miR-122 targeting with LNA/2′-O-methyl oligonucleotide mixmers, peptide nucleic acids (PNA), and PNA-peptide conjugates

RNA

Volumn 14, Issue 2, 2008, Pages 336-346

  Fabani, Martin M ^a   Gait, Michael J ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Antisense; microRNA; miR 122; Peptide; PNA; Targeting

Indexed keywords

LOCKED NUCLEIC ACID; MICRORNA; MICRORNA 122; OLIGONUCLEOTIDE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE CONTROL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA BINDING; RNA EXTRACTION;

ANIMALS; CELL LINE; GENE EXPRESSION; HUMANS; LIVER; MICRORNAS; OLIGONUCLEOTIDES; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDE NUCLEIC ACIDS; RATS; RNA, MESSENGER;

RATTUS;

EID: 38649105459     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.844108     Document Type: Article

References (56)

1. Abes, S., Williams, D., Prevot, P., Thierry, A.R., Gait, M.J., and Lebleu, B. 2006. Endosome trapping limits the efficiency of splicing correction by PNA-oligolysine conjugates. J. Control. Release 110: 595-604.
2. 6-Penetratin delivery peptide. Nucleic Acids Res. 35: 4495-4502. doi: 10.1093/nar/gkm418.
3. Ahn, D.-G., Kourakis, M.J., Rohde, L.A., Silver, L.M., and Ho, R.K. 2002. T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 417: 754-758.
4. Albertshofer, K., Siwkowski, A.M., Wancewicz, E.V., Esau, C.C., Watanabe, T., Nishihara, K.C., Kinberger, G.A., Malik, L., Eldrup, A.B., Manoharan, M., et al. 2005. Structure-activity relationship study on a simple cationic peptide motif for cellular delivery of antisense peptide nucleic acid. J. Med. Chem. 48: 6741-6749.
5. Arzumanov, A., Walsh, A.P., Rajwanshi, V.K., Kumar, R., Wengel, J., and Gait, M.J. 2001. Inhibition of HIV-1 Tat-dependent trans-activation by steric block chimeric 2′-O-methyl/LNA oligoribonucleotides. Biochemistry 40: 14645-14654.
6. Arzumanov, A., Stetsenko, D.A., Malakhov, A.D., Reichelt, S., Sørensen, M.D., Babu, B.R., Wengel, J., and Gait, M.J. 2003. A structure-activity study of the inhibition of HIV-1 Tat-dependent trans-activation by mixmer 2′-O-methyl oligoribonucleotides containing locked nucleic acid (LNA), α-LNA or 2′-thio-LNA residues. Oligonucleotides 13: 435-453.
7. Baker, B.F., Lot, S.S., Condon, T.P., Cheng-Flourney, S., Lesnik, E.A., Sasmor, H.M., and Bennett, C.F. 1997. 2′-O-(2-methoxy)ethyl- modified anti-intercellular adhesion molecule 1 (ICAM-1) oligonucleotides selectively increase the ICAM-1 mRNA level and inhibit formation of the ICAM-1 translation initiation complex in human umbilical vein endothelial cells. J. Biol. Chem. 272: 11994-12000.
8. Bhattacharyya, S.N., Habermacher, R., Martine, U., Closs, E.I., and Filipowicz, W. 2006a. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125: 1111-1124.
9. Bhattacharyya, S.N., Habermacher, R., Martine, U., Closs, E.I., and Filipowicz, W. 2006b. Stress-induced reversal of microRNA repression and mRNA P-body localization in human cells. Cold Spring Harb. Symp. Quant. Biol. 71: 513-521.
10. Boffa, L.C., Cutrona, G., Cilli, M., Mariani, M.R., Matis, S., Pastorini, M., Damonte, G., Millo, E., Roncella, S., and Ferrarini, M. 2005. Therapeutically promising PNA complementary to a regulatory sequence for c-myc: Pharmacokinetics in an animal model of human Burkitt's lymphoma. Oligonucleotides 15: 85-93.
11. Brown, D., Arzumanov, A.A., Turner, J.J., Stetsenko, D.A., Lever, A.M., and Gait, M.J. 2005. Antiviral activity of steric-block oligonucleotides targeting the HIV-1 trans-activation response and packaging signal stem-loop RNAs. Nucleosides Nucleotides Nucleic Acids 24: 393-396.
12. Brown, D.E., Arzumanov, A., Syed, S., Gait, M.G., and Lever, A.M. 2006. Inhibition of HIV-1 replication by oligonucleotide analogues directed to the packaging signal and trans-activating response region. Antivir. Chem. Chemother. 17: 1-9.
13. Chan, J.A., Krichevsky, A.M., and Kosik, K.S. 2005. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 65: 6029-6033.
14. Chang, J., Nicolas, E., Marks, D., Sander, C., Lerro, A., Buendia, M.A., Xu, C., Mason, W.S., Moloshok, T., Bort, R., et al. 2004. miR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high affinity cationic amino acid transporter CAT-1. RNA Biol. 1: 106-113.
