In vitro optimization of 2′-OMe-4′-thioribonucleoside-modified anti-microRNA oligonucleotides and its targeting delivery to mouse liver using a liposomal nanoparticle

Nucleic Acids Research

Volumn 41, Issue 22, 2013, Pages 10659-10667

  Takahashi, Mayumi ^a   Yamada, Naoki ^a   Hatakeyama, Hiroto ^a   Murata, Manami ^a   Sato, Yusuke ^a   Minakawa, Noriaki ^b   Harashima, Hideyoshi ^a   Matsuda, Akira ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2' O METHYL 4' THIORIBONUCLEOSIDE; COMPLEMENTARY RNA; LIPOSOME; MICRORNA; MICRORNA 122; MICRORNA 21; NANOPARTICLE; PHOSPHOROTHIOIC ACID; RIBONUCLEOSIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG DISTRIBUTION; DRUG POTENCY; DRUG STRUCTURE; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LIPOSOMAL DELIVERY; LIVER EXAMINATION; LOW DRUG DOSE; MOUSE; NANOPHARMACEUTICS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL LINE; FEMALE; HELA CELLS; HUMANS; LIPOSOMES; LIVER; MICE; MICE, INBRED BALB C; MICRORNAS; NANOPARTICLES; OLIGONUCLEOTIDES; THIONUCLEOSIDES;

EID: 84890334167     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt823     Document Type: Article

References (45)

