Mechanisms of single-stranded phosphorothioate modified antisense oligonucleotide accumulation in hepatocytes

Nucleic Acids Research

Volumn 39, Issue 11, 2011, Pages 4795-4807

  Koller, Erich ^a   Vincent, Thomas M ^a   Chappell, Alfred ^a   De, Soma ^b   Manoharan, Muthiah ^b   Bennett, C Frank ^a  

^a ISIS PHARMACEUTICALS   (United States)

^b ALNYLAM PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CAVEOLIN; CLATHRIN; ISIS 353382; MESSENGER RNA; PHOSPHOROTHIOIC ACID; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG TARGETING; ENDOCYTOSIS; ENDOSOME; IC 50; LIVER CELL; LYSOSOME; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL LINE, TUMOR; ENDOCYTOSIS; HEPATOCYTES; KINETICS; MALE; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; OLIGONUCLEOTIDES, ANTISENSE; PHOSPHOROTHIOATE OLIGONUCLEOTIDES;

ANIMALIA; MUS;

EID: 79959479529     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr089     Document Type: Article

References (47)

1. Bennett, C.F. and Swayze, E.E. (2010) RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Ann. Rev. Pharmacol. Toxicol., 50, 259-293.
2. Cerritelli, S.M. and Crouch, R.J. (2009) Ribonucelase H: the enzymes in eukaryotes. FEBS J., 276, 1494-1505.
3. Wu, H., Lima, W.F., Zhang, H., Fan, A., Sun, H. and Crooke, S.T. (2004) Determination of the role of the human RNase H1 in the pharmacology of DNA-like antisense drugs. J. Biol. Chem., 279, 17181-17189. (Pubitemid 38560475)
4. Dean, N.M. and McKay, R.A. (1994) Inhibition of protein kinase C-alpha expression in mice after systemic administration of phosphorothioate antisense oligodeoxynucleotides. Proc. Natl Acad. Sci. USA, 91, 11762-11766. (Pubitemid 24356425)
5. Butler, M., McKay, R.A., Popoff, I., Gaarde, W., Witchell, D., Murray, S., Dean, N.M., Bhanot, S. and Monia, B.P. (2002) Specific inhibition of PTEN expression reverses hyperglycemia in diabetic mice. Diabetes, 1028-1034. (Pubitemid 34438346)
6. Chi, K.M., Eisenhauer, E., Fazli, L., Jones, E.C., Goldenberg, S.L., Powers, J. and Gleave, M.E. (2005) A Phase I pharmacokinetic and pharmacodynamic study of OGX-011, a 20-methoxyethyl antisense to clusterin, in patients with localized prostate cancer prior to radical prostatectomy. J. Natl Cancer Inst., 97, 1287-1296. (Pubitemid 41535369)
7. Kastelein, J.J.P., Wedel, M.K., Baker, B.F., Su, J., Bradley, J.A., Yu, R.Z., Chuang, E., Graham, M.J. and Crooke, R.M. (2006) Potent reduction of Apolipoprotein B and LDL cholesterol by an antisense inhibitor of Apolipoprotein B. Circulation, 114, 1729-1735. (Pubitemid 44607121)
8. 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. (Pubitemid 35462487)
9. Vickers, T.A., Zhang, H., Graham, M.J., Lemonidis, K.M., Zhao, C. and Dean, N.M. (2006) Modification of MyD88 mRNA splicing and inhibition of IL-1beta signaling in cell culture and in mice with a 20-O-methoxyethyl-modified oligonucleotide. J. Immunol., 176, 3652-3661. (Pubitemid 43364012)
10. Geary, R.S., Wancewicz, E., Matson, J., Pearce, M., Siwkowski, A., Swayze, E. and Bennett, F. (2009) Effect of dose and plasma concentration on liver uptake and pharmacologic activity of a 20-methoxyethyl modified chimeric antisense oligonucleotide targeting PTEN. Biochem. Pharmacol., 78, 284-291.
11. Loke, S.L., Stein, C.A., Zhang, X.H., Mori, K., Nakanishi, M., Subasinghe, C., Cohen, J.S. and Neckers, L.M. (1989) Characterization of oligonucleotide transport into living cells. Proc. Natl Acad. Sci. USA, 86, 3474-3478. (Pubitemid 19141813)
12. Crooke, R.M., Graham, M.J., Cooke, M.E. and Crooke, S.T. (1995) In vitro pharmacokinetics of phosphorothioate antisense oligonucleotides. J. Pharmacol. Exp. Ther., 275, 462-473.
13. Krieg, A.M. (1993) Uptake and efficacy of phosphodiester and modified antisense oligonucleotides in primary cell cultures. Clin.Chem., 39, 710-712. (Pubitemid 23118346)
