Broad-spectrum aptamer inhibitors of HIV reverse transcriptase closely mimic natural substrates

Nucleic Acids Research

Volumn 39, Issue 18, 2011, Pages 8237-8247

  Ditzler, Mark A ^a   Bose, Debojit ^a,b   Shkriabai, Nikolozi ^c   Marchand, Bruno ^a   Sarafianos, Stefan G ^a   Kvaratskhelia, Mamuka ^c   Burke, Donald H ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; HYDROXYL RADICAL; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE; RNA DIRECTED DNA POLYMERASE INHIBITOR;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA PROTEIN COMPLEX; ENZYME SUBSTRATE; HUMAN IMMUNODEFICIENCY VIRUS 1; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOOTPRINTING;

ANTI-HIV AGENTS; APTAMERS, NUCLEOTIDE; BINDING SITES; HIV REVERSE TRANSCRIPTASE; HYDROXYL RADICAL; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN FOOTPRINTING; PROTEIN STRUCTURE, TERTIARY; REVERSE TRANSCRIPTASE INHIBITORS;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; PRIMATES; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 80054055875     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr381     Document Type: Article

References (41)

1. Jellinek, D., Green, L.S., Bell, C. and Janjic, N. (1994) Inhibition of receptor binding by high-affinity RNA ligands to vascular endothelial growth factor. Biochemistry, 33, 10450-10456. (Pubitemid 24281813)
2. Ng, E.W., Shima, D.T., Calias, P., Cunningham, E.T. Jr, Guyer, D.R. and Adamis, A.P. (2006) Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat. Rev. Drug Discov., 5, 123-132.
3. Dyke, C.K., Steinhubl, S.R., Kleiman, N.S., Cannon, R.O., Aberle, L.G., Lin, M., Myles, S.K., Melloni, C., Harrington, R.A., Alexander, J.H. et al. (2006) First-in-human experience of an antidote-controlled anticoagulant using RNA aptamer technology: a phase 1a pharmacodynamic evaluation of a drug-antidote pair for the controlled regulation of factor IXa activity. Circulation, 114, 2490-2497. (Pubitemid 44901522)
4. Keefe, A.D. and Schaub, R.G. (2008) Aptamers as candidate therapeutics for cardiovascular indications. Curr. Opin. Pharmacol., 8, 147-152.
5. de Soultrait, V.R., Lozach, P.Y., Altmeyer, R., Tarrago-Litvak, L., Litvak, S. and Andreola, M.L. (2002) DNA aptamers derived from HIV-1 RNase H inhibitors are strong anti-integrase agents. J. Mol. Biol., 324, 195-203. (Pubitemid 35379020)
6. Tuerk, C., MacDougal, S. and Gold, L. (1992) RNA pseudoknots that inhibit human immunodeficiency virus type 1 reverse transcriptase. Proc. Natl Acad. Sci. USA, 89, 6988-6992.
7. Schneider, D.J., Feigon, J., Hostomsky, Z. and Gold, L. (1995) High-affinity ssDNA inhibitors of the reverse transcriptase of type 1 human immunodeficiency virus. Biochemistry, 34, 9599-9610.
8. Li, N., Wang, Y., Pothukuchy, A., Syrett, A., Husain, N., Gopalakrisha, S., Kosaraju, P. and Ellington, A.D. (2008) Aptamers that recognize drug-resistant HIV-1 reverse transcriptase. Nucleic Acids Res., 36, 6739-6751.
9. Michalowski, D., Chitima-Matsiga, R., Held, D.M. and Burke, D.H. (2008) Novel bimodular DNA aptamers with guanosine quadruplexes inhibit phylogenetically diverse HIV-1 reverse transcriptases. Nucleic Acids Res., 36, 7124-7135.
10. Somasunderam, A., Ferguson, M.R., Rojo, D.R., Thiviyanathan, V., Li, X., O'Brien, W.A. and Gorenstein, D.G. (2005) Combinatorial selection, inhibition, and antiviral activity of DNA thioaptamers targeting the RNase H domain of HIV-1 reverse transcriptase. Biochemistry, 44, 10388-10395. (Pubitemid 41076834)
11. Mosing, R.K., Mendonsa, S.D. and Bowser, M.T. (2005) Capillary electrophoresis-SELEX selection of aptamers with affinity for HIV-1 reverse transcriptase. Anal. Chem., 77, 6107-6112. (Pubitemid 41436941)