1. Liu, Z., Sall, A. and Yang, D. (2008) MicroRNA: an emerging therapeutic target and intervention. Int. J. Mol. Sci., 9, 978-999.
2. Krol, J., Loedige, I. and Filipowicz, W. (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet., 11, 597-610.
3. Lewis, B., Shih, I., Jones-Rhoades, M., Bartel, D. and Burge, C. (2003) Prediction of mammalian microRNA targets. Cell, 115, 787-798.
4. Krek, D., Grü n, D., Poy, M.N., Wolf, R., Rosenberg, L., Epstein, E.J., MacMenamin, P., Da P. I., Gunsalus, K.C., Stoffel, M. et al. (2005) Combinatorial microRNA target predictions. Nat. Genet., 37, 495-500.
5. Betel, D., Wilson, M., Gabow, A., Marks, D.S. and Sander, C. (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res., 36, D149-D153.
6. 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.
7. 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.
8. Sayed, D. and Abdellatif, M. (2011) MicroRNAs in development and disease. Physiol. Rev., 91, 827-887.
9. Esau, C.C. (2008) Inhibition of microRNA with antisense oligonucleotides. Methods, 44, 55-60.
10. Inoue, H., Hayase, Y., Iwai, S. and Ohtsuka, E. (1987) Sequencedependent hydrolysis of RNA using modified oligonucleotide splints and RNase H. FEBS Lett., 215, 327-330.
11. Inoue, H., Hayase, Y., Imura, A., Iwai, S., Miura, K. and Ohtsuka, E. (1987) Sythesis and hybridization studies on two complementary nona(20-O-methyl)ribonucleotides. Nucleic Acids Res., 15, 6131-6148.
12. Lesnik, E.A., Guinosso, C.J., Kawasaki, A.M., Sasmor, H., Zounes, M., Cummins, L.L., Ecker, D.J., Cook, P.D. and Freier, S.M. (1993) Oligodeoxynucleotides containing 20-O-modifies adenosine: synthesis and effects on stability of DNA: RNA duplexes. Biochemistry, 32, 7832-7838.
13. Cummins, L.L., Owens, S.R., Risen, L.M., Lesnik, E.A., Freier, S.M., McGee, D., Guinosso, C.J. and Cook, P.D. (1995) Characterization of fully 20-modified oligonucleotide hetero-and homoduplex hybridization and nuclease sensitivity. Nucleic Acids Res., 23, 2019-2024.
14. Teplova, M., Minasov, G., Tereshko, V., Inamati, G.B., Cook, P.D., Manoharan, M. and Egli, M. (1999) Crystal structure and improved antisense properties of 20-O-(2-methoxyethyl)-RNA. Nat. Struct. Biol., 6, 535-539.
15. Obika, S., Nanbu, D., Hari, Y., Morio, K., In, Y., Ishida, T. and Imanishi, T. (1997) Synthesis of 20-O, 40-C-methyleneuridine andcytidine: novel bicyclic nucleosides having a fixed C3'-endo sugar puckering. Tetrahedron Lett., 38, 8735-8738.
16. Christensen, N.K., Petersen, M., Nielsen, P., Jacobsen, J.P., Olsen, C.E. and Wengel, J. (1998) A novel class of oligonucleotide analogues containing 20-O, 3'-C-linked [3.2.0]bicycloarabinonucleoside monomers: synthesis, thermal affinity studies, and molecular modeling. J. Am. Chem. Soc., 120, 5458-5463.
17. Bennett, C.F. and Swayze, E.E. (2010) RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Annu. Rev. Pharmacol. Toxicol., 50, 259-293.
18. Meister, G., Landthaler, M., Dorsett, Y. and Tuschl, T. (2004) Sequence-specific inhibition of micro-RNA-and siRNA-induced RNA silencing. RNA, 10, 544-550.
19. Hutvagner, G., Simard, M.J., Mello, C.C. and Zamore, P.D. (2004) Sequence-specific inhibition of small RNA function. PLoS Biol., 2, E98.
20. Lanford, R.E., Hildebrandt-Eriksen, E.S., Petri, A., Persson, R., Lindow, M., Munk, M.E., Kauppinen, S. and Emptyv;rum, H. (2010) Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science, 327, 198-201.
21. Takahashi, M., Minakawa, N. and Matsuda, A. (2009) Synthesis and characterization of 20-modified-40-thioRNA: a comprehensive comparison of nuclease stability. Nucleic Acids Res., 37, 1353-1362.
22. Naka, T., Minakawa, N., Abe, H., Kaga, D. and Matsuda, A. (2000) The stereoselective synthesis of 40-b-thioribonucleosides via the Pummerer reaction. J. Am. Chem. Soc., 122, 7233-7243.
23. Hoshika, S., Minakawa, N. and Matsuda, A. (2004) Synthesis and physical and physiological properties of 40-thioRNA: application to post-modification of RNA aptamer toward NF-kB. Nucleic Acids Res., 32, 3815-3825.
24. Hoshika, S., Minakawa, N., Kamiya, H., Harashima, H. and Matsuda, A. (2005) RNA interference induced by siRNAs modified with 40-thioribonucleosides in cultured mammalian cells. FEBS Lett., 579, 3115-3118.
25. Hoshika, S., Minakawa, N., Shionoya, A., Imada, K., Ogawa, N. and Matsuda, A. (2007) Study of modification pattern-RNAi activity relationships by using siRNAs modified with 40-thioribonucleosides. Chembiochem., 8, 2133-2138.
26. Kato, Y., Minakawa, N., Komatsu, Y., Kamiya, H., Ogawa, N., Harashima, H. and Matsuda, A. (2005) New NTP analogs: the synthesis of 40-thioUTP and 40-thioCTP and their utility for SELEX. Nucleic Acids Res., 33, 2942-2951.
27. Minakawa, N., Sanji, M., Kato, Y. and Matsuda, A. (2008) Investigations toward the selection of fully-modified 40-thioRNA aptamers: optimization of in vitro transcription steps in the presence of 40-thioNTPs. Bioorg. Med. Chem., 16, 9450-9456.
28. Dande, P., Prakash, T.P., Sioufi, N., Gaus, H., Jarres, R., Berdeja, A., Swayze, E.E., Griffey, R.H. and Bhat, B. (2006) Improving RNA interference in mammalian cells by 40-thio-modified small interfering RNA (siRNA): effect on siRNA activity and nuclease stability when used in combination with 20-O-alkyl modifications. J. Med. Chem., 49, 1624-1634.
29. Takahashi, M., Nagai, C., Hatakeyama, H., Minakawa, N., Harashima, H. and Matsuda, A. (2012) Intracellular stability of 20-OMe-40-thioribonucleoside modified siRNA leads to long-term RNAi effect. Nucleic Acids Res., 40, 5787-5793.
30. Sato, Y., Hatakeyama, H., Sakurai, Y., Hyodo, M., Akita, H. and Harashima, H. (2012) A pH-sensitive cationic lipid facilitates the delivery of liposomal siRNA and gene silencing activity in vitro and in vivo. J. Control. Release, 163, 267-276.
31. Sakurai, Y., Hatakeyama, H., Sato, Y., Hyodo, M., Akita, H. and Harashima, H. (2013) Gene silencing via RNAi and siRNA quantification in tumor tissue using MEND, a liposomal siRNA delivery system. Mol. Ther., 21, 1195-1203.
32. Krichevsky, A.M. and Gabriely, G. (2009) miR-21: a small multi-faceted RNA.J. Cell. Mol. Med., 13, 39-53.
33. Takahashi, M., Daidouji, S., Shiro, M., Minakawa, N. and Matsuda, A. (2008) Synthesis and crystal structure of 20-deoxy-20-fluoro-40- thioribonucleosides: substrates for the synthesis of novel modified RNAs. Tetrahedron, 64, 4313-4324.
34. Horwich, M. and Zamore, P. (2008) Design and delivery of antisense oligonucleotides to block microRNA function in cultured Drosophila and human cells. Nat. Protoc., 3, 1537-1549.
35. Lennox, K.A. and Behlke, M.A. (2010) A direct comparison of anti-microRNA oligonucleotide potency. Pharm. Res., 9, 1788-99.
36. 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.
37. 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.
38. Krü tzfeldt, 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.
39. Davis, S., Lollo, B., Freier, S. and Esau, C. (2006) Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res., 34, 2294-2304.
40. Davis, S., Propp, S., Freier, S.M., Jones, L.E., Serra, M.J., Kinberger, G., Bhat, B., Swayze, E.E., Bennett, C.F. and Esau, C. (2009) Potent inhibition of microRNA in vivo without degradation. Nucleic Acids Res., 37, 70-77.
41. Elmé N, J., Lindow, M., Silahtaroglu, A., Bak, M., Christensen, M., Lind-Thomsen, A., Hedtjärn, 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 upregulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res., 36, 1153-1162.
42. 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.
43. Freier, S.M. and Altmann, K.H. (1997) The ups and downs of nucleic acid duplex stability: structure-stability studies on chemically-modified DNA: RNA duplexes. Nucleic Acids Res., 25, 4429-4443.
44. Stein, C.A., Subasinghe, C., Shinozuka, K. and Cohen, J.S. (1988) Physicochemical properties of phosphorothioate oligodeoxynucleotides. Nucleic Acids Res., 16, 3209-3221.
45. Wang, Y., Juranek, S., Li, H., Sheng, G., Wardle, G.S., Tuschl, T. and Patel, D.J. (2009) Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature, 461, 754-761.