A potent combination microbicide that targets SHIV-RT, HSV-2 and HPV

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Kizima, Larisa ^a   Rodríguez, Aixa ^a   Kenney, Jessica ^a   Derby, Nina ^a   Mizenina, Olga ^a   Menon, Radhika ^a   Seidor, Samantha ^a   Zhang, Shimin ^a   Levendosky, Keith ^a   Jean Pierre, Ninochka ^a   Pugach, Pavel ^a   Villegas, Guillermo ^a   Ford, Brian E ^a   Gettie, Agegnehu ^b   Blanchard, James ^c   Piatak Jr , Michael ^d   Lifson, Jeffrey D ^d   Paglini, Gabriela ^e   Teleshova, Natalia ^a   Zydowsky, Thomas M ^a   Robbiani, Melissa ^a   Fernández Romero, José A ^a,e   more..

^a POPULATION COUNCIL   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^e FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

MICROBICIDE; PLACEBO; ANTIINFECTIVE AGENT; CARRAGEENAN; GEL; MIV 150; PYRIDINE DERIVATIVE; RNA DIRECTED DNA POLYMERASE INHIBITOR; UREA; ZINC ACETATE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG DISTRIBUTION; DRUG POTENCY; DRUG SAFETY; DRUG STABILITY; DRUG TARGETING; FEMALE; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 2; HISTOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MACACA; MOUSE; NONHUMAN; PAPILLOMAVIRUS INFECTION; SEXUALLY TRANSMITTED DISEASE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN VIRUS; TREATMENT DURATION; WART VIRUS; ALPHAPAPILLOMAVIRUS; ANAL CANAL; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; CACO 2 CELL LINE; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GEL; HELA CELL LINE; HOST PATHOGEN INTERACTION; PAPILLOMAVIRUS INFECTIONS; PHYSIOLOGY; RECTUM; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; TREATMENT OUTCOME; VAGINA; VIROLOGY;

ALPHAPAPILLOMAVIRUS; ANAL CANAL; ANIMALS; ANTI-INFECTIVE AGENTS; CACO-2 CELLS; CARRAGEENAN; FEMALE; GELS; HELA CELLS; HERPES SIMPLEX; HERPESVIRUS 2, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA MULATTA; MICE, INBRED BALB C; PAPILLOMAVIRUS INFECTIONS; PYRIDINES; RECTUM; REVERSE TRANSCRIPTASE INHIBITORS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TREATMENT OUTCOME; UREA; VAGINA; ZINC ACETATE;

EID: 84899721240     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094547     Document Type: Article

References (70)

