miR-21 Might be Involved in Breast Cancer Promotion and Invasion Rather than in Initial Events of Breast Cancer Development

Molecular Diagnosis and Therapy

Volumn 20, Issue 2, 2016, Pages 97-110

  Petrović, Nina ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TROPOMYOSIN; MICRORNA 21; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROGRAMMED CELL DEATH RECEPTOR 4; PROTEIN; RECK PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 3; UNCLASSIFIED DRUG; MICRORNA; MIRN21 MICRORNA, HUMAN;

ANGIOGENESIS; BREAST CANCER; BREAST CARCINOGENESIS; BREAST CARCINOMA; CANCER GRADING; CANCER GROWTH; CANCER PROGNOSIS; CANCER STAGING; CANCER TISSUE; CELL CONTACT; CELL PROLIFERATION; CIRCULATING TUMOR CELL; COMPUTER MODEL; EARLY DIAGNOSIS; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE CONTROL; HUMAN; INFLAMMATION; METASTASIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; ANIMAL; BREAST TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; BREAST NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICRORNAS; NEOPLASM INVASIVENESS;

EID: 84958779478     PISSN: 11771062     EISSN: 11792000     Source Type: Journal    
DOI: 10.1007/s40291-016-0186-3     Document Type: Review

References (101)

