Structure-activity analysis of vinylogous urea inhibitors of human immunodeficiency virus-encoded ribonuclease H

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 9, 2010, Pages 3913-3921

  Chung, Suhman ^a   Wendeler, Michaela ^a   Rausch, Jason W ^a   Beilhartz, Greg ^b   Gotte, Matthias ^b   O'Keefe, Barry R ^a   Bermingham, Alun ^a   Beutler, John A ^a   Liu, Shixin ^c   Zhuang, Xiaowei ^c,d   Le Grice, Stuart F J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c HARVARD UNIVERSITY   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5,6,7,8 TETRAHYDRO 4H CYCLOHEPTA[B]THIOPHENE 3 CARBOXAMIDE; AMIDE; AMINE; ANTIVIRUS AGENT; CYCLOALKANE DERIVATIVE; CYCLOHEPTANE DERIVATIVE; CYCLOHEXANE DERIVATIVE; CYCLOOCTANE DERIVATIVE; ENZYME INHIBITOR; N [3 (AMINOCARBONYL) 4,5 DIMETHYL 2 THIENYL] 2 FURANCARBOXAMIDE; PROTEIN P51; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE; THIOPHENE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; BINDING SITE; CONTROLLED STUDY; DRUG POTENCY; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; MOLECULAR MODEL; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION;

ANTI-HIV AGENTS; CATALYTIC DOMAIN; ENZYME INHIBITORS; HUMANS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; RIBONUCLEASE H, HUMAN IMMUNODEFICIENCY VIRUS; TEMPERATURE; THERMODYNAMICS;

EID: 77956131587     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00434-10     Document Type: Article

References (35)