15. Cheng, A.M., Byrom, M.W., Shelton, J., and Ford, L.P. 2005. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res. 33: 1290-1297. doi: 10.1093/nar/gki200.
16. Cimmino, A., Calin, G.A., Fabbri, M., Iorio, M.V., Ferracin, M., Shimizu, M., Wojcik, S.E., Aqeilan, R.I., Zupo, S., Dono, M., et al. 2005. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl. Acad. Sci. 102: 13944-13949.
17. Davis, S., Lollo, B., Freier, S., and Esau, C. 2006. Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res. 34: 2294-2304. doi: 10.1093/nar/gkl183.
18. Ebert, M.S., Neilson, J.R., and Sharp, P.A. 2007. MicroRNA sponges: Competitive inhibitors of small RNAs in mammalian cells. Nature 4: 721-726.
19. Esau, C., Kang, X., Peralta, E., Hanson, E., Marcusson, E.G., Ravichandran, L.V., Sun, Y., Koo, S., Perera, R.J., Jain, R., et al. 2004. MicroRNA-143 regulates adipocyte differentiation. J. Biol. Chem. 279: 52361-52365.
20. 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.
21. Fletcher, S., Honeyman, K., Fall, A.M., Harding, P.L., Johnsen, R.D., Steinhaus, J.P., Moulton, H.M., Iversen, P.L., and Wilton, S.D. 2007. Morpholino oligomer-mediated exon skipping averts the onset of dystrophic pathology in the mdx mouse. Mol. Ther. 151: 587-592.
22. Garzon, R., Fabbri, M., Cimmino, A., Calin, G.A., and Croce, C.M. 2006. MicroRNA expression and function in cancer. Trends Mol. Med. 12: 580-587.
23. Griffith-Jones, S., Grocock, R.J., van Dongen, S., Bateman, A., and Enright, A.J. 2006. miRBase: MicroRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34: D140-D144. doi: 10.1093/nar/gkj112.
24. He, L., Thomson, J.M., Hemann, M.T., Hernando-Monge, E., Mu, D., Goodson, S., Powers, S., Cordon-Cardo, C., Lowe, S.W., Hannon, G.J., et al. 2005. A microRNA polycistron as a potential human oncogene. Nature 435: 828-833.
25. Jopling, C.L., Yi, M., Lancaster, A.M., Lemon, S.M., and Sarnow, P. 2005. Modulation of Hepatitis C Virus RNA abundance by a liver-specific microRNA. Science 309: 1577-1581.
26. Jopling, C.L., Norman, K.L., and Sarnow, P. 2006. Positive and negative modulation of viral and cellular mRNAs by liver-specific microRNA miR-122. Cold Spring Harb. Symp. Quant. Biol. 71: 369-376.
27. Kaihatsu, K., Huffman, K.E., and Corey, D.R. 2004. Intracellular uptake and inhibition of gene expression by PNAs and PNA-peptide conjugates. Biochemistry 43: 14340-14347.
28. Kloosterman, W.P., Agendijk, A.K., Ketting, R.F., Moulton, J.D., and Plasterk, R.H.A. 2007. Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 5: e203.
29. Knudsen, H. and Nielsen, P. 1996. Antisense properties of duplex-and triplex-forming PNAs. Nucleic Acids Res. 24: 494-500. doi: 10.1093/nar/24.3.494.
30. Koppelhus, U., Zachar, V., Nielsen, P., Liu, X., Eugen-Olsen, J., and Ebbesen, P. 1997. Efficient in vitro inhibition of HIV-1 gag reverse transcription by peptide nucleic acid (PNA) at minimal ratios of PNA/RNA. Nucleic Acids Res. 25: 2167-2173. doi: 10.1093/nar/25.11.2167.
31. Koshkin, A.A., Singh, S.K., Nielsen, P., Rajwanshi, V.K., Kumar, R., Meldgaard, M., Olsen, C.E., and Wengel, J. 1998. LNA (locked nucleic acids): Synthesis of the adenine, cytosine, guanine, 5-methylcytosine, thymine and uracil bicyclonucleoside monomers, oligomerisation, and unprecedented nucleic acid recognition. Tetrahedron 54: 3607-3630.
32. 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.
33. Krutzfeldt, J., Kuwajima, S., Braich, R., Rajeev, K.G., Pena, J., Tuschl, T., Manoharan, M., and Stoffel, M. 2007. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res. 35: 2885-2892. doi: 10.1093/nar/gkm024.
34. Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W., and Tuschl, T. 2002. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12: 735-739.
35. Lee, R.C., Feinbaum, R.L., and Ambros, V. 1993. The C. elegans heterochromic gene lin-4 encodes small RNAs with antisense complementary to lin-14. Cell 75: 843-854.
36. Liu, J., Valencia-Sanchez, M.A., Hannon, G.J., and Parker, R. 2005. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7: 719-723.
