Incomplete protection against simian immunodeficiency virus vaginal transmission in rhesus macaques by a topical antiviral agent revealed by repeat challenges

Journal of Virology

Volumn 82, Issue 13, 2008, Pages 6591-6599

  Ambrose, Zandrea ^a,e   Compton, Lara ^b   Piatak Jr , Michael ^c   Lu, Ding ^b   Alvord, W Gregory ^a   Lubomirski, Mariusz S ^a   Hildreth, James E K ^d   Lifson, Jeffrey D ^c   Miller, Christopher J ^b   KewalRamani, Vineet N ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAIC FREDERICK INC   (United States)

^d MEHARRY MEDICAL COLLEGE   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYPROPYL BETA CYCLODEXTRIN; MICROBICIDE; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; CELL STRAIN CACO 2; CONTROLLED STUDY; DRUG CYTOTOXICITY; FEMALE; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROPHYLAXIS; RHESUS MONKEY; SEXUAL TRANSMISSION; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA; VIRUS INFECTION; VIRUS INHIBITION;

ANIMALS; ANTIVIRAL AGENTS; BETA-CYCLODEXTRINS; DISEASE TRANSMISSION, HORIZONTAL; FEMALE; HELA CELLS; HUMANS; MACACA MULATTA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VAGINAL CREAMS, FOAMS, AND JELLIES;

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

EID: 45749113763     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02730-07     Document Type: Article

References (47)

