Non-Human Primate Models of Hormonal Contraception and HIV

American Journal of Reproductive Immunology

Volumn 71, Issue 6, 2014, Pages 513-522

  Mcnicholl, Janet M ^a   Henning, Tara C ^a   Vishwanathan, Sundaram A ^a   Kersh, Ellen N ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

Acquisition risk; Immune; Macaque; Progesterone; Simian immunodeficiency viruses (SIV); SIVs expressing HIV genes

Indexed keywords

BIOLOGICAL MARKER; CONTRACEPTIVE AGENT; DESOGESTREL PLUS ETHINYLESTRADIOL; EMTRICITABINE PLUS TENOFOVIR DISOPROXIL; ESTRADIOL; ESTRIOL; ESTROGEN; GESTAGEN; LEVONORGESTREL; MEDROXYPROGESTERONE ACETATE; PROGESTERONE; ORAL CONTRACEPTIVE AGENT;

ARTICLE; HORMONAL CONTRACEPTION; HORMONAL REGULATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFECTION PREVENTION; INFECTION RISK; MACACA FASCICULARIS; MACACA NEMESTRINA; MENSTRUAL CYCLE; NONHUMAN; PATHOGENESIS; PRIMATE MODEL; PRIORITY JOURNAL; RHESUS MONKEY; RISK FACTOR; SIMIAN IMMUNODEFICIENCY VIRUS; ANIMAL; ANIMAL MODEL; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; METABOLISM; PATHOGENICITY; PATHOLOGY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TRANSMISSION; VAGINA;

ANIMALS; CONTRACEPTIVES, ORAL, HORMONAL; ESTRADIOL; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; MACACA; MEDROXYPROGESTERONE ACETATE; MODELS, ANIMAL; PROGESTERONE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VAGINA;

EID: 84900829748     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12246     Document Type: Article

References (90)

