Hsp90 protein interacts with phosphorothioate oligonucleotides containing hydrophobic 2′-modifications and enhances antisense activity

Nucleic Acids Research

Volumn 44, Issue 8, 2016, Pages 3892-3907

  Liang, Xue Hai ^a   Shen, Wen ^a   Sun, Hong ^a   Kinberger, Garth A ^a   Prakash, Thazha P ^a   Nichols, Joshua G ^a   Crooke, Stanley T ^a  

^a ISIS PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CHAPERONIN CONTAINING TCP1; ETHYL BICYCLIC NUCLEIC ACID; HEAT SHOCK PROTEIN 90; KU ANTIGEN; LOCKED NUCLEIC ACID; NUCLEIC ACID; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; PHOSPHOROTHIOIC ACID; UNCLASSIFIED DRUG; OLIGONUCLEOTIDE; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; CHEMICAL MODIFICATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN NUCLEIC ACID INTERACTION; STRUCTURE ACTIVITY RELATION; CELL LINE; CHEMICAL PHENOMENA; CHEMISTRY; HELA CELL LINE; METABOLISM;

CELL LINE; HELA CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; OLIGONUCLEOTIDES; OLIGONUCLEOTIDES, ANTISENSE; PHOSPHOROTHIOATE OLIGONUCLEOTIDES; PROTEIN BINDING; PROTEIN DOMAINS;

EID: 84966269313     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw144     Document Type: Article

References (43)

