Modulation of cancer traits by tumor suppressor microRNAs

International Journal of Molecular Sciences

Volumn 14, Issue 1, 2013, Pages 1822-1842

  Grammatikakis, Ioannis ^a   Gorospe, Myriam ^a   Abdelmohsen, Kotb ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Carcinogenesis; OncomiR; Post transcriptional gene regulation; Senescence; Tumor suppressor microRNA

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 101; MICRORNA 125A; MICRORNA 125B; MICRORNA 128; MICRORNA 135A; MICRORNA 143; MICRORNA 145; MICRORNA 146A; MICRORNA 148A; MICRORNA 148B; MICRORNA 17 5P; MICRORNA 181A; MICRORNA 181D; MICRORNA 205; MICRORNA 216B; MICRORNA 24; MICRORNA 28; MICRORNA 296; MICRORNA 29B; MICRORNA 322; MICRORNA 340; MICRORNA 34A; MICRORNA 451; MICRORNA 519; MICRORNA 519C; MICRORNA 9; TUMOR SUPPRESSIVE MICRORNA; UNCLASSIFIED DRUG; UNINDEXED DRUG; RNA;

ANTIANGIOGENIC ACTIVITY; ANTIGEN RECOGNITION; ANTINEOPLASTIC ACTIVITY; CANCER CELL; CANCER GENETICS; CANCER INHIBITION; CANCER SURVIVAL; CANCER THERAPY; COLORECTAL CANCER; DRUG EFFICACY; DRUG RESEARCH; DRUG TARGETING; EPIGENETICS; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; GENETIC REGULATION; GENETIC TRANSCRIPTION; GROWTH INHIBITION; HUMAN; METASTASIS INHIBITION; MULTIPLE MYELOMA; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; TUMOR INVASION; ANIMAL; GENETICS; METABOLISM; NEOPLASM; QUANTITATIVE TRAIT LOCUS; TUMOR SUPPRESSOR GENE;

MAMMALIA;

ANIMALS; GENES, TUMOR SUPPRESSOR; HUMANS; MICRORNAS; NEOPLASMS; QUANTITATIVE TRAIT LOCI; RNA, MESSENGER; RNA, NEOPLASM;

EID: 84878634049     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14011822     Document Type: Review

References (140)

1. Bartel, D.P. MicroRNAs: Target recognition and regulatory functions. Cell 2004, 136, 215-233.
2. Fabian, M.R.; Sonenberg, N.; Filipowicz, W. Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 2010, 79, 351-379.
3. Lal, A.; Navarro, F.; Maher, C.A.; Maliszewski, L.E.; Yan, N.; O'Day, E.; Chowdhury, D.; Dykxhoorn, D.M.; Tsai, P.; Hofmann, O.; et al. MiR-24 inhibits cell proliferation by targeting E2F2, MYC and other cell-cycle genes via binding to "seedless" 3'UTR microRNA recognition elements. Mol. Cell 2009, 35, 610-625.
4. Thomas, M.; Lieberman, J.; Lal, A. Desperately seeking microRNA targets. Nat. Struct. Mol. Biol. 2010, 17, 1169-1174.
5. Kloosterman, W.P.; Plasterk, R.H.A. The diverse functions of MicroRNAs in animal development and disease. Dev. Cell 2006, 11, 441-450.
6. Bushati, N.; Cohen, S.M. MicroRNA functions. Annu. Rev. Cell. Dev. Biol. 2007, 23, 175-205.
7. Braun, T.; Gautel, M. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat. Rev. Mol. Cell. Bio. 2011, 12, 349-361.
8. Lima, R.T.; Busacca, S.; Almeida, G.M.; Gaudino, G.; Fennell, D.A.; Vasconcelos, M.H. MicroRNA regulation of core apoptosis pathways in cancer. Eur. J. Cancer 2011, 47, 163-174.
9. Daoud, M.S.A.; Nuin, P.; Chen, J.; Zhang, X.; Feilloter, H.; Tron, V.A. MicroRNAs as prognostic biomarkers in malignant melanoma. Mod. Pathol. 2012, 25, 113a.
10. Wang, Q.M.; Wang, S.; Wang, H.J.; Li, P.; Ma, Z.Y. MicroRNAs: Novel biomarkers for lung cancer diagnosis, prediction and treatment. Exp. Biol. Med. 2012, 237, 227-235.
11. Chen, Z.H.; Zhang, G.L.; Li, H.R.; Luo, J.D.; Li, Z.X.; Chen, G.M.; Yang, J. A panel of five circulating microRNAs as potential biomarkers for prostate cancer. Prostate 2012, 72, 1443-1452.
12. Chen, X.; Hu, Z.B.; Wang, W.J.; Ba, Y.; Ma, L.J.; Zhang, C.N.; Wang, C.; Ren, Z.J.; Zhao, Y.; Wu, S.J.; et al. Identification of ten serum microRNAs from a genome-wide serum microRNA expression profile as novel noninvasive biomarkers for nonsmall cell lung cancer diagnosis. Inter. J. Cancer 2012, 130, 1620-1628.