1. Kersh E, Henning T, Vishwanathan SA, Hanson DL, Morris M, Butler K, Adams DR, Guenthner P, Srinivasan P, Smith J, Radzio J, Garcia-Lerma JG, Dobard C, Heneine W, McNicholl J: SHIV susceptibility changes during the menstrual cycle of pigtail macaques. J Med Primatol 2014, In press.
2. Marx PA, Spira AI, Gettie A, Dailey PJ, Veazey RS, Lackner AA, Mahoney CJ, Miller CJ, Claypool LE, Ho DD, Alexander NJ: Progesterone implants enhance SIV vaginal transmission and early virus load. Nat Med 1996; 2:1084-1089.
3. Smith SM, Baskin GB, Marx PA: Estrogen protects against vaginal transmission of simian immunodeficiency virus. J Infect Dis 2000; 182:708-715.
4. Smith SM, Mefford M, Sodora D, Klase Z, Singh M, Alexander N, Hess D, Marx PA: Topical estrogen protects against SIV vaginal transmission without evidence of systemic effect. AIDS 2004; 18:1637-1643.
5. Sodora DL, Gettie A, Miller CJ, Marx PA: Vaginal transmission of SIV: assessing infectivity and hormonal influences in macaques inoculated with cell-free and cell-associated viral stocks. AIDS Res Hum Retroviruses 1998; 14(Suppl 1):S119-S123.
6. Vishwanathan SA, Guenthner PC, Lin CY, Dobard C, Sharma S, Adams DR, Otten RA, Heneine W, Hendry RM, McNicholl JM, Kersh EN: High susceptibility to repeated, low-dose, vaginal SHIV exposure late in the luteal phase of the menstrual cycle of pigtail macaques. J Acquir Immune Defic Syndr 2011; 57:261-264.
7. Veazey RS: Animal models for microbicide safety and efficacy testing. Curr Opin HIV AIDS 2013; 8:295-303.
8. Polis CB, Curtis KM: Use of hormonal contraceptives and HIV acquisition in women: a systematic review of the epidemiological evidence. Lancet Infect Dis 2013; 13:797-808.
9. Ralph LJ, McCoy SI, Hallett T, Padian N: Next steps for research on hormonal contraception and HIV. Lancet 2013; 382:1467-1469.
10. Food and Drug Administration: FDA approves first drug for reducing risk of sexually acquired HIV infection (Press Release), 2012. Available at http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm312210.htm.
11. Food and Drug Administration: US prescribing information for truvada (emtricitabine/tenofovir disoproxil fumarate) tablets, for oral use, 2012. Available at http://www.accessdata.fda.gov/drugsatfda_docs/label/2012/021752s031lbl.pdf.
12. Dobard C, Sharma S, Martin A, Pau CP, Holder A, Kuklenyik Z, Lipscomb J, Hanson DL, Smith J, Novembre FJ, Garcia-Lerma JG, Heneine W: Durable protection from vaginal simian-human immunodeficiency virus infection in macaques by tenofovir gel and its relationship to drug levels in tissue. J Virol 2012; 86:718-725.
13. Garcia-Lerma JG, Cong ME, Mitchell J, Youngpairoj AS, Zheng Q, Masciotra S, Martin A, Kuklenyik Z, Holder A, Lipscomb J, Pau CP, Barr JR, Hanson DL, Otten R, Paxton L, Folks TM, Heneine W: Intermittent prophylaxis with oral truvada protects macaques from rectal SHIV infection. Sci Transl Med 2010; 2:14ra14.
14. Garcia-Lerma JG, Otten RA, Qari SH, Jackson E, Cong ME, Masciotra S, Luo W, Kim C, Adams DR, Monsour M, Lipscomb J, Johnson JA, Delinsky D, Schinazi RF, Janssen R, Folks TM, Heneine W: Prevention of rectal SHIV transmission in macaques by daily or intermittent prophylaxis with emtricitabine and tenofovir. PLoS Med 2008; 5:e28.
15. Parikh UM, Dobard C, Sharma S, Cong ME, Jia H, Martin A, Pau CP, Hanson DL, Guenthner P, Smith J, Kersh E, Garcia-Lerma JG, Novembre FJ, Otten R, Folks T, Heneine W: Complete protection from repeated vaginal simian-human immunodeficiency virus exposures in macaques by a topical gel containing tenofovir alone or with emtricitabine. J Virol 2009; 83:10358-10365.
16. Subbarao S, Otten RA, Ramos A, Kim C, Jackson E, Monsour M, Adams DR, Bashirian S, Johnson J, Soriano V, Rendon A, Hudgens MG, Butera S, Janssen R, Paxton L, Greenberg AE, Folks TM: Chemoprophylaxis with tenofovir disoproxil fumarate provided partial protection against infection with simian human immunodeficiency virus in macaques given multiple virus challenges. J Infect Dis 2006; 194:904-911.
17. Garcia-Lerma JG, Heneine W: Animal models of antiretroviral prophylaxis for HIV prevention. Curr Opin HIV AIDS 2012; 7:505-513.
18. Baeten JM, Haberer JE, Liu AY, Sista N: Preexposure prophylaxis for HIV prevention: where have we been and where are we going? J Acquir Immune Defic Syndr 2013; 63(Suppl 2):S122-S129.
19. Garcia-Lerma JG, Aung W, Cong ME, Zheng Q, Youngpairoj AS, Mitchell J, Holder A, Martin A, Kuklenyik S, Luo W, Lin CY, Hanson DL, Kersh E, Pau CP, Ray AS, Rooney JF, Lee WA, Heneine W: Natural substrate concentrations can modulate the prophylactic efficacy of nucleotide HIV reverse transcriptase inhibitors. J Virol 2011; 85:6610-6617.
