Human immunodeficiency virus type 1 nucleocapsid inhibitors impede trans infection in cellular and explant models and protect nonhuman primates from infection

Journal of Virology

Volumn 83, Issue 18, 2009, Pages 9175-9182

  Wallace, Gregory S ^a   Cheng Mayer, Cecilia ^b   Schito, Marco L ^c,f   Fletcher, Patricia ^a   Miller Jenkins, Lisa M ^c   Hayashi, Ryo ^c   Neurath, A Robert ^d   Appella, Ettore ^c,e   Shattock, Robin J ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b ROCKEFELLER UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d Virotech   (United States)

^e NONE   (United States)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CAPSID PROTEIN; MEDROXYPROGESTERONE ACETATE; MICROBICIDE; N [2 (3,4,5 TRIMETHOXYBENZOYLTHIO)BENZOYL] ALANINAMIDE; N [2 (ACETYLTHIO)BENZOYL] BETA ALANINAMIDE; N [2 (NICOTINOYLTHIO)BENZOYL] BETA ALANINAMIDE; S ACYL 2 MERCAPTOBENZAMIDE THIOESTER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; EXPLANT; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNITY; MONKEY; NONHUMAN; PRIMATE; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN VIRUS; STRUCTURE ACTIVITY RELATION; VAGINA; VIRUS INFECTION; VIRUS INHIBITION; VIRUS TRANSMISSION;

ANIMALS; ANTI-HIV AGENTS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HUMANS; MACACA MULATTA; NUCLEOCAPSID; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA MULATTA; PRIMATES; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 69449098051     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00820-09     Document Type: Article

References (39)

