Efficient HIV-1 inhibition by a 16 nt-long RNA aptamer designed by combining in vitro selection and in silico optimisation strategies

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Sánchez Luque, Francisco J ^a,b   Stich, Michael ^c   Manrubia, Susanna ^c   Briones, Carlos ^c,d,e   Berzal Herranz, Alfredo ^a,b  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c CENTRO DE ASTROBIOLOGÍA CSIC INTA   (Spain)

^d ASTON UNIVERSITY   (United Kingdom)

^e INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

5' UNTRANSLATED REGION; APTAMER; VIRUS RNA;

5' UNTRANSLATED REGION; CELL LINE; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT; VIRUS GENOME; VIRUS REPLICATION;

5' UNTRANSLATED REGIONS; APTAMERS, NUCLEOTIDE; BASE SEQUENCE; CELL LINE; GENOME, VIRAL; HEK293 CELLS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; RNA, VIRAL; SEQUENCE ALIGNMENT; VIRUS REPLICATION;

EID: 84906861535     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06242     Document Type: Article

References (60)

1. Berkhout, B. Structure and function of the human immunodeficiency virus leader RNA. Prog Nucleic Acid Res Mol Biol. 54, 1-34 (1996).
2. Berkhout, B. HIV-1 as RNA evolution machine. RNA Biol. 8, 225-229 (2011).
3. Bannwarth, S. & Gatignol, A. HIV-1 TAR RNA: the target of molecular interactions between the virus and its host. Current HIV Res. 3, 61-71 (2005). (Pubitemid 40081286)
4. Zarudnaya, M. I., Potyahaylo, A. L., Kolomiets, I. M. & Hovorun, D. Structural model of the complete poly(A) region of HIV-1 pre-mRNA. J Biomol Struct & Dyn 31, 1044-1056 (2012).
5. Sleiman, D. et al. Initiation of HIV-1 reverse transcription and functional role of nucleocapsid-mediated tRNA/viral genome interactions. Virus Res. 169, 324-339 (2012).
6. Ulyanov, N. B. et al. NMR structure of the full-length linear dimer of stem-loop-1 RNA in the HIV-1 dimer initiation site. J Biol Chem 281, 16168-16177 (2006). (Pubitemid 43848512)
7. Harrison, G. P. & Lever, A. M. The human immunodeficiency virus type 1 packaging signal andmajor splice donor region have a conserved stable secondary structure. J Virol 66, 4144-4153 (1992).
8. Clever, J. L., Miranda, D. Jr. & Parslow, T. G. RNA structure and packaging signals in the 59 leader region of the human immunodeficiency virus type 1 genome. J Virol 76, 12381-12387 (2002). (Pubitemid 35304340)
9. Huthoff, H. & Berkhout, B. Two alternating structures of the HIV-1 leader RNA. RNA (New York, N. Y 7, 143-157 (2001).
10. Allen, P., Worland, S. & Gold, L. Isolation of high-affinity RNA ligands to HIV-1 integrase from a random pool. Virology 209, 327-336 (1995).
11. Barroso-DelJesus, A. et al. Inhibition of HIV-1 replication by an improved hairpin ribozyme that includes an RNA decoy. RNA Biol. 2, 75-79 (2005).
12. Duconge, F. & Toulme, J. J. In vitro selection identifies key determinants for looploop interactions: RNA aptamers selective for the TAR RNA element of HIV-1. RNA (New York, N. Y 5, 1605-1614 (1999).
13. Kim, S. J., Kim, M. Y., Lee, J. H., You, J. C. & Jeong, S. Selection and stabilization of the RNA aptamers against the human immunodeficiency virus type-1 nucleocapsid protein. Biochem Biophys Res Commun. 291, 925-931 (2002). (Pubitemid 34694364)
14. Puerta-Fernandez, E. et al. Inhibition of HIV-1 replication by RNA targeted against the LTR region. AIDS (London, England) 19, 863-870 (2005).
15. Tuerk, C., MacDougal, S. & Gold, L. RNA pseudoknots that inhibit human immunodeficiency virus type 1 reverse transcriptase. Proc Natl Acad Sci USA 89, 6988-6992 (1992).
16. Reyes-Darias, J. A., Sanchez-Luque, F. J. & Berzal-Herranz, A. Inhibition of HIV-1 replication by RNA-based strategies. Current HIV Res. 6, 500-514 (2008).