14. Iversen, P.L., Zhu, S., Meyer, A. and Zon, G. (1992) Cellular Uptake and Subcellular Distribution of Phosphorothioate Oligonucleotides into Cultured Cells. Antisense Res. Dev., 2, 211-222.
15. Bennett, C.F., Chiang, M.Y., Chan, H., Shoemaker, J.E.E. and Mirabelli, C.K. (1992) Cationic lipids enhance cellular uptake and activity of phosphorothioate antisense oligonucleotides. Mol. Pharmacol., 41, 1023-1033. (Pubitemid 23026100)
16. Juliano, R., Alam, M.R., Dixit, V. and Kang, H. (2008) Mechanisms and strategies for effective delivery of antisense and siRNA oligonucleotides. Nucleic Acids Res., 36, 4158-4171. (Pubitemid 351984831)
17. Stein, C.A., Hansen, J.B., Lai, J., Wu, S., Voskresenskiy, A., Hog, A., Worm, J., Hedtjarn, M., Souleimanian, N., Miller, P. et al. (2010) Efficient gene silencing by delivery of locked nucleic acid antisense oligonucleotides, unassisted by transfection reagents. Nucleic Acids Res., 38, e3.
18. Nestle, F.O., Mitra, R.S., Bennett, C.F., Chan, H. and Nickoloff, B.J. (1994) Cationic lipid is not required for uptake and selective inhibitory activity of ICAM-1 phosphorothioate antisense oligonucleotides in keratinocytes. J. Invest. Dermatol., 103, 569-575. (Pubitemid 24314848)
19. Giachetti, C. and Chin, D.J. (1996) Increased oligonucleotide permeability in keratinocytes of artificial skin correlates with differentiation and altered membrane function. J. Invest. Dermatol., 107, 256-262. (Pubitemid 26254844)
20. Yu, R.Z., Zhang, H., Geary, R.S., Graham, M., Masarjian, L., Lemonidis, K., Crooke, R., Dean, N.M. and Levin, A.A. (2001) Pharmacokinetics and pharmacodynamics of an antisense phosphorothioate oligonucleotide targeting Fas mRNA in mice. J. Pharmacol. Exp. Ther., 296, 388-395. (Pubitemid 32112464)
21. Dean, N.M., McKay, R., Condon, T.P. and Bennett, C.F. (1994) Inhibition of protein kinase C-alpha expression in human A549 cells by antisense oligonucleotides inhibits induction of intercellular adhesion molecule 1 (ICAM-1) mRNA by phorbol esters. J. Biol. Chem., 269, 16416-16424. (Pubitemid 24209342)
22. Dean, N.M. and Griffey, R.H. (1997) Identification and characterization of second-generation antisense oligonucleotides. Antisense Nucleic Acid Drug Dev., 7, 229-233. (Pubitemid 27323085)
23. Ruther, U., Woodroofe, C., Fattori, E. and Ciliberto, G. (1993) Inducible formation of liver tumors in transgenic mice. Oncogene, 8, 87-93. (Pubitemid 23047233)
24. Neufeld, D.S. (1997) Isolation of rat liver hepatocytes. Methods Mol. Biol., 75, 145-151.
25. McKay, R.A., Miraglia, L.J., Cummins, L.L., Owens, S.R., Sasmor, H. and Dean, N.M. (1999) Characterization of a potent and specific class of antisense oligonucleotide inhibitor of human protein kinase C-alpha expression. J. Biol. Chem., 274, 1715-1722.
26. Ravikumar, V.T., Andrade, M., Carty, R.L., Dan, A. and Barone, S. (2006) Development of siRNA for therapeutics: efficient synthesis of phosphorothioate RNA utilizing phenylacetyl disulfide (PADS). Bioorg. Med. Chem. Lett., 16, 2513-2517.
27. 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.
28. Gaus, H.J., Owens, S.R., Winniman, M., Cooper, S. and Cummins, L.L. (1997) On-line HPLC electrospray mass spectrometry of phosphorothioate oligonucleotide metabolites. Anal. Chem., 69, 313-319.
29. Akinc, A., Zumbuehl, A., Goldberg, M., Leshchiner, E.S., Busini, V., Hossain, N., Bacallado, S.A., Nguyen, D.N., Fuller, J., Alvarez, R. et al. (2008) A combinatorial library of lipid-like materials for delivery of RNAi therapeutics. Nat. Biotechnol., 26, 561-569. (Pubitemid 351668042)
30. Wilusz, J.E., Freier, S.M. and Spector, D.L. (2008) 30 end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell, 135, 919-932.
