MicroRNAs in cancer: Small molecules, big chances

Anti-Cancer Agents in Medicinal Chemistry

Volumn 12, Issue 7, 2012, Pages 733-743

  Abba, Mohammed ^a   Mudduluru, Giridhar ^a   Allgayer, Heike ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Antisense inhibition; Cancer; MicroRNAs; MiRNA mimics; MMPs; Replacement therapy; Therapeutic agents

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; EXPORTIN 5; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GELATINASE B; LET 7; MATRIX METALLOPROTEINASE 14; MICRORNA; MICRORNA 100; MICRORNA 101; MICRORNA 122; MICRORNA 141; MICRORNA 143 145; MICRORNA 145; MICRORNA 155; MICRORNA 199A 3P; MICRORNA 21; MICRORNA 210; MICRORNA 27A; MICRORNA 29; MICRORNA 29B; MICRORNA 31; MICRORNA 326; MICRORNA 340; MICRORNA 451; MICRORNA 99A B 3P; PROTEIN MDMX; RNA POLYMERASE II; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; BRAIN CANCER; BREAST CANCER; CANCER CELL; CANCER INHIBITION; CARCINOGENESIS; CELL DIFFERENTIATION; CELL METABOLISM; CELL PROLIFERATION; CHRONIC LYMPHATIC LEUKEMIA; COLON CANCER; COLORECTAL CANCER; GENE CONTROL; GENETIC TRANSCRIPTION; HEAD AND NECK CANCER; HEMATOLOGIC MALIGNANCY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIVER CANCER; LUNG CANCER; NEOPLASM; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PROSTATE CANCER; PROTEIN EXPRESSION; SOLID TUMOR; STATISTICAL SIGNIFICANCE; THYROID CANCER;

EID: 84866396585     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/187152012802650273     Document Type: Article

References (151)

1. Ruvkun, G. B. The tiny RNA world. Harvey Lect., 2003, 99, 1-21.
2. Ruvkun, G. Molecular biology. Glimpses of a tiny RNA world. Science, 2001, 294 (5543), 797-799.
3. Lee, Y.; Jeon, K.; Lee, J. T.; Kim, S.; Kim, V. N. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J., 2002, 21 (17), 4663-4670.
4. 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.
5. Han, J.; Lee, Y.; Yeom, K. H.; Kim, Y. K.; Jin, H.; Kim, V. N. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev., 2004, 18 (24), 3016-3027.
6. Yi, R.; Qin, Y.; Macara, I. G.; Cullen, B. R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev., 2003, 17 (24), 3011-3016.
7. Denli, A. M.; Tops, B. B.; Plasterk, R. H.; Ketting, R. F.; Hannon, G. J. Processing of primary microRNAs by the Microprocessor complex. Nature, 2004, 432 (7014), 231-235.
8. Bernstein, E.; Caudy, A. A.; Hammond, S. M.; Hannon, G. J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature, 2001, 409 (6818), 363-366.
9. Hutvagner, G.; Zamore, P. D. A microRNA in a multiple-turnover RNAi enzyme complex. Science, 2002, 297 (5589), 2056-2060.
10. Davis, E.; Caiment, F.; Tordoir, X.; Cavaille, J.; Ferguson-Smith, A.; Cockett, N.; Georges, M.; Charlier, C. RNAi-mediated allelic trans-interaction at the imprinted Rtl1/Peg11 locus. Curr. Biol., 2005, 15 (8), 743-749.
11. Yekta, S.; Shih, I. H.; Bartel, D. P. MicroRNA-directed cleavage of HOXB8 mRNA. Science, 2004, 304 (5670), 594-596.
12. Brennecke, J.; Stark, A.; Russell, R. B.; Cohen, S. M. Principles of microRNA-target recognition. PLoS. Biol., 2005, 3 (3), e85.
13. Grun, D.; Wang, Y. L.; Langenberger, D.; Gunsalus, K. C.; Rajewsky, N. microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS. Comput. Biol., 2005, 1 (1), e13.
14. Krek, A.; Grun, D.; Poy, M. N.; Wolf, R.; Rosenberg, L.; Epstein, E. J.; MacMenamin, P.; da, P., I; Gunsalus, K. C.; Stoffel, M.; Rajewsky, N. Combinatorial microRNA target predictions. Nat. Genet., 2005, 37 (5), 495-500.
15. Lewis, B. P.; Shih, I. H.; Jones-Rhoades, M. W.; Bartel, D. P.; Burge, C. B. Prediction of mammalian microRNA targets. Cell, 2003, 115 (7), 787-798.
16. Lewis, B. P.; Burge, C. B.; Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 2005, 120 (1), 15-20.
17. Rajewsky, N.; Socci, N. D. Computational identification of microRNA targets. Dev. Biol., 2004, 267 (2), 529-535.
18. Ruby, J. G.; Jan, C.; Player, C.; Axtell, M. J.; Lee, W.; Nusbaum, C.; Ge, H.; Bartel, D. P. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell, 2006, 127 (6), 1193-1207.
19. Haley, B.; Zamore, P. D. Kinetic analysis of the RNAi enzyme complex. Nat. Struct. Mol. Biol., 2004, 11 (7), 599-606.