12. Hannoush, R.N., Carriero, S., Min, K.L. and Damha, M.J. (2004) Selective inhibition of HIV-1 reverse transcriptase (HIV-1 RT) RNase H by small RNA hairpins and dumbbells. Chembiochem., 5, 527-533. (Pubitemid 39257110)
13. Burke, D.H., Scates, L., Andrews, K. and Gold, L. (1996) Bent pseudoknots and novel RNA inhibitors of type 1 human immunodeficiency virus (HIV-1) reverse transcriptase. J. Mol. Biol., 264, 650-666. (Pubitemid 27013551)
14. Andreola, M.L., Pileur, F., Calmels, C., Ventura, M., Tarrago-Litvak, L., Toulme, J.J. and Litvak, S. (2001) DNA aptamers selected against the HIV-1 RNase H display in vitro antiviral activity. Biochemistry, 40, 10087-10094. (Pubitemid 32800116)
15. Boomer, R.M., Lewis, S.D., Healy, J.M., Kurz, M., Wilson, C. and McCauley, T.G. (2005) Conjugation to polyethylene glycol polymer promotes aptamer biodistribution to healthy and inflamed tissues. Oligonucleotides, 15, 183-195. (Pubitemid 41395995)
16. Wilson, C. and Keefe, A.D. (2006) Building oligonucleotide therapeutics using non-natural chemistries. Curr. Opin. Chem. Biol., 10, 607-614. (Pubitemid 44821893)
17. McNamara, J.O. II, Andrechek, E.R., Wang, Y., Viles, K.D., Rempel, R.E., Gilboa, E., Sullenger, B.A. and Giangrande, P.H. (2006) Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras. Nat. Biotechnol., 24, 1005-1015. (Pubitemid 44215395)
18. Zhou, J., Li, H., Li, S., Zaia, J. and Rossi, J.J. (2008) Novel dual inhibitory function aptamer-siRNA delivery system for HIV-1 therapy. Mol. Ther., 16, 1481-1489.
19. Joshi, P. and Prasad, V.R. (2002) Potent inhibition of human immunodeficiency virus type 1 replication by template analog reverse transcriptase inhibitors derived by SELEX (systematic evolution of ligands by exponential enrichment). J. Virol., 76, 6545-6557. (Pubitemid 34633520)
20. Chen, F., Hu, Y., Li, D., Chen, H. and Zhang, X.L. (2009) CS-SELEX generates high-affinity ssDNA aptamers as molecular probes for hepatitis C virus envelope glycoprotein E2. PLoS One, 4, e8142.
21. Bellecave, P., Cazenave, C., Rumi, J., Staedel, C., Cosnefroy, O., Andreola, M.L., Ventura, M., Tarrago-Litvak, L. and Astier-Gin, T. (2008) Inhibition of hepatitis C virus (HCV) RNA polymerase by DNA aptamers: mechanism of inhibition of in vitro RNA synthesis and effect on HCV-infected cells. Antimicrob. Agents Chemother., 52, 2097-2110. (Pubitemid 351758547)
22. Pan, Q., Zhang, X.L., Wu, H.Y., He, P.W., Wang, F., Zhang, M.S., Hu, J.M., Xia, B. and Wu, J. (2005) Aptamers that preferentially bind type IVB pili and inhibit human monocytic-cell invasion by Salmonella enterica serovar typhi. Antimicrob. Agents Chemother., 49, 4052-4060. (Pubitemid 41400946)
23. Kissel, J.D., Held, D.M., Hardy, R.W. and Burke, D.H. (2007) Single-stranded DNA aptamer RT1t49 inhibits RT polymerase and RNase H functions of HIV type 1, HIV type 2, and SIVCPZ RTs. AIDS Res. Hum. Retroviruses, 23, 699-708. (Pubitemid 46867468)
24. Fisher, T.S., Joshi, P. and Prasad, V.R. (2005) HIV-1 reverse transcriptase mutations that confer decreased in vitro susceptibility to anti-RT DNA aptamer RT1t49 confer cross resistance to other anti-RT aptamers but not to standard RT inhibitors. AIDS Res. Ther., 2, 8.
25. Held, D.M., Kissel, J.D., Thacker, S.J., Michalowski, D., Saran, D., Ji, J., Hardy, R.W., Rossi, J.J. and Burke, D.H. (2007) Cross-clade inhibition of recombinant human immunodeficiency virus type 1 (HIV-1), HIV-2, and simian immunodeficiency virus SIVcpz reverse transcriptases by RNA pseudoknot aptamers. J. Virol., 81, 5375-5384. (Pubitemid 46744446)
26. Kissel, J.D., Held, D.M., Hardy, R.W. and Burke, D.H. (2007) Active site binding and sequence requirements for inhibition of HIV-1 reverse transcriptase by the RT1 family of single-stranded DNA aptamers. Nucleic Acids Res., 35, 5039-5050. (Pubitemid 47394189)