13. Corsini, L.R.; Bronte, G.; Terrasi, M.; Amodeo, V.; Fanale, D.; Fiorentino, E.; Cicero, G.; Bazan, V.; Russo, A. The role of microRNAs in cancer: Diagnostic and prognostic biomarkers and targets of therapies. Expert Opin. Ther. Targets 2012, 16, S103-S109.
14. Thomson, J.M.; Newman, M.; Parker, J.S.; Morin-Kensicki, E.M.; Wright, T.; Hammond, S.M. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 2006, 20, 2202-2207.
15. Faggad, A.; Budczies, J.; Tchernitsa, O.; Darb-Esfahani, S.; Sehouli, J.; Muller, B.M.; Wirtz, R.; Chekerov, R.; Weichert, W.; Sinn, B.; et al. Prognostic significance of Dicer expression in ovarian cancer-Link to global microRNA changes and oestrogen receptor expression. J. Pathol. 2010, 220, 382-391.
16. Dedes, K.J.; Natrajan, R.; Lambros, M.B.; Geyer, F.C.; Lopez-Garcia, M.A.; Savage, K.; Jones, R.L.; Reis-Filho, J.S. Down-regulation of the miRNA master regulators Drosha and Dicer is associated with specific subgroups of breast cancer. Eur. J. Cancer 2011, 47, 138-150.
17. Hanahan, D.; Weinberg, R.A. Hallmarks of Cancer: The Next Generation. Cell 2011, 144, 646-674.
18. Malumbres, M.; Barbacid, M. Cell cycle, CDKs and cancer: A changing paradigm. Nat. Rev. Cancer 2009, 9, 153-166.
19. Witsch, E.; Sela, M.; Yarden, Y. Roles for growth factors in cancer progression. Physiology 2010, 25, 85-101.
20. Li, L.; Yuan, L.; Luo, J.; Gao, J.; Guo, J.; Xie, X. MiR-34a inhibits proliferation and migration of breast cancer through down-regulation of Bcl-2 and SIRT1. Clin. Exp. Med. 2012, doi:10.1007/s10238-012-0186-5.
21. Sun, L.; Wu, Z.; Shao, Y.; Pu, Y.; Miu, W.; Yao, J.; Wu, Y.; Yang, Z.X. MicroRNA-34a suppresses cell proliferation and induces apoptosis in U87 glioma stem cells. Technol. Cancer Res. Treat. 2012, 11, 483-490.
22. Yang, J.; Liu, X.; Bhalla, K.; Kim, C.N.; Ibrado, A.M.; Cai, J.; Peng, T.I.; Jones, D.P.; Wang, X. Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 1997, 275, 1129-1132.
23. Concepcion, C.P.; Han, Y.C.; Mu, P.; Bonetti, C.; Yao, E.; D'Andrea, A.; Vidigal, J.A.; Maughan, W.P.; Ogrodowski, P.; Ventura, A. Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet. 2012, 8, e1002797.
24. 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, 8191-8201.
25. Tilli, M.T.; Reiter, R.; Oh, A.S.; Henke, R.T.; McDonnell, K.; Gallicano, G.I.; Furth, P.A.; Riegel, A.T. Overexpression of an N-terminally truncated isoform of the nuclear receptor coactivator amplified in breast cancer 1 leads to altered proliferation of mammary epithelial cells in transgenic mice. Mol. Endocrinol. 2005, 19, 644-656.
26. Fereshteh, M.P.; Tilli, M.T.; Kim, S.E.; Xu, J.; O'Malley, B.W.; Wellstein, A.; Furth, P.A.; Riegel, A.T. The nuclear receptor coactivator amplified in breast cancer-1 is required for Neu (ErbB2/HER2) activation, signaling and mammary tumorigenesis in mice. Cancer Res. 2008, 68, 3697-3706.
27. Abdelmohsen, K.; Gorospe, M. Posttranscriptional regulation of cancer traits by HuR. Wiley Interdiscip. Rev. RNA 2010, 1, 214-229.
28. Guo, X.; Wu, Y.; Hartley, R.S. MicroRNA-125a represses cell growth by targeting HuR in breast cancer. RNA Biol. 2009, 6, 575-583.
29. Abdelmohsen, K.; Srikantan, S.; Kuwano, Y.; Gorospe, M. miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels. Proc. Natl. Acad. Sci. USA 2008, 105, 20297-20302.
30. Abdelmohsen, K.; Kim, M.M.; Srikantan, S.; Mercken, E.M.; Brennan, S.E.; Wilson, G.M.; Cabo, R.; Gorospe, M. MiR-519 suppresses tumor growth by reducing HuR levels. Cell Cycle 2010, 9, 1354-1359.
31. Zhang, Y.; Yan, L.X.; Wu, Q.N.; Du, Z.M.; Chen, J.; Liao, D.Z.; Huang, M.Y.; Hou, J.H.; Wu, Q.L.; Zeng, M.S.; et al. MiR-125b is methylated and functions as a tumor suppressor by regulating the ETS1 proto-oncogene in human invasive breast cancer. Cancer Res. 2011, 71, 3552-3562.