1. Tomaskovic-Crook E, Thompson EW, Thiery J. Epithelial to mesenchymal transition and breast cancer. Breast Cancer Res. 2009;11(6):213.
2. Polyak K. Breast cancer: origins and evolution. J Clin Invest. 2007;117(11):3155–63.
3. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 1996;87(2):159–70.
4. Rakoff-Nahoum S. Why cancer and inflammation? Yale J Biol Med. 2006;79(3–4):123–30.
5. Raval GN, Bharadwaj S, Levine EA, Willingham MC, Geary RL, Kute T, et al. Loss of expression of tropomyosin-1, a novel class II tumor suppressor that induces anoikis, in primary breast tumors. Oncogene. 2003;22(40):6194–203.
6. Volinsky N, McCarthy Cormac J, von Kriegsheim A, Saban N, Okada-Hatakeyama M, Kolch W, et al. Signalling mechanisms regulating phenotypic changes in breast cancer cells. Biosci Rep. 2015;35(2):e00178.
7. Martin GS. Cell signaling and cancer. Cancer Cell. 2003;4(3):167–74.
8. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57–70.
9. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.
10. Jovanovic J, Rønneberg JA, Tost J, Kristensen V. The epigenetics of breast cancer. Mol Oncol. 2010;4(3):242–54.
11. Huang Y, Nayak S, Jankowitz R, Davidson NE, Oesterreich S. Epigenetics in breast cancer: what’s new? Breast Cancer Res. 2011;13(6):225.
12. Byler S, Goldgar S, Heerboth S, Leary M, Housman G, Moulton K, et al. Genetic and epigenetic aspects of breast cancer progression and therapy. Anticancer Res. 2014;34(3):1071–7.
13. Dworkin AM, Huang THM, Toland AE. Epigenetic alterations in the breast: implications for breast cancer detection, prognosis and treatment. Semin Cancer Biol. 2009;19(3):165–71.
14. Wilson RC, Doudna JA. Molecular mechanisms of RNA interference. Annu Rev Biophys. 2013;42(1):217–39.
15. Foroni C, Broggini M, Generali D, Damia G. Epithelial–mesenchymal transition and breast cancer: role, molecular mechanisms and clinical impact. Cancer Treat Rev. 2012;38(6):689–97.
16. Gu S, Kay MA. How do miRNAs mediate translational repression? Silence. 2010;1(1):11.
17. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 2006;20(5):515–24.
18. Goh JN, Loo SY, Datta A, Siveen KS, Yap WN, Cai W, et al. microRNAs in breast cancer: regulatory roles governing the hallmarks of cancer. Biol Rev Camb Philos Soc. 2015. doi:10.1111/brv.12176.
19. Rajewsky N. microRNA target predictions in animals. Nat Genet. 2006;38(6s):S8–13.
20. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature. 2008;455(7209):58–63.
21. Jansson MD, Lund AH. MicroRNA and cancer. Mol Oncol. 2012;6(6):590–610.
22. Chuang JC, Jones PA. Epigenetics and microRNAs. Pediatr Res. 2007;61(5 Part 2):24R–9R.
23. Lehmann U. Aberrant DNA methylation of microRNA genes in human breast cancer: a critical appraisal. Cell Tissue Res. 2014;356(3):657–64.
24. Vrba L, Muñoz-Rodríguez JL, Stampfer MR, Futscher BW. miRNA gene promoters are frequent targets of aberrant DNA methylation in human breast cancer. PLoS One. 2013;8(1):e54398.
25. Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, et al. MicroRNA signatures in human ovarian cancer. Cancer Res. 2007;67(18):8699–707.
26. Brueckner B, Stresemann C, Kuner R, Mund C, Musch T, Meister M, et al. The human let-7a-3 locus contains an epigenetically regulated microRNA gene with oncogenic function. Cancer Res. 2007;67(4):1419–23.
27. Qu H, Xu W, Huang Y, Yang S. Circulating miRNAs: promising biomarkers of human cancer. Asian Pac J Cancer Prev. 2011;12(5):1117–25.
28. Roth C, Rack B, Müller V, Janni W, Pantel K, Schwarzenbach H. Circulating microRNAs as blood-based markers for patients with primary and metastatic breast cancer. Breast Cancer Res. 2010;12(6):R90.
29. Bertoli G, Cava C, Castiglioni I. MicroRNAs: new biomarkers for diagnosis, prognosis, therapy prediction and therapeutic tools for breast cancer. Theranostics. 2015;5(10):1122–43.
30. Mar-Aguilar F, Mendoza-Ramírez JA, Malagón-Santiago I, Espino-Silva PK, Santuario-Facio SK, Ruiz-Flores P, et al. Serum circulating microRNA profiling for identification of potential breast cancer biomarkers. Dis Markers. 2013;34(3):163–9.
31. Pan X, Wang ZX, Wang R. MicroRNA-21: a novel therapeutic target in human cancer. Cancer Biol Ther. 2010;10(12):1224–32.
32. Cheng Y, Zhang C. MicroRNA-21 in cardiovascular disease. J Cardiovasc Transl Res. 2010;3(3):251–5.
33. Lu TX, Lim EJ, Itskovich S, Besse JA, Plassard AJ, Mingler MK, et al. Targeted ablation of miR-21 decreases murine eosinophil progenitor cell growth. PLoS One. 2013;8(3):e59397.
34. Krichevsky AM, Gabriely G. miR-21: a small multi-faceted RNA. J Cell Mol Med. 2009;13(1):39–53.
35. Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005;65(14):6029–33.
36. Lou Y, Yang X, Wang F, Cui Z, Huang Y. MicroRNA-21 promotes the cell proliferation, invasion and migration abilities in ovarian epithelial carcinomas through inhibiting the expression of PTEN protein. Int J Mol Med. 2010;26(6):819–27.
37. Liu M, Tang Q, Qiu M, Lang N, Li M, Zheng Y, et al. miR-21 targets the tumor suppressor RhoB and regulates proliferation, invasion and apoptosis in colorectal cancer cells. FEBS Lett. 2011;585(19):2998–3005.
