The systemic administration of an anti-miRNA oligonucleotide encapsulated pH-sensitive liposome results in reduced level of hepatic microRNA-122 in mice

Journal of Controlled Release

Volumn 173, Issue 1, 2014, Pages 43-50

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

^a HOKKAIDO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Antisense oligonucleotide; Drug delivery system; Liposomes; miR 122; miRNA

Indexed keywords

ANTISENSE OLIGONUCLEOTIDES; DRUG DELIVERY SYSTEM; MIR-122; MIRNA; MULTIFUNCTIONAL ENVELOPE-TYPE NANO DEVICES; PH-SENSITIVE LIPOSOMES; PHOSPHOROTHIOATE MODIFICATIONS; SYSTEMIC ADMINISTRATION;

CYTOTOXICITY; DRUG DELIVERY; LIPOSOMES; MAMMALS; OLIGONUCLEOTIDES;

RNA;

LIPOFECTAMINE; LIPOFECTAMINE2000; LIPOSOME; MICRORNA 122; OLIGONUCLEOTIDE; PHOSPHOROTHIOIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER CELL; CELL ACTIVITY; CELL ENCAPSULATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; GENE EXPRESSION; GENE SILENCING; KIDNEY CELL; LIVER CANCER; LIVER TOXICITY; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL;

ANIMALS; CELL LINE; FEMALE; GENE SILENCING; HYDROGEN-ION CONCENTRATION; LIPIDS; LIPOSOMES; LIVER; MICE; MICRORNAS; OLIGONUCLEOTIDES, ANTISENSE; PIPERIDINES; TRANSFECTION;

EID: 84887730354     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.10.023     Document Type: Article

References (37)