32. Zhao, A.H.; Zeng, Q.; Xie, X.Y.; Zhou, J.N.; Yue, W.; Li, Y.L.; Pei, X.T. MicroRNA-125b induces cancer cell apoptosis through suppression of Bcl-2 expression. J. Genet. Genomics 2012, 39, 29-35.
33. Bousquet, M.; Harris, M.H.; Zhou, B.; Lodish, H.F. MicroRNA miR-125b causes leukemia. Proc. Natl. Acad. Sci. USA 2012, 107, 21558-21563.
34. Klusmann, J.H.; Li, Z.; Böhmer, K.; Maroz, A.; Koch, M.L.; Emmrich, S.; Godinho, F.J.; Orkin, S.H.; Reinhardt, D. MiR-125b-2 is a potential oncomiR on human chromosome 21 in megakaryoblastic leukemia. Genes Dev. 2010, 24, 478-490.
35. Leone, V.; D'Angelo, D.; Rubio, I.; de Freitas, P.M.; Federico, A.; Colamaio, M.; Pallante, P.; Medeiros-Neto, G.; Fusco, A. MiR-1 is a tumor suppressor in thyroid carcinogenesis targeting CCND2, CXCR4 and SDF-1alpha. J. Clin. Endocrinol. MeTable 2011, 96, E1388-E1398.
36. Hudson, R.S.; Yi, M.; Esposito, D.; Watkins, S.K.; Hurwitz, A.A.; Yfantis, H.G.; Lee, D.H.; Borin, J.F.; Naslund, M.J.; Alexander, R.B.; et al. MicroRNA-1 is a candidate tumor suppressor and prognostic marker in human prostate cancer. Nucleic Acids Res. 2012, 40, 3689-3703.
37. Datta, J.; Kutay, H.; Nasser, M.W.; Nuovo, G.J.; Wang, B.; Majumder, S.; Liu, C.G.; Volinia, S.; Croce, C.M.; Schmittgen, T.D.; et al. Methylation mediated silencing of MicroRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res. 2008, 68, 5049-5058.
38. Nasser, M.W.; Datta, J.; Nuovo, G.; Kutay, H.; Motiwala, T.; Majumder, S.; Wang, B.; Suster, S.; Jacob, S.T.; Ghoshal, K. Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1. J. Biol. Chem. 2008, 283, 33394-33405.
39. Almeida, M.I.; Nicoloso, M.S.; Zeng, L.Z.; Ivan, C.; Spizzo, R.; Gafa, R.; Xiao, L.C.; Zhang, X.N.; Vannini, I.; Fanini, F.; et al. Strand-specific miR-28-5p and miR-28-3p have distinct effects in colorectal cancer cells. Gastroenterology 2012, 142, 886-896. e9.
40. Majid, S.; Dar, A.A.; Saini, S.; Yamamura, S.; Hirata, H.; Tanaka, Y.; Deng, G.R.; Dahiya, R. MicroRNA-205-directed transcriptional activation of tumor suppressor egnes in prostate cancer. Cancer 2010, 116, 5637-5649.
41. Wei, J.J.; Wu, X.Y.; Peng, Y.; Shi, G.Z.; Olca, B.; Yang, X.M.; Daniels, G.; Osman, I.; Ouyang, J.Y.; Hernando, E.; et al. Regulation of HMGA1 expression by microRNA-296 affects prostate cancer growth and invasion. Clin. Cancer Res. 2011, 17, 1297-1305.
42. Song, Y.X.; Yue, Z.Y.; Wang, Z.N.; Xu, Y.Y.; Luo, Y.; Xu, H.M.; Zhang, X.; Jiang, L.; Xing, C.Z.; Zhang, Y. MicroRNA-148b is frequently down-regulated in gastric cancer and acts as a tumor suppressor by inhibiting cell proliferation. Mol. Cancer 2011, 10, 1.
43. Wu, H.; Huang, M.; Cao, P.; Wang, T.S.; Shu, Y.Q.; Liu, P. MiR-135a targets JAK2 and inhibits gastric cancer cell proliferation. Cancer Biol. Ther. 2012, 13, 281-288.
44. Labbaye, C.; Testa, U. The emerging role of MIR-146A in the control of hematopoiesis, immune function and cancer. J. Hematol. Oncol. 2012, 5, 13.
45. Paik, J.H.; Jang, J.Y.; Jeon, Y.K.; Kim, W.Y.; Kim, T.M.; Heo, D.S.; Kim, C.W. MicroRNA-146a downregulates NF kappa B Activity via targeting TRAF6 and functions as a tumor suppressor having strong prognostic implications in NK/T cell lymphoma. Clin. Cancer Res. 2011, 17, 4761-4771.
46. Zou, C.; Xu, Q.; Mao, F.; Li, D.; Bian, C.X.; Liu, L.Z.; Jiang, Y.; Chen, X.N.; Qi, Y.T.; Zhang, X.L.; et al. MiR-145 inhibits tumor angiogenesis and growth by N-RAS and VEGF. Cell Cycle 2012, 11, 2137-2145.
47. Xu, Q.; Liu, L.Z.; Qian, X.; Chen, Q.; Jiang, Y.; Li, D.; Lai, L.H.; Jiang, B.H. MiR-145 directly targets p70S6K1 in cancer cells to inhibit tumor growth and angiogenesis. Nucleic Acids Res. 2012, 40, 761-774.
