RNA/aTNA chimeras: RNAi effects and nucleases resistance of single and double stranded RNAs

Molecules

Volumn 19, Issue 11, 2014, Pages 17872-17896

  Alagia, Adele ^a   Terrazas, Montserrat ^a,b   Eritja, Ramon ^a  

^a INSTITUTE OF ADVANCED CHEMISTRY OF CATALONIA IQAC CSIC   (Spain)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

3' exonuclease; 3' overhang chemical modification; 5' exonuclease; ApoB gene; L threoninol; RNAi; Serum resistance; Single stranded siRNA; SiRNA

Indexed keywords

AMINOALCOHOL; BUTANEDIOL; DOUBLE STRANDED RNA; ENDONUCLEASE; RNA; SMALL INTERFERING RNA; THREONINOL;

CHIMERA; HELA CELL LINE; HEPG2 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

AMINO ALCOHOLS; BUTYLENE GLYCOLS; CELL LINE, TUMOR; CHIMERA; ENDONUCLEASES; HELA CELLS; HEP G2 CELLS; HUMANS; RNA; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING;

EID: 84914162482     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules191117872     Document Type: Article

References (58)

1. Paterson, B.M.; Roberts, B.E.; Kuff, E.L. Structural gene identification and mapping by DNA-mRNA hybrid-arrested cell-free translation. Proc. Natl. Acad. Sci. USA 1977, 74, 4370-4374.
2. Fire, A.; Xu, S.; Montgomery, M.K.; Kostas, S.A.; Driver, S.E.; Mello, C.C. Potent and specific genetic interference by double-stranded RNA in caenorhabditis elegans. Nature 1998, 391, 806-811.
3. Elbashir, S.M.; Harborth, J.; Lendeckel, W.; Yalcin, A.; Weber, K.; Tuschl, T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411, 494-498.
4. Rana, T.M. Illuminating the silence: Understanding the structure and function of small RNAs. Nat. Rev. Mol. Cell Biol. 2007, 8, 23-36.
5. Wilson, J.; Doudna, J.A. Molecular Mechanisms of RNA Interference. Ann. Rev. Biophys. 2013, 42, 217-239.
6. Deng, Y.; Wang, C.C.; Choy, K.W.; Du, Q.; Chen, J.; Wang, Q.; Li, L.; Chung, T.K.; Tang, T. Therapeutic potentials of gene silencing by RNA interference: Principles, challenges, and new strategies. Gene 2014, 538, 217-227.
7. Sledz, C.A.; Holko, M.; de Veer, M.J.; Silverman, R.H.; Williams, B.R. Activation of the interferon system by short-interfering RNAs. Nat. Cell Biol. 2003, 5, 834-839.
8. Judge, A.D.; Sood, V.; Shaw, J.R.; Fang, D.; McClintock, K.; MacLachlan, I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 2005, 23, 457-462.
9. Deleavey, G.F.; Damha, M.J. Designing chemically modified oligonucleotides for targeted gene silencing. Chem. Biol. 2012, 8, 937-954.
10. Martinez, J.; Patkaniowska, A.; Urlaub, H.; Lührmann, R.; Tuschl, T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 2002, 110, 563-574.
11. Holen, T.; Amarzguioui, M.; Babaie, E.; Prydz, H. Similar behaviour of single-strand and double-strand siRNAs suggests they act through a common RNAi pathway. Nucl. Acids Res. 2003, 31, 2401-2407.
12. Haringsma, H.J.; Li, J.J.; Soriano, F.; Kenski, D.M.; Flanagan, W.M.; Willingham, A.T. mRNA knockdown by single strand RNA is improved by chemical modifications. Nucl. Acids Res. 2012, 40, 4125-4136.