37. Meister, G., Landthaler, M., Dorsett, Y., and Tuschl, T. 2004. Sequence-specific inhibition of microRNA- and siRNA-induced RNA silencing. RNA 10: 544-550.
38. Moschos, S.A., Williams, A.E., Perry, M.M., Birrell, M.A., Belvisi, M.G., and Lindsay, M.A. 2007. Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics 8: 240. doi: 10.1186/1471-2164-8-240.
39. Naguibneva, I., Ameyar-Zazoua, M., Nonne, N., Polesskaya, A., Ait-Si-Ali, S., Groisman, R., Souidi, M., Pritchard, L.L., and Harel-Bellan, A. 2006. An LNA-based loss-of-function assay for micro-RNAs. Biomed. Pharmacother. 60: 633-638.
40. Nielsen, P.E., Egholm, M., and Buchardt, O. 1994. Peptide nucleic acid (PNA). A DNA mimic with a peptide backbone. Bioconjug. Chem. 5: 3-7.
41. O'Connell, R.M., Taganov, K.D., Boldin, M.P., Cheng, G., and Baltimore, D. 2007. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. 104: 1604-1609.
42. O'Donnell, K.A., Wentzel, E.A., Zeller, K.I., Dang, C.V., and Mendell, J.T. 2005. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435: 839-843.
43. Ørom, U.A., Kauppinen, S., and Lund, A.H. 2006. LNA-modified oligonucleotides mediate specific inhibition of microRNA function. Gene 372: 137-141.
44. Richard, J.P., Melikov, K., Brooks, H., Prevot, P., Lebleu, B., and Chernomordik, L.V. 2005. Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J. Biol. Chem. 280: 15300-15306.
45. Roberts, J., Palma, E., Sazani, P., Ørum, H., Cho, M., and Kole, R. 2006. Efficient and persistent splice switching by systemically delivered LNA oligonucleotides in mice. Mol. Ther. 14: 471-475.
46. Saetrom, P., Heale, B.S.E., Snove Jr., O., Aagaard, L., Alluin, J., and Rossi, J.J. 2007. Distance constraints between microRNA target sites dictate efficacy and cooperativity. Nucleic Acids Res. 35: 2333-2342. doi: 10.1093/nar/gkm133.
47. Sazani, P., Gemignani, F., Kang, S.-H., Maier, M.A., Manoharan, M., Persmark, M., Bortner, D., and Kole, R. 2002. Systemically delivered antisense oligomers upregulate gene expression in mouse tissues. Nat. Biotechnol. 20: 1228-1233.
48. Suwanmanee, T., Sierakowska, H., Fucharoen, S., and Kole, R. 2002. Repair of a splicing defect in erythroid cells from patients with β-thalassemia/ HbE disorder. Mol. Ther. 6: 718-726.
49. Triboulet, R., Mari, B., Lin, Y.-L., Chable-Bessia, C., Bennasser, Y., Lebrigand, K., Cardinaud, B., Maurin, T., Barbry, P., Baillat, V., et al. 2007. Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315: 1579-1582.
50. Turner, J.J., Arzumanov, A.A., and Gait, M.J. 2005a. Synthesis, cellular uptake and HIV-1 Tat-dependent trans-activation inhibition activity of oligonucleotide analogues disulphide-conjugated to cell-penetrating peptides. Nucleic Acids Res. 33: 27-42. doi: 10.1093/nar/gki142.
51. Turner, J.J., Ivanova, G.D., Verbeure, B., Williams, D., Arzumanov, A.A., Abes, S., Lebleu, B., and Gait, M.J. 2005b. Cell-penetrating peptide conjugates of peptide nucleic acids (PNA) as inhibitors of HIV-1 Tat-dependent trans-activation in cells. Nucleic Acids Res. 33: 6837-6849. doi: 10.1093/nar/gki991.
52. Turner, J.J., Williams, D., Owen, D., and Gait, M.J. 2006. Disulfide conjugation of peptides to oligonucleotides and their analogs. In Current protocols in nucleic acid chemistry, pp 4.28.21-24.28.21. Wiley, New York.
53. Válóczi, A., Hornyik, C., Varga, N., Burgyán, J., Kauppinen, S., and Havelda, Z. 2004. Sensitive and specific detection of microRNAs by northern blot analysis using LNA-modified oligonucleotide probes. Nucleic Acids Res. 32: e175. doi: 10.1093/nar/gnh171.
54. Weiler, J., Hunziker, J., and Hall, J. 2006. Anti-miRNA oligonucleotides (AMOs): Ammunition to target miRNAs implicated in human disease? Gene Ther. 13: 496-502.
55. Xu, P., Vernooy, S.Y., Guo, M., and Hay, B.A. 2003. The Drosophila microRNA miR-14 suppresses cell death and is required for normal fat metabolism. Curr. Biol. 13: 790-795.
56. Xue-Wen, H., Jie, P., Xian-Yuan, A., and Hong-Xiang, Z. 2007. Inhibition of bacterial translation and growth by peptide nucleic acids targeted to domain II of 23S rRNA. J. Pept. Sci. 13: 220-226.