Inhibition of HIV-1 replication by a bis-thiadiazolbenzene-1,2-diamine that chelates zinc ions from retroviral nucleocapsid zinc fingers

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 4, 2010, Pages 1461-1468

  Pannecouque, Christophe ^a   Szafarowicz, Beata ^b   Volkova, Natalia ^c   Bakulev, Vasiliy ^c   Dehaen, Wim ^d   Mély, Yves ^b   Daelemans, Dirk ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c URAL FEDERAL UNIVERSITY   (Russian Federation)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; COMPLEMENTARY DNA; CYSTEINE; DEXTRAN SULFATE; DISULFIDE; GAG PROTEIN; N,N' BIS(1,2,3 THIADIAZOL 5 YL)BENZENE 1,2 DIAMINE; NEVIRAPINE; NUCLEOCAPSID PROTEIN; NUCLEOCAPSID PROTEIN 7; NV 037; NV 038; NV 039; PLERIXAFOR; RITONAVIR; THIOL; UNCLASSIFIED DRUG; ZINC ION;

ANTIVIRAL ACTIVITY; ARTICLE; CHELATION; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; VIRUS ENTRY; VIRUS INHIBITION; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; ZINC FINGER MOTIF;

ANTI-HIV AGENTS; BENZOTHIAZOLES; CELL LINE; CHELATING AGENTS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; HUMANS; MODELS, MOLECULAR; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION; ZINC; ZINC FINGERS;

EID: 77950135317     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01671-09     Document Type: Article

References (41)

