Developing microRNA therapeutics: Approaching the unique complexities

Nucleic Acid Therapeutics

Volumn 22, Issue 4, 2012, Pages 213-225

  Jackson, Aimee L ^a   Levin, Arthur A ^b  

^a Jackson BioConsulting   (United States)

^b Levin BioSciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LETHAL 7; MICRORNA; MICRORNA 10B; MICRORNA 375; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTISENSE THERAPY; ARTICLE; BIOMIMETICS; CAENORHABDITIS ELEGANS; DOSE RESPONSE; DRUG TARGETING; GENE CONTROL; GENE EXPRESSION; GENE LOSS; GENE REGULATORY NETWORK; HEPATITIS C; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROCESSING; VIRUS LOAD;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DISCOVERY; HUMANS; MICRORNAS; MOLECULAR MIMICRY; MOLECULAR TARGETED THERAPY; SPECIES SPECIFICITY;

EID: 84865434716     PISSN: 21593337     EISSN: None     Source Type: Journal    
DOI: 10.1089/nat.2012.0356     Document Type: Article

References (139)

1. ALI, S., AHMAD, A., ABOUKAMEEL, A., BAO, B., PADHYE, S., PHILIP, P.A., and SARKAR, F.H. (2012). Increased Ras GTPase activity is regulated by miRNAs that can be attenuated by CDF treatment in pancreatic cancer cells. Cancer Lett. 28, 173-178.
2. AVNIT-SAGI, T., KANTOROVICH, L., KREDO-RUSSO, S., HORNSTEIN, E., and WALKER, M.D. (2009). The promoter of the pri-miR-375 gene directs expression selectively to the endocrine pancreas. PloS One 4, e5033.
3. BADER, A.G., BROWN, D., STOUDEMIRE, J., and LAMMERS, P. (2011). Developing therapeutic microRNAs for cancer. Gene Ther. 18, 1121-1126.
4. BAEK, D., VILLEN, J., SHIN, C., CAMARGO, F.D., GYGI, S.P., and BARTEL, D.P. (2008). The impact of microRNAs on protein output. Nature 455, 64-71.
5. BARTEL, D.P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
6. BOURGUIGNON, L.Y., WONG, G., EARLE, C., KRUEGER, K., and SPEVAK, C.C. (2010). Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, microRNA-10b expression, and RhoA/RhoC up-regulation, leading to Rhokinase- associated cytoskeleton activation and breast tumor cell invasion. J. Biol. Chem. 285, 36721-36735.
7. BRACONI, C., KOGURE, T., VALERI, N., HUANG, N., NUOVO, G., COSTINEAN, S., NEGRINI, M., MIOTTO, E., CROCE, C.M., and PATEL, T. (2011). microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 30, 4750-4756.
8. BUECHNER, J., TOMTE, E., HAUG, B.H., HENRIKSEN, J.R., LOKKE, C., FLAEGSTAD, T., and EINVIK, C. (2011). Tumour-suppressor microRNAs let-7 and mir-101 target the proto-oncogene MYCN and inhibit cell proliferation in MYCN-amplified neuroblastoma. Br. J. Cancer 105, 296-303.
9. CAI, X., SCHAFER, A., LU, S., BILELLO, J.P., DESROSIERS, R.C., EDWARDS, R., RAAB-TRAUB, N., and CULLEN, B.R. (2006). Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2, e23.
10. CAMERON, J.E., FEWELL, C., YIN, Q., MCBRIDE, J., WANG, X., LIN, Z., and FLEMINGTON, E.K. (2008a). Epstein-Barr virus growth/latency III program alters cellular microRNA expression. Virology 382, 257-266.
11. CAMERON, J.E., YIN, Q., FEWELL, C., LACEY, M., MCBRIDE, J., WANG, X., LIN, Z., SCHAEFER, B.C., and FLEMINGTON, E.K. (2008b). Epstein-Barr virus latent membrane protein 1 induces cellular MicroRNA miR-146a, a modulator of lymphocyte signaling pathways. J. Virol. 82, 1946-1958. (Pubitemid 351206940)
12. CARTHEW, R.W., and SONTHEIMER, E.J. (2009). Origins and Mechanisms of miRNAs and siRNAs. Cell 136, 642-655.
13. CHAI, G., LIU, N., MA, J., LI, H., OBLINGER, J.L., PRAHALAD, A.K., GONG, M., CHANG, L.S., WALLACE, M., MUIR, D., et al. (2010). MicroRNA-10b regulates tumorigenesis in neurofibromatosis type 1. Cancer Sci. 101, 1997-2004.
14. CHEN, K., and RAJEWSKY, N. (2006a). Deep conservation of microRNA-target relationships and 3¢UTR motifs in vertebrates, flies, and nematodes. Cold Spring Harb. Symp. Quant. Biol.71, 149-156.