48. Papagiannakopoulos, T.; Friedmann-Morvinski, D.; Neveu, P.; Dugas, J.C.; Gill, R.M.; Huillard, E.; Liu, C.; Zong, H.; Rowitch, D.H.; Barres, B. A; et al. Pro-neural miR-128 is a glioma tumor suppressor that targets mitogenic kinases. Oncogene 2012, 31, 1884-1895.
49. Friedman, J.M.; Liang, G.N.; Liu, C.C.; Wolff, E.M.; Tsai, Y.C.; Ye, W.; Zhou, X.H.; Jones, P.A. The putative tumor suppressor microRNA-101 modulates the cancer epigenome by repressing the polycomb group protein EZH2. Cancer Res. 2009, 69, 2623-2629.
50. Ugras, S.; Brill, E.; Jacobsen, A.; Hafner, M.; Socci, N.D.; DeCarolis, P.L.; Khanin, R.; O'Connor, R.; Mihailovic, A.; Taylor, B.S.; et al. Small RNA sequencing and functional characterization reveals microRNA-143 tumor suppressor activity in Liposarcoma. Cancer Res. 2011, 71, 5659-5669.
51. Guo, Y.; Fu, W.N.; Chen, H.; Shang, C.; Zhong, M. MiR-24 functions as a tumor suppressor in Hep2 laryngeal carcinoma cells partly through down-regulation of the S100A8 protein. Oncol. Rep. 2012, 27, 1097-1103.
52. Deng, M.; Tang, H.L.; Zhou, Y.H.; Zhou, M.; Xiong, W.; Zheng, Y.; Ye, Q.R.; Zeng, X.; Liao, Q.J.; Guo, X.F.; et al. MiR-216b suppresses tumor growth and invasion by targeting KRAS in nasopharyngeal carcinoma. J. Cell Sci. 2011, 124, 2997-3005.
53. Levati, L.; Alvino, E.; Pagani, E.; Arcelli, D.; Caporaso, P.; Bondanza, S.; di Leva, G.; Ferracin, M.; Volinia, S.; Bonmassar, E.; et al. Altered expression of selected microRNAs in melanoma: Antiproliferative and proapoptotic activity of miRNA-155. Int. J. Oncol. 2009, 35, 393-400.
54. Zhai, Q.N.; Zhou, L.; Zhao, C.J.; Wan, J.; Yu, Z.D.; Guo, X.; Qin, J.; Chen, J.; Lu, R.J. Identification of miR-508-3p and miR-509-3p that are associated with cell invasion and migration and involved in the apoptosis of renal cell carcinoma. Biochem. Biophys. Res. Commun. 2012, 419, 621-626.
55. Sigal, A.; Rotter, V. Oncogenic mutations of the p53 tumor suppressor: The demons of the guardian of the genome. Cancer Res. 2000, 60, 6788-6793.
56. Oren, M.; Vousden, K.H. Hot papers-Cancer research-Mdm2 promotes the rapid degradation of p53 by Y. Haupt, R. Maya, A. Kazaz, M. Oren and Regulation of p53 stability by Mdm2 by M.H.G. Kubbutat, S.N. Jones, K.H. Vousden-Comments. The Scientist 1999, 13, 11-11.
57. Levine, A.J. p53, the cellular gatekeeper for growth and division. Cell 1997, 88, 323-331.
58. Lukashchuk, N.; Vousden, K.H. Ubiquitination and degradation of mutant p53. Mol. Cell. Biol. 2007, 27, 8284-8295.
59. Zenz, T.; Mohr, J.; Eldering, E.; Kater, A.P.; Bühler, A.; Kienle, D.; Winkler, D.; Dürig, J.; van Oers, M.H.; Mertens, D.; et al. miR-34a as part of the resistance network in chronic lymphocytic leukemia. Blood 2009, 113, 3801-3808.
60. Chang, T.C.; Wentzel, E.A.; Kent, O.A.; Ramachandran, K.; Mullendore, M.; Lee, K.H.; Feldmann, G.; Yamakuchi, M.; Ferlito, M.; Lowenstein, C.J.; et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 2007, 26, 745-752.
61. Liston, P.; Fong, W.G.; Korneluk, R.G. The inhibitors of apoptosis: There is more to life than Bcl2. Oncogene 2003, 22, 8568-8580.
62. Sheikh, M.S.; Fornace, A.J. Death and decoy receptors and p53-mediated apoptosis. Leukemia 2000, 14, 1509-1513.
63. Uren, A.G.; Pakusch, M.; Hawkins, C.J.; Puls, K.L.; Vaux, D.L. Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proc. Natl. Acad. Sci. USA 1996, 93, 4974-4978.
64. Ashkenazi, A.; Dixit, V.M. Apoptosis control by death and decoy receptors. Curr. Opin. Cell Biol. 1999, 11, 255-260.
65. Guessous, F.; Zhang, Y.; Kofman, A.; Catania, A.; Li, Y.; Schiff, D.; Purow, B.; Abounader, R. MicroRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 2010, 9, 1031-1036.