31. Donaldson, J.G., Finazzi, D. and Klausner, R.D. (1992) Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature, 360, 350-352. (Pubitemid 23000673)
32. Helms, J.B. and Rothman, J.E. (1992) Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature, 360, 352-354. (Pubitemid 23000674)
33. Neufeld, E.B., Cooney, A.M., Pitha, J., Dawidowicz, E.A., Dwyer, N.K., Pentchev, P.G. and Blanchette-Mackie, E.J. (1996) Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem., 271, 21604-21613. (Pubitemid 26293030)
34. Alberts, A.W., Chen, J., Kuron, G., Hunt, V., Huff, J., Hoffman, C., Rothrock, J., Lopez, M., Joshua, H., Harris, E. et al. (1980) Mevinolin: a highly potent competitive inhibitor of hydroxymethylglutaryl-coenzyme A reductase and a cholesterol-lowering agent. Proc. Natl Acad. Sci. USA, 77, 3957-3961. (Pubitemid 10015499)
35. Kolokoltsov, A.A., Deniger, D., Fleming, E.H., Roberts, N.J. Jr., Karpilow, J.M. and Davey, R.A. (2007) Small interfering RNA profiling reveals key role of clathrin-mediated endocytosis and early endosome formation for infection by respiratory syncytial virus. J. Virol., 81, 7786-7800. (Pubitemid 47047865)
36. Schmid, E.M. and McMahon, H.T. (2007) Integrating molecular and network biology to decode endocytosis. Nature, 448, 883-888. (Pubitemid 47312770)
37. Wieffer, M., Maritzen, T. and Haucke, V. (2009) SnapShot: endocytic trafficking. Cell, 137, 382e381-e383.
38. Frank-Kamenetsky, M., Grefhorst, A., Anderson, N.N., Racie, T.S., Bramlage, B., Akinc, A., Butler, D., Charisse, K., Dorkin, R., Fan, Y. et al. (2008) Therapeutic RNAi targeting PCSK9 acutely lowers plasma cholesterol in rodents and LDL cholesterol in nonhuman primates. Proc. Natl Acad. Sci. USA, 105, 11915-11920.
39. Bennett, C.F., Chiang, M.Y., Chan, H., Shoemaker, J.E. and Mirabelli, C.K. (1992) Cationic lipids enhance cellular uptake and activity of phosphorothioate antisense oligonucleotides. Mol. Pharmacol., 41, 1023-1033. (Pubitemid 23026100)
40. Dean, N.M. and McKay, R. (1994) Inhibition of protein kinase C-alpha expression in mice after systemic administration of phosphorothioate antisense oligodeoxynucleotides. Proc. Natl Acad. Sci. USA, 91, 11762-11766. (Pubitemid 24356425)
41. Butler, M., McKay, R.A., Popoff, I.J., Gaarde, W.A., Witchell, D., Murray, S.F., Dean, N.M., Bhanot, S. and Monia, B.P. (2002) Specific inhibition of PTEN expression reverses hyperglycemia in diabetic mice. Diabetes, 51, 1028-1034. (Pubitemid 34438346)
42. Wahlestedt, C. (1994) Antisense oligonucleotide strategies in neuropharmacology. Trends Pharmacol. Sci., 15, 42-46. (Pubitemid 24053888)
43. Smith, R.A., Miller, T.M., Yamanaka, K., Monia, B.P., Condon, T.P., Hung, G., Lobsiger, C.S., Ward, C.M., McAlonis- Downes, M., Wei, H. et al. (2006) Antisense oligonucleotide therapy for neurodegenerative disease. J. Clin. Invest., 116, 2290-2296. (Pubitemid 44162339)
44. Zhang, H., Cook, J., Nickel, J., Yu, R., Stecker, K., Myers, K. and Dean, N.M. (2000) Reduction of liver Fas expression by an antisense oligonucleotide protects mice from fulminant hepatitis. Nat. Biotechnol., 18, 862-867. (Pubitemid 30640912)
45. Snyers, L., Zwickl, H. and Blaas, D. (2003) Human rhinovirus type 2 is internalized by clathrin-mediated endocytosis. J. Virol., 77, 5360-5369. (Pubitemid 36460950)
46. Khan, A.G., Pickl-Herk, A., Gajdzik, L., Marlovits, T.C., Fuchs, R. and Blaas, D. (2010) Human rhinovirus 14 enters rhabdomyosarcoma cells expressing icam-1 by a clathrin-, caveolin-, and flotillin-independent pathway. J. Virol., 84, 3984-3992.
47. Bayer, N., Schober, D., Huttinger, M., Blaas, D. and Fuchs, R. (2001) Inhibition of clathrin-dependent endocytosis has multiple effects on human rhinovirus serotype 2 cell entry. J. Biol. Chem., 276, 3952-3962.