15. CHEN, K., and RAJEWSKY, N. (2006b). Natural selection on human microRNA binding sites inferred from SNP data. Nat. Genet. 38, 1452-1456. (Pubitemid 44837570)
16. CHI, S.W., HANNON, G.J., and DARNELL, R.B. (2012). An alternative mode of microRNA target recognition. Nat. Struct. Mol. Biol. 19, 321-327.
17. CHI, S.W., ZANG, J.B., MELE, A. and DARNELL, R.B. (2009). Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460, 479-486.
18. CROOKE, S.T. (2008). Antisense Drug Technology: Principles, Strategies, and Applications, 2nd ed. (CRC Press, Boca Raton, FL).
19. DE SOUZA ROCHA SIMONINI, P., BREILING, A., GUPTA, N., MALEKPOUR, M., YOUNS, M., OMRANIPOUR, R., MALEKPOUR, F., VOLINIA, S., CROCE, C.M., NAJMABADI, H., et al. (2010). Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor alpha in breast cancer cells. Cancer Res. 70, 9175-9184.
20. DIDIANO, D., and HOBERT, O. (2006). Perfect seed pairing is not a generally reliable predictor for miRNA-target interactions. Nat. Struct. Mol. Biol.13, 849-851. (Pubitemid 44338780)
21. DING, L., XU, Y., ZHANG, W., DENG, Y., SI, M., DU, Y., YAO, H., LIU, X., KE, Y., SI, J., et al. (2010). MiR-375 frequently downregulated in gastric cancer inhibits cell proliferation by targeting JAK2. Cell Res. 20, 784-793.
22. DOENCH, J.G., and SHARP, P.A. (2004). Specificity of micro- RNA target selection in translational repression. Genes Dev. 18, 504-511. (Pubitemid 38372808)
23. DONG, Q., MENG, P., WANG, T., QIN, W., WANG, F., YUAN, J., CHEN, Z., YANG, A., and WANG, H. (2010). MicroRNA let-7a inhibits proliferation of human prostate cancer cells in vitro and in vivo by targeting E2F2 and CCND2. PloS One 5, e10147.
24. DUURSMA, A.M., KEDDE, M., SCHRIER, M., LE SAGE, C., and AGAMI, R. (2008). miR-148 targets human DNMT3b protein coding region. RNA 14, 872-877. (Pubitemid 351574909)
25. EASOW, G., TELEMAN, A.A., and COHEN, S.M. (2007). Isolation of microRNA targets by miRNP immunopurification. RNA 13, 1198-1204. (Pubitemid 47080465)
26. ELMEN, J., LINDOW, M., SCHUTZ, S., LAWRENCE, M., PETRI, A., OBAD, S., LINDHOLM, M., HEDTJARN, M., HANSEN, H.F., BERGER, U., et al. (2008). LNA-mediated microRNA silencing in non-human primates. Nature 452, 896-899. (Pubitemid 351550859)
27. ELMEN, J., LINDOW, M., SILAHTAROGLU, A., BAK, M., CHRISTENSEN, M., LIND-THOMSEN, A., HEDTJARN, M., HANSEN, J.B., HANSEN, H.F., STRAARUP, E.M., et al. (2008). Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res. 36, 1153-1162. (Pubitemid 351330933)
28. ESAU, C., DAVIS, S., MURRAY, S.F., YU, X.X., PANDEY, S.K., PEAR, M., WATTS, L., BOOTEN, S.L., GRAHAM, M., MCKAY, R., et al. (2006). miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 3, 87-98.
29. ESQUELA-KERSCHER, A., and SLACK, F.J. (2006). Oncomirs: microRNAs with a role in cancer. Nature reviews. Cancer 6, 259-269.
30. FEEDERLE, R., HAAR, J., BERNHARDT, K., LINNSTAEDT, S.D., BANNERT, H., LIPS, H., CULLEN, B.R., and DELECLUSE, H.J. (2011). The members of an Epstein-Barr virus microRNA cluster cooperate to transform B lymphocytes. J. Virol. 85, 9801-9810.
31. FORMAN, J.J., LEGESSE-MILLER, A., and COLLER, H.A. (2008). A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc. Natl. Acad. Sci. U. S. A. 105, 14879-14884.
32. FRIEDMAN, R.C., FARH, K.K., BURGE, C.B., and BARTEL, D.P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92-105.
33. FROST, R.J., and OLSON, E.N. (2011). Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc. Natl. Acad. Sci. U. S. A. 108, 21075-21080.