66. Chen, F.; Hu, S.J. Effect of microRNA-34a in cell cycle, differentiation and apoptosis: A review. J. Biochem. Mol. Toxicol. 2012, 26, 79-86.
67. Tazawa, H.; Tsuchiya, N.; Izumiya, M.; Nakagama, H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc. Natl. Acad. Sci. USA 2007, 104, 15472-15477.
68. Wang, X.F.; Shi, Z.M.; Wang, X.R.; Cao, L.; Wang, Y.Y.; Zhang, J.X.; Yin, Y.; Luo, H.; Kang, C.S.; Liu, N.; et al. MiR-181d acts as a tumor suppressor in glioma by targeting K-ras and Bcl-2. J. Cancer Res. Clin. 2012, 138, 573-584.
69. Nan, Y.; Han, L.; Zhang, A.L.; Wang, G.X.; Jia, Z.F.; Yang, Y.; Yue, X.A.; Pu, P.Y.; Zhong, Y.; Kang, C.S. MiRNA-451 plays a role as tumor suppressor in human glioma cells. Brain Res. 2010, 1359, 14-21.
70. Abdelmohsen, K.; Srikantan, S.; Tominaga, K.; Kang, M.J.; Yaniv, Y.; Martindale, J.L.; Yang, X.; Park, S.S.; Becker, K.G.; Subramanian, M.; et al. Growth inhibition by miR-519 via multiple p21-inducing pathways. Mol. Cell. Biol. 2012, 32, 2530-2548.
71. Marasa, B.S.; Srikantan, S.; Martindale, J.L.; Kim, M.M.; Lee, E.K.; Gorospe, M.; Abdelmohsen, K. MicroRNA profiling in human diploid fibroblasts uncovers miR-519 role in replicative senescence. Aging 2010, 2, 333-343
72. Carmeliet, P. VEGF as a key mediator of angiogenesis in cancer. Oncology 2005, 69, 4-10.
73. Baeriswyl, V.; Christofori, G. The angiogenic switch in carcinogenesis. Semin. Cancer Biol. 2009, 19, 329-337.
74. Pugh, C.W.; Ratcliffe, P.J. Regulation of angiogenesis by hypoxia: Role of the HIF system. Nat. Med. 2003, 9, 677-684.
75. Egeblad, M.; Werb, Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2, 161-174.
76. Rundhaug, J.E. Matrix metalloproteinases, angiogenesis and cancer-Commentary re: A.C. Lockhart et al., reduction of wound angiogenesis in patients treated with BMS-275291, a broad spectrum matrix metalloproteinase inhibitor. Clin. Cancer Res. 2003, 9, 551-554.
77. Shi, Z.M.; Wang, J.; Yan, Z.P.; You, Y.P.; Li, C.Y.; Qian, X.; Yin, Y.; Zhao, P.; Wang, Y.Y.; Wang, X.F.; et al. MiR-128 inhibits tumor growth and angiogenesis by targeting p70S6K1. PLoS One 2012, 7, e32709.
78. Yue, X.; Wang, P.G.; Xu, J.; Zhu, Y.F.; Sun, G.; Pang, Q.; Tao, R.J. MicroRNA-205 functions as a tumor suppressor in human glioblastoma cells by targeting VEGF-A. Oncol. Rep. 2012, 27, 1200-1206.
79. Cha, S.T.; Chen, P.S.; Johansson, G.; Chu, C.Y.; Wang, M.Y.; Jeng, Y.M.; Yu, S.L.; Chen, J.S.; Chang, K.J.; Jee, S.H.; et al. MicroRNA-519c suppresses hypoxia-inducible factor-1 alpha expression and tumor angiogenesis. Cancer Res. 2010, 70, 2675-2685.
80. Ristimaki, A. Tumor suppressor effect of the microRNA miR-519 is mediated via the mRNA-binding protein HuR. Cell Cycle 2010, 9, 1234-1234.
81. Wu, Z.S.; Wu, Q.; Wang, C.Q.; Wang, X.N.; Huang, J.; Zhao, J.J.; Mao, S.S.; Zhang, G.H.; Xu, X.C.; Zhang, N. MiR-340 inhibition of breast cancer cell migration and invasion through targeting of oncoprotein c-Met. Cancer 2011, 117, 2842-2852.
82. Fang, J.H.; Zhou, H.C.; Zeng, C.X.; Yang, J.; Liu, Y.L.; Huang, X.Z.; Zhang, J.P.; Guan, X.Y.; Zhuang, S.M. MicroRNA-29b suppresses tumor angiogenesis, invasion and metastasis by regulating matrix metalloproteinase 2 expression. Hepatology 2011, 54, 1729-1740.
83. Zhang, H.Y.; Qi, M.; Li, S.W.; Qi, T.; Mei, H.; Huang, K.; Zheng, L.D.; Tong, Q.S. MicroRNA-9 targets matrix metalloproteinase 14 to inhibit invasion, metastasis and angiogenesis of neuroblastoma cells. Mol. Cancer Ther. 2012, 11, 1454-1466.