1. Aldovini, A., and R. A. Young. 1990. Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus. J. Virol. 64:1920-1926.
2. Al-Mawsawi, L. Q., and N. Neamati. 2007. Blocking interactions between HIV-1 integrase and cellular cofactors: an emerging anti-retroviral strategy. Trends Pharmacol. Sci. 28:526-535.
3. Azoulay, J., J. P. Clamme, J. L. Darlix, B. P. Roques, and Y. Mely. 2003. Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations. J. Mol. Biol. 326:691-700.
4. Balvay, L., M. Lopez Lastra, B. Sargueil, J. L. Darlix, and T. Ohlmann. 2007. Translational control of retroviruses. Nat. Rev. Microbiol. 5:128-140.
5. Beltz, H., J. Azoulay, S. Bernacchi, J. P. Clamme, D. Ficheux, B. Roques, J. L. Darlix, and Y. Mely. 2003. Impact of the terminal bulges of HIV-1 cTAR DNA on its stability and the destabilizing activity of the nucleocapsid protein NCp7. J. Mol. Biol. 328:95-108.
6. Beltz, H., C. Clauss, E. Piemont, D. Ficheux, R. J. Gorelick, B. Roques, C. Gabus, J. L. Darlix, H. de Rocquigny, and Y. Mely. 2005. Structural determinants of HIV-1 nucleocapsid protein for cTAR DNA binding and destabilization, and correlation with inhibition of self-primed DNA synthesis. J. Mol. Biol. 348:1113-1126.
7. Bernacchi, S., and Y. Mely. 2001. Exciton interaction in molecular beacons: a sensitive sensor for short range modifications of the nucleic acid structure. Nucleic Acids Res. 29:E62.
8. Bernacchi, S., S. Stoylov, E. Piemont, D. Ficheux, B. P. Roques, J. L. Darlix, and Y. Mely. 2002. HIV-1 nucleocapsid protein activates transient melting of least stable parts of the secondary structure of TAR and its complementary sequence. J. Mol. Biol. 317:385-399.
9. Bombarda, E., N. Morellet, H. Cherradi, B. Spiess, S. Bouaziz, E. Grell, B. P. Roques, and Y. Mely. 2001. Determination of the pK(a) of the four Zn2+-coordinating residues of the distal finger motif of the HIV-1 nucleocapsid protein: consequences on the binding of Zn2+. J. Mol. Biol. 310:659-672.
10. Carteau, S., R. J. Gorelick, and F. D. Bushman. 1999. Coupled integration of human immunodeficiency virus type 1 cDNA ends by purified integrase in vitro: stimulation by the viral nucleocapsid protein. J. Virol. 73:6670-6679.
11. Clapham, P. R., and A. McKnight. 2002. Cell surface receptors, virus entry and tropism of primate lentiviruses. J. Gen. Virol. 83:1809-1829.
12. Daelemans, D., C. Pannecouque, G. N. Pavlakis, O. Tabarrini, and E. De Clercq. 2005. A novel and efficient approach to discriminate between preand post-transcription HIV inhibitors. Mol. Pharmacol. 67:1574-1580.
13. Daelemans, D., E. De Clercq, and A. M. Vandamme. 2001. A quantitative GFP-based bioassay for the detection of HIV-1 Tat transactivation inhibitors. J. Virol. Methods 96:183-188.
14. Darlix, J. L., J. L. Garrido, N. Morellet, Y. Mely, and H. de Rocquigny. 2007. Properties, functions, and drug targeting of the multifunctional nucleocapsid protein of the human immunodeficiency virus. Adv. Pharmacol. 55:299-346.
15. de Rocquigny, H., V. Shvadchak, S. Avilov, C. Z. Dong, U. Dietrich, J. L. Darlix, and Y. Mely. 2008. Targeting the viral nucleocapsid protein in anti-HIV-1 therapy. Mini Rev. Med. Chem. 8:24-35.
16. Dorfman, T., J. Luban, S. P. Goff, W. A. Haseltine, and H. G. Gottlinger. 1993. Mapping of functionally important residues of a cysteine-histidine box in the human immunodeficiency virus type 1 nucleocapsid protein. J. Virol. 67:6159-6169.
17. Driscoll, M. D., and S. H. Hughes. 2000. Human immunodeficiency virus type 1 nucleocapsid protein can prevent self-priming of minus-strand strong stop DNA by promoting the annealing of short oligonucleotides to hairpin sequences. J. Virol. 74:8785-8792.
18. Gorelick, R. J., W. Fu, T. D. Gagliardi, W. J. Bosche, A. Rein, L. E. Henderson, and L. O. Arthur. 1999. Characterization of the block in replication of nucleocapsid protein zinc finger mutants from Moloney murine leukemia virus. J. Virol. 73:8185-8195.
19. Gorelick, R. J., S. M. Nigida, Jr., J. W. Bess, Jr., L. O. Arthur, L. E. Henderson, and A. Rein. 1990. Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. J. Virol. 64:3207-3211.
20. Guo, J., T. Wu, J. Anderson, B. F. Kane, D. G. Johnson, R. J. Gorelick, L. E. Henderson, and J. G. Levin. 2000. Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus-and plus-strand transfer. J. Virol. 74:8980-8988.
21. Jenkins, L. M., J. C. Byrd, T. Hara, P. Srivastava, S. J. Mazur, S. J. Stahl, J. K. Inman, E. Appella, J. G. Omichinski, and P. Legault. 2005. Studies on the mechanism of inactivation of the HIV-1 nucleocapsid protein NCp7 with 2-mercaptobenzamide thioesters. J. Med. Chem. 48:2847-2858.
22. Levin, J. G., J. Guo, I. Rouzina, and K. Musier-Forsyth. 2005. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog. Nucleic Acid Res. Mol. Biol. 80:217-286.