34. FU, T.Y., CHANG, C.C., LIN, C.T., LAI, C.H., PENG, S.Y., KO, Y.J., and TANG, P.C. (2011). Let-7b-mediated suppression of basigin expression and metastasis in mouse melanoma cells. Exper. Cell Res. 317, 445-451.
35. GABRIELY, G., YI, M., NARAYAN, R.S., NIERS, J.M., WURDINGER, T., IMITOLA, J., LIGON, K.L., KESARI, S., ESAU, C., STEPHENS, R.M., et al. (2011). Human glioma growth is controlled by microRNA-10b. Cancer Res. 71, 3563-3572.
36. GEARY, R.S., YU, R.Z., SIWKOWSKI, A., and LEVIN, A.A. (2008). Pharmacokinetic/pharmacodynamic properties of phsphorothioate 2¢-O-(2-methoxyethyl)-modified antisense oligonucleotides in animals and man. In: Antisense Drug Technology: Principles, Strategies, and Applications, 2nd ed. R. M. Crooke, ed. CRC Press, Boca Raton, FL) pp. 305-326.
37. GENG, L., ZHU, B., DAI, B.H., SUI, C.J., XU, F., KAN, T., SHEN, W.F., and YANG, J.M. (2011). A let-7/Fas double-negative feedback loop regulates human colon carcinoma cells sensitivity to Fas-related apoptosis. Biochem. Biophys. Res. Comm. 408, 494-499.
38. GEORGES, S.A., BIERY, M.C., KIM, S.Y., SCHELTER, J.M., GUO, J., CHANG, A.N., JACKSON, A.L., CARLETON, M.O., LINSLEY, P.S., CLEARY, M.A., et al. (2008). Coordinated regulation of cell cycle transcripts by p53-Inducible micro- RNAs, miR-192 and miR-215. Cancer Res. 68, 10105-10112.
39. GODSHALK, S.E., BHADURI-MCINTOSH, S., and SLACK, F.J. (2008). Epstein-Barr virus-mediated dysregulation of human microRNA expression. Cell Cycle 7, 3595-3600.
40. GRIMM, D., STREETZ, K.L., JOPLING, C.L., STORM, T.A., PANDEY, K., DAVIS, C.R., MARION, P., SALAZAR, F., and KAY, M.A. (2006). Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441, 537-541. (Pubitemid 44050158)
41. GRUN, D., WANG, Y.L., LANGENBERGER, D., GUNSALUS, K.C., and RAJEWSKY, N. (2005). microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput. Biol. 1, e13.
42. GUO, H., INGOLIA, N.T., WEISSMAN, J.S., and BARTEL, D.P. (2010). Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840.
43. HA, I., WIGHTMAN, B., and RUVKUN, G. (1996). A bulged lin- 4/lin-14 RNA duplex is sufficient for Caenorhabditis elegans lin-14 temporal gradient formation. Genes Dev. 10, 3041-3050. (Pubitemid 26412530)
44. HAFNER, M., LANDTHALER, M., BURGER, L., KHORSHID, M., HAUSSER, J., BERNINGER, P., ROTHBALLER, A., ASCANO, M., JR., JUNGKAMP, A.C., MUNSCHAUER, M., et al. (2010). Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129-141.
45. HE, X.X., CHANG, Y., MENG, F.Y., WANG, M.Y., XIE, Q.H., TANG, F., LI, P.Y., SONG, Y.H., and LIN, J.S. (2011). Micro- RNA-375 targets AEG-1 in hepatocellular carcinoma and suppresses liver cancer cell growth in vitro and in vivo. Oncogene 31, 3357-3369.
46. HENRY, S.P., KIM, T.-W., KRAMER-STICKLAND, K., ZANARDI, T.A., FEY, R.A., and LEVIN, A.A. (2008). Toxicologic properties of 2¢-O-methoxyethyl chimeric antisense inhibitors in animals and man. In: Antisense Drug Technology: Principles, Strategies, and Applications, 2nd ed. R. M. Crooke, ed. (CRC Press, Boca Raton, FL) pp. 327-363.
47. HILDEBRANDT-ERIKSEN, E., AARUP, V., PERSSON, R., HANSEN, H.F., MUNK, M., and OERUM, H. (2012). A locked nucleic acid oligonucleotide targeting microRNA 122 is well tolerated in cynomolgus monkeys. Nucl. Acid. Therap. 22, 152-161
48. HULLINGER, T.G., MONTGOMERY, R.L., SETO, A.G., DICKINSON, B.A., SEMUS, H.M., LYNCH, J.M., DALBY, C.M., ROBINSON, K., STACK, C., LATIMER, P.A., et al. (2012). Inhibition of miR-15 protects against cardiac ischemic injury. Circ. Res. 110, 71-81.