27. Michailidis, E., Marchand, B., Kodama, E.N., Singh, K., Matsuoka, M., Kirby, K.A., Ryan, E.M., Sawani, A.M., Nagy, E., Ashida, N. et al. (2009) Mechanism of inhibition of HIV-1 reverse transcriptase by 4'-Ethynyl-2-fluoro- 2'-deoxyadenosine triphosphate, a translocation-defective reverse transcriptase inhibitor. J. Biol. Chem., 284, 35681-35691.
28. Gotte, M., Maier, G., Gross, H.J. and Heumann, H. (1998) Localization of the active site of HIV-1 reverse transcriptase-associated RNase H domain on a DNA template using site-specific generated hydroxyl radicals. J. Biol. Chem., 273, 10139-10146. (Pubitemid 28227612)
29. Metzger, W., Hermann, T., Schatz, O., Le Grice, S.F. and Heumann, H. (1993) Hydroxyl radical footprint analysis of human immunodeficiency virus reverse transcriptase-template.primer complexes. Proc. Natl Acad. Sci. USA, 90, 5909-5913. (Pubitemid 23191423)
30. Kvaratskhelia, M., Miller, J.T., Budihas, S.R., Pannell, L.K. and Le Grice, S.F. (2002) Identification of specific HIV-1 reverse transcriptase contacts to the viral RNA:tRNA complex by mass spectrometry and a primary amine selective reagent. Proc. Natl Acad. Sci. USA, 99, 15988-15993. (Pubitemid 35462736)
31. Jaeger, J., Restle, T. and Steitz, T.A. (1998) The structure of HIV-1 reverse transcriptase complexed with an RNA pseudoknot inhibitor. EMBO J., 17, 4535-4542. (Pubitemid 28362641)
32. Rodgers, D.W., Gamblin, S.J., Harris, B.A., Ray, S., Culp, J.S., Hellmig, B., Woolf, D.J., Debouck, C. and Harrison, S.C. (1995) The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1. Proc. Natl Acad. Sci. USA, 92, 1222-1226.
33. Jacobo-Molina, A., Ding, J., Nanni, R.G., Clark, A.D. Jr, Lu, X., Tantillo, C., Williams, R.L., Kamer, G., Ferris, A.L., Clark, P. et al. (1993) Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA. Proc. Natl Acad. Sci. USA, 90, 6320-6324. (Pubitemid 23191507)
34. Kensch, O., Restle, T., Wohrl, B.M., Goody, R.S. and Steinhoff, H.J. (2000) Temperature-dependent equilibrium between the open and closed conformation of the p66 subunit of HIV-1 reverse transcriptase revealed by site-directed spin labelling. J. Mol. Biol., 301, 1029-1039.
35. Seckler, J.M., Howard, K.J., Barkley, M.D. and Wintrode, P.L. (2009) Solution structural dynamics of HIV-1 reverse transcriptase heterodimer. Biochemistry, 48, 7646-7655.
36. Fisher, T.S., Joshi, P. and Prasad, V.R. (2002) Mutations that confer resistance to template-analog inhibitors of human immunodeficiency virus (HIV) type 1 reverse transcriptase lead to severe defects in HIV replication. J. Virol., 76, 4068-4072. (Pubitemid 34250570)
37. Tullius, T.D. and Dombroski, B.A. (1986) Hydroxyl radical 'footprinting': high-resolution information about DNA-protein contacts and application to lambda repressor and Cro protein. Proc. Natl Acad. Sci. USA, 83, 5469-5473. (Pubitemid 16001244)
38. Balasubramanian, B., Pogozelski, W.K. and Tullius, T.D. (1998) DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc. Natl Acad. Sci. USA, 95, 9738-9743. (Pubitemid 28415239)
39. Palaniappan, C., Fuentes, G.M., Rodriguez-Rodriguez, L., Fay, P.J. and Bambara, R.A. (1996) Helix structure and ends of RNA/DNA hybrids direct the cleavage specificity of HIV-1 reverse transcriptase RNase H. J. Biol. Chem., 271, 2063-2070. (Pubitemid 26047792)
40. Ambrus, A., Chen, D., Dai, J., Jones, R.A. and Yang, D. (2005) Solution structure of the biologically relevant G-quadruplex element in the human c-MYC promoter. Implications for G-quadruplex stabilization. Biochemistry, 44, 2048-2058. (Pubitemid 40227475)
41. Burge, S., Parkinson, G.N., Hazel, P., Todd, A.K. and Neidle, S. (2006) Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res., 34, 5402-5415. (Pubitemid 44742430)