17. Cheng, C. et al. Potent inhibition of human influenza H5N1 virus by oligonucleotides derived by SELEX. Biochem Biophys Res Commun. 366, 670-674 (2008).
18. Kumar, P. K. et al. Isolation of RNA aptamers specific to the NS3 protein of hepatitis C virus from a pool of completely random RNA. Virology 237, 270-282 (1997). (Pubitemid 27489266)
19. Romero-Lopez, C., Berzal-Herranz, B., Gomez, J. & Berzal-Herranz, A. An engineered inhibitor RNA that efficiently interferes with hepatitis C virus translation and replication. Antiviral Res 94, 131-138 (2012).
20. Romero-Lopez, C., Diaz-Gonzalez, R. & Berzal-Herranz, A. Inhibition of hepatitis C virus internal ribosome entry site-mediated translation by an RNA targeting the conserved IIIf domain. Cell Mol Life Sci 64, 2994-3006 (2007). (Pubitemid 351152253)
21. Ellington, A. D. & Szostak, J. W. In vitro selection of RNA molecules that bind specific ligands. Nature 346, 818-822 (1990).
22. Tuerk, C. & Gold, L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science (New York, N. Y 249, 505-510 (1990).
23. Cerchia, L. & de Franciscis, V. Targeting cancer cells with nucleic acid aptamers. Trends Biotech. 28, 517-525 (2010).
24. Marton, S., Reyes-Darias, J. A., Sanchez-Luque, F. J., Romero-Lopez, C. & Berzal- Herranz, A. In vitro and ex vivo selection procedures for identifying potentially therapeutic DNA and RNA molecules. Molecules (Basel, Switzerland) 15, 4610-4638 (2010).
25. Wang, P. et al. Aptamers as therapeutics in cardiovascular diseases. Current Med Chem 18, 4169-4174 (2011).
26. Berezhnoy, A. et al. Isolation and optimization of murine IL-10 receptor blocking oligonucleotide aptamers using high-throughput sequencing. Mol Ther 20, 1242-1250 (2012).
27. Shigdar, S. et al. RNA aptamers targeting cancer stem cell marker CD133. Cancer Lett 330, 84-95 (2013).
28. Chushak, Y. & Stone, M. O. In silico selection of RNA aptamers. Nucleic Acids Res 37, e87 (2009).
29. Hoon, S., Zhou, B., Janda, K. D., Brenner, S. & Scolnick, J. Aptamer selection by high-throughput sequencing and informatic analysis. BioTechniques 51, 413-416 (2011).
30. Thiel, W. H. et al. Rapid identification of cell-specific, internalizing RNAaptamers with bioinformatics analyses of a cell-based aptamer selection. PloS One 7, e43836 (2012).
31. Rockey, W. M. et al. Rational truncation of an RNA aptamer to prostate-specific membrane antigen using computational structural modeling. Nucleic Acid Ther 21, 299-314 (2012).
32. Romero-Lopez, C., Diaz-Gonzalez, R., Barroso-delJesus, A. & Berzal-Herranz, A. Inhibition of hepatitis C virus replication and internal ribosome entry sitedependent translation by an RNA molecule. J Gen Virol 90, 1659-1669 (2009).
33. Good, P. D. et al. Expression of small, therapeutic RNAs in human cell nuclei. Gene Ther 4, 45-54 (1997).
34. Chaloin, L., Lehmann, M. J., Sczakiel, G. & Restle, T. Endogenous expression of a high-affinity pseudoknot RNA aptamer suppresses replication of HIV-1. Nucleic Acids Res 30, 4001-4008 (2002).
35. Ditzler, M. A. et al. High-throughput sequence analysis reveals structural diversity and improved potency among RNA inhibitors of HIV reverse transcriptase. Nucleic Acids Res 41, 1873-1884 (2013).
36. Lange, M. J. et al. Robust suppression of HIV replication by intracellularly expressed reverse transcriptase aptamers is independent of ribozyme processing. Mol Ther 20, 2304-2314 (2013).
37. Whatley, A. S. et al. Potent Inhibition of HIV-1 Reverse Transcriptase and Replication by Nonpseudoknot, "UCAA-motif"RNA Aptamers. Mol Ther 2, e71 (2013).
38. Whipple, J. M., Lane, E. A., Chernyakov, I., D'Silva, S. & Phizicky, E. M. The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and T-stems of mature tRNA. Genes & Dev 25, 1173-1184 (2011).