1. Crooke,S.T., Vickers,T.A., Lima,W.F. and Wu,H.-J. (2008) In: Crooke,ST (ed). Antisense Drug Technology - Principles, Strategies, and Applications. 2nd edn. CRC Press, Boca Raton, pp. 3-46.
2. Kurreck,J. (2009) RNA interference: from basic research to therapeutic applications. Angew Chem. Int. Ed. Engl., 48, 1378-1398.
3. Dias,N. and Stein,C.A. (2002) Antisense oligonucleotides: basic concepts and mechanisms. Mol. Canc. Therap., 1, 347-355.
4. Swayze,E.E. and Bhat,B. (2008) In: Crooke,ST (ed). Antisense Drug Technology - Principles, Strategies, and Applications. 2nd edn. CRC Press, Boca Raton, pp. 143-182.
5. Kurreck,J. (2003) Antisense technologies. Improvement through novel chemical modifications. Europ. J. Biochem./FEBS, 270, 1628-1644.
6. Bennett,C.F. and Swayze,E.E. (2010) RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Annu. Rev. Pharmac. Toxicol., 50, 259-293.
7. Geary,R.S. (2009) Antisense oligonucleotide pharmacokinetics and metabolism. Expert Opin. Drug Metab. Toxicol., 5, 381-391.
8. Juliano,R.L., Carver,K., Cao,C. and Ming,X. (2013) Receptors, endocytosis, and trafficking: the biological basis of targeted delivery of antisense and siRNA oligonucleotides. J. Drug Targeting, 21, 27-43.
9. Juliano,R.L., Ming,X. and Nakagawa,O. (2012) Cellular uptake and intracellular trafficking of antisense and siRNA oligonucleotides. Bioconjugate Chem., 23, 147-157.
10. Koller,E., Vincent,T.M., Chappell,A., De,S., Manoharan,M. and Bennett,C.F. (2011) Mechanisms of single-stranded phosphorothioate modified antisense oligonucleotide accumulation in hepatocytes. Nucleic Acids Res., 39, 4795-4807.
11. Simoes-Wust,A.P., Hopkins-Donaldson,S., Sigrist,B., Belyanskaya,L., Stahel,R.A. and Zangemeister-Wittke,U. (2004) A functionally improved locked nucleic acid antisense oligonucleotide inhibits Bcl-2 and Bcl-xL expression and facilitates tumor cell apoptosis. Oligonucleotides, 14, 199-209.
12. Murray,S., Ittig,D., Koller,E., Berdeja,A., Chappell,A., Prakash,T.P., Norrbom,M., Swayze,E.E., Leumann,C.J. and Seth,P.P. (2012) TricycloDNA-modified oligo-2′-deoxyribonucleotides reduce scavenger receptor B1 mRNA in hepatic and extra-hepatic tissues-a comparative study of oligonucleotide length, design and chemistry. Nucleic Acids Res., 40, 6135-6143.
13. Seth,P.P., Siwkowski,A., Allerson,C.R., Vasquez,G., Lee,S., Prakash,T.P., Kinberger,G., Migawa,M.T., Gaus,H., Bhat,B. et al. (2008) Design, synthesis and evaluation of constrained methoxyethyl (cMOE) and constrained ethyl (cEt) nucleoside analogs. Nucleic Acids Symposium Series, 52, 553-554.
14. 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.
15. Stanton,R., Sciabola,S., Salatto,C., Weng,Y., Moshinsky,D., Little,J., Walters,E., Kreeger,J., DiMattia,D., Chen,T. et al. (2012) Chemical modification study of antisense gapmers. Nucleic Acid Ther., 22, 344-359.
16. Kurreck,J., Wyszko,E., Gillen,C. and Erdmann,V.A. (2002) Design of antisense oligonucleotides stabilized by locked nucleic acids. Nucleic Acids Res., 30, 1911-1918.
17. Brown,D.A., Kang,S.H., Gryaznov,S.M., DeDionisio,L., Heidenreich,O., Sullivan,S., Xu,X. and Nerenberg,M.I. (1994) Effect of phosphorothioate modification of oligodeoxynucleotides on specific protein binding. J. Biol. Chem., 269, 26801-26805.
18. Weidner,D.A., Valdez,B.C., Henning,D., Greenberg,S. and Busch,H. (1995) Phosphorothioate oligonucleotides bind in a non sequence-specific manner to the nucleolar protein C23/nucleolin. FEBS Lett., 366, 146-150.
19. Abdul-Manan,N. and Williams,K.R. (1996) hnRNP A1 binds promiscuously to oligoribonucleotides: utilization of random and homo-oligonucleotides to discriminate sequence from base-specific binding. Nucleic Acids Res., 24, 4063-4070.
20. Eckstein,F. (2000) Phosphorothioate oligodeoxynucleotides: what is their origin and what is unique about them? Antisense Nucleic Acid Drug Dev., 10, 117-121.
21. Liang,X.H., Sun,H., Shen,W. and Crooke,S.T. (2015) Identification and characterization of intracellular proteins that bind oligonucleotides with phosphorothioate linkages. Nucleic Acids Res., 43, 2927-2945.
22. Liang,X.H., Shen,W., Sun,H., Prakash,T.P. and Crooke,S.T. (2014) TCP1 complex proteins interact with phosphorothioate oligonucleotides and can co-localize in oligonucleotide-induced nuclear bodies in mammalian cells. Nucleic Acids Res., 42, 7819-7832.
23. Shen,W., Liang,X.H. and Crooke,S.T. (2014) Phosphorothioate oligonucleotides can displace NEAT1 RNA and form nuclear paraspeckle-like structures. Nucleic Acids Res., 42, 8648-8662.
24. Shen,W., Liang,X.H., Sun,H. and Crooke,S.T. (2015) 2′ -Fluoro-modified phosphorothioate oligonucleotide can cause rapid degradation of P54nrb and PSF. Nucleic Acids Res., 43, 4569-4578.
25. Vickers,T.A. and Crooke,S.T. (2014) Antisense oligonucleotides capable of promoting specific target mRNA reduction via competing RNase H1-dependent and independent mechanisms. PLOS One, 9, e108625.
26. Liang,X.H. and Crooke,S.T. (2011) Depletion of key protein components of the RISC pathway impairs pre-ribosomal RNA processing. Nucleic Acids Res., 39, 4875-4889.
27. Jin,S. and Weaver,D.T. (1997) Double-strand break repair by Ku70 requires heterodimerization with Ku80 and DNA binding functions. EMBO J., 16, 6874-6885.
28. Taipale,M., Jarosz,D.F. and Lindquist,S. (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol., 11, 515-528.
29. Li,J., Soroka,J. and Buchner,J. (2012) The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochim. Biophys. Acta, 1823, 624-635.
30. Jackson,S.E. (2013) Hsp90: structure and function. Topics Curr. Chem., 328, 155-240.
31. Sreedhar,A.S., Kalmar,E., Csermely,P. and Shen,Y.F. (2004) Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett., 562, 11-15.
32. Liang,X.H., Hart,C.E. and Crooke,S.T. (2013) Transfection of siRNAs can alter miRNA levels and trigger non-specific protein degradation in mammalian cells. Biochim. Biophys. Acta, 1829, 455-468.
33. Liang,X.H. and Crooke,S.T. (2013) RNA helicase A is not required for RISC activity. Biochim. Biophys. Acta, 1829, 1092-1101.
34. Krieg,A.M. and Stein,C.A. (1995) Phosphorothioate oligodeoxynucleotides: antisense or anti-protein? Antisense Res. Dev., 5, 241.
35. Stein,C.A., Tonkinson,J.L., Zhang,L.M., Yakubov,L., Gervasoni,J., Taub,R. and Rotenberg,S.A. (1993) Dynamics of the internalization of phosphodiester oligodeoxynucleotides in HL60 cells. Biochem., 32, 4855-4861.
36. Watanabe,T.A., Geary,R.S. and Levin,A.A. (2006) Plasma protein binding of an antisense oligonucleotide targeting human ICAM-1 (ISIS 2302). Oligonucleotides, 16, 169-180.
37. Bennett,C.F. (2006) In:Crooke,ST (ed). Antisense Drug Technology - Principles, Strategies, and Applications. CRC Press, Boca Raton, pp. 273-304.
38. 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 2′-O-(2-methoxyethyl)-RNA. Nat. Struc. Biol., 6, 535-539.
39. Pallan,P.S., Allerson,C.R., Berdeja,A., Seth,P.P., Swayze,E.E., Prakash,T.P. and Egli,M. (2012) Structure and nuclease resistance of 2′,4′-constrained 2′-O-methoxyethyl (cMOE) and 2′-O-ethyl (cEt) modified DNAs. Chem. Commun., 48, 8195-8197.
40. Huang,Y.W., Hu,C.C., Liou,M.R., Chang,B.Y., Tsai,C.H., Meng,M., Lin,N.S. and Hsu,Y.H. (2012) Hsp90 interacts specifically with viral RNA and differentially regulates replication initiation of Bamboo mosaic virus and associated satellite RNA. PLOS Pathog., 8, e1002726.
41. Xu,Z., Horwich,A.L. and Sigler,P.B. (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature, 388, 741-750.
42. Vashist,S., Urena,L., Gonzalez-Hernandez,M.B., Choi,J., de Rougemont,A., Rocha-Pereira,J., Neyts,J., Hwang,S., Wobus,C.E. and Goodfellow,I. (2015) Molecular chaperone Hsp90 is a therapeutic target for noroviruses. J. Virol., 89, 6352-6363.
43. Naito,T., Momose,F., Kawaguchi,A. and Nagata,K. (2007) Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J. Virol., 81, 1339-1349.