13. Lima, W.F.; Prakash, T.P.; Murray, H.M.; Kinberger, G.A.; Li, W.; Chappell, A.E.; Li, C.S.; Murray, S.F.; Gaus, H.; Seth, P.P.; et al. Single-stranded siRNAs activate RNAi in animals. Cell 2012, 150, 883-894.
14. Asanuma, H.; Toda, T.; Murayama, K.; Liang, X.; Kashida, H. Unexpectedly stable artificial duplex from flexible acyclic threoninol. J. Am. Chem. Soc. 2010, 132, 14702-14703.
15. Murayama, K.; Tanaka, Y.; Toda, T.; Kashida, H.; Asanuma, H. Highly stable duplex formation by artificial nucleic acids acyclic threoninol nucleic acid (aTNA) and serinol nucleic acid (SNA) with acyclic scaffolds. Chem. Eur. J. 2013, 19, 14151-14158.
16. Li, M.; Meares, C.F. Synthesis, metal chelate stability studies, and enzyme digestion of a peptide-linked DOTA derivative and its corresponding radiolabeled immunoconjugates. Bioconjug. Chem. 1993, 4, 275-283.
17. Bramsen, J.B.; Kjems, J. Development of therapeutic-grade small interfering RNAs by chemical engineering. Front. Genet. 2012, 3, 154.
18. Lima, W.F.; Wu, H.; Nichols, J.G.; Sun, H.; Murray, H.M.; Crooke, S.T. Binding and cleavage specificities of human Argonaute2. J. Biol. Chem. 2009, 284, 26017-26028.
19. Meister, G.; Landthaler, M.; Patkaniowska, A.; Dorsett, Y.; Teng, G.; Tuschl, T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 2004, 15, 185-197.
20. Hong, J.; Huang, Y.; Li, J.; Yi, F.; Zheng, J.; Huang, H.; Wei, N.; Shan, Y.; An, M.; Zhang, H.; et al. Comprehensive analysis of sequence-specific stability of siRNA. FASEB J. 2010, 24, 4844-4855.
21. Choung, S.; Kim, Y.J.; Kim, S.; Park, H.O.; Choi, Y.C. Chemical modification of siRNAs to improve serum stability without loss of efficacy. Biochem. Biophys. Res. Commun. 2006, 342, 919-927.
22. Wojcik, M.; Cieslak, M.; Stec, W.J.; Goding, J.W.; Koziolkiewicz, M. Nucleotide pyrophosphatase/Phosphodiesterase 1 is responsible for degradation of antisense phosphorothioate oligonucleotides. Oligonucleotides 2007, 17, 134-145.
23. Gijsbers, R.; Aoki, J.; Arai, H.; Bollen, M. The hydrolysis of lysophospholipids and nucleotides by autotaxin (NPP2) involves a single catalytic site. FEBS Lett. 2003, 538, 60-64.
24. Linn, S.M.; Lloyd, R.S.; Roberts, R.J. Nucleases; Cold Spring Harbor Laboratory Press: New York, NY, USA, 1993.
25. Volkov, A.A.; Kruglova, N.S.; Meschaninova, M.I.; Venyaminova, A.G.; Zenkova, M.A.; Vlassov, V.V.; Chernolovskaya, E.L. Selective protection of nuclease-sensitive sites in siRNA prolongs silencing effect. Oligonucleotides 2009, 19, 191-202.
26. Bartlett, D.W.; Davis, M.E. Effect of siRNA nuclease stability on the in vitro and in vivo kinetics of siRNA-mediated gene silencing. Biotechnol. Bioeng. 2007, 97, 909-921.
27. Kamiya, Y.; Ito, A.; Ito, H.; Urushihara, M.; Takai, J.; Fujii, T.; Liang, X.; Kashida, H.; Asanuma, H. Selective labeling of mature RISC using a siRNA carrying fluophore-quencher pair. Chem. Sci. 2013, 4, 4016-4021.
