Identification of specific small molecule ligands for stem loop 3 ribonucleic acid of the packaging signal Ψ of human immunodeficiency virus-1

Journal of Medicinal Chemistry

Volumn 52, Issue 17, 2009, Pages 5462-5473

  Warui, Douglas M ^a   Baranger, Anne M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; LIGAND; NSC 123111; NSC 252359; PEPTIDE LIBRARY; RNA; SIGNAL PEPTIDE; SINGLE STRANDED RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; COMPUTER PROGRAM; COMPUTER SIMULATION; DISSOCIATION CONSTANT; DNA FOOTPRINTING; DNA PACKAGING; DRUG PROTEIN BINDING; DRUG SELECTIVITY; FLUORESCENCE SPECTROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS 1; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; RNA BINDING; RNA STRUCTURE; STRUCTURE ACTIVITY RELATION;

ACRIDINES; BASE SEQUENCE; BINDING SITES; CALORIMETRY; DRUG EVALUATION, PRECLINICAL; HIV-1; INVERTED REPEAT SEQUENCES; LIGANDS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; RNA STABILITY; RNA, VIRAL; SMALL MOLECULE LIBRARIES; SUBSTRATE SPECIFICITY; TITRIMETRY; VIRUS ASSEMBLY;

EID: 69949106235     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm900599v     Document Type: Article

References (64)