1. Alliance for Microbicide Development. 2007. Ongoing microbicide clinical trials (by product). Alliance for Microbicide Development, Silver Spring, MD.
2. Bibby, D. C., N. M. Davies, and I. G. Tucker. 2000. Mechanisms by which cyclodextrins modify drug release from polymeric drug delivery systems. Int J. Pharm. 197:1-11.
3. 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.
4. Cecilia, D., V. N. KewalRamani, J. O'Leary, B. Volsky, P. Nyambi, S. Burda, S. Xu, D. R. Littman, and S. Zolla-Pazner. 1998. Neutralization profiles of primary human immunodeficiency virus type 1 isolates in the context of coreceptor usage. J. Virol. 72:6988-6996.
5. Degim, Z., T. Degim, F. Acarturk, D. Erdogan, C. Ozogul, and M. Koksal. 2005. Rectal and vaginal administration of insulin-chitosan formulations: an experimental study in rabbits. J. Drug Target. 13:563-572.
6. + T cells. Nature 417:95-98.
7. Fleischman, J., and K. Cravero. 8 March 2004. A focus on women and AIDS. The Boston Globe, Boston, MA.
8. Graham, D. R. M., E. Chertova, J. M. Hilburn, L. O. Arthur, and J. E. K. Hildreth. 2003. Cholesterol depletion of HIV-1 and SIV with beta-cyclodextrin inactivates and permeabilizes the virions: evidence for virion-associated lipid rafts. J. Virol. 77:8237-8248.
9. Guyader, M., E. Kiyokawa, L. Abrami, P. Turelli, and D. Trono. 2002. Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization. J. Virol. 76:10356-10364.
10. Khanna, K. V., K. J. Whaley, L. Zeitlin, T. R. Moench, K. Mehrazar, R. A. Cone, Z. Liao, J. E. Hildreth, T. E. Hoen, L. Shultz, and R. B. Markham. 2002. Vaginal transmission of cell-associated HIV-1 in the mouse is blocked by a topical, membrane-modifying agent. J. Clin. Investig. 109:205-211.
11. Kilsdonk, E. P., P. G. Yancey, G. W. Stoudt, F. W. Bangerter, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1995. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270:17250-17256.
12. Kim, C. N., D. R. Adams, S. Bashirian, S. Butera, T. M. Folks, and R. A. Otten. 2006. Repetitive exposures with simian/human immunodeficiency viruses: strategy to study HIV pre-clinical interventions in non-human primates. J. Med. Primatol. 35:210-216.
13. Kish-Catalone, T., R. Pal, J. Parrish, N. Rose, L. Hocker, L. Hudacik, M. Reitz, R. Gallo, and A. Devico. 2007. Evaluation of -2 RANTES vaginal microbicide formulations in a nonhuman primate simian/human immunodeficiency virus (SHIV) challenge model. AIDS Res. Hum. Retrovir. 23:33-42.
14. Kreiss, J., E. Ngugi, K. Holmes, J. Ndinya-Achola, P. Waiyaki, P. L. Roberts, I. Ruminjo, R. Sajabi, J. Kimata, and T. R. Fleming. 1992. Efficacy of nonoxynol 9 contraceptive sponge use in preventing heterosexual acquisition of HIV in Nairobi prostitutes. JAMA 268:477-482.
15. Lederman, M. M., R. S. Veazey, R. Offord, D. E. Mosier, J. Dufour, M. Mefford, M. Piatak, Jr., J. D. Lifson, J. R. Salkowitz, B. Rodriguez, A. Blauvelt, and O. Hartley. 2004. Prevention of vaginal SHIV transmission in rhesus macaques through inhibition of CCR5. Science 306:485-487.
16. Lee, P. P., and M. L. Linial. 1994. Efficient particle formation can occur if the matrix domain of human immunodeficiency virus type 1 Gag is substituted by a myristylation signal. J. Virol. 68:6644-6654.
17. Lehner, T., L. A. Bergmeier, C. Panagiotidi, L. Tao, R. Brookes, L. S. Klavinskis, P. Walker, J. Walker, R. G. Ward, L. Hussein, et al. 1992. Induction of mucosal and systemic immunity to a recombinant simian immunodeficiency viral protein. Science 258:1365-1369.
18. Liao, Z., L. M. Cimakasky, R. Hampton, D. H. Nguyen, and J. E. Hildreth. 2001. Lipid rafts and HIV pathogenesis: host membrane cholesterol is required for infection by HIV type 1. AIDS Res. Hum. Retrovir. 17:1009-1019.
19. Liao, Z., D. R. Graham, and J. E. Hildreth. 2003. Lipid rafts and HIV pathogenesis: virion-associated cholesterol is required for fusion and infection of susceptible cells. AIDS Res. Hum Retrovir. 19:675-687.
20. Lu, X., H. Kiyono, D. Lu, S. Kawabata, J. Torten, S. Srinivasan, P. J. Dailey, J. R. McGhee, T. Lehner, and C. J. Miller. 1998. Targeted lymph-node immunization with whole inactivated simian immunodeficiency virus (SIV) or envelope and core subunit antigen vaccines does not reliably protect rhesus macaques from vaginal challenge with SIVmac251. AIDS 12:1-10.
21. Manes, S., G. del Real, R. A. Lacalle, P. Lucas, C. Gomez-Mouton, S. Sanchez-Palomino, R. Delgado, J. Alcami, E. Mira, and A. C. Martinez. 2000. Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. EMBO Rep. 1:190-196.
22. Manson, K. H., M. S. Wyand, C. Miller, and A. R. Neurath. 2000. Effect of a cellulose acetate phthalate topical cream on vaginal transmission of simian immunodeficiency virus in rhesus monkeys. Antimicrob. Agents Chemother. 44:3199-3202.
23. Mascola, J. R., G. Stiegler, T. C. VanCott, H. Katinger, C. B. Carpenter, C. E. Hanson, H. Beary, D. Hayes, S. S. Frankel, D. L. Birx, and M. G. Lewis. 2000. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6:207-210.
24. Nguyen, D. H., and J. E. Hildreth. 2000. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74:3264-3272.