49. HUNTZINGER, E., and IZAURRALDE, E. (2011). Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99-110.
50. JACKSON, A., and LINSLEY, P.S. (2010). The therapeutic potential of microRNA modulation. Discov. Med. 9, 311-318.
51. JANSSEN, H.L.A., REESINK, H.W., LAWITZ, E.J., ZEUZEM, S., RODRIGUEZ-TORRES, M., CHEN, A., DAVIS, C., KING, B., LEVIN, A.A., and HODGES, M.R. (2011). Anti-viral proof of concept study of MiraVirsen, an oligonucleotide targeting miR-122, in treatment naïve patients with genotype 1 chronic HCV infection. AASLD abstract LB-6.
52. JIANG, J., LEE, E.J., and SCHMITTGEN, T.D. (2006). Increased expression of microRNA-155 in Epstein-Barr virus transformed lymphoblastoid cell lines. Genes Chromosomes Cancer 45, 103-106. (Pubitemid 46930866)
53. JOHN, M., CONSTIEN, R., AKINC, A., GOLDBERG, M., MOON, Y.A., SPRANGER, M., HADWIGER, P., SOUTSCHEK, J., VORNLOCHER, H.P., MANOHARAN, M., et al. (2007). Effective RNAi-mediated gene silencing without interruption of the endogenous microRNA pathway. Nature 449, 745-747. (Pubitemid 47552094)
54. KHAN, A.A., BETEL, D., MILLER, M.L., SANDER, C., LESLIE, C.S., and MARKS, D.S. (2009). Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs. Nat. Biotechnol. 27, 549-555.
55. KIM, K., LEE, H.C., PARK, J.L., KIM, M., KIM, S.Y., NOH, S.M., SONG, K.S., KIM, J.C., and KIM, Y.S. (2011). Epigenetic regulation of microRNA-10b and targeting of oncogenic MAPRE1 in gastric cancer. Epigenetics 6, 740-751.
56. KINOSHITA, T., NOHATA, N., YOSHINO, H., HANAZAWA, T., KIKKAWA, N., FUJIMURA, L., CHIYOMARU, T., KAWAKAMI, K., ENOKIDA, H., NAKAGAWA, M., et al. (2012). Tumor suppressive microRNA-375 regulates lactate dehydrogenase B in maxillary sinus squamous cell carcinoma. Int. J. Oncol. 40, 185-193.
57. KLOOSTERMAN, W.P., LAGENDIJK, A.K., KETTING, R.F., MOULTON, J.D., and PLASTERK, R.H. (2007). Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol.5, e203.
58. KONG, K.L., KWONG, D.L., CHAN, T.H., LAW, S.Y., CHEN, L., LI, Y., QIN, Y.R., and GUAN, X.Y. (2012). MicroRNA-375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin-like growth factor 1 receptor. Gut 61, 33-42.
59. KOZOMARA, A., and GRIFFITHS-JONES, S. (2011). miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, D152-157.
60. KREK, A., GRUN, D., POY, M.N., WOLF, R., ROSENBERG, L., EPSTEIN, E.J., MACMENAMIN, P., DA PIEDADE, I., GUNSALUS, K.C., STOFFEL, M., et al. (2005). Combinatorial microRNA target predictions. Nat. Genet. 37, 495-500. (Pubitemid 40617277)
61. KRUTZFELDT, J., RAJEWSKY, N., BRAICH, R., RAJEEV, K.G., TUSCHL, T., MANOHARAN, M., and STOFFEL, M. (2005). Silencing of microRNAs in vivo with 'antagomirs.' Nature 438, 685-689.
62. KUMAR, M.S., ERKELAND, S.J., PESTER, R.E., CHEN, C.Y., EBERT, M.S., SHARP, P.A., and JACKS, T. (2008). Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc. Natl. Acad. Sci. U. S. A. 105, 3903-3908. (Pubitemid 351723497)
63. LAGOS-QUINTANA, M., RAUHUT, R., LENDECKEL, W., and TUSCHL, T. (2001). Identification of novel genes coding for small expressed RNAs. Science 294, 853-858. (Pubitemid 33032103)
64. LAGOS-QUINTANA, M., RAUHUT, R., MEYER, J., BORKHARDT, A., and TUSCHL, T. (2003). New microRNAs from mouse and human. RNA 9, 175-179. (Pubitemid 36206285)
65. LAI, E.C. (2002). Micro RNAs are complementary to 3¢ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genetics 30, 363-364.
66. LALL, S., GRUN, D., KREK, A., CHEN, K., WANG, Y.L., DEWEY, C.N., SOOD, P., COLOMBO, T., BRAY, N., MACMENAMIN, P., et al. (2006). A genome-wide map of conserved microRNA targets in C. elegans. Curr. Biol. 16, 460-471. (Pubitemid 43343706)
67. LANFORD, R.E., HILDEBRANDT-ERIKSEN, E.S., PETRI, A., PERSSON, R., LINDOW, M., MUNK, M.E., KAUPPINEN, S., and ORUM, H. (2010). Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327, 198-201.