1. Nierhaus, K. H.; Wilson, D. N. Protein Synthesis and Ribosome Structure: Translating the Genome; Wiley-VCH: Weinheim, Germany, 2004.
2. Bloomfield, V. A.; Crothers, D. M.; Tinoco, I., Nucleic Acids: Structures, Properties, and Functions; University Science Books: Sausalito, CA, 2000.
3. Thomas, J. R.; Hergenrother, P. J. Targeting RNA with Small Molecules. Chem. Rev. 2008, 108, 1171-1224.
4. Chow, C.; Bogdan, F. A structural basis for RNA-ligand interactions. Chem. Rev. 1997, 97, 1489-1513.
5. Sucheck, S. J.; Wong, C. H. RNA as a target for small molecules. Curr. Opin. Chem. Biol. 2000, 4, 678-686.
6. Be'langer, F. G.; M., G.; Steinberg, S. V.; Cunningham, P. R.; Brakier-Gingras, L. Study of the functional interaction of the 900 tetraloop of 16S ribosomal RNA with helix 24 within the bacterial ribosome. J. Mol. Biol. 2004, 338, 683-693.
7. Costa, M.; Deme, E.; Jacquier, A.; Michel, F. Multiple tertiary interactions involving domain II of group II self-splicing introns. J. Mol. Biol. 1997, 267, 520-536.
8. Costa, M.; Michel, F. Frequent use of the same tertiary motif by self-folding RNAs. EMBO J. 1995, 14, 1276-1285.
9. Hedenstierna, K. O. F.; Siefert, J. L.; Fox, G. E.; Murgola, E. J. Co-conservation of rRNA tetraloop sequences and helix length suggests involvement of the tetraloops in higher-order interactions. Biochimie 2000, 82, 221-227.
10. Ikawa, Y.; Naito, D.; Aono, N.; Shiraishi, H.; Inoue, T. A conserved motif in group IC3 introns is a new class of GNRA receptor. Nucleic Acids Res. 1999, 27, 1859-1865. (Pubitemid 29209628)
11. Klosterman, P. S.; Hendrix, D. K.; Tamura, M.; Holbrook, S. R.; Brenner, S. E. Three dimensional motifs from the SCOR, structural classification of RNA database: extruded strands, base triples, tetraloops and U-turns. Nucleic Acids Res. 2004, 32, 2342-2352.
12. Krummel, D. A. P.; Altman, S. Verification of phylogenetic predictions in vivo and the importance of the tetraloop motif in a catalytic RNA. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 11200-11205.
13. Varani, G. Exceptionally stable nucleic acid hairpins. Annu. Rev. Biophys. Biomol. Struct. 1995, 24, 379-404.
14. Woese, C. R.; Gutell, R.; Gupta, R.; Noller, H. F. Detailed analysis of the higher-order structure of 16s-like ribosomal ribonucleicacids. Microbiol. Rev. 1983, 47, 621-669.
15. Woese, C. R.; Winker, S.; Gutell, R. R. Architecture of ribosomal RNA: constraints on the sequence of "tetra-loops". Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 8467-8471.
16. Yan, Z.; Sikri, S.; Beveridge, D. L.; Baranger, A. M. Identification of aminoacridine derivative that binds to RNA tetraloops. J. Med. Chem. 2007, 50, 4096-4104.
17. Clever, J. L.; Parslow, T. G. Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J. Virol. 1997, 71, 3407-3414. (Pubitemid 27172349)
18. De Guzman, R. N.; Wu, Z. R.; Stalling, C. C.; Pappalardo, L.; Borer, P. N.; Summers, M. F. Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 1998, 249, 384-388. (Pubitemid 28063374)
19. Clever, J. L.; Eckstein, D. A.; Parslow, T. G. Genetic dissociation of the encapsidation and reverse transcription functions in the 5′ R region of human immunodeficiency virus type 1. J. Virol. 1999, 73, 101-109.
20. Clever, J.; Sassetti, C.; Parslow, T. G. RNA secondary structure and binding sites for gag gene products in the 5′ packaging signal of human immunodeficiency virus type 1. J. Virol. 1995, 69, 2101-2109.
21. Damgaard, C. K.; Dyhr-Mikkelsen, H.; Kjems, J. Mapping the RNA binding sites for human immunodeficiency virus type-1 Gag and NC proteins within the complete HIV-1 and -2 untranslated leader regions. Nucleic Acids Res. 1998, 26, 3667-3676. (Pubitemid 28367971)
22. Hayashi, T.; Shioda, T.; Iwakura, Y.; Shibuta, H. RNA packaging signal of human immunodeficiency virus type 1. Virology 1992, 188, 590-599.
23. Lucia, P.; Deborah, J. K.; István, P.; Philip, N. B. Three-dimensional folding of an RNA hairpin required for packaging HIV-1. J. Mol. Biol. 1998, 282, 801-818.