38. Wang Z. miR-21 promotes migration and invasion by the miR-21-PDCD4-AP-1 feedback loop in human hepatocellular carcinoma. Oncol Rep. 2012;27(5):1660–8.
39. Rask L, Balslev EVA, Jørgensen S, Eriksen J, Flyger H, Møller S, et al. High expression of miR-21 in tumor stroma correlates with increased cancer cell proliferation in human breast cancer. APMIS. 2011;119(10):663–73.
40. Yan LX, Wu QN, Zhang Y, Li YY, Liao DZ, Hou JH, et al. 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.
41. Walter BA, Gomez-Macias G, Valera VA, Sobel M, Merino MJ. miR-21 expression in pregnancy-associated breast cancer: a possible marker of poor prognosis. J Cancer. 2011;2:67–75.
42. 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(4):269–75.
43. Huang GL, Zhang XH, Guo GL, Huang KT, Yang KY, Shen X, et al. Clinical significance of miR-21 expression in breast cancer: SYBR-green I-based real-time RT-PCR study of invasive ductal carcinoma. Oncol Rep. 2009;21(3):673–9.
44. Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL, et al. 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):2348–60.
45. Qian B, Katsaros D, Lu L, Preti M, Durando A, Arisio R, et al. High miR-21 expression in breast cancer associated with poor disease-free survival in early stage disease and high TGF-β1. Breast Cancer Res Treat. 2008;117(1):131–40.
46. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1420–8.
47. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006;103(7):2257–61.
48. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 2005;33(20):e179.
49. 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(1):29.
50. Yang Y, Chaerkady R, Beer MA, Mendell JT, Pandey A. Identification of miR-21 targets in breast cancer cells using a quantitative proteomic approach. Proteomics. 2009;9(5):1374–84.
51. Wickramasinghe NS, Manavalan TT, Dougherty SM, Riggs KA, Li Y, Klinge CM. Estradiol downregulates miR-21 expression and increases miR-21 target gene expression in MCF-7 breast cancer cells. Nucleic Acids Res. 2009;37(8):2584–95.
52. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology. 2007;133(2):647–58.
53. Wang ZX, Lu BB, Wang H, Cheng ZX, Yin YM. MicroRNA-21 modulates chemosensitivity of breast cancer cells to doxorubicin by targeting PTEN. Arch Med Res. 2011;42(4):281–90.
54. Altuvia Y, Landgraf P, Lithwick G, Elefant N, Pfeffer S, Aravin A, et al. Clustering and conservation patterns of human microRNAs. Nucleic Acids Res. 2005;33(8):2697–706.
55. Zhu S, Si ML, Wu H, Mo YY. MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem. 2007;282(19):14328–36.
56. Qi L, Bart J, Tan L, 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(1):163.
57. Wang N, Zhang CQ, He JH, Duan XF, Wang YY, Ji X, et al. miR-21 down-regulation suppresses cell growth, invasion and induces cell apoptosis by targeting FASL, TIMP3, and RECK genes in esophageal carcinoma. Dig Dis Sci. 2013;58(7):1863–70.
58. Hatley ME, Patrick DM, Garcia MR, Richardson JA, Bassel-Duby R, Van Rooij E, et al. Modulation of K-Ras-dependent lung tumorigenesis by microRNA-21. Cancer Cell. 2010;18(3):282–93.
59. Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY. miR-21-mediated tumor growth. Oncogene. 2007;26(19):2799–803.
60. Medina PP, Nolde M, Slack FJ. OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature. 2010;467(7311):86–90.
61. Iorio MV. MicroRNA Gene expression deregulation in human breast cancer. Cancer Res. 2005;65(16):7065–70.
62. Buscaglia LEB, Li Y. Apoptosis and the target genes of miR-21. Chin J Cancer. 2011;30(6):371–80.
63. Hannafon BN, Sebastiani P, de las Morenas A, Lu J, Rosenberg CL. Expression of microRNA and their gene targets are dysregulated in preinvasive breast cancer. Breast Cancer Res. 2011;13(2):R24.
64. Emery LA, Tripathi A, King C, Kavanah M, Mendez J, Stone MD, et al. Early dysregulation of cell adhesion and extracellular matrix pathways in breast cancer progression. Am J Path. 2009;175(3):1292–302.
65. Chen L, Li Y, Fu Y, Peng J, Mo MH, Stamatakos M, et al. Role of deregulated microRNAs in breast cancer progression using FFPE tissue. PLoS One. 2013;8(1):e54213.
66. Petrović N, Mandušić V, Stanojević B, Lukić S, Todorović L, Roganović J, et al. The difference in miR-21 expression levels between invasive and non-invasive breast cancers emphasizes its role in breast cancer invasion. Med Oncol. 2014;31(3):1–9.
67. 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. 2012;109(8):3024–9.
68. Petrović N, Mandušić V, Dimitrijević B, Roganović J, Lukić S, Todorović L, et al. Higher miR-21 expression in invasive breast carcinomas is associated with positive estrogen and progesterone receptor status in patients from Serbia. Med Oncol. 2014;31(6):1–9.
69. 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(6):1058–64.
70. Han M, Liu M, Wang Y, Chen X, Xu J, Sun Y, et al. Antagonism of miR-21 reverses epithelial-mesenchymal transition and cancer stem cell phenotype through AKT/ERK1/2 inactivation by targeting PTEN. PLoS One. 2012;7(6):e39520.
71. Jiang LH, Ge MH, Hou XX, Cao J, Hu SS, Lu XX, et al. miR-21 regulates tumor progression through the miR-21-PDCD4-Stat3 pathway in human salivary adenoid cystic carcinoma. Lab Invest. 2015;95(12):1398–408.