68. LAU, N.C., LIM, L.P., WEINSTEIN, E.G. and BARTEL, D.P. (2001). An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858-862. (Pubitemid 33032104)
69. LEE, C.T., RISOM, T., and STRAUSS, W.M. (2007). Evolutionary conservation of microRNA regulatory circuits: an examination of microRNA gene complexity and conserved microRNAtarget interactions through metazoan phylogeny. DNA Cell Biol. 26, 209-218. (Pubitemid 46776605)
70. LEE, R.C., and AMBROS, V. (2001). An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862-864. (Pubitemid 33032105)
71. LEE, Y.S., and DUTTA, A. (2007). The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 21, 1025-1030. (Pubitemid 46686471)
72. LEVIN, A.A., YU, R.Z., and GEARY, R.S. (2008). Basic principles of the pharmacokinetics of antisense oligonucleotide drugs. In: Antisense Drug Technology: Principles, Strategies, and Applications. R. M. Crooke, ed. (CRC Press, Boca Raton, FL), pp. 183-215.
73. LEWIS, B.P., BURGE, C.B., and BARTEL, D.P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20. (Pubitemid 40094598)
74. LEWIS, B.P., SHIH, I.H., JONES-RHOADES, M.W., BARTEL, D.P., and BURGE, C.B. (2003). Prediction of mammalian microRNA targets. Cell 115, 787-798. (Pubitemid 38058492)
75. LI, X., LIN, R., and LI, J. (2011). Epigenetic silencing of micro- RNA-375 regulates PDK1 expression in esophageal cancer. Dig. Dis. Sci. 56, 2849-2856.
76. LIANG, S., HE, L., ZHAO, X., MIAO, Y., GU, Y., GUO, C., XUE, Z., DOU, W., HU, F., WU, K., et al. (2011). MicroRNA let-7f inhibits tumor invasion and metastasis by targeting MYH9 in human gastric cancer. PloS One 6, e18409.
77. LIM, L.P., LAU, N.C., GARRETT-ENGELE, P., GRIMSON, A., SCHELTER, J.M., CASTLE, J., BARTEL, D.P., LINSLEY, P.S., and JOHNSON, J.M. (2005). Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769-773. (Pubitemid 40292988)
78. LINSLEY, P.S., SCHELTER, J., BURCHARD, J., KIBUKAWA, M., MARTIN, M.M., BARTZ, S.R., JOHNSON, J.M., CUMMINS, J.M., RAYMOND, C.K., DAI, H., et al. (2007). Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol 27(6), 2240-2252. (Pubitemid 46418479)
79. LIU, A.M., POON, R.T., and LUK, J.M. (2010). MicroRNA-375 targets Hippo-signaling effector YAP in liver cancer and inhibits tumor properties. Biochem. Biophys. Res. Commun. 394, 623-627.
80. LIU, J.L., LIANG, X.H., SU, R.W., LEI, W., JIA, B., FENG, X.H., LI, Z.X., and YANG, Z.M. (2012a). The combined analysis of microRNome and 3¢-UTRome reveals a species-specific regulation of progesterone receptor expression in the endometrium of rhesus monkey. J. Biol. Chem. 287, 13899-13910.
81. LIU, Z., ZHU, J., CAO, H., REN, H., and FANG, X. (2012b). miR- 10b promotes cell invasion through RhoC-AKT signaling pathway by targeting HOXD10 in gastric cancer. Int. J. Oncol. 40, 1553-1560.
82. LU, F., WEIDMER, A., LIU, C.G., VOLINIA, S., CROCE, C.M., and LIEBERMAN, P.M. (2008). Epstein-Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence. J. Virol. 82, 10436-10443. (Pubitemid 352691173)
83. MA, L., TERUYA-FELDSTEIN, J., and WEINBERG, R.A. (2007). Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682-688. (Pubitemid 47552092)
84. MARQUES, A.C., and PONTING, C.P. (2009). Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol. 10, R124.
85. MARQUITZ, A.R., MATHUR, A., SHAIR, K.H., and RAABTRAUB, N. (2012). Infection of Epstein-Barr virus in a gastric carcinoma cell line induces anchorage independence and global changes in gene expression. Proc. Natl. Acad. Sci. U. S. A. 109, 9593-9598.
86. MAYR, C., HEMANN, M.T., and BARTEL, D.P. (2007). Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315,, 1576-1579. (Pubitemid 46449474)
87. MCDERMOTT, A.M., HENEGHAN, H.M., MILLER, N. and KERIN, M.J. (2011). The therapeutic potential of microRNAs: disease modulators and drug targets. Pharm. Res. 28, 3016-3029.