1. Houlihan CF, Larke NL, Watson-Jones D, Smith-McCune KK, Shiboski S, et al. (2012) Human papillomavirus infection and increased risk of HIV acquisition. A systematic review and meta-analysis. AIDS 26:. 2211-2222.
2. Corey L (2007) Herpes simplex virus type 2 and HIV-1: The dialogue between the 2 organisms continues. J Infect Dis 195: 1242-1244. (Pubitemid 46649606)
3. Jin XW, Lipold L, Sikon A, Rome E (2013) Human papillomavirus vaccine: safe, effective, underused. Cleve Clin J Med 80: 49-60.
4. Karim QA, Karim SSA, Frohlich JA, Grobler AC, Baxter C, et al. (2010) Effectiveness and Safety of Tenofovir Gel, an Antiretroviral Microbicide, for the Prevention of HIV Infection in Women. Science 329: 1168-1174.
5. Nel AM, Coplan P, Smythe SC, McCord K, Mitchnick M, et al. (2010) Pharmacokinetic assessment of dapivirine vaginal microbicide gel in healthy, HIV-negative women. AIDS Res Hum Retroviruses 26: 1181-1190.
6. Nel AM, Smythe SC, Habibi S, Kaptur PE, Romano JW (2010) Pharmacokinetics of 2 dapivirine vaginal microbicide gels and their safety vs. Hydroxyethyl cellulose-based universal placebo gel. J Acquir Immune Defic Syndr 55: 161- 169.
7. Johnson TJ, Gupta KM, Fabian J, Albright TH, Kiser PF (2010) Segmented polyurethane intravaginal rings for the sustained combined delivery of antiretroviral agents dapivirine and tenofovir. Eur J Pharm Sci 39: 203-212.
8. Fetherston SM, Boyd P, McCoy CF, McBride MC, Edwards KL, et al. (2012) A silicone elastomer vaginal ring for HIV prevention containing two microbicides with different mechanisms of action. Eur J Pharm Sci 48: 406-415.
9. Herrera C, Cranage M, McGowan I, Anton P, Shattock RJ (2011) Colorectal microbicide design: Triple combinations of reverse transcriptase inhibitors are optimal against HIV-1 in tissue explants. AIDS 25: 1971-1979.
10. Schader SM, Colby-Germinario SP, Schachter JR, Xu H, Wainberg MA (2011) Synergy against drug-resistant HIV-1 with the microbicide antiretrovirals, dapivirine and tenofovir, in combination. AIDS 25: 1585-1594.
11. Derby N, Zydowsky T, Robbiani M (2013) In search of the optimal delivery method for anti-HIV microbicides: Are intravaginal rings the way forward? Expert Rev Anti Infect Ther 11: 5-8.
12. Kenney J, Aravantinou M, Singer R, Hsu M, Rodriguez A, et al. (2011) An antiretroviral/zinc combination gel provides 24 hours of complete protection against vaginal SHIV infection in macaques. PLoS One 6: e15835.
13. Kenney J SR, Derby N, Aravantinou M, Abraham CJ, Menon R, et al. (2012) A Single Dose of a MIV-150/Zinc Acetate Gel Provides 24 h of Protection Against Vaginal Simian Human Immunodeficiency Virus Reverse Transcriptase Infection, with More Limited Protection Rectally 8-24 h After Gel Use. AIDS Res Hum Retroviruses. 2012 Nov;28(11):1476-84.
14. Fernandez-Romero JA, Abraham CJ, Rodriguez A, Kizima L, Jean-Pierre N, et al. (2012) Zinc acetate/carrageenan gels exhibit potent activity in vivo against high-dose herpes simplex virus 2 vaginal and rectal challenge. Antimicrob Agents Chemother 56: 358-368.
15. Buck CB, Thompson CD, Roberts JN, Muller M, Lowy DR, et al. (2006) Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog 2: e69.
16. Marais D, Gawarecki D, Allan B, Ahmed K, Altini L, et al. (2011) The effectiveness of Carraguard, a vaginal microbicide, in protecting women against high-risk human papillomavirus infection. Antivir Ther 16: 1219-1226.
17. Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, et al. (2007) Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med 13: 857-861. (Pubitemid 47038188)
18. Roberts JN, Kines RC, Katki HA, Lowy DR, Schiller JT (2011) Effect of Pap smear collection and carrageenan on cervicovaginal human papillomavirus-16 infection in a rhesus macaque model. J Natl Cancer Inst 103: 737-743.
19. National Research Council (2010) Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
20. Code of Federal Regulations (2001) Animal Welfare Act and Regulation. Chapter 1, subchapter A: Animals and animal products, Ed. (U.S Department of Agriculture, Beltsville, MD).
21. Geitmann M, Unge T, Danielson UH (2006) Biosensor-based kinetic characterization of the interaction between HIV-1 reverse transcriptase and non-nucleoside inhibitors. Journal of medicinal chemistry 49: 2367-2374.
22. Tien D, Schnaare RL, Kang F, Cohl G, McCormick TJ, et al. (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. (Pubitemid 43150316)
23. Kenney J, Rodriguez A, Kizima L, Seidor S, Menon R, et al. (2013) A Potential Non-ARV Microbicide - A Modified Zinc Acetate Gel is Safe and Effective Against SHIV-RT and HSV-2 infection In Vivo. Antimicrobial agents and chemotherapy. 2013 Aug;57(8):4001-9.