20. Aleman, L. M.; Doench, J.; Sharp, P. A. Comparison of siRNAinduced off-target RNA and protein effects. RNA, 2007, 13 (3), 385-395.
21. Doench, J. G.; Sharp, P. A. Specificity of microRNA target selection in translational repression. Genes Dev., 2004, 18 (5), 504-511.
22. Lewis, B. P.; Shih, I. H.; Jones-Rhoades, M. W.; Bartel, D. P.; Burge, C. B. Prediction of mammalian microRNA targets. Cell, 2003, 115 (7), 787-798.
23. Griffiths-Jones, S. miRBase: the microRNA sequence database. Methods Mol. Biol., 2006, 342, 129-138.
24. Griffiths-Jones, S.; Saini, H. K.; van, D. S.; Enright, A. J. miRBase: tools for microRNA genomics. Nucleic Acids Res., 2008, 36 (Database issue), D154-D158.
25. Garzon, R.; Calin, G. A.; Croce, C. M. MicroRNAs in Cancer. Annu. Rev. Med., 2009, 60, 167-179.
26. Lee, Y. S.; Dutta, A. MicroRNAs in cancer. Annu. Rev. Pathol., 2009, 4, 199-227.
27. Croce, C. M. Oncogenes and cancer. N. Engl. J. Med., 2008, 358 (5), 502-511.
28. Meltzer, P. S. Cancer genomics: small RNAs with big impacts. Nature, 2005, 435 (7043), 745-746.
29. Calin, G. A.; Sevignani, C.; Dumitru, C. D.; Hyslop, T.; Noch, E.; Yendamuri, S.; Shimizu, M.; Rattan, S.; Bullrich, F.; Negrini, M.; Croce, C. M. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. USA, 2004, 101 (9), 2999-3004.
30. Ceppi, P.; Mudduluru, G.; Kumarswamy, R.; Rapa, I.; Scagliotti, G. V.; Papotti, M.; Allgayer, H. Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol. Cancer Res., 2010, 8 (9), 1207-1216.
31. Erson, A. E.; Petty, E. M. MicroRNAs in development and disease. Clin. Genet., 2008, 74 (4), 296-306.
32. Eulalio, A.; Huntzinger, E.; Nishihara, T.; Rehwinkel, J.; Fauser, M.; Izaurralde, E. Deadenylation is a widespread effect of miRNA regulation. RNA, 2009, 15 (1), 21-32.
33. Lundstrom, K. Micro-RNA in Disease and Gene Therapy. Curr. Drug Discov. Technol., 2011, 8 (2), 76-86.
34. Yu, F.; Yao, H.; Zhu, P.; Zhang, X.; Pan, Q.; Gong, C.; Huang, Y.; Hu, X.; Su, F.; Lieberman, J.; Song, E. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell, 2007, 131 (6), 1109-1123.
35. Zhao, Y.; Srivastava, D. A developmental view of microRNA function. Trends Biochem. Sci., 2007, 32 (4), 189-197.
36. Asangani, I. A.; Rasheed, S. A.; Nikolova, D. A.; Leupold, J. H.; Colburn, N. H.; Post, S.; Allgayer, H. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene, 2008, 27 (15), 2128-2136.
37. Krichevsky, A. M.; Gabriely, G. miR-21: a small multi-faceted RNA. J. Cell Mol. Med., 2009, 13 (1), 39-53.
38. Meng, F.; Henson, R.; Lang, M.; Wehbe, H.; Maheshwari, S.; Mendell, J. T.; Jiang, J.; Schmittgen, T. D.; Patel, T. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology, 2006, 130 (7), 2113-2129.
39. Selcuklu, S. D.; Donoghue, M. T.; Spillane, C. miR-21 as a key regulator of oncogenic processes. Biochem. Soc. Trans., 2009, 37 (Pt 4), 918-925.
40. Zhu, S.; Si, M. L.; Wu, H.; Mo, Y. Y. MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J. Biol. Chem., 2007, 282 (19), 14328-14336.
41. nd Annual Meeting Education Book, 73. 2011.
42. Gallardo, E.; Navarro, A.; Vinolas, N.; Marrades, R. M.; Diaz, T.; Gel, B.; Quera, A.; Bandres, E.; Garcia-Foncillas, J.; Ramirez, J.; Monzo, M. miR-34a as a prognostic marker of relapse in surgically resected non-small-cell lung cancer. Carcinogenesis, 2009, 30 (11), 1903-1909.
43. Li, J.; Huang, H.; Sun, L.; Yang, M.; Pan, C.; Chen, W.; Wu, D.; Lin, Z.; Zeng, C.; Yao, Y.; Zhang, P.; Song, E. MiR-21 indicates poor prognosis in tongue squamous cell carcinomas as an apoptosis inhibitor. Clin. Cancer Res., 2009, 15 (12), 3998-4008.
44. Li, W.; Xie, L.; He, X.; Li, J.; Tu, K.; Wei, L.; Wu, J.; Guo, Y.; Ma, X.; Zhang, P.; Pan, Z.; Hu, X.; Zhao, Y.; Xie, H.; Jiang, G.; Chen, T.; Wang, J.; Zheng, S.; Cheng, J.; Wan, D.; Yang, S.; Li, Y.; Gu, J. Diagnostic and prognostic implications of microRNAs in human hepatocellular carcinoma. Int. J. Cancer, 2008, 123 (7), 1616-1622.