25. O'Brien, W. A., Y. Koyanagi, A. Namazie, J. Q. Zhao, A. Diagne, K. Idler, J. A. Zack, and I. S. Chen. 1990. HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature 348:69-73.
26. Ono, A., and E. O. Freed. 2001. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. USA 98:13925-13930.
27. Parr, E. L., M. B. Parr, and M. Thapar. 1988. A comparison of specific antibody responses in mouse vaginal fluid after immunization by several routes. J. Reprod. Immunol. 14:165-176.
28. Parren, P. W., P. A. Marx, A. J. Hessell, A. Luckay, J. Harouse, C. Cheng-Mayer, J. P. Moore, and D. R. Burton. 2001. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75:8340-5347.
29. Ramjee, G., R. Govinden, N. S. Morar, and A. Mbewu. 2007. South Africa's experience of the closure of the cellulose sulphate microbicide trial. PLoS Med. 4:e235.
30. Rockefeller Foundation. 2002. Mobilization for microbicides: the decisive decade. Rockefeller Foundation, New York, NY.
31. Roddy, R. E., L. Zekeng, K. A. Ryan, U. Tamoufe, S. S. Weir, and E. L. Wong. 1998. A controlled trial of nonoxynol 9 film to reduce male-to-female transmission of sexually transmitted diseases. N. Engl. J. Med. 339:504-510.
32. Rustomjee, R., Q. Abdool Karim, S. S. Abdool Karim, M. Laga, and Z. Stein. 1999. Phase 1 trial of nonoxynol-9 film among sex workers in South Africa. AIDS 13:1511-1515.
33. Smith, S. M., G. B. Baskin, and P. A. Marx. 2000. Estrogen protects against vaginal transmission of simian immunodeficiency virus. J. Infect. Dis. 182:708-715.
34. Sodora, D. L., A. Gettie, C. J. Miller, and P. A. Marx. 1998. Vaginal transmission of SIV: assessing infectivity and hormonal influences in macaques inoculated with cell-free and cell-associated viral stocks. AIDS Res. Hum. Retrovir. 14(Suppl. 1):S119-123.
35. Spira, A. I., P. A. Marx, B. K. Patterson, J. Mahoney, R. A. Koup, S. M. Wolinsky, and D. D. Ho. 1996. Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J. Exp. Med. 183:215-225.
36. Suryanarayana, K., T. A. Wiltrout, G. M. Vasquez, V. M. Hirsch, and J. D. Lifson. 1998. Plasma SIV RNA viral load determination by real-time quantification of product generation in reverse transcriptase-polymerase chain reaction. AIDS Res. Hum. Retrovir. 14:183-189.
37. Tevi-Benissan, C., M. Makuva, A. Morelli, M. C. Georges-Courbot, M. Matta, A. Georges, and L. Belec. 2000. Protection of cynomolgus macaque against cervicovaginal transmission of SIVmac251 by the spermicide benzalkonium chloride. J. Acquir. Immune Defic. Syndr. Hum. Retroviral. 24:147-153.
38. Thapar, M. A., E. L. Parr, and M. B. Parr. 1990. The effect of adjuvants on antibody titers in mouse vaginal fluid after intravaginal immunization. J. Reprod. Immunol. 17:207-216.
39. Tsai, C. C., P. Emau, Y. Jiang, M. B. Agy, R. J. Shattock, A. Schmidt, W. R. Morton, K. R. Gustafson, and M. R. Boyd. 2004. Cyanovirin-N inhibits AIDS virus infections in vaginal transmission models. AIDS Res. Hum. Retrovir. 20:11-18.
40. Tsai, C. C., P. Emau, Y. Jiang, B. Tian, W. R. Morton, K. R. Gustafson, and M. R. Boyd. 2003. Cyanovirin-N gel as a topical microbicide prevents rectal transmission of SHIV89.6P in macaques. AIDS Res. Hum. Retrovir. 19:535-541.
41. UNAIDS. 2006. AIDS epidemic update. Joint United Nations Programme on HIV/AIDS and World Health Organization, Geneva, Switzerland.
42. Van Rompay, K. K., K. A. Schmidt, J. R. Lawson, R. Singh, N. Bischofberger, and M. L. Marthas. 2002. Topical administration of low-dose tenofovir disoproxil fumarate to protect infant macaques against multiple oral exposures of low doses of simian immunodeficiency virus. J. Infect. Dis. 186:1508-1513.
43. Veazey, R. S., P. J. Klasse, T. J. Ketas, J. D. Reeves, M. Piatak, Jr., K. Kunstman, S. E. Kuhmann, P. A. Marx, J. D. Lifson, J. Dufour, M. Mefford, I. Pandrea, S. M. Wolinsky, R. W. Doms, J. A. DeMartino, S. J. Siciliano, K. Lyons, M. S. Springer, and J. P. Moore. 2003. Use of a small molecule CCR5 inhibitor in macaques to treat simian immunodeficiency virus infection or prevent simian-human immunodeficiency virus infection. J. Exp. Med. 198:1551-1562.
44. Veazey, R. S., P. J. Klasse, S. M. Schader, Q. Hu, T. J. Ketas, M. Lu, P. A. Marx, J. Dufour, R. J. Colonno, R. J. Shattock, M. S. Springer, and J. P. Moore. 2005. Protection of macaques from vaginal SHIV challenge by vaginally delivered inhibitors of virus-cell fusion. Nature 438:99-102.
45. Veazey, R. S., R. J. Shattock, M. Pope, J. C. Kirijan, J. Jones, Q. Hu, T. Ketas, P. A. Marx, P. J. Klasse, D. R. Burton, and J. P. Moore. 2003. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat. Med. 9:343-346.
46. Veazey, R. S., M. S. Springer, P. A. Marx, J. Dufour, P. J. Klasse, and J. P. Moore. 2005. Protection of macaques from vaginal SHIV challenge by an orally delivered CCR5 inhibitor. Nat. Med. 11:1293-1294.
47. Wyand, M. S., K. H. Manson, C. J. Miller, and A. R. Neurath. 1999. Effect of 3-hydroxyphthaloyl-beta-lactoglobulin on vaginal transmission of simian immunodeficiency virus in rhesus monkeys. Antimicrob. Agents Chemother. 43:978-980.