24. McBride, M. S.; Panganiban, A. T. The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J. Virol. 1996, 70, 2963-2973.
25. McBride, M. S.; Panganiban, A. T. Position dependence of functional hairpins important for human immunodeficiency virus type 1 RNA encapsidation in vivo. J. Virol. 1997, 71, 2050-2058. (Pubitemid 27078583)
26. McBride, M. S.; Schwartz, M. D.; Panganiban, A. T. Efficient encapsidation of human immunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation. J. Virol. 1997, 71, 4544-4554. (Pubitemid 27204147)
27. Michael, F. S.; Andrew, C. P.; Bruce, S. H.; Philip, N. B. Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein. Biochemistry 2002, 41, 5276-5282. (Pubitemid 34411683)
28. Hayashi, T.; Ueno, Y.; Okamoto, T. Elucidation of a conserved RNA stem-loop structure in the packaging signal of human immunodeficiency virus type 1. FEBS Lett. 1993, 327, 213-218. (Pubitemid 23211191)
29. Turner, K. B.; Hagan, N. A.; Fabris, D. Inhibitory effects of archetypical nucleic acid ligands on the interactions of HIV-1 nucleocapsid protein with elements of psi-RNA. Nucleic Acids Res. 2006, 34, 1305-1316.
30. McPike, M. P.; Goodisman, J.; Dabrowiak, J. C. Footprinting and Cirular Dichroism Studies on Paromomycin Binding to the Packaging Region of Human Immunodeficiency Virus Type-1. Bioorg. Med. Chem. 2002, 10, 3663-3672.
31. McPike, M. P.; Goodisman, J.; Dabrowiak, J. C. Specificity of neomycin analogues bound to the packaging region of human immunodeficiency virus type 1 RNA. Bioorg. Med. Chem. 2004, 12, 1835-1843.
32. McPike, M. P.; Sullivan, J. M.; Goodisman, J.; Dabrowiak, J. C. Footprinting, circular dichroism and UV melting studies on neomycin B binding to the packaging region of human immunodeficiency virus type-1 RNA. Nucleic Acids Res. 2002, 30, 2825-2831. (Pubitemid 34778142)
33. Yan, Z.; Baranger, A. M. Binding of an Aminoacridine Derivative to a GAAA RNA Tetraloop. Bioorg. Med. Chem. Lett. 2004, 14, 5889-5893.
34. Pustowka, A.; Dietz, J.; Ferner, J.; Baumann, M.; Landersz, M.; Konigs, C.; Schwalbe, H.; Dietrich, U. Identification of Peptide Ligands for Target RNA Structures Derived from the HIV-1 Packaging Signal Y by Screening Phage-Displayed Peptide Libraries. ChemBioChem 2003, 4, 1093-1097. (Pubitemid 37267599)
35. Dietz, J.; Koch, J.; Kaur, A.; Raja, C.; Stein, S.; Grez, M.; Pustowka, A.; Mensch, S.; Ferner, J.; Moller, L.; Bannert, N.; Tampé, R.; Divita, G.; Mély, Y.; Schwalbe, H.; Dietrich, U. Inhibition of HIV-1 by a peptide ligand of the genomic RNA packaging signal psi. ChemMedChem 2008, 3, 749-755.
36. Ewing, T. J. A.; Makino, S.; Skillman, A. G.; Kuntz, I. D. DOCK 4.0: search strategies for automated molecular docking of flexible molecule databases. J. Comput-Aided Mol. Des 2001, 15, 411-428.
37. Kuntz, I. D. Structure-based strategies for drug design and discovery. Science 1992, 257, 1078-1082.
38. Kuntz, I. D.; Blaney, J. M.; Oatley, S. J.; Langridge, R.; Ferrin, T. E. A geometric approach to macromolecule-ligand interactions. J. Mol. Biol. 1982, 161, 269-288.
39. Morris, G. M.; Goodsell, D. S.; Halliday, R. S.; Huey, R.; Hart, W. E.; Belew, R. K.; Olson, A. J. Automated docking using a Lamarckian genetic algorithmand an empirical binding free energy function. J. Comput. Chem. 1998, 19, 1639-1662.
40. Barbault, F.; Zhang, L.; Zhang, L.; Fan, B. T. Parametrization of a specific free energy function for automated docking against RNA targets using neural networks. Chemom. Intell. Lab. Syst 2006, 82, 269-275.
41. Chen, Q.; Kuntz, I. D.; Shafer, R. H., Structure-Based Design of Nucleic Acid Binding Drugs. In Structure, Motion, Interaction and Expression of Biological Macromolecules; Adenine Press: New York, 1997; pp 227-231.
42. Detering, C.; Varani, G. Validation of automated docking programs for docking and database screening against RNA drug targets. J. Med. Chem. 2004, 47, 4188-4201.