88. MEOLA, N., GENNARINO, V.A., and BANFI, S. (2009). microRNAs and genetic diseases. Pathogenetics 2, 7.
89. MIRANDA, K.C., HUYNH, T., TAY, Y., ANG, Y.S., TAM, W.L., THOMSON, A.M., LIM, B., and RIGOUTSOS, I. (2006). A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126, 1203-1217. (Pubitemid 44380294)
90. MOLNAR, A., SCHWACH, F., STUDHOLME, D.J., THUENEMANN, E.C., and BAULCOMBE, D.C. (2007). miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447, 1126-1129. (Pubitemid 47014429)
91. MONTGOMERY, R.L., HULLINGER, T.G., SEMUS, H.M., DICKINSON, B.A., SETO, A.G., LYNCH, J.M., STACK, C., LATIMER, P.A., OLSON, E.N., and VAN ROOIJ, E. (2011). Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure. Circulation 124, 1537-1547.
92. MORIARTY, C.H., PURSELL, B., and MERCURIO, A.M. (2010). miR-10b targets Tiam1: implications for Rac activation and carcinoma migration. The J. Biol. Chem. 285, 20541-20546.
93. NADIMINTY, N., TUMMALA, R., LOU, W., ZHU, Y., ZHANG, J., CHEN, X., EVERE WHITE, R.W., KUNG, H.J., EVANS, C.P., and GAO, A.C. (2012). MicroRNA let-7c suppresses androgen receptor expression and activity via regulation of Myc expression in prostate cancer cells. J. Biol. Chem. 287, 1527-1537.
94. NAKAMOTO, M., JIN, P., O'DONNELL, W.T., and WARREN, S.T. (2005). Physiological identification of human transcripts translationally regulated by a specific microRNA. Hum. Mol. Genet. 14, 3813-3821. (Pubitemid 43020083)
95. NIMMO, R.A., and SLACK, F.J. (2009). An elegant miRror: microRNAs in stem cells, developmental timing and cancer. Chromosoma 118, 405-418.
96. NISHIKAWA, E., OSADA, H., OKAZAKI, Y., ARIMA, C., TOMIDA, S., TATEMATSU, Y., TAGUCHI, A., SHIMADA, Y., YANAGISAWA, K., YATABE, Y., et al. (2011). miR-375 is activated by ASH1 and inhibits YAP1 in a lineage-dependent manner in lung cancer. Cancer Res. 71, 6165-6173.
97. NOHATA, N., HANAZAWA, T., KIKKAWA, N., MUTALLIP, M., SAKURAI, D., FUJIMURA, L., KAWAKAMI, K., CHIYOMARU, T., YOSHINO, H., ENOKIDA, H., et al. (2011). Tumor suppressive microRNA-375 regulates oncogene AEG-1/MTDH in head and neck squamous cell carcinoma (HNSCC). J. Hum. Genet. 56, 595-601.
98. OBAD, S., DOS SANTOS, C.O., PETRI, A., HEIDENBLAD, M., BROOM, O., RUSE, C., FU, C., LINDOW, M., STENVANG, J., STRAARUP, E.M., et al. (2011). Silencing of microRNA families by seed-targeting tiny LNAs. Nat. Genet. 43, 371-378.
99. PANG, K.C., FRITH, M.C., and MATTICK, J.S. (2006). Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet. 22, 1-5. (Pubitemid 43011990)
100. PASQUINELLI, A.E., MCCOY, A., JIMENEZ, E., SALO, E., RUVKUN, G., MARTINDALE, M.Q. and BAGUNA, J. (2003). Expression of the 22 nucleotide let-7 heterochronic RNA throughout the Metazoa: a role in life history evolution? Evol. Dev. 5, 372-378. (Pubitemid 36893146)
101. PASQUINELLI, A.E., REINHART, B.J., SLACK, F., MARTINDALE, M.Q., KURODA, M.I., MALLER, B., SPRING, J., SRINIVASAN, A., FISHMAN, M., FINNERTY, J., et al. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89.
102. PFEFFER, S., ZAVOLAN, M., GRASSER, F.A., CHIEN, M., RUSSO, J.J., JU, J., JOHN, B., ENRIGHT, A.J., MARKS, D., SANDER, C., et al. (2004). Identification of virus-encoded microRNAs. Science 304, 734-736. (Pubitemid 38560879)
103. POLISENO, L., SALMENA, L., ZHANG, J., CARVER, B., HAVEMAN, W.J., and PANDOLFI, P.P. (2010). A codingindependent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465, 1033-1038.
