasion of gastric cancer cells by targeting JAK2. PLoS One. 2014;9:e99516.
104. Cheng CW, Wang HW, Chang CW, Chu HW, Chen CY, Yu JC, et al. MicroRNA-30a inhibits cell migration and invasion by downregulating vimentin expression and is a potential prognostic marker in breast cancer. Breast Cancer Res Treat. 2012;134:1081-93.
105. Agrawal R, Tran U, Wessely O. The miR-30 miRNA family regulates xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development. 2009;136:3927-36.
106. Martinez I, Cazalla D, Almstead LL, Steitz JA, DiMaio D. miR-29 and miR-30 regulate B-Myb expression during cellular senescence. Proc Natl Acad Sci U S A. 2011;108:522-7.
107. Xia Z, Zhang N, Jin H, Yu Z, Xu G, Huang Z. Clinical significance of astrocyte elevated gene-1 expression in human oligodendrogliomas. Clin Neurol Neurosurg. 2010;112:413-9.
108. Zhang N, Wang X, Huo Q, Sun M, Cai C, Liu Z, et al. MicroRNA-30a suppresses breast tumor growth and metastasis by targeting metadherin. Oncogene. 2014;33:3119-28.
109. Leivonen S-K, Sahlberg KK, Mäkelä R, Due EU, Kallioniemi O, Børresen-Dale A-L, et al. High-throughput screens identify microRNAs essential for HER2 positive breast cancer cell growth. Mol Oncol. 2014;8:93-104.
110. Shen L, Li J, Xu L, Ma J, Li H, Xiao X, et al. miR-497 induces apoptosis of breast cancer cells by targeting Bcl-w. Exp Ther Med. 2012;3:475-80.
111. Wang S, Li H, Wang J, Wang D. Expression of microRNA-497 and its prognostic significance in human breast cancer. Diagn Pathol. 2013;8:172.
112. Guttilla IK, White BA. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J Biol Chem. 2009;284:23204-16.
113. Shen S, Sun Q, Liang Z, Cui X, Ren X, Chen H, et al. A prognostic model of triple-negative breast cancer based on miR-27b-3p and node status. PLoS One. 2014;9:e100664.
114. Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY. miR-21-mediated tumor growth. Oncogene. 2007;26:2799-803.
115. Lee JA, Lee HY, Lee ES, Kim I, Bae JW. Prognostic implications of microRNA-21 overexpression in invasive ductal carcinomas of the breast. J Breast Cancer. 2011;14:269.
116. Li M, Ma X, Li M, Zhang B, Huang J, Liu L, et al. Prognostic role of microRNA-210 in various carcinomas: a systematic review and meta-analysis. Dis Markers. 2014;2014:106197.
117. Wang J, Zhao J, Shi M, Ding Y, Sun H, Yuan F, et al. Elevated expression of miR-210 predicts poor survival of cancer patients: a systematic review and meta-analysis. PLoS One. 2014;9:e89223.
118. Yuva-Aydemir Y, Simkin A, Gascon E, Gao FB. MicroRNA-9: functional evolution of a conserved small regulatory RNA. RNA Biol. 2011;8:557-64.
119. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 2010;12:247-56.
120. Zhou X, Marian C, Makambi KH, Kosti O, Kallakury BVS, Loffredo CA, et al. MicroRNA-9 as potential biomarker for breast cancer local recurrence and tumor estrogen receptor status. PLoS One. 2012;7:e39011.
121. Mulrane L, Madden SF, Brennan DJ, Gremel G, McGee SF, McNally S, et al. miR-187 is an independent prognostic factor in breast cancer and confers increased invasive potential in vitro. Clin Cancer Res. 2012;18:6702-13.
122. Song CG, Wu XY, Wang C, Fu FM, Shao ZM. Correlation of miR-155 on formalin-fixed paraffin embedded tissues with invasiveness and prognosis of breast cancer. Zhonghua Wai Ke Za Zhi. 2012;50:1011-4.
123. 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;33:679-89.
124. Grelier G, Voirin N, Ay A-S, Cox DG, Chabaud S, Treilleux I, et al. Prognostic value of Dicer expression in human breast cancers and association with the mesenchymal phenotype. Br J Cancer. 2009;101:673-83.
125. Khoshnaw SM, Rakha EA, Abdel-Fatah T, Nolan CC, Hodi Z, Macmillan RD, et al. The microRNA maturation regulator Drosha is an independent predictor of outcome in breast cancer patients. Breast Cancer Res Treat. 2013;137:139-53.
126. Leaderer D, Hoffman AE, Zheng T, Fu A, Weidhaas J, Paranjape T, et al. Genetic and epigenetic association studies suggest a role of microRNA biogenesis gene exportin-5 (XPO5) in breast tumorigenesis. Int J Mol Epidemiol Genet. 2011;2:9-18.
127. Sung H, Jeon S, Lee K-M, Han S, Song M, Choi J-Y, et al. Common genetic polymorphisms of microRNA biogenesis pathway genes and breast cancer survival. BMC Cancer. 2012;12:1-12.
128. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature. 2003;425:415-20.
129. Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science. 2004;303:95-8.
130. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature. 2001;409:364-6.
131. Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature. 2005;436:740-4.
132. Kok KH, Ng MH, Ching YP, Jin DY. Human TRBP and PACT directly interact with each other and associate with Dicer to facilitate the production of small interfering RNA. J Biol Chem. 2007;282:17649-57.
133. Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, Zamore PD. Asymmetry in the assembly of the RNAi enzyme complex. Cell. 2003;115:199-208.