39. Xing, Y. Y. & Worcel, A. A 39 exonuclease activity degrades the pseudogene 5S RNA transcript and processes the major oocyte 5S RNA transcript in Xenopus oocytes. Genes & Dev 3, 1008-1018 (1989).
40. Kuiken, C. et al. HIV Sequence Compendium 2011. Los Alamos National Laboratory, Theoretical Biology and Biophysics, Los Alamos, NewMexico. LA-UR- 11-11440 (2011).
41. Pollom, E. et al. Comparison of SIV and HIV-1 genomic RNA structures reveals impact of sequence evolution on conserved and non-conserved structural motifs. PLoS Pathogens 9, e1003294 (2013).
42. Gee, A. H., Kasprzak, W. & Shapiro, B. A. Structural differentiation of the HIV-1 polyA signals. J Biomol Struct & Dyn 23, 417-428 (2006). (Pubitemid 43099654)
43. Abbink, T. E. & Berkhout, B. A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. J Biol Chem 278, 11601-11611 (2003). (Pubitemid 36792722)
44. Ashe, M. P., Griffin, P., James, W. & Proudfoot, N. J. Poly(A) site selection in the HIV-1 provirus: inhibition of promoter-proximal polyadenylation by the downstream major splice donor site. Genes & Dev 9, 3008-3025 (1995).
45. Paillart, J. C. et al. First snapshots of the HIV-1 RNA structure in infected cells and in virions. J Biol Chem 279, 48397-48403 (2004).
46. Paillart, J. C., Skripkin, E., Ehresmann, B., Ehresmann, C. & Marquet, R. In vitro evidence for a long range pseudoknot in the 59-untranslated and matrix coding regions of HIV-1 genomic RNA. J Biol Chem 277, 5995-6004 (2002). (Pubitemid 34968382)
47. Esteban, R., Vega, L. & Fujimura, T. 20S RNA narnavirus defies the antiviral activity of SKI1/XRN1 in Saccharomyces cerevisiae. J Biol Chem 283, 25812-25820 (2008).
48. Behlke, M. A. Chemical modification of siRNAs for in vivo use. Oligonucleotides 18, 305-319 (2008). (Pubitemid 352791344)
49. Thiel, K. W. & Giangrande, P. H. Therapeutic applications of DNA and RNA aptamers. Oligonucleotides 19, 209-222 (2009).
50. Neff, C. P. et al. An aptamer-siRNA chimera suppresses HIV-1 viral loads and protects from helper CD4(1) T cell decline in humanized mice. Science Transl Med 3, 66ra6 (2011).
51. Sanchez-Luque, F. J., Reyes-Darias, J. A., Puerta-Fernandez, E. & Berzal-Herranz, A. Inhibition of HIV-1 replication and dimerization interference by dual inhibitory RNAs. Molecules (Basel, Switzerland) 15, 4757-4772 (2010).
52. Romero-Lopez, C., Barroso-delJesus, A., Puerta-Fernandez, E. & Berzal-Herranz, A. Interfering with hepatitis C virus IRES activity using RNA molecules identified by a novel in vitro selection method. Biol Chem 386, 183-190 (2005). (Pubitemid 40361445)
53. Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biology Evol 4, 406-425 (1987).
54. Felsenstein, J. PHYLIP (Phylogeny Inference Package) version 3. 6. Department of Genome Sciences, University of Washington, Seattle (2005).
55. Hofacker, I. L. et al. Fast Folding and Comparison of RNA Secondary Structures. Monatschefte F. Chemie 125, 911-940 (1994).
56. Mathews, D. H., Sabina, J., Zuker, M. & Turner, D. H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288, 911-940 (1999). (Pubitemid 29248642)
57. Ding, Y., Chan, C. Y. & Lawrence, C. E. RNA secondary structure prediction by centroids in a Boltzmann weighted ensemble. RNA (New York, N. Y 11, 1157-1166 (2005).
58. Shapiro, B. A. An algorithm for comparing multiple RNA secondary structures. Comput Appl Biosci 4, 387-393 (1988).
59. Gruber, A. R., Lorenz, R., Bernhart, S. H., Neubock, R. & Hofacker, I. L. The Vienna RNA websuite. Nucleic Acids Res 36, W70-74 (2008).
60. Mueckstein, U. et al. Thermodynamics of RNA-RNA Binding. Bioinformatics 22, 1177-1182 (2006).