28. Braasch, D.A.; Jensen, S.; Liu, Y.; Kaur, K.; Arar, K.; White, M.A.; Corey, D.R. RNA interference in mammalian cells by chemically-modified RNA. Biochemistry 2003, 42, 7967-7975.
29. Hoerter, J.A.; Krishnan, V.; Lionberger, T.A.; Walter, N.G. SiRNA-Like double-stranded RNAs are specifically protected against degradation in human cell extract. PLoS One 2011, 6, e20359.
30. Raemdonck, K.; Remaut, K.; Lucas, B.; Sanders, N.N.; Demeester, J.; de Smedt, S.C. In situ analysis of single-stranded and duplex siRNA integrity in living cells. Biochemistry 2006, 45, 10614-10623.
31. Whitfield, A.J.; Barrett, P.H.; van Bockxmeer, F.M.; Burnett, J.R. Lipid disorders and mutations in the APOB gene. Clin. Chem. 2004, 50, 1725-1732.
32. Pullinger, C.R.; North, J.D.; Teng, B.B.; Rifici, V.A.; Ronhild de Brito, A.E.; Scott, J. The apolipoprotein B gene is constitutively expressed in HepG2 cells: Regulation of secretion by oleic acid, albumin, and insulin, and measurement of the mRNA half-life. J. Lipid Res. 1989, 7, 1065-1077.
33. Aston, N.S.; Watt, N.; Morton, I.E.; Tanner, M.S.; Evans, G.S. Copper toxicity affects proliferation and viability of human hepatoma cells (HepG2 line). Hum. Exp. Toxicol. 2000, 19, 367-376.
34. Der, S.D.; Zhou, A.; Williams, B.R.; Silverman, R.H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 1998, 95, 15623-15628.
35. Jackson, A.L.; Linsley, P.S. Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat. Rev. Drug Discov. 2010, 9, 57-67.
36. Whitehead, K.A.; Dahlman, J.E.; Langer, R.S.; Anderson, D.G. Silencing or stimulation? SiRNA delivery and the immune system. Annu. Rev. Chem. Biomol. Eng. 2011, 2, 77-96.
37. Robbins, M.; Judge, A.; MacLachlan, I. SiRNA and innate immunity. Oligonucleotides 2009, 19, 89-102.
38. Sioud, M. Induction of inflammatory cytokines and interferon responses by double-stranded and single-stranded siRNAs is sequence-dependent and requires endosomal localization. J. Mol. Biol. 2005, 348, 1079-1090.
39. Reyes-Darias, J.A.; Berzal-Herranz, A. Detection of immune response activation by exogenous nucleic acids by a multiplex RT-PCR method. Mol. Cell. Probes 2014, 28, 181-185.
40. Sioud, M. Single-stranded small interfering RNA are more immunostimulatory than their double-stranded counterparts: A central role for 2′-hydroxyl uridines in immune responses. Eur. J. Immunol. 2006, 36, 1222-1230.
41. Schroecksnadel, S.; Jenny, M.; Fuchs, D. Myelomonocytic THP-1 cells for in vitro testing of immunomodulatory properties of nanoparticles. J. Biomed. Nanotechnol. 2011, 7, 209-210.
42. Bartok, E.; Bauernfeind, F.; Khaminets, M.G.; Jakobs, C.; Monks, B.; Fitzgerald, K.A.; Latz, E.; Hornung, V. iGLuc: A luciferase-based inflammasome and protease activity reporter. Nat. Methods 2013, 10, 147-154.
43. Villalobos, X.; Rodríguez, L.; Prévot, J.; Oleaga, C.; Ciudad, C.J.; Noé, V. Stability and immunogenicity properties of the gene-silencing polypurine reverse Hoogsteen hairpins. Mol. Pharm. 2014, 11, 254-264.