104. POY, M.N., ELIASSON, L., KRUTZFELDT, J., KUWAJIMA, S., MA, X., MACDONALD, P.E., PFEFFER, S., TUSCHL, T., RAJEWSKY, N., RORSMAN, P., et al. (2004). A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432, 226-230. (Pubitemid 39545853)
105. POY, M.N., HAUSSER, J., TRAJKOVSKI, M., BRAUN, M., COLLINS, S., RORSMAN, P., ZAVOLAN, M., and STOFFEL, M. (2009). miR-375 maintains normal pancreatic alpha- and beta-cell mass. Proc. Natl. Acad. Sci. U. S. A. 106, 5813-5818.
106. REINHART, B.J., SLACK, F.J., BASSON, M., PASQUINELLI, A.E., BETTINGER, J.C., ROUGVIE, A.E., HORVITZ, H.R., and RUVKUN, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenhorhabditis elegans. Nature 403, 901-906. (Pubitemid 30130993)
107. RIGOUTSOS, I. (2009). New tricks for animal microRNAS: targeting of amino acid coding regions at conserved and nonconserved sites. Cancer Res. 69, 3245-3248.
108. RILEY, K.J., RABINOWITZ, G.S., YARIO, T.A., LUNA, J.M., DARNELL, R.B., and STEITZ, J.A. (2012). EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. The EMBO Journal 31(9), 2207-2221.
109. ROSA, A., SPAGNOLI, F.M., and BRIVANLOU, A.H. (2009). The miR-430/427/302 family controls mesendodermal fate specification via species-specific target selection. Dev. Cell 16, 517-527.
110. ROSATO, P., ANASTASIADOU, E., GARG, N., LENZE, D., BOCCELLATO, F., VINCENTI, S., SEVERA, M., COCCIA, E.M., BIGI, R., CIRONE, M., et al. (2012). Differential regulation of miR-21 and miR-146a by Epstein-Barr virus-encoded EBNA2. Leukemia doi:10.038/leu.2012.08.
111. ROUSH, S., and SLACK, F.J. (2008). The let-7 family of micro- RNAs. Trends Cell Biol. 18, 505-516.
112. SALMENA, L., POLISENO, L., TAY, Y., KATS, L., and PANDOLFI, P.P. (2011). A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146, 353-358.
113. SELBACH, M., SCHWANHAUSSER, B., THIERFELDER, N., FANG, Z., KHANIN, R., and RAJEWSKY, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature 4, 58-63.
114. SETO, E., MOOSMANN, A., GROMMINGER, S., WALZ, N., GRUNDHOFF, A., and HAMMERSCHMIDT, W. (2010). Micro RNAs of Epstein-Barr virus promote cell cycle progression and prevent apoptosis of primary human B cells. PLoS Pathog. 6, e1001063.
115. SHI, X.B., TEPPER, C.G., and DEVERE WHITE, R.W. (2008). Cancerous miRNAs and their regulation. Cell Cycle 7, 1529-1538. (Pubitemid 351881316)
116. SHIMIZU, S., TAKEHARA, T., HIKITA, H., KODAMA, T., MIYAGI, T., HOSUI, A., TATSUMI, T., ISHIDA, H., NODA, T., NAGANO, H., et al. (2010). The let-7 family of microRNAs inhibits Bcl-xL expression and potentiates sorafenib-induced apoptosis in human hepatocellular carcinoma. J. Hepatol. 52, 698-704.
117. SHIN, C., NAM, J.W., FARH, K.K., CHIANG, H.R., SHKUMATAVA, A., and BARTEL, D.P. (2010). Expanding the microRNA targeting code: functional sites with centered pairing. Mol. Cell 38, 789-802.
118. SOKOL, N.S., XU, P., JAN, Y.N., and AMBROS, V. (2008). Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev. 22, 1591-1596. (Pubitemid 351846839)
119. SOOD, P., KREK, A., ZAVOLAN, M., MACINO, G., and RAJEWSKY, N. (2006). Cell-type-specific signatures of micro- RNAs on target mRNA expression. Proc. Natl. Acad. Sci. U. S. A. 103, 2746-2751.
120. SOUTSCHEK, J., AKINC, A., BRAMLAGE, B., CHARISSE, K., CONSTIEN, R., DONOGHUE, M., ELBASHIR, S., GEICK, A., HADWIGER, P., HARBORTH, J., et al. (2004). Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 432, 173-178. (Pubitemid 39545841)
121. STARK, A., BRENNECKE, J., RUSSELL, R.B., and COHEN, S.M. (2003). Identification of Drosophila MicroRNA targets. PLoS Biol. 1, E60.