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. (Pubitemid 20148432)
2. Allain, B., M. Lapadat-Tapolsky, C. Berlioz, and J. L. Darlix. 1994. Transactivation of the minus-strand DNA transfer by nucleocapsid protein during reverse transcription of the retroviral genome. EMBO J. 13:973-981. (Pubitemid 24057530)
3. Berthoux, L., C. Pechoux, and J. L. Darlix. 1999. Multiple effects of an anti-human immunodeficiency virus nucleocapsid inhibitor on virus morphology and replication. J. Virol. 73:10000-10009.
4. Boadi, T., E. Schneider, S. Chung, L. Tsai, A. Gettie, M. Ratterree, J. Blanchard, A. R. Neurath, and C. Cheng-Mayer. 2005. Cellulose acetate 1,2-benzenedicarboxylate protects against challenge with pathogenic X4 and R5 simian/human immunodeficiency virus. AIDS 19:1587-1594. (Pubitemid 41502670)
5. Buckman, J. S., W. J. Bosche, and R. J. Gorelick. 2003. Human immunodeficiency virus type 1 nucleocapsid Zn2 fingers are required for efficient reverse transcription, initial integration processes, and protection of newly synthesized viral DNA. J. Virol. 77:1469-1480.
6. Burruano, B. T., R. L. Schnaare, and D. Malamud. 2002. Synthetic cervical mucus formulation. Contraception 66:137-140.
7. Cruceanu, M., M. A. Urbaneja, C. V. Hixson, D. G. Johnson, S. A. Datta, M. J. Fivash, A. G. Stephen, R. J. Fisher, R. J. Gorelick, J. R. Casas-Finet, A. Rein, I. Rouzina, and M. C. Williams. 2006. Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins. Nucleic Acids Res. 34:593-605. (Pubitemid 43240247)
8. Cutler, B., and J. Justman. 2008. Vaginal microbicides and the prevention of HIV transmission. Lancet Infect. Dis. 8:685-697.
9. Darlix, J. L., C. Gabus, M. T. Nugeyre, F. Clavel, and F. Barre-Sinoussi. 1990. Cis elements and trans-acting factors involved in the RNA dimerization of the human immunodeficiency virus HIV-1. J. Mol. Biol. 216:689-699.
10. Dezzutti, C. S., V. N. James, A. Ramos, S. T. Sullivan, A. Siddig, T. J. Bush, L. A. Grohskopf, L. Paxton, S. Subbarao, and C. E. Hart. 2004. In vitro comparison of topical microbicides for prevention of human immunodeficiency virus type 1 transmission. Antimicrob. Agents Chemother. 48:3834-3844.
11. Fletcher, P. S., G. S. Wallace, P. M. Mesquita, and R. J. Shattock. 2006. Candidate polyanion microbicides inhibit HIV-1 infection and dissemination pathways in human cervical explants. Retrovirology 3:46.
12. 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.
13. Greenhead, P., P. Hayes, P. S. Watts, K. G. Laing, G. E. Griffin, and R. J. Shattock. 2000. Parameters of human immunodeficiency virus infection of human cervical tissue and inhibition by vaginal virucides. J. Virol. 74:5577-5586. (Pubitemid 30346592)
14. Hendrix, C. W., Y. J. Cao, and E. J. Fuchs. 2009. Topical microbicides to prevent HIV: clinical drug development challenges. Annu. Rev. Pharmacol. Toxicol. 49:349-375.
15. Hu, Q., I. Frank, V. Williams, J. J. Santos, P. Watts, G. E. Griffin, J. P. Moore, M. Pope, and R. J. Shattock. 2004. Blockade of attachment and fusion receptors inhibits HIV-1 infection of human cervical tissue. J. Exp. Med. 199:1065-1075.
16. Klasse, P. J., R. Shattock, and J. P. Moore. 2008. Antiretroviral drug-based microbicides to prevent HIV-1 sexual transmission. Annu. Rev. Med. 59:455-471.
17. Klasse, P. J., R. J. Shattock, and J. P. Moore. 2006. Which topical microbicides for blocking HIV-1 transmission will work in the real world? PLoS Med. 3:e351.
18. Lys in vitro: studies of viral RNA molecules mutated in regions that flank the primer binding site. J. Virol. 70:4996-5004.
19. Marx, P. A., A. I. Spira, A. Gettie, P. J. Dailey, R. S. Veazey, A. A. Lackner, C. J. Mahoney, C. J. Miller, L. E. Claypool, D. D. Ho, and N. J. Alexander. 1996. Progesterone implants enhance SIV vaginal transmission and early virus load. Nat. Med. 2:1084-1089.
20. Miedema, F. 2008. A brief history of HIV vaccine research: stepping back to the drawing board? AIDS 22:1699-1703.
21. Miller Jenkins, L. M., T. Hara, S. R. Durell, R. Hayashi, J. K. Inman, J. P. Piquemal, N. Gresh, and E. Appella. 2007. Specificity of acyl transfer from 2-mercaptobenzamide thioesters to the HIV-1 nucleocapsid protein. J. Am. Chem. Soc. 129:11067-11078.
22. 1H NMR. EMBO J. 11:3059-3065.
23. Nagele, P. 2003. Misuse of standard error of the mean (SEM) when reporting variability of a sample. A critical evaluation of four anaesthesia journals. Br. J. Anaesth. 90:514-516.
24. Neurath, A. R., N. Strick, and Y. Y. Li. 2006. Role of seminal plasma in the anti-HIV-1 activity of candidate microbicides. BMC Infect. Dis. 6:150.
25. Omichinski, J. G., G. M. Clore, K. Sakaguchi, E. Appella, and A. M. Gronenborn. 1991. Structural characterization of a 39-residue synthetic peptide containing the two zinc binding domains from the HIV-1 p7 nucleocapsid protein by CD and NMR spectroscopy. FEBS Lett. 292:25-30.
26. Poljak, L., S. M. Batson, D. Ficheux, B. P. Roques, J. L. Darlix, and E. Kas. 2003. Analysis of NCp7-dependent activation of HIV-1 cDNA integration and its conservation among retroviral nucleocapsid proteins. J. Mol. Biol. 329:411-421.
27. Potts, B. 1990. Mini reverse transcriptase (RT) assay. In A. Aldovini and B. D. Walker (ed.), Techniques in HIV research. Stockton Press/MacMillan Publishers, New York, NY.
28. Rein, A., L. E. Henderson, and J. G. Levin. 1998. Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem. Sci. 23:297-301.
29. 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, S. L. Orloff, J. Mendeleyev, and E. Kun. 1993. Inhibition of HIV-1 infectivity by zinc-ejecting aromatic C-nitroso compounds. Nature 361:473-475.
30. 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.
31. Schito, M. L., A. Goel, Y. Song, J. K. Inman, R. J. Fattah, W. G. Rice, J. A. Turpin, A. Sher, and E. Appella. 2003. In vivo antiviral activity of novel human immunodeficiency virus type 1 nucleocapsid p7 zinc finger inhibitors in a transgenic murine model. AIDS Res. Hum. Retroviruses 19:91-101.
32. Schito, M. L., P. E. Kennedy, R. P. Kowal, E. A. Berger, and A. Sher. 2001. A human immunodeficiency virus-transgenic mouse model for assessing interventions that block microbial-induced proviral expression. J. Infect. Dis. 183:1592-1600.
33. Sekaly, R. P. 2008. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development? J. Exp. Med. 205:7-12.
34. South, T. L., P. R. Blake, D. R. Hare, and M. F. Summers. 1991. C-terminal retroviral-type zinc finger domain from the HIV-1 nucleocapsid protein is structurally similar to the N-terminal zinc finger domain. Biochemistry 30:6342-6349.
35. Srivastava, P., M. Schito, R. J. Fattah, T. Hara, T. Hartman, R. W. Buckheit, Jr., J. A. Turpin, J. K. Inman, and E. Appella. 2004. Optimization of unique, uncharged thioesters as inhibitors of HIV replication. Bioorg. Med. Chem. 12:6437-6450.
36. Tien, D., R. L. Schnaare, F. Kang, G. Cohl, T. J. McCormick, T. R. Moench, G. Doncel, K. Watson, R. W. Buckheit, M. G. Lewis, J. Schwartz, K. Douville, and J. W. Romano. 2005. In vitro and in vivo characterization of a potential universal placebo designed for use in vaginal microbicide clinical trials. AIDS Res. Hum. Retroviruses 21:845-853.
37. Trunova, N., L. Tsai, S. Tung, E. Schneider, J. Harouse, A. Gettie, V. Simon, J. Blanchard, and C. Cheng-Mayer. 2006. Progestin-based contraceptive suppresses cellular immune responses in SHIV-infected rhesus macaques. Virology 352:169-177. (Pubitemid 44142685)
38. 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.
39. Turpin, J. A., S. J. Terpening, C. A. Schaeffer, G. Yu, C. J. Glover, R. L. Felsted, E. A. Sausville, and W. G. Rice. 1996. Inhibitors of human immunodeficiency virus type 1 zinc fingers prevent normal processing of Gag precursors and result in the release of noninfectious virus particles. J. Virol. 70:6180-6189.