45. Markou, A.; Tsaroucha, E. G.; Kaklamanis, L.; Fotinou, M.; Georgoulias, V.; Lianidou, E. S. Prognostic value of mature microRNA-21 and microRNA-205 overexpression in non-small cell lung cancer by quantitative real-time RT-PCR. Clin. Chem., 2008, 54 (10), 1696-1704.
46. Mudduluru, G.; Ceppi, P.; Kumarswamy, R.; Scagliotti, G. V.; Papotti, M.; Allgayer, H. Regulation of Axl receptor tyrosine kinase expression by miR-34a and miR-199a/b in solid cancer. Oncogene, 2011, 30 (25), 2888-2899.
47. Wang, Z.; Chen, Z.; Gao, Y.; Li, N.; Li, B.; Tan, F.; Tan, X.; Lu, N.; Sun, Y.; Sun, J.; Sun, N.; He, J. DNA hypermethylation of microRNA-34b/c has prognostic value for stage non-small cell lung cancer. Cancer Biol. Ther., 2011, 11 (5), 490-496.
48. Lawrie, C. H.; Gal, S.; Dunlop, H. M.; Pushkaran, B.; Liggins, A. P.; Pulford, K.; Banham, A. H.; Pezzella, F.; Boultwood, J.; Wainscoat, J. S.; Hatton, C. S.; Harris, A. L. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br. J. Haematol., 2008, 141 (5), 672-675.
49. Mitchell, P. S.; Parkin, R. K.; Kroh, E. M.; Fritz, B. R.; Wyman, S. K.; Pogosova-Agadjanyan, E. L.; Peterson, A.; Noteboom, J.; O'Briant, K. C.; Allen, A.; Lin, D. W.; Urban, N.; Drescher, C. W.; Knudsen, B. S.; Stirewalt, D. L.; Gentleman, R.; Vessella, R. L.; Nelson, P. S.; Martin, D. B.; Tewari, M. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. USA, 2008, 105 (30), 10513-10518.
50. Rabinowits, G.; Gercel-Taylor, C.; Day, J. M.; Taylor, D. D.; Kloecker, G. H. Exosomal microRNA: a diagnostic marker for lung cancer. Clin. Lung Cancer, 2009, 10 (1), 42-46.
51. Taylor, D. D.; Gercel-Taylor, C. MicroRNA signatures of tumorderived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol., 2008, 110 (1), 13-21.
52. Keller, A.; Leidinger, P.; Borries, A.; Wendschlag, A.; Wucherpfennig, F.; Scheffler, M.; Huwer, H.; Lenhof, H. P.; Meese, E. miRNAs in lung cancer - studying complex fingerprints in patient's blood cells by microarray experiments. BMC. Cancer, 2009, 9, 353.
53. Yan, W.; Zhang, W.; Sun, L.; Liu, Y.; You, G.; Wang, Y.; Kang, C.; You, Y.; Jiang, T. Identification of MMP-9 specific microRNA expression profile as potential targets of anti-invasion therapy in glioblastoma multiforme. Brain Res., 2011, 1411, 108-115.
54. Sun, L.; Yan, W.; Wang, Y.; Sun, G.; Luo, H.; Zhang, J.; Wang, X.; You, Y.; Yang, Z.; Liu, N. MicroRNA-10b induces glioma cell invasion by modulating MMP-14 and uPAR expression via HOXD10. Brain Res., 2011, 1389, 9-18.
55. Fang, J. H.; Zhou, H. C.; Zeng, C.; Yang, J.; Liu, Y.; Huang, X.; Zhang, J. P.; Guan, X. Y.; Zhuang, S. M. MicroRNA-29b suppresses tumor angiogenesis, invasion and metastasis by regulating MMP-2 expression. Hepatology, 2011, 54 (5), 1729-1740.
56. Steele, R.; Mott, J. L.; Ray, R. B. MBP-1 upregulates miR-29b that represses Mcl-1, collagens, and matrix-metalloproteinase-2 in prostate cancer cells. Genes Cancer, 2010, 1 (4), 381-387.
57. Alpini, G.; Glaser, S. S.; Zhang, J. P.; Francis, H.; Han, Y.; Gong, J.; Stokes, A.; Francis, T.; Hughart, N.; Hubble, L.; Zhuang, S. M.; Meng, F. Regulation of placenta growth factor by microRNA-125b in hepatocellular cancer. J. Hepatol., 2011.
58. Wang, B.; Hsu, S. H.; Majumder, S.; Kutay, H.; Huang, W.; Jacob, S. T.; Ghoshal, K. TGFbeta-mediated upregulation of hepatic miR- 181b promotes hepatocarcinogenesis by targeting TIMP3. Oncogene, 2010, 29 (12), 1787-1797.
59. Gabriely, G.; Wurdinger, T.; Kesari, S.; Esau, C. C.; Burchard, J.; Linsley, P. S.; Krichevsky, A. M. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol. Cell Biol., 2008, 28 (17), 5369-5380.
60. 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 (13), 2842-2852.
61. Boutla, A.; Delidakis, C.; Tabler, M. Developmental defects by antisense-mediated inactivation of micro-RNAs 2 and 13 in Drosophila and the identification of putative target genes. Nucleic Acids Res., 2003, 31 (17), 4973-4980.