1. Abbondanzieri, E. A., G. Bokinsky, J. W. Rausch, J. X. Zhang, S. F. Le Grice, and X. Zhuang. 2008. Dynamic binding orientations direct activity of HIV reverse transcriptase. Nature 453:184-189. (Pubitemid 351667984)
2. Beard, W. A., S. J. Stahl, H. R. Kim, K. Bebenek, A. Kumar, M. P. Strub, S. P. Becerra, T. A. Kunkel, and S. H. Wilson. 1994. Structure/function studies of human immunodeficiency virus type 1 reverse transcriptase. Alanine scanning mutagenesis of an alpha-helix in the thumb subdomain. J. Biol. Chem. 269:28091-28097.
3. Beilhartz, G. L., M. Wendeler, N. Baichoo, J. Rausch, S. Le Grice, and M. Gotte. 2009. HIV-1 reverse transcriptase can simultaneously engage its DNA/RNA substrate at both DNA polymerase and RNase H active sites: implications for RNase H inhibition. J. Mol. Biol. 388:462-474.
4. Bokesch, H. R., A. Wamiru, S. F. Le Grice, J. A. Beutler, T. C. McKee, and J. B. McMahon. 2008. HIV-1 ribonuclease H inhibitory phenolic glycosides from Eugenia hyemalis. J. Nat. Prod. 71:1634-1636.
5. Bonache, M. C., E. Quesada, C. W. Sheen, J. Balzarini, N. Sluis-Cremer, M. J. Perez-Perez, M. J. Camarasa, and A. San-Felix. 2008. Novel N-3 substituted TSAO-T derivatives: synthesis and anti-HIV-evaluation. Nucleosides Nucleotides Nucleic Acids 27:351-367.
6. Borkow, G., R. S. Fletcher, J. Barnard, D. Arion, D. Motakis, G. I. Dmitrienko, and M. A. Parniak. 1997. Inhibition of the ribonuclease H and DNA polymerase activities of HIV-1 reverse transcriptase by N-(4-tert-butylbenzoyl)- 2-hydroxy-1-naphthaldehyde hydrazone. Biochemistry 36:3179-3185.
7. Budihas, S. R., I. Gorshkova, S. Gaidamakov, A. Wamiru, M. K. Bona, M. A. Parniak, R. J. Crouch, J. B. McMahon, J. A. Beutler, and S. F. Le Grice. 2005. Selective inhibition of HIV-1 reverse transcriptase-associated ribonuclease H activity by hydroxylated tropolones. Nucleic Acids Res. 33:1249-1256.
8. Cellitti, S. E., D. H. Jones, L. Lagpacan, X. Hao, Q. Zhang, H. Hu, S. M. Brittain, A. Brinker, J. Caldwell, B. Bursulaya, G. Spraggon, A. Brock, Y. Ryu, T. Uno, P. G. Schultz, and B. H. Geierstanger. 2008. In vivo incorporation of unnatural amino acids to probe structure, dynamics, and ligand binding in a large protein by nuclear magnetic resonance spectroscopy. J. Am. Chem. Soc. 130:9268-9281.
9. Chiba, J., A. Yamaguchi, Y. Suzuki, M. Nakano, W. Zhu, H. Ohba, A. Saito, H. Shinagawa, Y. Yamakawa, T. Kobayashi, and T. Kurata. 1996. A novel neutralization epitope on the 'thumb' subdomain of human immunodeficiency virus type 1 reverse transcriptase revealed by a monoclonal antibody. J. Gen. Virol. 77(Pt 12):2921-2929.
10. Dat, N. T., K. Bae, A. Wamiru, J. B. McMahon, S. F. Le Grice, M. Bona, J. A. Beutler, and Y. H. Kim. 2007. A dimeric lactone from Ardisia japonica with inhibitory activity for HIV-1 and HIV-2 ribonuclease H. J. Nat. Prod. 70: 839-841.
11. Dunn, L. L., M. J. McWilliams, K. Das, E. Arnold, and S. H. Hughes. 2009. Mutations in the thumb allow human immunodeficiency virus type 1 reverse transcriptase to be cleaved by protease in virions. J. Virol. 83:12336-12344.
12. Himmel, D. M., S. G. Sarafianos, S. Dharmasena, M. M. Hossain, K. McCoy-Simandle, T. Ilina, A. D. Clark, Jr., J. L. Knight, J. G. Julias, P. K. Clark, K. Krogh-Jespersen, R. M. Levy, S. H. Hughes, M. A. Parniak, and E. Arnold. 2006. HIV-1 reverse transcriptase structure with RNase H inhibitor dihydroxy benzoyl naphthyl hydrazone bound at a novel site. ACS Chem. Biol. 1:702-712.
13. Horn, J. R., D. Russell, E. A. Lewis, and K. P. Murphy. 2001. Van't Hoff and calorimetric enthalpies from isothermal titration calorimetry: are there significant discrepancies? Biochemistry 40:1774-1778.
14. Huang, H., R. Chopra, G. L. Verdine, and S. C. Harrison. 1998. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282:1669-1675.
15. Jochmans, D., J. Deval, B. Kesteleyn, H. Van Marck, E. Bettens, I. De Baere, P. Dehertogh, T. Ivens, M. Van Ginderen, B. Van Schoubroeck, M. Ehteshami, P. Wigerinck, M. Gotte, and K. Hertogs. 2006. Indolopyridones inhibit human immunodeficiency virus reverse transcriptase with a novel mechanism of action. J. Virol. 80:12283-12292.
16. Kirschberg, T. A., M. Balakrishnan, N. H. Squires, T. Barnes, K. M. Brendza, X. Chen, E. J. Eisenberg, W. Jin, N. Kutty, S. Leavitt, A. Liclican, Q. Liu, X. Liu, J. Mak, J. K. Perry, M. Wang, W. J. Watkins, and E. B. Lansdon. 2009. RNase H active site inhibitors of human immunodeficiency virus type 1 reverse transcriptase: design, biochemical activity, and structural information. J. Med. Chem. 52:5781-5784.