23. Li, X., Y. Quan, E. J. Arts, Z. Li, B. D. Preston, H. de Rocquigny, B. P. Roques, J. L. Darlix, L. Kleiman, M. A. Parniak, and M. A. Wainberg. 1996. Human immunodeficiency virus type 1 nucleocapsid protein (NCp7) directs specific initiation of minus-strand DNA synthesis primed by human tRNA(Lys3) in vitro: studies of viral RNA molecules mutated in regions that flank the primer binding site. J. Virol. 70:4996-5004.
24. Loo, J. A., T. P. Holler, J. Sanchez, R. Gogliotti, L. Maloney, and M. D. Reily. 1996. Biophysical characterization of zinc ejection from HIV nucleocapsid protein by anti-HIV 2,2′-dithiobis[benzamides] and benzisothiazolones. J. Med. Chem. 39:4313-4320.
25. Mely, Y., H. De Rocquigny, N. Morellet, B. P. Roques, and D. Gerad. 1996. Zinc binding to the HIV-1 nucleocapsid protein: a thermodynamic investigation by fluorescence spectroscopy. Biochemistry 35:5175-5182.
26. Nathans, R., H. Cao, N. Sharova, A. Ali, M. Sharkey, R. Stranska, M. Stevenson, and T. M. Rana. 2008. Small-molecule inhibition of HIV-1 Vif. Nat. Biotechnol. 26:1187-1192.
27. Ottmann, M., C. Gabus, and J. L. Darlix. 1995. The central globular domain of the nucleocapsid protein of human immunodeficiency virus type 1 is critical for virion structure and infectivity. J. Virol. 69:1778-1784.
28. Pannecouque, C., D. Daelemans, and E. De Clercq. 2008. Tetrazolium-based colorimetric assay for the detection of HIV replication inhibitors: revisited 20 years later. Nat. Protoc. 3:427-434.
29. Ren, J., and D. K. Stammers. 2005. HIV reverse transcriptase structures: designing new inhibitors and understanding mechanisms of drug resistance. Trends Pharmacol. Sci. 26:4-7.
30. Rice, W. G., D. C. Baker, C. A. Schaeffer, L. Graham, M. Bu, S. Terpening, D. Clanton, R. Schultz, J. P. Bader, R. W. Buckheit, Jr., L. Field, P. K. Singh, and J. A. Turpin. 1997. Inhibition of multiple phases of human immunodeficiency virus type 1 replication by a dithiane compound that attacks the conserved zinc fingers of retroviral nucleocapsid proteins. Antimicrob. Agents Chemother. 41:419-426.
31. Rice, W. G., C. A. Schaeffer, B. Harten, F. Villinger, T. L. South, M. F. Summers, L. E. Henderson, J. W. Bess, Jr., L. O. Arthur, J. S. McDougal, et al. 1993. Inhibition of HIV-1 infectivity by zinc-ejecting aromatic C-nitroso compounds. Nature 361:473-475.
32. Rice, W. G., J. G. Supko, L. Malspeis, R. W. Buckheit, Jr., D. Clanton, M. Bu, L. Graham, C. A. Schaeffer, J. A. Turpin, J. Domagala, R. Gogliotti, J. P. Bader, S. M. Halliday, L. Coren, R. C. Sowder II, L. O. Arthur, and L. E. Henderson. 1995. Inhibitors of HIV nucleocapsid protein zinc fingers as candidates for the treatment of AIDS. Science 270:1194-1197.
33. Rice, W. G., J. A. Turpin, M. Huang, D. Clanton, R. W. Buckheit, Jr., D. G. Covell, A. Wallqvist, N. B. McDonnell, R. N. DeGuzman, M. F. Summers, L. Zalkow, J. P. Bader, R. D. Haugwitz, and E. A. Sausville. 1997. Azodicarbonamide inhibits HIV-1 replication by targeting the nucleocapsid protein. Nat. Med. 3:341-345.
34. Schneider, R., M. Campbell, G. Nasioulas, B. K. Felber, and G. N. Pavlakis. 1997. Inactivation of the human immunodeficiency virus type 1 inhibitory elements allows Rev-independent expression of Gag and Gag/protease and particle formation. J. Virol. 71:4892-4903.
35. Shvadchak, V., S. Sanglier, S. Rocle, P. Villa, J. Haiech, M. Hibert, A. Van Dorsselaer, Y. Mely, and H. de Rocquigny. 2009. Identification by high throughput screening of small compounds inhibiting the nucleic acid destabilization activity of the HIV-1 nucleocapsid protein. Biochimie 91:916-923.
36. Turpin, J. A., Y. Song, J. K. Inman, M. Huang, A. Wallqvist, A. Maynard, D. G. Covell, W. G. Rice, and E. Appella. 1999. Synthesis and biological properties of novel pyridinioalkanoyl thiolesters (PATE) as anti-HIV-1 agents that target the viral nucleocapsid protein zinc fingers. J. Med. Chem. 42:67-86.
37. Valentin, A., W. Lu, M. Rosati, R. Schneider, J. Albert, A. Karlsson, and G. N. Pavlakis. 1998. Dual effect of interleukin 4 on HIV-1 expression: implications for viral phenotypic switch and disease progression. Proc. Natl. Acad. Sci. U. S. A. 95:8886-8891.
38. Witvrouw, M., J. Balzarini, C. Pannecouque, S. Jhaumeer-Laulloo, J. A. Este, D. Schols, P. Cherepanov, J. C. Schmit, Z. Debyser, A. M. Vandamme, J. Desmyter, S. R. Ramadas, and E. de Clercq. 1997. SRR-SB3, a disulfide-containing macrolide that inhibits a late stage of the replicative cycle of human immunodeficiency virus. Antimicrob. Agents Chemother. 41:262-268.
39. Xiao, Z., E. Ehrlich, K. Luo, Y. Xiong, and X. F. Yu. 2007. Zinc chelation inhibits HIV Vif activity and liberates antiviral function of the cytidine deaminase APOBEC3G. FASEB J. 21:217-222.
40. Zhang, H., Y. Zhou, C. Alcock, T. Kiefer, D. Monie, J. Siliciano, Q. Li, P. Pham, J. Cofrancesco, D. Persaud, and R. F. Siliciano. 2004. Novel singlecell-level phenotypic assay for residual drug susceptibility and reduced replication capacity of drug-resistant human immunodeficiency virus type 1. J. Virol. 78:1718-1729.
41. Zhang, Y., and E. Barklis. 1995. Nucleocapsid protein effects on the specificity of retrovirus RNA encapsidation. J. Virol. 69:5716-5722.