62. Davis, S.; Lollo, B.; Freier, S.; Esau, C. Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res., 2006, 34 (8), 2294-2304.
63. Elmen, J.; Lindow, M.; Schutz, S.; Lawrence, M.; Petri, A.; Obad, S.; Lindholm, M.; Hedtjarn, M.; Hansen, H. F.; Berger, U.; Gullans, S.; Kearney, P.; Sarnow, P.; Straarup, E. M.; Kauppinen, S. LNA-mediated microRNA silencing in non-human primates. Nature, 2008, 452 (7189), 896-899.
64. Esau, C.; Kang, X.; Peralta, E.; Hanson, E.; Marcusson, E. G.; Ravichandran, L. V.; Sun, Y.; Koo, S.; Perera, R. J.; Jain, R.; Dean, N. M.; Freier, S. M.; Bennett, C. F.; Lollo, B.; Griffey, R. MicroRNA-143 regulates adipocyte differentiation. J. Biol. Chem., 2004, 279 (50), 52361-52365.
65. Esau, C.; Davis, S.; Murray, S. F.; Yu, X. X.; Pandey, S. K.; Pear, M.; Watts, L.; Booten, S. L.; Graham, M.; McKay, R.; Subramaniam, A.; Propp, S.; Lollo, B. A.; Freier, S.; Bennett, C. F.; Bhanot, S.; Monia, B. P. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab., 2006, 3 (2), 87-98.
66. Hutvagner, G.; Simard, M. J.; Mello, C. C.; Zamore, P. D. Sequence-specific inhibition of small RNA function. PLoS. Biol., 2004, 2 (4), E98.
67. Krutzfeldt, J.; Rajewsky, N.; Braich, R.; Rajeev, K. G.; Tuschl, T.; Manoharan, M.; Stoffel, M. Silencing of microRNAs in vivo with 'antagomirs'. Nature, 2005, 438 (7068), 685-689.
68. Leaman, D.; Chen, P. Y.; Fak, J.; Yalcin, A.; Pearce, M.; Unnerstall, U.; Marks, D. S.; Sander, C.; Tuschl, T.; Gaul, U. Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell, 2005, 121 (7), 1097-1108.
69. Meister, G.; Landthaler, M.; Dorsett, Y.; Tuschl, T. Sequencespecific inhibition of microRNA- and siRNA-induced RNA silencing. RNA, 2004, 10 (3), 544-550.
70. Tsourkas, A.; Behlke, M. A.; Bao, G. Hybridization of 2'-O-methyl and 2'-deoxy molecular beacons to RNA and DNA targets. Nucleic Acids Res., 2003, 31 (6), 5168-5174.
71. Krutzfeldt, J.; Kuwajima, S.; Braich, R.; Rajeev, K. G.; Pena, J.; Tuschl, T.; Manoharan, M.; Stoffel, M. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res., 2007, 35 (9), 2885-2892.
72. Fabani, M. M.; Gait, M. J. miR-122 targeting with LNA/2'-Omethyl oligonucleotide mixmers, peptide nucleic acids (PNA), and PNA-peptide conjugates. RNA, 2008, 14 (2), 336-346.
73. Desjardins, J.; Mata, J.; Brown, T.; Graham, D.; Zon, G.; Iversen, P. Cholesteryl-conjugated phosphorothioate oligodeoxynucleotides modulate CYP2B1 expression in vivo. J. Drug Target, 1995, 2 (6), 477-485.
74. Letsinger, R. L.; Zhang, G. R.; Sun, D. K.; Ikeuchi, T.; Sarin, P. S. Cholesteryl-conjugated oligonucleotides: synthesis, properties, and activity as inhibitors of replication of human immunodeficiency virus in cell culture. Proc. Natl. Acad. Sci. USA, 1989, 86 (17), 6553-6556.
75. Soutschek, J.; Akinc, A.; Bramlage, B.; Charisse, K.; Constien, R.; Donoghue, M.; Elbashir, S.; Geick, A.; Hadwiger, P.; Harborth, J.; John, M.; Kesavan, V.; Lavine, G.; Pandey, R. K.; Racie, T.; Rajeev, K. G.; Rohl, I.; Toudjarska, I.; Wang, G.; Wuschko, S.; Bumcrot, D.; Koteliansky, V.; Limmer, S.; Manoharan, M.; Vornlocher, H. P. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature, 2004, 432 (7014), 173-178.
76. Ebert, M. S.; Neilson, J. R.; Sharp, P. A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods, 2007, 4 (9), 721-726.
77. Gentner, B.; Schira, G.; Giustacchini, A.; Amendola, M.; Brown, B. D.; Ponzoni, M.; Naldini, L. Stable knockdown of microRNA in vivo by lentiviral vectors. Nat. Methods, 2009, 6 (1), 63-66.
78. Bader, A. G.; Brown, D.; Winkler, M. The promise of microRNA replacement therapy. Cancer Res., 2010, 70 (18), 7027-7030.
79. Vincent T. DeVita Jr., T. S. L. S. A. R. DeVita, Hellman, and Rosenberg's Cancer: Principles & Practice of Oncology. [Eighth Edition]. 2011. Lippincott Williams & Wilkins.