44. Terrazas, M.; Alagia, A.; Faustino, I.; Orozco, M.; Eritja R. Functionalization of the 3'-ends of DNA and RNA strands with N-ethyl-N-coupled nucleosides: A promising approach to avoid 3'-exonuclease-catalyzed hydrolysis of therapeutic oligonucleotides. ChemBioChem 2013, 14, 510-520.
45. Vaish, N.; Chen, F.; Seth, S.; Fosnaugh, K.; Liu, Y.; Adami, R.; Brown, T.; Chen, Y.; Harvie, P.; Johns, R.; et al. Improved specificity of gene silencing by siRNAs containing unlocked nucleobase analogs. Nucl. Acids Res. 2011, 39, 1823-1832.
46. O'Carroll, D.; Mecklenbrauker, I.; Das, P.P.; Santana, A.; Koenig, U.; Enright, A.J.; Miska, E.A.; Tarakhovsky, A. A Slicer-independent role for Argonaute 2 in hematopoiesis and the microRNA pathway. Genes Dev . 2007, 21, 1999-2004.
47. Waaler, J.; Machon, O.; von Kries, J.P.; Wilson, S.R.; Lundenes, E.; Wedlich, D.; Gradl, D.; Paulsen, J.E.; Machonova, O.; Dembinski, J.L.; et al. Novel synthetic antagonists of canonical Wnt signaling inhibit colorectal cancer cell growth. Cancer Res. 2011, 71, 197-205.
48. Grijalvo, S.; Alagia, A.; Puras, G.; Zárate, J.; Pedraz, J.L.; Eritja, R. Cationic vesicles based on non-ionic surfactant and synthetic aminolipids mediate delivery of antisense oligonucleotides into mammalian cells. Colloids Surf. B 2014, 119, 30-37.
49. Rajan, J.V.; Warren, S.E.; Miao, E.A.; Aderem, A. Activation of the NLRP3 inflammasome by intracellular poly I:C. FEBS Lett. 2010, 584, 4627-4632.
50. NIH/NCBI/Primer-BLAST. http://www.ncbi.nlm.nih.gov/tools/primer-blast/ (accessed on 3 November 2014).
51. Somoza, A.; Terrazas, M.; Eritja, R. Modified siRNAs for the study of the paz domain. Chem. Commun. 2010, 46, 4270-4272.
52. Potenza, N.; Moggio, L.; Milano, G.; Salvatore, V.; di Blasio, B.; Russo, A.; Messere, A. RNA interference in mammalia cells by RNA-3'-PNA chimeras. Int. J. Mol. Sci. 2008, 9, 299-315.
53. Ittig, D.; Luisier, S.; Weiler, J.; Schümperli, D.; Leumann, C.J. Improving gene silencing of siRNAs via tricyclo-DNA modification. Artif. DNA PNA XNA 2010, 1, 9-16.
54. Ueno, Y.; Watanabe, Y.; Shibata, A.; Yoshikawa, K.; Takano, T.; Kohara, M.; Kitade, Y. Synthesis of nuclease-resistant siRNAs possessing universal overhangs. Bioorg. Med. Chem. 2009, 17, 1974-1981.
55. Gaglione, M.; Potenza, N.; di Fabio, G.; Romanucci, V.; Mosca, N.; Russo, A.; Novellino, E.; Cosconati, S.; Messere, A. Tuning RNA interference by enhancing siRNA/PAZ recognition. ACS Med. Chem. Lett. 2013, 4, 75-78.
56. Ueno, Y.; Inoue, T.; Yoshida, M.; Yoshikawa, K.; Shibata, A.; Kitamura, Y.; Kitade, Y. Synthesis of nuclease-resistant siRNAs possessing benzene-phosphate backbones in their 3'-overhang regions. Bioorg. Med. Chem. Lett. 2008, 18, 5194-5196.
57. Lingel, A.; Simon, B.; Izaurralde, E.; Sattler, M. Nucleic acid 3'-end recognition by the Argonaute2 PAZ domain. Nat. Struct. Mol. Biol. 2004, 11, 576-577.
58. Wang, Y.; Juranek, S.; Li, H.; Sheng, G.; Wardle, G.S.; Tuschl, T.; Patel, D.J. Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 2009, 461, 754-761.