43. Moitessier, N.; Westhof, E.; Hanessian, S. Docking of aminoglycosides to hydrated and flexible RNA. J. Med. Chem. 2006, 49, 1023-1033.
44. Zhang, X.; Wang, X.; Liu, C. Molecular docking and 3D-QSAR study of pyranmycin derivatives against 16S rRNA A site. J. Mol. Struct.: THEOCHEM 2005, 730, 85-94. (Pubitemid 41420921)
45. Haddad, J.; Kotra, L. P.; Liano-Sotelo, B.; Kim, C.; Azucena, E. F.; Liu, M.; Vakulenko, S. B.; Chow, C. S.; Mobashery, S. Design of Novel Antibiotics that Bind to the Ribosomal Acyltransfer Site. J. Am. Chem. Soc. 2002, 124, 3229-3237.
46. Evans, D. A.; Neidle, S. Virtual screening of DNA minor groove binders. J. Med. Chem. 2006, 49, 4232-4238.
47. Kuntz, I. D.Ewing, T. J. A. DOCK Version 4.0 User Manual; University of California: San Francisco, 1998; pp 20-21
48. Case, D. A.; Darden, T. A.; Cheatham, T. E.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Merz, K. M.; Wang, B.; Pearlman, D. A.; Crowley, M.; Brozell, S.; Tsui, V.; Gohlke, H.; Mongan, J.; Hornak, V.; Cui, G.; Beroza, P.; Schafmeister, C.; Caldwell, J. W.; Ross, W. S.; Kollman, P. A. AMBER8; University of California: San Franscisco, 2004.
49. Cheatham, T. E., III; Cieplak, P.; Kollman, P. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeats. J. Biomol. Struct. Dyn. 1999, 16, 845-862.
50. Llano-Sotelo, B.; Chow, C. S. RNA-aminoglycoside antibiotic interactions: fluorescence detection of binding and conformational change. Bioorg. Med. Chem. Lett. 1999, 8, 213-216.
51. Thomas, J. R.; Liu, X.; Hergenrother, P. J. Size-specific ligands for RNA hairpin loops. J. Am. Chem. Soc. 2005, 127, 12434-12435.
52. Llano-Sotelo, B.; Azucena, E.; Kotra, L.; Mobashery, S.; Chow, C. Aminoglycosides modified by resistance enzymes display diminished binding to the bacterial ribosomal aminoacyl-tRNA site. Chem. Biol. 2002, 9, 455-463.
53. Li, V.-S.; Tang, M.-s.; Kohn, H. The Effect of C(5) Cytosine Methylation at CpG Sequences on Mitomycin-DNA Bonding Profiles. Bioorg. Med. Chem. 2001, 9, 863-873.
54. Tomasz, M.; Chawla, A. K.; Lipman, R. Mechanism of Monofunctional and Bifunctional Alkylation of DNA by Mitomycin C. Biochemistry 1988, 27, 3182-3187. (Pubitemid 18132112)
55. Li, V.-S.; Choi, D.; Tang, M.-S.; Kohn, H. Concerning in Vitro Mitomycin-DNA Alkylation. J. Am. Chem. Soc. 1996, 118, 3765-3766.
56. Erikson, M.; Norden, B. Linear and circular dichroism of drug-nucleic acid complexes. Methods Enzymol. 2001, 340, 68-98.
57. Ratmeyer, L.; Zapp, M. L.; Green, M. R.; Vinayak, R.; Kumar, A.; Boykin, D. W.; Wilson, W. D. Inhibition of HIV-1 Rev-RRE interaction by diphenylfuran derivatives. Biochemistry 1996, 35, 13689-13696.
58. McPike, M. P.; Sullivan, J. M.; Goodisman, J.; Dabrowiak, J. C. Footprinting, circular dichroism and UV melting studies on neomycin B binding to the packaging region of human immunodeficiency virus type-1 RNA. Nucleic Acids Res. 2002, 30, 2825-2831. (Pubitemid 34778142)
59. Proctor, D. J.; Schaak, J. E.; Bevilacqua, J. M.; Falzone, C. J.; Bevilacqua, P. C. Isolation and characterization of a family of stable RNA tetraloops with motif YNMG that participate in tertiary interactions. Biochemistry 2002, 41, 12062-12075.
60. Litovchik, A.; Evdokimov, A. G.; Lapidot, A. Aminoglycoside-arginine conjugates that bind TAR RNA: synthesis, characterization, and antiviral activity. Biochemistry 2000, 39, 2838-2852. (Pubitemid 30159388)
61. Brunel, C.; Romby, P. Probing RNA structure and RNA-ligand complexes with chemical probes. Methods Enzymol. 2000, 318, 3-21. (Pubitemid 30421636)
62. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field. J. Comput. Chem. 2004, 25, 1157-1173.
63. Yrckaert, J. P.; C., G.; Berendsen, H. J. C. Numerical-integration of cartesian equations of motions of a system with constraints - molecular dynamics of n-alkanes. J. Comput. Phys. 1977, 23, 327-341.
64. Liu, X.; Thomas, J. R.; Hergenrother, P. J. Deoxystreptamine dimers bind to RNA hairpin loops. J. Am. Chem. Soc. 2004, 126, 9196-9197.