Phenylpyrrolocytosine as an unobtrusive base modification for monitoring activity and cellular trafficking of siRNA

ACS Chemical Biology

Volumn 6, Issue 9, 2011, Pages 912-919

  Wahba, Alexander S ^a   Azizi, Fereshteh ^a   Deleavey, Glen F ^a   Brown, Claire ^a   Robert, Francis ^c   Carrier, Marilyn ^c   Kalota, Anna ^d   Gewirtz, Alan M ^d   Pelletier, Jerry ^c   Hudson, Robert H E ^b   Damha, Masad J ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE DERIVATIVE; PHENYLPYRROLOCYTOSINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL TRANSPORT; CHEMICAL MODIFICATION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GENE SILENCING; HELA CELL; HUMAN; HUMAN CELL; MELTING POINT; MOLECULAR PROBE; PRIORITY JOURNAL; THERMOSTABILITY;

EID: 80053595546     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200070k     Document Type: Article

References (51)

1. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans Nature 391, 806-811 (Pubitemid 28099681)
2. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells Nature 411, 494-498 (Pubitemid 32494397)
3. Watts, J. K. and Corey, D. R. (2010) Clinical status of duplex RNA Bioorg. Med. Chem. Lett. 20, 3203-3207
4. Schmidt, C. (2011) RNAi momentum fizzles as pharma shifts priorities Nat. Biotechnol. 29, 93-94
5. Chiu, Y. L., Ali, A., Chu, C. Y., Cao, H., and Rana, T. M. (2004) Visualizing a correlation between siRNA localization, cellular uptake, and RNAi in living cells Chem. Biol. 11, 1165-1175 (Pubitemid 39138769)
6. Berezhna, S. Y., Supekova, L., Supev, F., Schultz, P. G., and Deniz, A. A. (2006) siRNA in human cells selectively localizes to target RNA sites Proc. Natl. Acad. Sci. U.S.A. 103, 7682-7687
7. Ohrt, T., Merkle, D., Birkenfeld, K., Echeverri, C. J., and Schwille, P. (2006) In situ fluorescence analysis demonstrates active siRNA exclusion from the nucleus by Exportin 5 Nucleic Acids Res. 34, 1369-1380
8. Jarve, A., Muller, J., Kim, I. H., Rohr, K., MacLean, C., Fricker, G., Massing, U., Eberle, F., Dalpke, A., Fischer, R., Trendelenburg, M. F., and Helm, M. (2007) Surveillance of siRNA integrity by FRET imaging Nucleic Acids Res. 35, e124
9. Portis, A. M., Carballo, G., Baker, G. L., Chan, C., and Walton, S. P. (2010) Confocal microscopy for the analysis of siRNA delivery by polymeric nanoparticles Microsc. Res. Tech. 73, 878-885
10. Ohrt, T., Muetze, J., Staroske, W., Weinmann, L., Hock, J., Crell, K., Meister, G., and Schwille, P. (2008) Fluorescence correlation spectroscopy and fluorescence cross-correlation spectroscopy reveal the cytoplasmic origination of loaded nuclear RISC in vivo in human cells Nucleic Acids Res. 36, 6439-6449
11. Zimmermann, T. S., Lee, A. C. H., Akinc, A., Bramlage, B., Bumcrot, D., Fedoruk, M. N., Harborth, J., Heyes, J. A., Jeffs, L. B., John, M., Judge, A. D., Lam, K., McClintock, K., Nechev, L. V., Palmer, L. R., Racie, T., Rohl, I., Seiffert, S., Shanmugam, S., Sood, V., Soutschek, J., Toudjarska, I., Wheat, A. J., Yaworski, E., Zedalis, W., Koteliansky, V., Manoharan, M., Vornlocher, H. P., and MacLachlan, I. (2006) RNAi-mediated gene silencing in non-human primates Nature 441, 111-114
12. Rist, M. J. and Marino, J. P. (2002) Fluorescent nucleotide base analogs as probes of nucleic acid structure, dynamics and interactions Curr. Org. Chem. 6, 775-793 (Pubitemid 34752183)
13. Sinkeldam, R. W., Greco, N. J., and Tor, Y. (2010) Fluorescent analogs of biomolecular building blocks: Design, properties, and applications Chem. Rev. 110, 2579-2619
14. Dodd, D. W. and Hudson, R. H. E. (2009) Intrinsically fluorescent base-discriminating nucleoside analogs Mini Rev. Org. Chem. 6, 378-391
15. Wahba, A. S., Esmaeili, A., Damha, M. J., and Hudson, R. H. E. (2010) A single-label phenylpyrrolocytidine provides a molecular beacon-like response reporting HIV-1 RT RNase H activity Nucleic Acids Res. 38, 1048-1056