84. Teng, M.W.L.; Swann, J.B.; Koebel, C.M.; Schreiber, R.D.; Smyth, M.J. Immune-mediated dormancy: An equilibrium with cancer. J. Leukocyte Biol. 2008, 84, 988-993.
85. Kim, R.; Emi, M.; Tanabe, K. Cancer immunoediting from immune surveillance to immune escape. Immunology 2007, 121, 1-14.
86. Yang, R.Y.; Rabinovich, G.A.; Liu, F.T. Galectins: Structure, function and therapeutic potential. Expert Rev. Mol. Med. 2008, 10, e17.
87. Rubinstein, N.; Ilarregui, J.M.; Toscano, M.A.; Rabinovich, G.A. The role of galectins in the initiation, amplification and resolution of the inflammatory response. Tissue Antigens 2004, 64, 1-12.
88. Uyttenhove, C.; Pilotte, L.; Theate, I.; Stroobant, V.; Colau, D.; Parmentier, N.; Boon, T.; van den Eynde, B.J. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 2003, 9, 1269-1274.
89. Teicher, B.A. Transforming growth factor-beta and the immune response to malignant disease. Clin. Cancer Res. 2007, 13, 6247-6251.
90. Khong, H.T.; Restifo, N.P. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat. Immunol. 2002, 3, 999-1005.
91. Wang, T.; Niu, G.L.; Kortylewski, M.; Burdelya, L.; Shain, K.; Zhang, S.M.; Bhattacharya, R.; Gabrilovich, D.; Heller, R.; Coppola, D.; et al. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat. Med. 2004, 10, 209.
92. Groh, V.; Rhinehart, R.; Randolph-Habecker, J.; Topp, M.S.; Riddell, S.R.; Spies, T. Costimulation of CD8αβ T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2001, 2, 255-260.
93. Kusmartsev, S.; Nagaraj, S.; Gabrilovich, D.I. Tumor-associated CD8+ T cell tolerance induced by bone marrow-derived immature myeloid cells. J. Immunol. 2005, 175, 4583-4592.
94. Ramasamy, S.; Duraisamy, S.; Barbashov, S.; Kawano, T.; Kharbanda, S.; Kufe, D. The MUC1 and galectin-3 oncoproteins function in a microRNA-dependent regulatory loop. Mol. Cell 2007, 27, 992-1004.
95. Liu, L.; Wang, Y.; Fan, H.; Zhao, X.; Liu, D.; Hu, Y.; Kidd, A.R., III; Bao, J.; Hou, Y. MicroRNA-181a regulates local immune balance by inhibiting proliferation and immunosuppressive properties of mesenchymal stem cells. Stem cells 2012, 30, 1756-1770.
96. Lynch, J.; Fay, J.; Meehan, M.; Bryan, K.; Watters, K.M.; Murphy, D.M.; Stallings, R.L. MiRNA-335 suppresses neuroblastoma cell invasiveness by direct targeting of multiple genes from the non-canonical TGF-β signalling pathway. Carcinogenesis 2012, 33, 976-985.
97. Zheng, B.; Liang, L.; Wang, C.; Huang, S.; Cao, X.; Zha, R.; Liu, L.; Jia, D.; Tian, Q.; Wu, J.; et al. MicroRNA-148a suppresses tumor cell invasion and metastasis by downregulating ROCK1 in gastric cancer. Clin. Cancer Res. 2011, 17, 7574-7583.
98. Sharma, A.; Kumar, M.; Aich, J.; Hariharan, M.; Brahmachari, S.K.; Agrawal, A.; Ghosh, B. Posttranscriptional regulation of interleukin-10 expression by hsa-miR-106a. Proc. Natl. Acad. Sci. USA 2009, 106, 5761-5766.
99. Yang, G.; Zhang, R.; Chen, X.; Mu, Y.; Ai, J.; Shi, C.; Liu, Y.; Shi, C.; Sun, L.; Rainov, N.G.; et al. MiR-106a inhibits glioma cell growth by targeting E2F1 independent of p53 status. J. Mol. Med. 2011, 89, 1037-1050.
100. Wang, Y.; Lu, Y.; Toh, S.T.; Sung, W.K.; Tan, P.; Chow, P.; Chung, A.Y.; Jooi, L.L.; Lee, C.G. Lethal-7 is down-regulated by the hepatitis B virus x protein and targets signal transducer and activator of transcription 3. J. Hepatol. 2010, 53, 57-66.
101. Zhang, M.; Liu, Q.; Mi, S.; Liang, X.; Zhang, Z.; Su, X.; Liu, J.; Chen, Y.; Wang, M.; Zhang, Y.; et al. Both miR-17-5p and miR-20a alleviate suppressive potential of myeloid-derived suppressor cells by modulating STAT3 expression. J. Immunol. 2011, 186, 4716-4724.
102. Liu, S.; Patel, S.H.; Ginestier, C.; Ibarra, I.; Martin-Trevino, R.; Bai, S.; McDermott, S.P.; Shang, L.; Ke, J.; Ou, S.J.; et al. MicroRNA93 regulates proliferation and differentiation of normal and malignant breast stem cells. PLoS Genet. 2012, 8, e1002751.