122. SUN, L., YAN, W.,WANG, Y., SUN, G., LUO, H., ZHANG, J., WANG, X., YOU, Y., YANG, Z., and LIU, N. (2011). MicroRNA-10b induces glioma cell invasion by modulating MMP-14 and uPAR expression via HOXD10.Brain Res. 1389, 9-18.
123. SZCZYRBA, J., NOLTE, E., WACH, S., KREMMER, E., STOHR, R., HARTMANN, A., WIELAND, W., WULLICH, B., and GRASSER, F.A. (2011). Downregulation of Sec23A protein by miRNA-375 in prostate carcinoma. Mol. Cancer Res. 9, 791-800.
124. TAY, Y., ZHANG, J., THOMSON, A.M., LIM, B., and RIGOUTSOS, I. (2008). MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455, 1124-1128.
125. TIAN, Y., LUO, A., CAI, Y., SU, Q., DING, F., CHEN, H., and LIU, Z. (2010). MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J. Biol. Chem. 285, 7986-7994.
126. TRANG, P., WIGGINS, J.F., DAIGE, C.L., CHO, C., OMOTOLA, M., BROWN, D., WEIDHAAS, J.B., BADER, A.G., and SLACK, F.J. (2011). Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol. Ther. 19, 1116-1122.
127. TSUKAMOTO, Y., NAKADA, C., NOGUCHI, T., TANIGAWA, M., NGUYEN, L.T., UCHIDA, T., HIJIYA, N., MATSUURA, K., FUJIOKA, T., SETO, M., et al. (2010). MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res. 70, 2339-2349.
128. VAISHNAW, A.K., GOLLOB, J., GAMBA-VITALO, C., HUTABARAT, R., SAH, D., MEYERS, R., DE FOUGEROLLES, T., and MARAGANORE, J. (2010). A status report on RNAi therapeutics. Silence 1, 14.
129. VALASTYAN, S., BENAICH, N., CHANG, A., REINHARDT, F., and WEINBERG, R.A. (2009). Concomitant suppression of three target genes can explain the impact of a microRNA on metastasis. Genes Dev. 23, 2592-2597.
130. VAN ROOIJ, E., PURCELL, A.L., and LEVIN, A.A. (2012). Developing microRNA therapeutics. Circ. Res. 110, 496-507.
131. VELLA, M.C., CHOI, E.Y., LIN, S.Y., REINERT, K., and SLACK, F.J. (2004). The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3¢UTR. Genes Dev. 18, 132-137. (Pubitemid 38141781)
132. WANG, F., LI, Y., ZHOU, J., XU, J., PENG, C., YE, F., SHEN, Y., LU, W., WAN, X., and XIE, X. (2011). miR-375 is downregulated in squamous cervical cancer and inhibits cell migration and invasion via targeting transcription factor SP1.Am. J. Pathol. 179, 2580-2588.
133. XIAO, C., CALADO, D.P., GALLER, G., THAI, T.H., PATTERSON, H.C., WANG, J., RAJEWSKY, N., BENDER, T.P., and RAJEWSKY, K. (2007). MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131, 146-159. (Pubitemid 47498525)
134. YIN, Q., MCBRIDE, J., FEWELL, C., LACEY, M., WANG, X., LIN, Z., CAMERON, J., and FLEMINGTON, E.K. (2008). MicroRNA- 155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J. Virol. 82, 5295-5306. (Pubitemid 351705237)
135. ZHANG, L., HOU, D., CHEN, X., LI, D., ZHU, L., ZHANG, Y., LI, J., BIAN, Z., LIANG, X., CAI, X., et al. (2012). Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res. 22, 107-126.
136. ZHAO, Y., DENG, C., LU, W., XIAO, J., MA, D., GUO, M., RECKER, R.R., GATALICA, Z., WANG, Z., and XIAO, G.G. (2011). Let-7 microRNAs induce tamoxifen sensitivity by down-regulation of estrogen receptor alpha signaling in breast cancer. Mol. Med. 17, 1233-1241.
137. ZHOU, X., DUAN, X., QIAN, J., and LI, F. (2009). Abundant conserved microRNA target sites in the 5¢-untranslated region and coding sequence. Genetica 137, 159-164.
138. ZHU, H., SHYH-CHANG, N., SEGRE, A.V., SHINODA, G., SHAH, S.P., EINHORN, W.S., TAKEUCHI, A., ENGREITZ, J.M., HAGAN, J.P., KHARAS, M.G., et al. (2011). The Lin28/let-7 axis regulates glucose metabolism. Cell 147, 81-94.
139. ZHU, J.Y., PFUHL, T., MOTSCH, N., BARTH, S., NICHOLLS, J., GRASSER, F., and MEISTER, G. (2009). Identification of novel Epstein-Barr virus microRNA genes from nasopharyngeal carcinomas. J. Virol. 83, 3333-3341.