Distinct effects of two HIV-1 capsid assembly inhibitor families that bind the same site within the N-terminal domain of the viral CA protein

Journal of Virology

Volumn 86, Issue 12, 2012, Pages 6643-6655

  Lemke, Christopher T ^a   Titolo, Steve ^a,c   von Schwedler, Uta ^b   Goudreau, Nathalie ^a   Mercier, Jean François ^a   Wardrop, Elizabeth ^a   Faucher, Anne Marie ^a,d   Coulombe, René ^a   Banik, Soma S R ^a,e   Fader, Lee ^a   Gagnon, Alexandre ^a,f   Kawai, Stephen H ^a,g   Rancourt, Jean ^a   Tremblay, Martin ^a   Yoakim, Christiane ^a   Simoneau, Bruno ^a   Archambault, Jacques ^a,h   Sundquist, Wesley I ^b   Mason, Stephen W ^a,i  

^a BOEHRINGER INGELHEIM CANADA LTD   (Canada)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c AL G Technologies   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e Integral Molecular Inc   (United States)

^f UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^g Dept of Electrical and Computer Engineering   (Canada)

^h CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

ⁱ BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZIMIDAZOLE DERIVATIVE; BENZODIAZEPINE DERIVATIVE; CAPSID PROTEIN; LAMIVUDINE; LOPINAVIR; NEVIRAPINE; OLIGONUCLEOTIDE; RALTEGRAVIR;

AMINO TERMINAL SEQUENCE; ANTIVIRAL ACTIVITY; ARTICLE; BINDING SITE; DRUG DETERMINATION; DRUG PROTEIN BINDING; DRUG SCREENING; DRUG STRUCTURE; ELECTRON MICROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEIC ACID IMMOBILIZATION; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN BINDING; PROTEIN SYNTHESIS INHIBITION; VIRUS MUTATION; VIRUS RELEASE; VIRUS REPLICATION; X RAY CRYSTALLOGRAPHY;

ANTI-HIV AGENTS; BENZIMIDAZOLES; BENZODIAZEPINES; CAPSID; CELL LINE; GENE PRODUCTS, GAG; HIV INFECTIONS; HIV-1; HUMANS; PROTEIN STRUCTURE, TERTIARY; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 84864007910     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00493-12     Document Type: Article

References (42)