24. Trkola A, Matthews J, Gordon C, Ketas T, Moore JP (1999) A cell line-based neutralization assay for primary human immunodeficiency virus type 1 isolates that use either the CCR5 or the CXCR4 coreceptor. J Virol 73: 8966-8974. (Pubitemid 29487049)
25. Ashley R (1995) Diagnostic procedures for viral, rickettsial, and chlamydial infections. In: Schmidt NJ ER, editor. 7th ed: American public health Association. pp. 383.
26. Johnson KM, Kines RC, Roberts JN, Lowy DR, Schiller JT, et al. (2009) Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J Virol 83: 2067-2074.
27. Begay O, Jean-Pierre N, Abraham CJ, Chudolij A, Seidor S, et al. (2011) Identification of personal lubricants that can cause rectal epithelial cell damage and enhance HIV type 1 replication in vitro. AIDS Res Hum Retroviruses 27: 1019-1024.
28. Fernandez-Romero JA, Thorn M, Turville SG, Titchen K, Sudol K, et al. (2007) Carrageenan/MIV-150 (PC-815), a combination microbicide. Sex Transm Dis 34: 9-14. (Pubitemid 46041501)
29. Rohan LC, Moncla BJ, Kunjara Na Ayudhya RP, Cost M, Huang Y, et al. (2010) In vitro and ex vivo testing of tenofovir shows it is effective as an HIV-1 microbicide. PLoS One 5: e9310.
30. Singer R, Derby N, Rodriguez A, Kizima L, Kenney J, et al. (2011) The nonnucleoside reverse transcriptase inhibitor MIV-150 in carrageenan gel prevents rectal transmission of simian/human immunodeficiency virus infection in macaques. J Virol 85: 5504-5512.
31. Cline AN, Bess JW, Piatak M Jr., Lifson JD (2005) Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J Med Primatol 34: 303-312. (Pubitemid 41179592)
32. Smith SM, Holland B, Russo C, Dailey PJ, Marx PA, et al. (1999) Retrospective analysis of viral load and SIV antibody responses in rhesus macaques infected with pathogenic SIV: predictive value for disease progression. AIDS Res Hum Retroviruses 15: 1691-1701.
33. Aravantinou M, Singer R, Derby N, Calenda G, Mawson P, et al. (2012) The nonnucleoside reverse transcription inhibitor MIV-160 delivered from an intravaginal ring, but not from a carrageenan gel, protects against simian/human immunodeficiency virus-RT Infection. AIDS Res Hum Retroviruses 28: 1467-1475.
34. Catalone BJ, Kish-Catalone TM, Budgeon LR, Neely EB, Ferguson M, et al. (2004) Mouse model of cervicovaginal toxicity and inflammation for preclinical evaluation of topical vaginal microbicides. Antimicrobial agents and chemotherapy 48: 1837-1847. (Pubitemid 38544396)
35. Turville SG, Aravantinou M, Miller T, Kenney J, Teitelbaum A, et al. (2008) Efficacy of Carraguard-based microbicides in vivo despite variable in vitro activity. PLoS One 3: e3162.
36. Chvapil M, Chvapil TA, Owen JA, Kantor M, Ulreich JB, et al. (1979) Reaction of vaginal tissue of rabbits to inserted sponges made of various materials. J Biomed Mater Res 13: 1-13. (Pubitemid 9105594)
37. Fahim MS, Wang M (1996) Zinc acetate and lyophilized aloe barbadensis as vaginal contraceptive. Contraception 53: 231-236. (Pubitemid 26118152)
38. Alexander TH, Davidson TM (2006) Intranasal zinc and anosmia: The zincinduced anosmia syndrome. Laryngoscope 116: 217-220. (Pubitemid 44383926)
39. Bourne N, Stegall R, Montano R, Meador M, Stanberry LR, et al. (2005) Efficacy and toxicity of zinc salts as candidate topical microbicides against vaginal herpes simplex virus type 2 infection. Antimicrob Agents Chemother 49: 1181-1183. (Pubitemid 40327743)
40. Spinazzi M, Armani M (2009) Denture cream: An unusual source of excess zinc, leading to hypocupremia and neurologic disease. Neurology 73: 76.
41. Kilmarx PH, Blanchard K, Chaikummao S, Friedland BA, Srivirojana N, et al. (2008) A randomized, placebo-controlled trial to assess the safety and acceptability of use of carraguard vaginal gel by heterosexual couples in Thailand. Sex Transm Dis 35: 226-232. (Pubitemid 351619516)
42. Kilmarx PH, vandeWijgert JH, Chaikummao S, Jones HE, Limpakarnjanarat K, et al. (2006) Safety and acceptability of the candidate microbicide Carraguard in Thai Women: findings from a Phase II Clinical Trial. J Acquir Immune Defic Syndr 43: 327-334. (Pubitemid 44674014)
43. Martin S, Blanchard K, Manopaiboon C, Chaikummao S, Schaffer K, et al. (2010) Carraguard acceptability among men and women in a couples study in Thailand. J Womens Health (Larchmt) 19: 1561-1567.
44. McLean CA, vandeWijgert JH, Jones HE, Karon JM, McNicoll JM, et al. (2010) HIV genital shedding and safety of Carraguard use by HIV-infected women: A crossover trial in Thailand. AIDS 24: 717-722.