80. Lu, J.; Getz, G.; Miska, E. A.; Alvarez-Saavedra, E.; Lamb, J.; Peck, D.; Sweet-Cordero, A.; Ebert, B. L.; Mak, R. H.; Ferrando, A. A.; Downing, J. R.; Jacks, T.; Horvitz, H. R.; Golub, T. R. MicroRNA expression profiles classify human cancers. Nature, 2005, 435 (7043), 834-838.
81. Esquela-Kerscher, A.; Slack, F. J. Oncomirs-microRNAs with a role in cancer. Nat. Rev. Cancer, 2006, 6 (4), 259-269.
82. Wang, Z. The guideline of the design and validation of MiRNA mimics. Methods Mol. Biol., 2011, 676, 211-223.
83. Henry, J. C.; Azevedo-Pouly, A. C.; Schmittgen, T. D. microRNA Replacement Therapy for Cancer. Pharm. Res., 2011.
84. Esquela-Kerscher, A.; Trang, P.; Wiggins, J. F.; Patrawala, L.; Cheng, A.; Ford, L.; Weidhaas, J. B.; Brown, D.; Bader, A. G.; Slack, F. J. The let-7 microRNA reduces tumor growth in mouse models of lung cancer. Cell Cycle, 2008, 7 (6), 759-764.
85. Kumar, M. S.; Erkeland, S. J.; Pester, R. E.; Chen, C. Y.; Ebert, M. S.; Sharp, P. A.; Jacks, T. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc. Natl. Acad. Sci. USA, 2008, 105 (10), 3903-3908.
86. Bonci, D.; Coppola, V.; Musumeci, M.; Addario, A.; Giuffrida, R.; Memeo, L.; D'Urso, L.; Pagliuca, A.; Biffoni, M.; Labbaye, C.; Bartucci, M.; Muto, G.; Peschle, C.; De, M. R. The miR-15a-miR- 16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat. Med., 2008, 14 (11), 1271-1277.
87. Kota, J.; Chivukula, R. R.; O'Donnell, K. A.; Wentzel, E. A.; Montgomery, C. L.; Hwang, H. W.; Chang, T. C.; Vivekanandan, P.; Torbenson, M.; Clark, K. R.; Mendell, J. R.; Mendell, J. T. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell, 2009, 137 (6), 1005-1017.
88. Johnson, S. M.; Grosshans, H.; Shingara, J.; Byrom, M.; Jarvis, R.; Cheng, A.; Labourier, E.; Reinert, K. L.; Brown, D.; Slack, F. J. RAS is regulated by the let-7 microRNA family. Cell, 2005, 120 (5), 635-647.
89. Gatt, M. E.; Zhao, J. J.; Ebert, M. S.; Zhang, Y.; Chu, Z.; Mani, M.; Gazit, R.; Carrasco, D. E.; Dutta-Simmons, J.; Adamia, S.; Minvielle, S.; Tai, Y. T.; Munshi, N. C.; Avet-Loiseau, H.; Anderson, K. C.; Carrasco, D. R. MicroRNAs 15a/16-1 function as tumor suppressor genes in multiple myeloma. Blood, 2010.
90. Lu, J.; He, M. L.; Wang, L.; Chen, Y.; Liu, X.; Dong, Q.; Chen, Y. C.; Peng, Y.; Yao, K. T.; Kung, H. F.; Li, X. P. MiR-26a inhibits cell growth and tumorigenesis of nasopharyngeal carcinoma through repression of EZH2. Cancer Res., 2011, 71 (1), 225-233.
91. Bommer, G. T.; Gerin, I.; Feng, Y.; Kaczorowski, A. J.; Kuick, R.; Love, R. E.; Zhai, Y.; Giordano, T. J.; Qin, Z. S.; Moore, B. B.; MacDougald, O. A.; Cho, K. R.; Fearon, E. R. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol., 2007, 17 (15), 1298-1307.
92. 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.; Arking, D. E.; Beer, M. A.; Maitra, A.; Mendell, J. T. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell, 2007, 26 (5), 745-752.
93. He, L.; He, X.; Lim, L. P.; de, S. E.; Xuan, Z.; Liang, Y.; Xue, W.; Zender, L.; Magnus, J.; Ridzon, D.; Jackson, A. L.; Linsley, P. S.; Chen, C.; Lowe, S. W.; Cleary, M. A.; Hannon, G. J. A microRNA component of the p53 tumour suppressor network. Nature, 2007, 447 (7148), 1130-1134.
94. Hermeking, H. The miR-34 family in cancer and apoptosis. Cell Death. Differ., 2010, 17 (2), 193-199.
95. Liu, C.; Kelnar, K.; Liu, B.; Chen, X.; Calhoun-Davis, T.; Li, H.; Patrawala, L.; Yan, H.; Jeter, C.; Honorio, S.; Wiggins, J. F.; Bader, A. G.; Fagin, R.; Brown, D.; Tang, D. G. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat. Med., 2011, 17 (2), 211-215.
96. Raver-Shapira, N.; Marciano, E.; Meiri, E.; Spector, Y.; Rosenfeld, N.; Moskovits, N.; Bentwich, Z.; Oren, M. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell, 2007, 26 (5), 731-743.
97. Wiggins, J. F.; Ruffino, L.; Kelnar, K.; Omotola, M.; Patrawala, L.; Brown, D.; Bader, A. G. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res., 2010, 70 (14), 5923-5930.