16. Hua, J. X., Dodd, D. W., Hudson, R. H. E., and Corey, D. R. (2009) Cellular localization and allele-selective inhibition of mutant huntingtin protein by peptide nucleic acid oligomers containing the fluorescent nucleobase [bis-o-(aminoethoxy)phenyl]pyrrolocytosine Bioorg. Med. Chem. Lett. 19, 6181-6184
17. Wojciechowski, F. and Hudson, R. H. E. (2008) Fluorescence and hybridization properties of peptide nucleic acid containing a substituted phenylpyrrolocytosine designed to engage guanine with an additional H-bond J. Am. Chem. Soc. 130, 12574-12575
18. Hudson, R. H. E. and Ghorbani-Choghamarani, A. (2007) Selective fluorometric detection of guanosine-containing sequences by 6- phenylpyrrolocytidine in DNA Synlett 870-873 (Pubitemid 46603613)
19. Wahba, A. S., Damha, M. J., and Hudson, R. H. E. (2008) RNA containing pyrrolocytidine base analogs: Good binding affinity and fluorescence that responds to hybridization Nucleic Acids Symp. Ser. 52, 399-400
20. de Fougerolles, A., Vornlocher, H. P., Maraganore, J., and Lieberman, J. (2007) Interfering with disease: A progress report on siRNA-based therapeutics Nat. Rev. Drug Discovery 6, 443-453 (Pubitemid 47064567)
21. Watts, J. K., Deleavey, G. F., and Damha, M. J. (2008) Chemically modified siRNA: Tools and applications Drug Discov Today 13, 842-855
22. Parrish, S., Fleenor, J., Xu, S. Q., Mello, C., and Fire, A. (2000) Functional anatomy of a dsRNA trigger: Differential requirement for the two trigger strands in RNA interference Mol. Cell 6, 1077-1087
23. Chiu, Y. L. and Rana, T. M. (2003) siRNA function in RNAi: A chemical modification analysis RNA 9, 1034-1048 (Pubitemid 37093614)
24. Khvorova, A., Reynolds, A., and Jayasena, S. D. (2003) Functional siRNAs and miRNAs exhibit strand bias Cell 115, 209-216 (Pubitemid 37329584)
25. Schwarz, D. S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., and Zamore, P. D. (2003) Asymmetry in the assembly of the RNAi enzyme complex Cell 115, 199-208 (Pubitemid 37329583)
26. Sipa, K., Sochacka, E., Kazmierczak-Baranska, J., Maszewska, M., Janicka, M., Nowak, G., and Nawrot, B. (2007) Effect of base modifications on structure, thermodynamic stability, and gene silencing activity of short interfering RNA RNA 13, 1301-1316 (Pubitemid 47080475)
27. Terrazas, M. and Kool, E. T. (2009) RNA major groove modifications improve siRNA stability and biological activity Nucleic Acids Res. 37, 346-353
28. Somoza, A., Chelliserrykattil, J., and Kool, E. T. (2006) The roles of hydrogen bonding and sterics in RNA interference Angew. Chem., Int. Ed. 45, 4994-4997 (Pubitemid 44166139)
29. Somoza, A., Silverman, A. P., Miller, R. M., Chelliserrykattil, J., and Kool, E. T. (2008) Steric effects in RNA interference: Probing the influence of nucleobase size and shape Chem.-Eur. J. 14, 7978-7987
30. Xia, J., Noronha, A., Toudjarska, I., Li, F., Akinc, A., Braich, R., Frank-Kamenetsky, M., Rajeev, K. G., Egli, M., and Manoharan, M. (2006) Gene sitencing activity of siRNAs with a ribo-difluorotoluyl nucteotide ACS Chem. Biol. 1, 176-183
31. Peacock, H., Fostvedt, E., and Beal, P. A. (2010) Minor-groove-modulating adenosine replacements control protein binding and RNAi activity in siRNAs ACS Chem. Biol. 5, 1115-1124
32. Dowler, T., Bergeron, D., Tedeschi, A.-L., Paquet, L., Ferrari, N., and Damha, M. J. (2006) Improvements in siRNA properties mediated by 2′-deoxy-2′-fluoro-β- d -arabinonucleic acid (FANA) Nucleic Acids Res. 34, 1669-1675
33. Watts, J. K., Choubdar, N., Sadalapure, K., Robert, F., Wahba, A. S., Pelletier, J., Pinto, B. M., and Damha, M. J. (2007) 2′-Fluoro-4′- thioarabino-modified oligonucleotides: Conformational switches linked to siRNA activity Nucleic Acids Res. 35, 1441-1451 (Pubitemid 46592867)
34. Deleavey, G. F., Watts, J. K., Alain, T., Robert, F., Kalota, A., Aishwarya, V., Pelletier, J., Gewirtz, A. M., Sonenberg, N., and Damha, M. J. (2010) Synergistic effects between analogs of DNA and RNA improve the potency of siRNA-mediated gene silencing Nucleic Acids Res. 38, 4547-4557