72. Han M, Liu M, Wang Y, Mo Z, Bi X, Liu Z, et al. Re-expression of miR-21 contributes to migration and invasion by inducing epithelial-mesenchymal transition consistent with cancer stem cell characteristics in MCF-7 cells. Mol Cell Biochem. 2012;363(1–2):427–36.
73. Orso F, Balzac F, Marino M, Lembo A, Retta SF, Taverna D. miR-21 coordinates tumor growth and modulates KRIT1 levels. Biochem Biophys Res Commun. 2013;438(1):90–6.
74. Orimo A, Weinberg RA. Heterogeneity of stromal fibroblasts in tumor. Cancer Biol Ther. 2007;6(4):618–9.
75. Li J, Zhang Y, Zhang W, Jia S, Tian R, Kang Y, et al. Genetic heterogeneity of breast cancer metastasis may be related to miR-21 regulation of TIMP-3 in translation. Int J Surg Oncol. 2013;2013:875078.
76. Nassar FJ, El Sabban M, Zgheib NK, Tfayli A, Boulos F, Jabbour M, et al. miRNA as potential biomarkers of breast cancer in the Lebanese population and in young women: a pilot study. PLoS One. 2014;9(9):e107566.
77. Petrović N, Jovanović-Ćupić S, Brajušković G, Lukić S, Roganović J, Krajnović M, et al. Micro RNA-21 expression levels in invasive breast carcinoma with a non-invasive component. Arch Biol Sci. 2015;67(4):1285–95.
78. Si H, Sun X, Chen Y, Cao Y, Chen S, Wang H, et al. Circulating microRNA-92a and microRNA-21 as novel minimally invasive biomarkers for primary breast cancer. J Cancer Res Clin Oncol. 2013;139(2):223–9.
79. Yang X, Wang X, Shen H, Deng R, Xue K. Combination of miR-21 with circulating tumor cells markers improve diagnostic specificity of metastatic breast cancer. Cell Biochem Biophys. 2015;73(1):87–91.
80. Asaga S, Kuo C, Nguyen T, Terpenning M, Giuliano AE, Hoon DSB. Direct serum assay for microRNA-21 concentrations in early and advanced breast cancer. Clin Chem. 2011;57(1):84–91.
81. Walsh LA, Roy DM, Reyngold M, Giri D, Snyder A, Turcan S, et al. RECK controls breast cancer metastasis by modulating a convergent, STAT3-dependent neoangiogenic switch. Oncogene. 2015;34(17):2189–203.
82. Agarwal V, Bell GW, Nam JW, Bartel DP. Predicting effective microRNA target sites in mammalian mRNAs. Elife. 2015;4:e05005. doi:10.7554/eLife.05005.
83. Betel D, Koppal A, Agius P, Sander C, Leslie C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol. 2010;11(8):R90.
84. Wong N, Wang X. miRDB: an online resource for microRNA target prediction and functional annotations. Nucleic Acids Res. 2015;43(D1):D146–52.
85. Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014;42(D1):D68–73.
86. Hsu SD, Tseng YT, Shrestha S, Lin YL, Khaleel A, Chou CH, et al. miRTarBase update 2014: an information resource for experimentally validated miRNA-target interactions. Nucleic Acids Res. 2014;42(D1):D78–85.
87. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al. Combinatorial microRNA target predictions. Nat Genet. 2005;37(5):495–500.
88. Grimson A, Farh KKH, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell. 2007;27(1):91–105.
89. Sun T, Jiang D, Li J, Han D, Song Z. High expression of the RECK gene in breast cancer cells is related to low invasive capacity. Chin J Clin Oncol. 2006;3(5):322–5.
90. Qi JH, Ebrahem Q, Moore N, Murphy G, Claesson-Welsh L, Bond M, et al. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med. 2003;9(4):407–15.
91. Baker AH, George SJ, Zaltsman AB, Murphy G, Newby AC. Inhibition of invasion and induction of apoptotic cell death of cancer cell lines by overexpression of TIMP-3. Br J Cancer. 1999;79(9–10):1347–55.
92. Spurbeck WW, Ng CY, Strom TS, Vanin EF, Davidoff AM. Enforced expression of tissue inhibitor of matrix metalloproteinase-3 affects functional capillary morphogenesis and inhibits tumor growth in a murine tumor model. Blood. 2002;100(9):3361–8.
93. Kajabova V, Smolkova B, Zmetakova I, Sebova K, Krivulcik T, Bella V, et al. RASSF1A promoter methylation levels positively correlate with estrogen receptor expression in breast cancer patients. Transl Oncol. 2013;6(3):297–304.
94. Weng LP, Smith WM, Dahia PLM, Ziebold U, Gil E, Lees JA, et al. PTEN suppresses breast cancer cell growth by phosphatase activity-dependent G1 arrest followed by cell death. Cancer Res. 1999;59(22):5808–14.
95. Lui EL, Loo WT, Zhu L, Cheung MN, Chow LW. DNA hypermethylation of TIMP3 gene in invasive breast ductal carcinoma. Biomed Pharmacother. 2005;59(Suppl 2):S363–5.
96. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH. Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chemy. 2007;283(2):1026–33.
97. 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(27):18515–24.
98. Weng LP, Brown JL, Eng C. PTEN induces apoptosis and cell cycle arrest through phosphoinositol-3-kinase/Akt-dependent and independent pathways. Hum Mol Genet. 2001;10(3):237–42.
99. Pawlak G, Helfman DM. Cytoskeletal changes in cell transformation and tumorigenesis. Curr Opin Genet Dev. 2001;11(1):41–7.
100. Xu LF, Wu ZP, Chen Y, Zhu QS, Hamidi S, Navab R. MicroRNA-21 (miR-21) regulates cellular proliferation, invasion, migration, and apoptosis by targeting PTEN, RECK and Bcl-2 in lung squamous carcinoma, Gejiu City, China. PLoS One. 2014;9(8):e103698.
101. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, et al. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol. 2008;28(17):5369–80.