98. Yamakuchi, M.; Ferlito, M.; Lowenstein, C. J. miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl. Acad. Sci. USA, 2008, 105 (36), 13421-13426.
99. Trang, P.; Medina, P. P.; Wiggins, J. F.; Ruffino, L.; Kelnar, K.; Omotola, M.; Homer, R.; Brown, D.; Bader, A. G.; Weidhaas, J. B.; Slack, F. J. Regression of murine lung tumors by the let-7 microRNA. Oncogene, 2010, 29 (11), 1580-1587.
100. 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.
101. Mackiewicz, M.; Huppi, K.; Pitt, J. J.; Dorsey, T. H.; Ambs, S.; Caplen, N. J. Identification of the receptor tyrosine kinase AXL in breast cancer as a target for the human miR-34a microRNA. Breast Cancer Res. Treat, 2011.
102. Ji, Q.; Hao, X.; Zhang, M.; Tang, W.; Yang, M.; Li, L.; Xiang, D.; Desano, J. T.; Bommer, G. T.; Fan, D.; Fearon, E. R.; Lawrence, T. S.; Xu, L. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS. One, 2009, 4 (8), e6816.
103. Bai, S.; Nasser, M. W.; Wang, B.; Hsu, S. H.; Datta, J.; Kutay, H.; Yadav, A.; Nuovo, G.; Kumar, P.; Ghoshal, K. MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J. Biol. Chem., 2009, 284 (46), 32015-32027.
104. Silber, J.; Lim, D. A.; Petritsch, C.; Persson, A. I.; Maunakea, A. K.; Yu, M.; Vandenberg, S. R.; Ginzinger, D. G.; James, C. D.; Costello, J. F.; Bergers, G.; Weiss, W. A.; Alvarez-Buylla, A.; Hodgson, J. G. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC. Med., 2008, 6, 14.
105. Akao, Y.; Nakagawa, Y.; Hirata, I.; Iio, A.; Itoh, T.; Kojima, K.; Nakashima, R.; Kitade, Y.; Naoe, T. Role of anti-oncomirs miR- 143 and -145 in human colorectal tumors. Cancer Gene Ther., 2010, 17 (6), 398-408.
106. 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.
107. Greenberger, L. M.; Horak, I. D.; Filpula, D.; Sapra, P.; Westergaard, M.; Frydenlund, H. F.; Albaek, C.; Schroder, H.; Orum, H. A RNA antagonist of hypoxia-inducible factor-1alpha, EZN-2968, inhibits tumor cell growth. Mol. Cancer Ther., 2008, 7 (11), 3598-3608.
108. Sapra, P.; Wang, M.; Bandaru, R.; Zhao, H.; Greenberger, L. M.; Horak, I. D. Down-modulation of survivin expression and inhibition of tumor growth in vivo by EZN-3042, a locked nucleic acid antisense oligonucleotide. Nucleosides NucleotidesNucleic Acids, 2010, 29 (2), 97-112.
109. Clevers, H. The cancer stem cell: premises, promises and challenges. Nat. Med., 2011, 17 (3), 313-319.
110. Seiffert, S.; Debelak, H.; Hadwiger, P.; Jahn-Hofmann, K.; Roehl, I.; Vornlocher, H. P.; Noll, B. Characterization of side reactions during the annealing of small interfering RNAs. Anal. Biochem., 2011, 414 (1), 47-57.
111. Corey, D. R. Chemical modification: the key to clinical application of RNA interference? J. Clin. Invest., 2007, 117 (12), 3615-3622.
112. Sazani, P.; Astriab-Fischer, A.; Kole, R. Effects of base modifications on antisense properties of 2'-O-methoxyethyl and PNA oligonucleotides. Antisense Nucleic Acid Drug Dev., 2003, 13 (3), 119-128.
113. Baek, M. S.; Yu, R. Z.; Gaus, H.; Grundy, J. S.; Geary, R. S. In vitro metabolic stabilities and metabolism of 2'-O-(methoxyethyl) partially modified phosphorothioate antisense oligonucleotides in preincubated rat or human whole liver homogenates. Oligonucleotides, 2010, 20 (6), 309-316.
114. Allerson, C. R.; Sioufi, N.; Jarres, R.; Prakash, T. P.; Naik, N.; Berdeja, A.; Wanders, L.; Griffey, R. H.; Swayze, E. E.; Bhat, B. Fully 2'-modified oligonucleotide duplexes with improved in vitro potency and stability compared to unmodified small interfering RNA. J. Med. Chem., 2005, 48 (4), 901-904.
115. Kawasaki, A. M.; Casper, M. D.; Freier, S. M.; Lesnik, E. A.; Zounes, M. C.; Cummins, L. L.; Gonzalez, C.; Cook, P. D. Uniformly modified 2'-deoxy-2'-fluoro phosphorothioate oligonucleotides as nuclease-resistant antisense compounds with high affinity and specificity for RNA targets. J. Med. Chem., 1993, 36 (7), 831-841.
116. Schultz, R. G.; Gryaznov, S. M. Oligo-2'-fluoro-2'-deoxynucleotide N3'-->P5' phosphoramidates: synthesis and properties. Nucleic Acids Res., 1996, 24 (15), 2966-2973.