35. Seidel, C. A. M., Schulz, A., and Sauer, M. H. M. (1996) Nucleobase-specific quenching of fluorescent dyes 0.1. Nucleobase one-electron redox potentials and their correlation with static and dynamic quenching efficiencies J. Phys. Chem. 100, 5541-5553 (Pubitemid 126790528)
36. Lewis, F. D., Wu, T. F., Zhang, Y. F., Letsinger, R. L., Greenfield, S. R., and Wasielewski, M. R. (1997) Distance-dependent electron transfer in DNA hairpins Science 277, 673-676 (Pubitemid 27373910)
37. Frank, F., Sonenberg, N., and Nagar, B. (2010) Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2 Nature 465, 818-822
38. Alexopoulou, L., Holt, A. C., Medzhitov, R., and Flavell, R. A. (2001) Recognition of double-stranded RNA and activation of NF-kappa B by Toll-like receptor 3 Nature 413, 732-738 (Pubitemid 33009951)
39. Kleinman, M. E., Yamada, K., Takeda, A., Chandrasekaran, V., Nozaki, M., Baffi, J. Z., Albuquerque, R. J. C., Yamasaki, S., Itaya, M., Pan, Y. Z., Appukuttan, B., Gibbs, D., Yang, Z. L., Kariko, K., Ambati, B. K., Wilgus, T. A., DiPietro, L. A., Sakurai, E., Zhang, K., Smith, J. R., Taylor, E. W., and Ambati, J. (2008) Sequence- and target-independent angiogenesis suppression by siRNA via TLR3 Nature 452, 591-U591
40. Robbins, M., Judge, A., and MacLachlan, I. (2009) siRNA and Innate Immunity Oligonucleotides 19, 89-101
41. Kariko, K., Buckstein, M., Ni, H. P., and Weissman, D. (2005) Suppression of RNA recognition by Toll-like receptors: The impact of nucleoside modification and the evolutionary origin of RNA Immunity 23, 165-175 (Pubitemid 41169286)
42. Eberle, F., Giessler, K., Deck, C., Heeg, K., Peter, M., Richert, C., and Dalpke, A. H. (2008) Modifications in small interfering RNA that separate immunostimulation from RNA interference J. Immunol. 180, 3229-3237
43. Duysens, L. N. M. and Amesz, J. (1957) Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the near-ultraviolet and visible region Biochim. Biophys. Acta 24, 19-26
44. Holen, T., Amarzguioui, M., Wiiger, M. T., Babaie, E., and Prydz, H. (2002) Positional effects of short interfering RNAs targeting the human coagulation trigger tissue factor Nucleic Acids Res. 30, 1757-1766 (Pubitemid 34679753)
45. Frigault, M. M., Lacoste, J., Swift, J. L., and Brown, C. M. (2009) Live-cell microscopy-tips and tools J. Cell Sci. 122, 753-767
46. Chiu, Y. L. and Rana, T. M. (2002) RNAi in human cells: Basic structural and functional features of small interfering RNA Mol. Cell 10, 549-561 (Pubitemid 35284173)
47. Stein, C. A., Hansen, J. B., Lai, J., Wu, S., Voskresenskiy, A., Hog, A., Worm, J., Hedtjarn, M., Souleimanian, N., Miller, P., Soifer, H. S., Castanotto, D., Benimetskaya, L., Orum, H., and Koch, T. (2010) Efficient gene silencing by delivery of locked nucleic acid antisense oligonucleotides, unassisted by transfection reagents Nucleic Acids Res. 38, e3
48. Wolf, B., Lesnaw, J. A., and Reichman., Me. (1970) A mechanism of irreversible inactivation of bovine pancreatic ribonuclease by diethylpyrocarbonate-a general reaction of diethylpyrocarbonate with proteins Eur. J. Biochem. 13, 519-525
49. Bellon, L. (2001) Oligoribonucleotides with 2′- O -(tert -butyldimethylsilyl) groups, in Curr. Protoc. Nucleic Acid Chem. (Beaucage, S. L., Herdewijn, P., and Matsuda, A., Eds.) Unit 3.6, pp 1-8, John Wiley & Sons, New York.
50. Novac, O., Guenier, A.-S., and Pelletier, J. (2004) Inhibitors of protein synthesis identified by a high throughput multiplexed translation screen Nucleic Acids Res. 32, 902-915 (Pubitemid 38854693)
51. Pillai, R. S., Bhattacharyya, S. N., Artus, C. G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E., and Filipowicz, W. (2005) Inhibition of translational initiation by Let-7 MicroRNA in human cells Science 309, 1573-1576 (Pubitemid 41266485)