103. Berx, G.; van Roy, F. Involvement of members of the cadherin superfamily in cancer. CSH Perspect. Biol. 2009, 1, a003129.
104. Cavallaro, U.; Christofori, G. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat. Rev. Cancer 2004, 4, 118-132.
105. Micalizzi, D.S.; Farabaugh, S.M.; Ford, H.L. Epithelial-mesenchymal transition in cancer: Parallels between normal development and tumor progression. J. Mammary Gland Biol. Neopl. 2010, 15, 117-134.
106. Kerrigan, J.J.; Mansell, J.P.; Sandy, J.R. Matrix turnover. J. Orthodont. 2000, 27, 227-233.
107. Sennino, B.; Ishiguro-Oonuma, T.; Wei, Y.; Naylor, R.M.; Williamson, C.W.; Bhagwandin, V.; Tabruyn, S.P.; You, W.K.; Chapman, H.A.; Christensen, J.G.; et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov. 2012, 2, 270-287.
108. Belton, A.; Gabrovsky, A.; Bae, Y.K.; Reeves, R.; Iacobuzio-Donahue, C.; Huso, D.L.; Resar, L.M. HMGA1 induces intestinal polyposis in transgenic mice and drives tumor progression and stem cell properties in colon cancer cells. PLoS One 2012, 7, e30034.
109. Choi, J.; Choi, K.; Benveniste, E.N.; Rho, S.B.; Hong, Y.S.; Lee, J.H.; Kim, J.; Park, K. Bcl-2 promotes invasion and lung metastasis by inducing matrix metalloproteinase-2. Cancer Res. 2005, 65, 5554-5560.
110. Zhang, Y.; Zhang, M.; Dong, H.; Yong, S.; Li, X.; Olashaw, N.; Kruk, P.A.; Cheng, J.Q.; Bai, W.; Chen, J.; et al. Deacetylation of cortactin by SIRT1 promotes cell migration. Oncogene 2009, 28, 445-460.
111. Moon, A.; Kim, M.S.; Kim, T.G.; Kim, S.H.; Kim, H.E.; Chen, Y.Q.; Kim, H.R. H-ras, but not N-ras, induces an invasive phenotype in human breast epithelial cells: A role for MMP-2 in the H-ras-induced invasive phenotype. Int. Cancer J. 2000, 85, 176-181.
112. Meng, Y.; Lu, Z.; Yu, S.; Zhang, Q.; Ma, Y.; Chen, J. Ezrin promotes invasion and metastasis of pancreatic cancer cells. J. Transl. Med. 2010, 8, 61.
113. Campbell, P.M.; Groehler, A.L.; Lee, K.M.; Ouellette, M.M.; Khazak, V.; Der, C.J. K-Ras promotes growth transformation and invasion of immortalized human pancreatic cells by Raf and phosphatidylinositol 3-kinase signaling. Cancer Res. 2007, 67, 2098-2106.
114. Singh, A.P.; Chaturvedi, P.; Batra, S.K. Emerging roles of MUC4 in cancer: A novel target for diagnosis and therapy. Cancer Res. 2007, 67, 433-436.
115. Yoon, S.O.; Shin, S.; Mercurio, A.M. Ras stimulation of E2F activity and a consequent E2F regulation of integrin alpha6beta4 promote the invasion of breast carcinoma cells. Cancer Res. 2006, 66, 6288-6295.
116. Mahoney, M.G.; Simpson, A.; Jost, M.; Noe, M.; Kari, C.; Pepe, D.; Choi, Y.W.; Uitto, J.; Rodeck, U. Metastasis-associated protein (MTA)1 enhances migration, invasion and anchorage-independent survival of immortalized human keratinocytes. Oncogene 2002, 21, 2161-2170.
117. Liu, S.J.; Kumar, S.M.; Lu, H.Z.; Liu, A.H.; Yang, R.F.; Pushparajan, A.; Guo, W.; Xu, X.W. MicroRNA-9 up-regulates E-cadherin through inhibition of NF-κB1-Snail1 pathway in melanoma. J. Pathol. 2012, 226, 61-72.
118. Schmalhofer, O.; Brabletz, S.; Brabletz, T. E-cadherin, beta-catenin and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev. 2009, 28, 151-166.
119. Yan, D.S.; Zhou, X.T.; Chen, X.Y.; Hu, D.N.; Da Dong, X.; Wang, J.; Lu, F.; Tu, L.L.; Qu, J. MicroRNA-34a inhibits uveal melanoma cell proliferation and migration through downregulation of c-Met. Invest. Ophth. Vis. Sci. 2009, 50, 1559-1565.
120. Lowery, A.J.; Miller, N.; Dwyer, R.M.; Kerin, M.J. Dysregulated miR-183 inhibits migration in breast cancer cells. BMC Cancer 2010, 10, 502.
121. Yu, S.N.; Lu, Z.H.; Liu, C.Z.; Meng, Y.X.; Ma, Y.H.; Zhao, W.G.; Liu, J.P.; Yu, J.; Chen, J. MiRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer Res. 2010, 70, 6015-6025.