117. Dowler, T.; Bergeron, D.; Tedeschi, A. L.; Paquet, L.; Ferrari, N.; Damha, M. J. Improvements in siRNA properties mediated by 2'- deoxy-2'-fluoro-beta-D-arabinonucleic acid (FANA). Nucleic Acids Res., 2006, 34 (6), 1669-1675.
118. Watts, J. K.; Choubdar, N.; Sadalapure, K.; Robert, F.; Wahba, A. S.; Pelletier, J.; Pinto, B. M.; Damha, M. J. 2'-fluoro-4'-thioarabinomodified oligonucleotides: conformational switches linked to siRNA activity. Nucleic Acids Res., 2007, 35 (5), 1441-1451.
119. Elmen, J.; Thonberg, H.; Ljungberg, K.; Frieden, M.; Westergaard, M.; Xu, Y.; Wahren, B.; Liang, Z.; Orum, H.; Koch, T.; Wahlestedt, C. Locked nucleic acid (LNA) mediated improvements in siRNA stability and functionality. Nucleic Acids Res., 2005, 33 (1), 439-447.
120. Laursen, M. B.; Pakula, M. M.; Gao, S.; Fluiter, K.; Mook, O. R.; Baas, F.; Langklaer, N.; Wengel, S. L.; Wengel, J.; Kjems, J.; Bramsen, J. B. Utilization of unlocked nucleic acid (UNA) to enhance siRNA performance in vitro and in vivo. Mol. Biosyst., 2010, 6 (5), 862-870.
121. Summerton, J. Morpholino antisense oligomers: the case for an RNase H-independent structural type. Biochim. Biophys. Acta, 1999, 1489 (1), 141-158.
122. Summerton, J. E. Morpholino, siRNA, and S-DNA compared: impact of structure and mechanism of action on off-target effects and sequence specificity. Curr. Top. Med. Chem., 2007, 7 (7), 651-660.
123. Yamamoto, T.; Nakatani, M.; Narukawa, K.; Obika, S. Antisense drug discovery and development. Future. Med. Chem., 2011, 3 (3), 339-365.
124. Berthold, P. R.; Shiraishi, T.; Nielsen, P. E. Cellular delivery and antisense effects of peptide nucleic acid conjugated to polyethyleneimine via disulfide linkers. Bioconjug. Chem., 2010, 21 (10), 1933-1938.
125. Kaihatsu, K.; Huffman, K. E.; Corey, D. R. Intracellular uptake and inhibition of gene expression by PNAs and PNA-peptide conjugates. Biochemistry, 2004, 43 (45), 14340-14347.
126. Nielsen, P. E. Gene targeting and expression modulation by peptide nucleic acids (PNA). Curr. Pharm. Des., 2010, 16 (28), 3118-3123.
127. Lan, F. F.; Wang, H.; Chen, Y. C.; Chan, C. Y.; Ng, S. S.; Li, K.; Xie, D.; He, M. L.; Lin, M. C.; Kung, H. F. Hsa-let-7g inhibits proliferation of hepatocellular carcinoma cells by downregulation of c-Myc and upregulation of p16(INK4A). Int. J. Cancer, 2011, 128 (2), 319-331.
128. Xiong, Y.; Fang, J. H.; Yun, J. P.; Yang, J.; Zhang, Y.; Jia, W. H.; Zhuang, S. M. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology, 2010, 51 (3), 836-845.
129. Su, H.; Yang, J. R.; Xu, T.; Huang, J.; Xu, L.; Yuan, Y.; Zhuang, S. M. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res., 2009, 69 (3), 1135-1142.
130. Henry, J. C.; Park, J. K.; Jiang, J.; Kim, J. H.; Nagorney, D. M.; Roberts, L. R.; Banerjee, S.; Schmittgen, T. D. miR-199a-3p targets CD44 and reduces proliferation of CD44 positive hepatocellular carcinoma cell lines. Biochem. Biophys. Res. Commun., 2010, 403 (1), 120-125.
131. Hou, J.; Lin, L.; Zhou, W.; Wang, Z.; Ding, G.; Dong, Q.; Qin, L.; Wu, X.; Zheng, Y.; Yang, Y.; Tian, W.; Zhang, Q.; Wang, C.; Zhang, Q.; Zhuang, S. M.; Zheng, L.; Liang, A.; Tao, W.; Cao, X. Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma. Cancer Cell, 2011, 19 (2), 232-243.
132. Trang, P.; Wiggins, J. F.; Daige, C. L.; Cho, C.; Omotola, M.; Brown, D.; Weidhaas, J. B.; Bader, A. G.; Slack, F. J. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol. Ther., 2011, 19 (6), 1116-1122.
133. Akao, Y.; Nakagawa, Y.; Naoe, T. let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol. Pharm. Bull., 2006, 29 (5), 903-906.
134. Kitade, Y.; Akao, Y. MicroRNAs and their therapeutic potential for human diseases: microRNAs, miR-143 and -145, function as antioncomirs and the application of chemically modified miR-143 as an anti-cancer drug. J. Pharmacol. Sci., 2010, 114 (3), 276-280.
135. Zhu, H.; Wu, H.; Liu, X.; Evans, B. R.; Medina, D. J.; Liu, C. G.; Yang, J. M. Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells. Biochem. Pharmacol. 2008, 76 (5), 582-588.