1. V. Ambros The functions of animal microRNAs Nature 431 2004 350 355 (Pubitemid 39265675)
2. M. Lagos-Quintana, R. Rauhut, A. Yalcin, J. Meyer, W. Lendeckel, and T. Tuschl Identification of tissue-specific microRNAs from mouse Curr. Biol. 12 2002 735 739 (Pubitemid 34455427)
3. J. Krützfeldt, N. Rajewsky, R. Braich, K.G. Rajeev, T. Tuschl, M. Manoharan, and M. Stoffel Silencing of microRNAs in vivo with 'antagomirs' Nature 438 2005 685 689
4. Davis, S.F. Murray, X.X. Yu, S.K. Pandey, M. Pear, L. Watts, S.L. Booten, M. Graham, R. McKay, A. Subramaniam, S. Propp, B.A. Lollo, S. Freier, C.F. Bennett, S. Bhanot, and B.P. Monia miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting Cell Metab. 3 2006 87 98
5. C.L. Jopling, M. Yi, A.M. Lancaster, S.M. Lemon, and P. Sarnow Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA Science 309 2005 1577 1581 (Pubitemid 41266486)
6. C. Coulouarn, V.M. Factor, J.B. Andersen, M.E. Durkin, and S.S. Thorgeirsson Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties Oncogene 28 2009 3526 3536
7. X. Tang, J. Gal, X. Zhuang, W. Wang, H. Zhu, and G. Tang A simple array platform for microRNA analysis and its application in mouse tissues RNA 12 2007 1803 1822 (Pubitemid 47481688)
8. A.P. Lewis, and C.L. Jopling Regulation and biological function of the liver-specific miR-122 Biochem. Soc. Trans. 38 2010 1553 1557
9. M.S. Ebert, J.R. Neilson, and P.A. Sharp MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells Nat. Methods 4 2007 721 726 (Pubitemid 47338166)
10. J. Xie, S.L. Ameres, R. Friedline, J.H. Hung, Y. Zhang, Q. Xie, L. Zhong, Q. Su, R. He, M. Li, H. Li, X. Mu, H. Zhang, J.A. Broderick, J.K. Kim, Z. Weng, T.R. Flotte, P.D. Zamore, and G. Gao Long-term, efficient inhibition of microRNRNA function in mice using rAAV vectors Nat. Methods 9 2012 403 409
11. J. Stenvang, A. Petri, M. Lindow, S. Obad, and S.J. Kauppinen Inhibition of microRNA function by antimiR oligonucleotides Silence 3 2012 1
12. J. Elmén, M. Lindow, A. Silahtaroglu, M. Bak, M. Christensen, A. Lind-Thomsen, M. Hedtjärn, J.B. Hansen, H.F. Hansen, E.M. Straarup, K. McCullagh, P. Kearney, and S. Kauppinen 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 2008 1153 1162 (Pubitemid 351330933)
13. J. Elmén, M. Lindow, S. Schütz, M. Lawrence, A. Petri, S. Obad, M. Lindholm, M. Hedtjärn, H.F. Hansen, U. Berger, S. Gullans, P. Kearney, P. Sarnow, E.M. Straarup, and S. Kauppinen LNA-mediated microRNA silencing in non-human primates Nature 452 2008 896 899 (Pubitemid 351550859)
14. S. Obad, C.O. dos Santos, A. Petri, M. Heidenblad, O. Broom, C. Ruse, C. Fu, M. Lindow, J. Stenvang, E.M. Straarup, H.F. Hansen, T. Koch, D. Pappin, G.J. Hannon, and S. Kauppinen Silencing of microRNA families by seed-targeting tiny LNAs Nat. Genet. 43 2011 37378
15. H.L. Janssen, H.W. Reesink, F.J. Lawitz, S. Zeuzem, M. Rodriguez-Torres, K. Patel, A.J. van der Meer, A.K. Patick, A. Chen, Y. Zhou, R. Persson, B.D. King, S. Kauppinen, A.A. Levin, and M.R. Hodges Treatment of HCV infection by targeting microRNA N. Engl. J. Med. 368 2013 1685 1694
16. B. Haraldsson, J. Nyström, and W.M. Deen Properties of the glomerular barrier and mechanisms of proteinuria Physiol. Rev. 88 2008 451 487 (Pubitemid 351522745)
17. R.M. Bukowski, C. Tendler, D. Cutler, E. Rose, M.M. Laughlin, and P. Statkevich Treating cancer with PEG Intron: pharmacokinetic profile and dosing guidelines for an improved interferon-alpha-2b formulation Cancer 95 2002 389 396 (Pubitemid 34787605)
18. C.V. Pecot, G.A. Calin, R.L. Coleman, G. Lopez-Berestein, and A.K. Sood RNA interference in the clinic: challenges and future directions Nat. Rev. Cancer 11 2011 59 67
19. T.S. Zimmermann, A.C. Lee, A. Akinc, B. Bramlage, D. Bumcrot, and M.N. Fedoruk RNAi-mediated gene silencing in non-human primates Nature 441 2006 111 114
20. S.C. Semple, A. Akinc, J. Chen, A.P. Sandhu, B.L. Mui, C.K. Cho, D.W. Sah, D. Stebbing, E.J. Crosley, E. Yaworski, I.M. Hafez, J.R. Dorkin, J. Qin, K. Lam, K.G. Rajeev, K.F. Wong, L.B. Jeffs, L. Nechev, M.L. Eisenhardt, M. Jayaraman, M. Kazem, M.A. Maier, M. Srinivasulu, M.J. Weinstein, Q. Chen, R. Alvarez, S.A. Barros, S. De, S.K. Klimuk, T. Borland, V. Kosovrasti, W.L. Cantley, Y.K. Tam, M. Manoharan, M.A. Ciufolini, M.A. Tracy, A. de Fougerolles, I. MacLachlan, P.R. Cullis, T.D. Madden, and M.J. Hope Rational design of cationic lipids for siRNA delivery Nat. Biotechnol. 28 2010 172 176