17. Klumpp, K., J. Q. Hang, S. Rajendran, Y. Yang, A. Derosier, P. Wong Kai In, H. Overton, K. E. Parkes, N. Cammack, and J. A. Martin. 2003. Two-metal ion mechanism of RNA cleavage by HIV RNase H and mechanism-based design of selective HIV RNase H inhibitors. Nucleic Acids Res. 31:6852-6859.
18. Klumpp, K., and T. Mirzadegan. 2006. Recent progress in the design of small molecule inhibitors of HIV RNase H. Curr. Pharm. Des. 12:1909-1922.
19. Le Grice, S. F., T. Naas, B. Wohlgensinger, and O. Schatz. 1991. Subunitselective mutagenesis indicates minimal polymerase activity in heterodimerassociated p51 HIV-1 reverse transcriptase. EMBO J. 10:3905-3911.
20. Liu, S., E. A. Abbondanzieri, J. W. Rausch, S. F. Le Grice, and X. Zhuang. 2008. Slide into action: dynamic shuttling of HIV reverse transcriptase on nucleic acid substrates. Science 322:1092-1097.
21. Naghibi, H., A. Tamura, and J. M. Sturtevant. 1995. Significant discrepancies between van't Hoff and calorimetric enthalpies. Proc. Natl. Acad. Sci. U. S. A. 92:5597-5599.
22. Powell, K., J. L. Davis, A. M. Morris, A. Chi, M. R. Bensley, and L. Huang. 2009. Survival for patients with HIV admitted to the ICU continues to improve in the current era of combination antiretroviral therapy. Chest 135:11-17.
23. Ratner, L., A. Fisher, L. L. Jagodzinski, H. Mitsuya, R. S. Liou, R. C. Gallo, and F. Wong-Staal. 1987. Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Res. Hum. Retroviruses 3:57-69.
24. Rodgers, D. W., S. J. Gamblin, B. A. Harris, S. Ray, J. S. Culp, B. Hellmig, D. J. Woolf, C. Debouck, and S. C. Harrison. 1995. The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U. S. A. 92:1222-1226.
25. Ruane, P. J., and E. DeJesus. 2004. New nucleoside/nucleotide backbone options: a review of recent studies. J. Acquir. Immune Defic. Syndr. 37(Suppl. 1):S21-S29.
26. Sarafianos, S. G., K. Das, C. Tantillo, A. D. Clark, Jr., J. Ding, J. M. Whitcomb, P. L. Boyer, S. H. Hughes, and E. Arnold. 2001. Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA: DNA. EMBO J. 20:1449-1461.
27. Schatz, O., F. V. Cromme, F. Gruninger-Leitch, and S. F. Le Grice. 1989. Point mutations in conserved amino acid residues within the C-terminal domain of HIV-1 reverse transcriptase specifically repress RNase H function. FEBS Lett. 257:311-314.
28. Shaw-Reid, C. A., V. Munshi, P. Graham, A. Wolfe, M. Witmer, R. Danzeisen, D. B. Olsen, S. S. Carroll, M. Embrey, J. S. Wai, M. D. Miller, J. L. Cole, and D. J. Hazuda. 2003. Inhibition of HIV-1 ribonuclease H by a novel diketo acid, 4-[5-(benzoylamino)thien-2-yl]-2,4-dioxobutanoic acid. J. Biol. Chem. 278:2777-2780.
29. Sluis-Cremer, N., N. Hamamouch, A. San Felix, S. Velazquez, J. Balzarini, and M. J. Camarasa. 2006. Structure-activity relationships of [2′,5′-bis-O-(tertbutyldimethylsilyl)- beta-D-ribofuranosyl]- 3′-spiro-5″-(4″-amino-1″,2″-oxathiole- 2″,2″-dioxide)thymine derivatives as inhibitors of HIV-1 reverse transcriptase dimerization. J. Med. Chem. 49:4834-4841.
30. Spanner, M. F. 1999. Python: a programming language for software integration and development. J. Mol. Graphics Mod. 17:57-61.
31. Takada, K., A. Bermingham, B. R. O'Keefe, A. Wamiru, J. A. Beutler, S. F. Le Grice, J. Lloyd, K. R. Gustafson, and J. B. McMahon. 2007. An HIV RNase H inhibitory 1,3,4,5-tetragalloylapiitol from the African plant Hylodendron gabunensis. J. Nat. Prod. 70:1647-1649.
32. Tisdale, M., T. Schulze, B. A. Larder, and K. Moelling. 1991. Mutations within the RNase H domain of human immunodeficiency virus type 1 reverse transcriptase abolish virus infectivity. J. Gen. Virol. 72(Pt 1):59-66.
33. Weislow, O. S., R. Kiser, D. L. Fine, J. Bader, R. H. Shoemaker, and M. R. Boyd. 1989. New soluble-formazan assay for HIV-1 cytopathic effects: application to high-flux screening of synthetic and natural products for AIDSantiviral activity. J. Natl. Cancer Inst. 81:577-586.
34. Wendeler, M., H. F. Lee, A. Bermingham, J. T. Miller, O. Chertov, M. K. Bona, N. S. Baichoo, M. Ehteshami, J. Beutler, B. R. O'Keefe, M. Gotte, M. Kvaratskhelia, and S. Le Grice. 2008. Vinylogous ureas as a novel class of inhibitors of reverse transcriptase-associated ribonuclease H activity. ACS Chem. Biol. 3:635-644.
35. Wendeler, M., G. L. Beilhartz, J. A. Beutler, M. Goette, and S. F. J. Le Grice. 2009. HIV ribonuclease H: continuing the search for small molecule antagonists. HIV Ther. 3:39-53.