136. Liang, Z.; Wu, H.; Xia, J.; Li, Y.; Zhang, Y.; Huang, K.; Wagar, N.; Yoon, Y.; Cho, H. T.; Scala, S.; Shim, H. Involvement of miR- 326 in chemotherapy resistance of breast cancer through modulating expression of multidrug resistance-associated protein 1. Biochem. Pharmacol., 2010, 79 (6), 817-824.
137. Kovalchuk, O.; Filkowski, J.; Meservy, J.; Ilnytskyy, Y.; Tryndyak, V. P.; Chekhun, V. F.; Pogribny, I. P. Involvement of microRNA- 451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol. Cancer Ther., 2008, 7 (7), 2152-2159.
138. Noonan, E. J.; Place, R. F.; Pookot, D.; Basak, S.; Whitson, J. M.; Hirata, H.; Giardina, C.; Dahiya, R. miR-449a targets HDAC-1 and induces growth arrest in prostate cancer. Oncogene, 2009, 28 (14), 1714-1724.
139. Torrisani, J.; Bournet, B.; du Rieu, M. C.; Bouisson, M.; Souque, A.; Escourrou, J.; Buscail, L.; Cordelier, P. let-7 MicroRNA transfer in pancreatic cancer-derived cells inhibits in vitro cell proliferation but fails to alter tumor progression. Hum. Gene Ther., 2009, 20 (8), 831-844.
140. Wang, F.; Xue, X.; Wei, J.; An, Y.; Yao, J.; Cai, H.; Wu, J.; Dai, C.; Qian, Z.; Xu, Z.; Miao, Y. Hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations. Br. J. Cancer, 2010, 103 (4), 567-574.
141. Nan, Y.; Han, L.; Zhang, A.; Wang, G.; Jia, Z.; Yang, Y.; Yue, X.; Pu, P.; Zhong, Y.; Kang, C. MiRNA-451 plays a role as tumor suppressor in human glioma cells. Brain Res., 2010, 1359, 14-21.
142. Tsai, W. C.; Hsu, P. W.; Lai, T. C.; Chau, G. Y.; Lin, C. W.; Chen, C. M.; Lin, C. D.; Liao, Y. L.; Wang, J. L.; Chau, Y. P.; Hsu, M. T.; Hsiao, M.; Huang, H. D.; Tsou, A. P. MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology, 2009, 49 (5), 1571-1582.
143. Ji, J.; Shi, J.; Budhu, A.; Yu, Z.; Forgues, M.; Roessler, S.; Ambs, S.; Chen, Y.; Meltzer, P. S.; Croce, C. M.; Qin, L. X.; Man, K.; Lo, C. M.; Lee, J.; Ng, I. O.; Fan, J.; Tang, Z. Y.; Sun, H. C.; Wang, X. W. MicroRNA expression, survival, and response to interferon in liver cancer. N. Engl. J. Med., 2009, 361 (15), 1437-1447.
144. Sun, Y.; Bai, Y.; Zhang, F.; Wang, Y.; Guo, Y.; Guo, L. miR-126 inhibits non-small cell lung cancer cells proliferation by targeting EGFL7. Biochem. Biophys. Res. Commun., 2010, 391 (3), 1483-1489.
145. Chen, Z.; Zeng, H.; Guo, Y.; Liu, P.; Pan, H.; Deng, A.; Hu, J. miRNA-145 inhibits non-small cell lung cancer cell proliferation by targeting c-Myc. J. Exp. Clin. Cancer Res., 2010, 29, 151.
146. Bian, H. B.; Pan, X.; Yang, J. S.; Wang, Z. X.; De, W. Upregulation of microRNA-451 increases cisplatin sensitivity of non-small cell lung cancer cell line (A549). J. Exp. Clin. Cancer Res., 2011, 30, 20.
147. Sachdeva, M.; Zhu, S.; Wu, F.; Wu, H.; Walia, V.; Kumar, S.; Elble, R.; Watabe, K.; Mo, Y. Y. p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc. Natl. Acad. Sci. USA, 2009, 106 (9), 3207-3212.
148. Zhang, X.; Ladd, A.; Dragoescu, E.; Budd, W. T.; Ware, J. L.; Zehner, Z. E. MicroRNA-17-3p is a prostate tumor suppressor in vitro and in vivo, and is decreased in high grade prostate tumors analyzed by laser capture microdissection. Clin. Exp. Metastasis, 2009, 26 (8), 965-979.
149. Dong, Q.; Meng, P.; Wang, T.; Qin, W.; Qin, W.; Wang, F.; Yuan, J.; Chen, Z.; Yang, A.; Wang, H. MicroRNA let-7a inhibits proliferation of human prostate cancer cells in vitro and in vivo by targeting E2F2 and CCND2. PLoS. One, 2010, 5 (4), e10147.
150. Yu, S.; Lu, Z.; Liu, C.; Meng, Y.; Ma, Y.; Zhao, W.; Liu, J.; Yu, J.; Chen, J. miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer Res., 2010, 70 (14), 6015-6025.
151. Godlewski, J.; Nowicki, M. O.; Bronisz, A.; Williams, S.; Otsuki, A.; Nuovo, G.; Raychaudhury, A.; Newton, H. B.; Chiocca, E. A.; Lawler, S. Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and selfrenewal. Cancer Res., 2008, 68 (22), 9125-9130.