21. M. Jayaraman, S.M. Ansell, B.L. Mui, Y.K. Tam, J. Chen, X. Du, D. Butler, L. Eltepu, S. Matsuda, J.K. Narayanannair, K.G. Rajeev, I.M. Hafez, A. Akinc, M.A. Maier, M.A. Tracy, P.R. Cullis, T.D. Madden, M. Manoharan, and M.J. Hope Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo Angew. Chem. Int. Ed. Engl. 51 2012 8529 8533
22. D. Yang, Y. Sun, L. Hu, H. Zheng, P. Ji, C.V. Pecot, Y. Zhao, S. Reynolds, H. Cheng, R. Rupaimoole, D. Cogdell, M. Nykter, R. Broaddus, C. Rodriguez-Aguayo, G. Lopez-Berestein, J. Liu, I. Shmulevich, A.K. Sood, K. Chen, and W. Zhang Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer Cancer Cell 23 2013 186 199
23. S. Anand, B.K. Majeti, L.M. Acevedo, E.A. Murphy, R. Mukthavaram, L. Scheppke, M. Huang, D.J. Shields, J.N. Lindquist, P.E. Lapinski, P.D. King, S.M. Weis, and D.A. Cheresh MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis Nat. Med. 16 2010 909 914
24. H. Hatakeyama, H. Akita, and H. Harashima A multifunctional envelope type nano device (MEND) for gene delivery to tumours based on the EPR effect: a strategy for overcoming the PEG dilemma Adv. Drug Deliv. Rev. 63 2011 152 160 (H. Hatakeyama, H. Akita, H. Harashima, Adv. Drug Deliv. Rev. (2011) 152-160)
25. T. Nakamura, H. Akita, Y. Yamada, H. Hatakeyama, and H. Harashima A multifunctional envelope-type nanodevice for use in nanomedicine: concept and applications Acc. Chem. Res. 45 2012 1113 1121
26. Y. Sato, H. Hatakeyama, Y. Sakurai, M. Hyodo, H. Akita, and H. Harashima A pH-sensitive cationic lipid facilitates the delivery of liposomal siRNA and gene silencing activity in vitro and in vivo J. Control. Release 163 2012 267 276
27. Y. Sakurai, H. Hatakeyama, Y. Sato, M. Hyodo, H. Akita, and H. Harashima Gene silencing via RNAi and siRNA quantification in tumor tissue using MEND, a liposomal siRNA delivery system Mol. Ther. 21 2013 1195 1203
28. S. Davis, B. Lollo, S. Freier, and C. Esau Improved targeting of miRNA with antisense oligonucleotides Nucleic Acids Res. 34 2006 2294 2304 (Pubitemid 43985667)
29. S.H. Hsu, B. Wang, J. Kota, J. Yu, S. Costinean, H. Kutay, L. Yu, S. Bai, K. La Perle, R.R. Chivukula, H. Mao, M. Wei, K.R. Clark, J.R. Mendell, M.A. Caligiuri, S.T. Jacob, J.T. Mendell, and K. Ghoshal Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver J. Clin. Invest. 122 2012 2871 2883
30. X. Yan, F. Kuipers, L.M. Havekes, R. Havinga, B. Dontje, K. Poelstra, G.L. Scherphof, and J.A. Kamps The role of apolipoprotein E in the elimination of liposomes from blood by hepatocytes in the mouse Biochem. Biophys. Res. Commun. 328 2005 57 62 (Pubitemid 40164635)
31. A. Akinc, W. Querbes, S. De, J. Qin, M. Frank-Kamenetsky, K.N. Jayaprakash, M. Jayaraman, K.G. Rajeev, W.L. Cantley, J.R. Dorkin, J.S. Butler, L. Qin, T. Racie, A. Sprague, E. Fava, A. Zeigerer, M.J. Hope, M. Zerial, D.W. Sah, K. Fitzgerald, M.A. Tracy, M. Manoharan, V. Koteliansky, A.D. Fougerolles, and M.A. Maier Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms Mol. Ther. 18 2010 1357 1364
32. K.A. Mislick, and J.D. Baldeschwieler Evidence for the role of proteoglycans in cation-mediated gene transfer Proc. Natl. Acad. Sci. U.S.A. 93 1996 12349 12354 (Pubitemid 26367146)
33. L.C. Mounkes, W. Zhong, G. Cipres-Palacin, T.D. Heath, and R.J. Debs Proteoglycans mediate cationic liposome-DNA complex-based gene delivery in vitro and in vivo J. Biol. Chem. 273 1998 26164 26170 (Pubitemid 28475853)
34. H. Lv, S. Zhang, B. Wang, S. Cui, and J. Yan Toxicity of cationic lipids and cationic polymers in gene deliver J. Control. Release 114 2006 100 109 (Pubitemid 44128621)
35. J. Snoeys, J. Lievens, E. Wisse, F. Jacobs, H. Duimel, D. Collen, P. Frederik, and B.D. Geest Species differences in transgene DNA uptake in hepatocytes after adenoviral transfer correlate with the size of endothelial fenestrae Gene Ther. 14 2007 604 612 (Pubitemid 46444534)
36. J. Krützfeldt, S. Kuwajima, R. Braich, K.G. Rajeev, J. Pena, T. Tuschl, M. Manoharan, and M. Stoffel Specificity, duplex degradation and subcellular localization of antagomir Nucleic Acids Res. 35 2007 2885 2892 (Pubitemid 47073627)
37. M. Takahashi, C. Nagai, H. Hatakeyama, N. Minakawa, H. Harashima, and A. Matsuda Intracellular stability of 2′-OMe-4′-thioribonucleoside modified siRNA leads to long-term RNAi effect Nucleic Acids Res. 40 2012 5787 5793