1. Bartonova V, et al. 2008. Residues in the HIV-1 capsid assembly inhibitor binding site are essential for maintaining the assembly-competent quaternary structure of the capsid protein. J. Biol. Chem. 283:32024 -32033.
2. Blair WS, et al. 2010. HIV capsid is a tractable target for small molecule therapeutic intervention. PLoS Pathog. 6:e1001220. doi:10.1371/ journal.ppat.1001220.
3. Briggs JA, et al. 2009. Structure and assembly of immature HIV. Proc. Natl. Acad. Sci. U. S. A. 106:11090 -11095.
4. Byeon IJ, et al. 2009. Structural convergence between cryo-EM and NMR reveals intersubunit interactions critical for HIV-1 capsid function. Cell 139:780 -790.
5. De Clercq E. 2010. Antiretroviral drugs. Curr. Opin. Pharmacol. 10:507- 515.
6. Douglas CC, Thomas D, Lanman J, Prevelige PE, Jr. 2004. Investigation of N-terminal domain charged residues on the assembly and stability of HIV-1 CA. Biochemistry 43:10435-10441.
7. Doyon L, Tremblay S, Bourgon L, Wardrop E, Cordingley MG. 2005. Selection and characterization of HIV-1 showing reduced susceptibility to the non-peptidic protease inhibitor tipranavir. Antiviral Res. 68:27-35.
8. Fader LD, et al. 2011. Discovery of a 1,5-dihydrobenzo[1,4]diazepine-2,4-dione series of inhibitors of HIV-1 capsid assembly. Bioorg. Med. Chem. Lett. 21:398-404.
9. Feng YX, Li T, Campbell S, Rein A. 2002. Reversible binding of recombinant human immunodeficiency virus type 1 Gag protein to nucleic acids in virus-like particle assembly in vitro. J. Virol. 76:11757-11762.
10. Forshey BM, von Schwedler U, Sundquist WI, Aiken C. 2002. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76:5667-5677.
11. Freed EO. 1998. HIV-1 Gag proteins: diverse functions in the virus life cycle. Virology 251:1-15.
12. Freire E. 2008. Do enthalpy and entropy distinguish first in class from best in class? Drug Discov. Today 13:869-874.
13. Gamble TR, et al. 1996. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87:1285-1294.
14. Gamble TR, et al. 1997. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278:849-853.
15. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283:80-83.
16. Ganser-Pornillos BK, Cheng A, Yeager M. 2007. Structure of full-length HIV-1 CA: a model for the mature capsid lattice. Cell 131:70 -79.
17. Ganser-Pornillos BK, von Schwedler UK, Stray KM, Aiken C, Sundquist WI. 2004. Assembly properties of the human immunodeficiency virus type 1 CA protein. J. Virol. 78:2545-2552.
18. Ganser-Pornillos BK, Yeager M, Sundquist WI. 2008. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18:203-217.
19. Gitti RK, et al. 1996. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science 273:231-235.
20. Graham FL, van der Eb AJ. 1973. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52:456-467.
21. Hansen MS, et al. 1999. Integration complexes derived from HIV vectors for rapid assays in vitro. Nat. Biotechnol. 17:578 -582.
22. Ivanov D, et al. 2007. Domain-swapped dimerization of the HIV-1 capsid C-terminal domain. Proc. Natl. Acad. Sci. U. S. A. 104:4353- 4358.
23. Iwakuma T, Cui Y, Chang LJ. 1999. Self-inactivating lentiviral vectors with U3 and U5 modifications. Virology 261:120 -132.
24. Kelly BN, et al. 2007. Structure of the antiviral assembly inhibitor CAP-1 complex with the HIV-1 CA protein. J. Mol. Biol. 373:355-366.
25. Lanman J, Sexton J, Sakalian M, Prevelige PE, Jr. 2002. Kinetic analysis of the role of intersubunit interactions in human immunodeficiency virus type 1 capsid protein assembly in vitro. J. Virol. 76:6900-6908.
26. Li S, Hill CP, Sundquist WI, Finch JT. 2000. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407:409-413.
27. Monroe EB, Kang S, Kyere SK, Li R, Prevelige PE, Jr. 2010. Hydrogen/ deuterium exchange analysis of HIV-1 capsid assembly and maturation. Structure 18:1483-1491.
28. Moreno S, et al. 2010. The future of antiretroviral therapy: challenges and needs. J. Antimicrob. Chemother. 65:827- 835.
29. Pornillos O, et al. 2009. X-ray structures of the hexameric building block of the HIV capsid. Cell 137:1282-1292.
30. Pornillos O, Ganser-Pornillos BK, Yeager M. 2011. Atomic-level modelling of the HIV capsid. Nature 469:424-427.
31. Quinones-Mateu ME, Moore-Dudley DM, Jegede O, Weber J, Arts EJ. 2008. Viral drug resistance and fitness. Adv. Pharmacol. 56:257-296.
32. Shi J, Zhou J, Shah VB, Aiken C, Whitby K. 2011. Small-molecule inhibition of human immunodeficiency virus type 1 infection by virus capsid destabilization. J. Virol. 85:542-549.
33. Sticht J, et al. 2005. A peptide inhibitor of HIV-1 assembly in vitro. Nat. Struct. Mol. Biol. 12:671- 677.
34. Sundquist WI, Hill CP. 2007. How to assemble a capsid. Cell 131:17-19.
35. Sundquist WI, Krausslich H-G (ed). 13 March 2012. HIV-1 assembly, budding, and maturation. Cold Spring Harb. Perspect. Med. [Epub ahead of print.] doi:10.1101/cshperspect.a006924.
36. Taiwo B, Hicks C, Eron J. 2010. Unmet therapeutic needs in the new era of combination antiretroviral therapy for HIV-1. J. Antimicrob. Chemother. 65:1100 -1107.
37. Tang C, et al. 2003. Antiviral inhibition of the HIV-1 capsid protein. J. Mol. Biol. 327:1013-1020.
38. Ternois F, Sticht J, Duquerroy S, Krausslich HG, Rey FA. 2005. The HIV-1 capsid protein C-terminal domain in complex with a virus assembly inhibitor. Nat. Struct. Mol. Biol. 12:678-682.
39. von Schwedler UK, et al. 1998. Proteolytic refolding of the HIV-1 capsid protein amino-terminus facilitates viral core assembly. EMBO J. 17:1555- 1568.
40. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:5439 -5450.
41. Worthylake DK, Wang H, Yoo S, Sundquist WI, Hill CP. 1999. Structures of the HIV-1 capsid protein dimerization domain at 2.6Åresolution. Acta Crystallogr. D Biol. Crystallogr. 55:85-92.
42. Wright ER, et al. 2007. Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J. 26: 2218-2226.