122. Zhang, Q.Q.; Xu, H.; Huang, M.B.; Ma, L.M.; Huang, Q.J.; Yao, Q.; Zhou, H.; Qu, L.H. MicroRNA-195 plays a tumor-suppressor role in human glioblastoma cells by targeting signaling pathways involved in cellular proliferation and invasion. Neuro-Oncology 2012, 14, 278-287.
123. Zhou, H.J.; Xu, X.F.; Xun, Q.Y.; Yu, D.Q.; Ling, J.X.; Guo, F.F.; Yan, Y.H.; Shi, J.Y.; Hu, Y.L. MicroRNA-30c negatively regulates endometrial cancer cells by targeting metastasis-associated gene-1. Oncol. Rep. 2012, 27, 807-812.
124. Srivastava, S.K.; Bhardwaj, A.; Singh, S.; Arora, S.; Wang, B.; Grizzle, W.E.; Singh, A.P. MicroRNA-150 directly targets MUC4 and suppresses growth and malignant behavior of pancreatic cancer cells. Carcinogenesis 2011, 32, 1832-1839.
125. Kojima, S.; Chiyomaru, T.; Kawakami, K.; Yoshino, H.; Enokida, H.; Nohata, N.; Fuse, M.; Ichikawa, T.; Naya, Y.; Nakagawa, M.; Seki, N. Tumour suppressors miR-1 and miR-133a target the oncogenic function of purine nucleoside phosphorylase (PNP) in prostate cancer. Br. J. Cancer 2012, 106, 405-413.
126. Bader, A.G.; Brown, D.; Stoudemire, J.; Lammers, P. Developing therapeutic microRNAs for cancer. Gene Ther. 2011, 18, 1121-1126.
127. Bader, A.G.; Brown, D.; Winkler, M. The promise of microRNA replacement therapy. Cancer Res. 2010, 70, 7027-7030.
128. Di Martino, M.T.; Leone, E.; Amodio, N.; Foresta, U.; Lionetti, M.; Pitari, M.R.; Cantafio, M.E.G.; Gulla, A.; Conforti, F.; Morelli, E.; et al. Synthetic miR-34a mimics as a novel therapeutic agent for Multiple Myeloma: In vitro and in vivo evidence. Clin. Cancer Res. 2012, 18, 6260-6270.
129. Takahashi, M.; Cuatrecasas, M.; Balaguer, F.; Hur, K.; Toiyama, Y.; Castells, A.; Boland, C.R.; Goel, A. The clinical significance of miR-148a as a predictive biomarker in patients with advanced colorectal cancer. PLoS One 2012, 7, e46684.
130. Wahid, F.; Shehzad, A.; Khan, T.; Kim, Y.Y. MicroRNAs: Synthesis, mechanism, function and recent clinical trials. Biochim. Biophys. Acta 2010, 1803, 1231-1243.
131. Ryu, S.; Joshi, N.; McDonnell, K.; Woo, J.; Choi, H.; Gao, D.; McCombie, W.R.; Mittal, V. Discovery of novel human breast cancer microRNAs from deep sequencing data by analysis of pri-microRNA secondary structures. PLoS One 2011, 6, e16403.
132. Friedlander, M.R.; Mackowiak, S.D.; Li, N.; Chen, W.; Rajewsky, N. MiRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res. 2012, 40, 37-52.
133. Dhahbi, J.M.; Atamna, H.; Boffelli, D.; Magis, W.; Spindler, S.R.; Martin, D.I.K. Deep sequencing reveals novel microRNAs and regulation of microRNA expression during cell senescence. PLoS One 2011, 6, e20509.
134. Giovannetti, E.; Erozenci, A.; Smit, J.; Danesi, R.; Peters, G.J. Molecular mechanisms underlying the role of microRNAs (miRNAs) in anticancer drug resistance and implications for clinical practice. Crit. Rev. Oncol. Hematol. 2012, 81, 103-122.
135. Duttagupta, R.; Jiang, R.; Gollub, J.; Getts, R.C.; Jones, K.W. Impact of Cellular miRNAs on Circulating miRNA Biomarker Signatures. PLoS One 2011, 6, e20769.
136. Kosaka, N.; Iguchi, H.; Ochiya, T. Circulating microRNA in body fluid: A new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010, 101, 2087-2092.
137. Zhou, H.; Xiao, B.X.; Zhou, F.; Deng, H.X.; Zhang, X.J.; Lou, Y.R.; Gong, Z.H.; Du, C.G.; Guo, J.M. MiR-421 is a functional marker of circulating tumor cells in gastric cancer patients. Biomarkers 2012, 17, 104-110.
138. Wang, Y.; Zheng, D.L.; Tan, Q.L.; Wang, M.X.; Gu, L.Q. Nanopore-based detection of circulating microRNAs in lung cancer patients. Nat. Nanotechnol. 2011, 6, 668-674.
139. Brase, J.C.; Johannes, M.; Schlomm, T.; Falth, M.; Haese, A.; Steuber, T.; Beissbarth, T.; Kuner, R.; Sultmann, H. Circulating miRNAs are correlated with tumor progression in prostate cancer. Int. J. Cancer 2011, 128, 608-616.
140. ClinicalTrials. gov. Available online: http://www.clinicaltrials.gov/ (accessed on 28 December 2012).