45. Skoler-Karpoff S, Ramjee G, Ahmed K, Altini L, Plagianos MG, et al. (2008) Efficacy of Carraguard for prevention of HIV infection in women in South Africa: A randomised, double-blind, placebo-controlled trial. Lancet 372: 1977- 1987.
46. Whitehead SJ, Kilmarx PH, Blanchard K, Manopaiboon C, Chaikummao S, et al. (2006) Acceptability of Carraguard vaginal gel use among Thai couples. AIDS 20: 2141-2148. (Pubitemid 44684704)
47. Whitehead SJ, McLean C, Chaikummao S, Braunstein S, Utaivoravit W, et al. (2011) Acceptability of Carraguard vaginal microbicide gel among HIV-infected women in Chiang Rai, Thailand. PLoS One 6: e14831.
48. Fletcher PS, Wallace GS, Mesquita PM, Shattock RJ (2006) Candidate polyanion microbicides inhibit HIV-1 infection and dissemination pathways in human cervical explants. Retrovirology 3: 46.
49. Hirano T, Murakami M, Fukada T, Nishida K, Yamasaki S, et al. (2008) Roles of zinc and zinc signaling in immunity: zinc as an intracellular signaling molecule. Adv Immunol 97: 149-176. (Pubitemid 351697819)
50. Mocchegiani E, Giacconi R, Muzzioli M, Cipriano C (2000) Zinc, infections and immunosenescence. Mech Ageing Dev 121: 21-35. (Pubitemid 32115397)
51. Mocchegiani E, Muzzioli M, Giacconi R (2000) Zinc and immunoresistance to infection in aging: new biological tools. Trends Pharmacol Sci 21: 205-208. (Pubitemid 30331087)
52. Mocchegiani E, Muzzioli M, Giacconi R (2000) Zinc, metallothioneins, immune responses, survival and ageing. Biogerontology 1: 133-143.
53. Rink L, Kirchner H (2000) Zinc-altered immune function and cytokine production. J Nutr 130: 1407S-1411S. (Pubitemid 30244138)
54. Chateau M, Swanson MD, Garcia JV (2013) Inefficient vaginal transmission of tenofovir-resistant HIV-1. J Virol 87: 1274-1277.
55. Hurt CB, Eron JJ Jr., Cohen MS (2011) Pre-exposure prophylaxis and antiretroviral resistance: HIV prevention at a cost? Clin Infect Dis 53: 1265- 1270.
56. Bernstein DI, Stanberry LR, Sacks S, Ayisi NK, Gong YH, et al. (2003) Evaluations of unformulated and formulated dendrimer-based microbicide candidates in mouse and guinea pig models of genital herpes. Antimicrob Agents Chemother 47: 3784-3788. (Pubitemid 37484989)
57. Nixon B, Stefanidou M, Mesquita PM, Fakioglu E, Segarra T, et al. (2013) Griffithsin Protects Mice from Genital Herpes by Preventing Cell-to-Cell Spread. J Virol 87: 6257-6269.
58. Segarra TJ, Fakioglu E, Cheshenko N, Wilson SS, Mesquita PM, et al. (2011) Bridging the gap between preclinical and clinical microbicide trials: blind evaluation of candidate gels in murine models of efficacy and safety. PLoS One 6: e27675.
59. Delbello A, Colli C, Martinez Tdel R, Trevisan G (2010) Anal canal and rectal condylomatosis: exhaustive proctological examination and STD patients. Acta Dermatovenerol Alp Panonica Adriat 19: 13-16.
60. Handisurya A, Day PM, Thompson CD, Buck CB, Kwak K, et al. (2012) Murine skin and vaginal mucosa are similarly susceptible to infection by pseudovirions of different papillomavirus classifications and species. Virology 433: 385-394.
61. McGowan I (2011) Rectal microbicides: can we make them and will people use them? AIDS and behavior 15 Suppl 1: S66-S71.
62. Crostarosa F, Aravantinou M, Akpogheneta OJ, Jasny E, Shaw A, et al. (2009) A macaque model to study vaginal HSV-2/immunodeficiency virus co-infection and the impact of HSV-2 on microbicide efficacy. PLoS One 4: e8060.
63. Moench TR, Mumper RJ, Hoen TE, Sun M, Cone RA (2010) Microbicide excipients can greatly increase susceptibility to genital herpes transmission in the mouse. BMC infectious diseases 10: 331.
64. Moncla BJ, Pryke K, Rohan LC, Yang H (2012) Testing of viscous anti-HIV microbicides using Lactobacillus. J Microbiol Methods 88: 292-296.
65. Veazey RS (2013) Animal models for microbicide safety and efficacy testing. Current opinion in HIV and AIDS 8: 295-303.
66. Veazey RS, Shattock RJ, Klasse PJ, Moore JP (2012) Animal models for microbicide studies. Current HIV research 10: 79-87.
67. Veazey RS, Shattock RJ, Pope M, Kirijan JC, Jones J, et al. (2003) Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nature medicine 9: 343-346. (Pubitemid 36362791)
68. Wilson SS, Cheshenko N, Fakioglu E, Mesquita PM, Keller MJ, et al. (2009) Susceptibility to genital herpes as a biomarker predictive of increased HIV risk: expansion of a murine model of microbicide safety. Antiviral therapy 14: 1113- 1124.
69. Zak O, O'Reilly T (1991) Animal models in the evaluation of antimicrobial agents. Antimicrobial agents and chemotherapy 35: 1527-1531.
70. vanderStraten A, Van Damme L, Haberer JE, Bangsberg DR (2012) Unraveling the divergent results of pre-exposure prophylaxis trials for HIV prevention. AIDS 26: F13-F19. Development