Simultaneous recognition of HIV-1 TAR RNA bulge and loop sequences by cyclic peptide mimics of Tat protein

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 29, 2009, Pages 11931-11936

  Davidson, Amy ^a   Leeper, Thomas C ^a   Athanassiou, Zafiria ^a   Patora Komisarska, Krystyna ^b   Karn, Jonathan ^c   Robinson, John A ^b   Varani, Gabriele ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antiviral; NMR; RNA recognition; Tat TAR interaction; Transcription elongation factor b

Indexed keywords

COGNATE TRANSACTIVATION RESPONSE RNA; CYCLOPEPTIDE; NEVIRAPINE; PEPTIDE L 22; PEPTIDE L 50; PEPTIDE L 51; TRANSACTIVATOR PROTEIN; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION ELONGATION FACTOR B; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; BINDING SITE; DRUG STRUCTURE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ARGININE; BASE SEQUENCE; HIV LONG TERMINAL REPEAT; HIV-1; HYDROPHOBICITY; IMMUNODEFICIENCY VIRUS, BOVINE; LYSINE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PEPTIDES, CYCLIC; PHOSPHATES; PROTEIN BINDING; RNA STABILITY; RNA, VIRAL; SOLVENTS; STATIC ELECTRICITY; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 67749088605     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0900629106     Document Type: Article

References (33)

1. Peterlin MB, Price DH (2006) Controlling the elongation phase of transcription with P-TEFb. Mol Cell 23:297-305.
2. Karn J (1999) Tackling Tat. J Mol Biol 293:235-254.
3. Stevens M, De Clercq E, Balzarini J (2006) The regulation of HIV-1 transcription: Molecular targets for chemotherapeutic intervention. Med Res Rev 26:595-625.
4. Gallego J, Varani G (2001) Targeting RNA with small-molecule drugs: Therapeutic promise and chemical challenges. Acc Chem Res 34:836-843.
5. Huq I, Ping Y-H, Tamilarasu N, Rana TM (1999) Controlling human immunodeficiency virus type 1 gene expression by unnatural peptides. Biochemistry 38:5172-5177.
6. Murchie AIH, et al. (2004) Structure-based drug design targeting an inactive RNA conformation: Exploiting the flexibility of HIV-1 TAR RNA. J Mol Biol 336:625-638.
7. Baba M (2006) Recent status of HIV-1 gene expression inhibitors. Antiviral Res 71:301-306.
8. Wells JA, McClendon CL (2007) Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450:1001-1009.
9. Puglisi JD, Tan R, Calnan BJ, Frankel AD, Williamson JR (1992) Conformation of the TAR RNA-arginine complex by NMR spectroscopy. Science 257:76-80.
10. Aboul-ela F, Karn J, Varani G (1995) The structure of the human immunodeficiency virus type-1 TAR RNA reveals principles of RNA recognition by Tat protein. J Mol Biol 253:313-332.
11. Hamy F, et al. (1997) An inhibitor of the Tat/TAR RNA interaction that effectively suppresses HIV-1 replication. Proc Natl Acad Sci USA 94:3548-3553.
12. Ye X, Kumar RA, Patel DJ (1995) Molecular recognition in the bovine immunodeficiency virus Tat peptide-TAR RNA complex. Chem Biol 2:827-840.
13. Puglisi JD, Chen L, Blanchard S, Frankel AD (1995) Solution structure of a bovine immunodeficiency virus Tat-TAR Peptide-RNA complex. Science 270:1200-1203.
14. Leeper TC, Athanassiou Z, Dias RLA, Robinson JA, Varani G (2005) TAR RNA recognition by a cyclic peptidomimetic of Tat protein. Biochemistry 44:12362-12372.
15. Athanassiou Z, et al. (2004) Structural mimicry of retroviral Tat proteins by constrained, β-hairpin peptidomimetics: Ligands with high affinity and selectivity for viral TAR RNA regulatory elements. J Am Chem Soc 126:6906-6913.
16. Athanassiou Z, et al. (2007) Structure-guided peptidomimetic design leads to nanomolar β-hairpin inhibitors of the Tat-TAR interaction of bovine immunodeficiency virus. Biochemistry 46:741-751.
17. Robinson JA (2000) The design, synthesis, and conformation of some new β-hairpin mimetics: Novel reagents for drug and vaccine discovery. Syn Lett 2000:429-441.
18. Bardaro MFJ, Shajani Z, Patora-Komisarska K, Robinson JA, Varani G (2009) How binding of small molecule and peptide ligands to HIV-1 TAR alters the RNA motional landscape. Nucleic Acids Res 37:1529-1540.
19. Davis B, et al. (2004) Rational design of inhibitors of HIV-1 TAR RNA through stabilization of electrostatic "hot spots." J Mol Biol 336:343-356.
20. Calnan BJ, Tidor B, Biancalana S, Hudson D, Frankel AD (1991) Arginine-mediated recognition: The arginine fork. Science 252:1167-1171.
21. Raghunathan D, et al. (2006) TAR recognition by a novel cyclic aminoglycoside analogue. Nucleic Acids Res 34:3599-3608.
22. Jaeger JA, Tinoco I, Jr (1993) An NMR study of the HIV-1 element hairpin. Biochemistry 3:12522-12530.
23. Tao J, Chen L, Frankel AD (1997) Dissection of the proposed base triple in human immunodeficiency virus TAR RNA indicates the importance of the Hoogsteen interaction. Biochemistry 36:3491-3495.
24. Brodsky AS, Williamson JR (1997) Solution structure of the HIV-2 TAR-argininamide complex. J Mol Biol 267:624-639.
25. Al-Hashimi HM, et al. (2002) Concerted motions in HIV-1 TAR RNA may allow access to bound state conformations: RNA dynamics from NMR residual dipolar couplings. J Mol Biol 315:95-102.
26. Churcher MJ, et al. (1993) High-affinity binding of TAR RNA by the human immunodeficiency virus type-1 tat protein requires base pairs in the RNA stem and amino acid residues flanking the basic region. J Mol Biol 230:90-110.
27. Varani G, Aboul-Ela F, Allain FHT (1996) NMR investigation of RNA structure. Prog Nucl Mag Reson Spectrosc 29:51-127.
28. Delaglio F, et al. (1995) nmrPipe: A multidimensional spectral processing system based on unix pipes. J Biolmol NMR 6:277-293.
29. Goddard TD, Kneller DG (2006) Sparky 3 (University of California, San Francisco).
30. Peterson RD, Theimer CA, Wu HH, Feigon J (2004) New applications of 2D filtered/ edited NOESY for assignment and structure elucidation of RNA and RNA-protein complexes. J Biomol NMR 28:59-67.
31. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160:65-73.
32. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289-302.
33. Clore GM, Gronenborn AM, Tjandra N (1998) Direct structure refinement against residual dipolar couplings in the presence of rhombicity of unknown magnitude. J Magn Reson 131:159-162.