20. Nuttall J, Kashuba A, Wang R, White N, Allen P, Roberts J, Romano J: Pharmacokinetics of tenofovir following intravaginal and intrarectal administration of tenofovir gel to rhesus macaques. Antimicrob Agents Chemother 2012; 56:103-109.
21. Hendrix CW: Exploring concentration response in HIV pre-exposure prophylaxis to optimize clinical care and trial design. Cell 2013; 155:515-518.
22. Bourry O, Brochard P, Souquiere S, Makuwa M, Calvo J, Dereudre-Bosquet N, Martinon F, Benech H, Kazanji M, Le Grand R: Prevention of vaginal simian immunodeficiency virus transmission in macaques by postexposure prophylaxis with zidovudine, lamivudine and indinavir. AIDS 2009; 23:447-454.
23. Kish-Catalone T, Pal R, Parrish J, Rose N, Hocker L, Hudacik L, Reitz M, Gallo R, Devico A: Evaluation of -2 RANTES vaginal microbicide formulations in a nonhuman primate simian/human immunodeficiency virus (SHIV) challenge model. AIDS Res Hum Retroviruses 2007; 23:33-42.
24. Salle B, Brochard P, Bourry O, Mannioui A, Andrieu T, Prevot S, Dejucq-Rainsford N, Dereuddre-Bosquet N, Le Grand R: Infection of macaques after vaginal exposure to cell-associated simian immunodeficiency virus. J Infect Dis 2010; 202:337-344.
25. Tevi-Benissan C, Makuva M, Morelli A, Georges-Courbot MC, Matta M, Georges A, Belec L: Protection of cynomolgus macaque against cervicovaginal transmission of SIVmac251 by the spermicide benzalkonium chloride. J Acquir Immune Defic Syndr 2000; 24:147-153.
26. Patton DL, Sweeney YC, Tsai CC, Hillier SL: Macaca fascicularis vs. Macaca nemestrina as a model for topical microbicide safety studies. J Med Primatol 2004; 33:105-108.
27. Hashway SA, Bergin IL, Bassis CM, Uchihashi M, Schmidt KC, Young VB, Aronoff DM, Patton DL, Bell JD: Impact of a hormone-releasing intrauterine system on the vaginal microbiome: a prospective baboon model. J Med Primatol 2013; 43:89-99.
28. Ace CI, Okulicz WC: Microarray profiling of progesterone-regulated endometrial genes during the rhesus monkey secretory phase. Reprod Biol Endocrinol 2004; 2:54.
29. Batten CJ, De Rose R, Wilson KM, Agy MB, Chea S, Stratov I, Montefiori DC, Kent SJ: Comparative evaluation of simian, simian-human, and human immunodeficiency virus infections in the pigtail macaque (Macaca nemestrina) model. AIDS Res Hum Retroviruses 2006; 22:580-588.
30. Blakley GB, Beamer TW, Dukelow WR: Characteristics of the menstrual cycle in nonhuman primates. IV. Timed mating in Macaca nemestrina. Lab Anim 1981; 15:351-353.
31. Chang J, Jain S, Carl DJ, Paolella L, Darveau RP, Gravett MG, Adams Waldorf KM: Differential host response to LPS variants in amniochorion and the TLR4/MD-2 system in Macaca nemestrina. Placenta 2010; 31:811-817.
32. Crostarosa F, Aravantinou M, Akpogheneta OJ, Jasny E, Shaw A, Kenney J, Piatak M, Lifson JD, Teitelbaum A, Hu L, Chudolij A, Zydowsky TM, Blanchard J, Gettie A, Robbiani M: A macaque model to study vaginal HSV-2/immunodeficiency virus co-infection and the impact of HSV-2 on microbicide efficacy. PLoS ONE 2009; 4:e8060.
33. Engel RM, Morris M, Henning T, Ritter JM, Jones TL, Dietz S, Ayers J, Vishwanathan SA, Jenkins L, Zaki S, Wildemeersch D, Garber D, Powell N, Michael Hendry R, McNicholl J, Kersh EN: Evaluation of pigtail macaques as a model for the effects of copper intrauterine devices on HIV infection. J Med Primatol 2013; doi:10.1111/jmp.12096.
34. Hatziioannou T, Ambrose Z, Chung NP, Piatak M Jr, Yuan F, Trubey CM, Coalter V, Kiser R, Schneider D, Smedley J, Pung R, Gathuka M, Estes JD, Veazey RS, KewalRamani VN, Lifson JD, Bieniasz PD: A macaque model of HIV-1 infection. Proc Natl Acad Sci USA 2009; 106:4425-4429.
35. Henning T, Butler K, Hanson DL, Sturdevant G, Ellis S, Sweeney E, Mitchell J, Deyounks F, Phillips C, Farshy C, Fakile Y, Papp J, Secor WE, Caldwell HD, Patton D, McNicholl J, Kersh E: Increased Susceptibility to Vaginal SHIV Transmission in Pigtail Macaques Coinfected with Chlamydia trachomatis and Trichomonas vaginalis. J Infect Dis 2014 (under review).
36. Henning T, Fakile Y, Phillips C, Sweeney E, Mitchell J, Patton D, Sturdevant G, Caldwell HD, Secor WE, Papp J, Hendry RM, McNicholl J, Kersh E: Development of a pigtail macaque model of sexually transmitted infection/HIV coinfection using Chlamydia trachomatis, Trichomonas vaginalis, and SHIV(SF162P3). J Med Primatol 2011; 40:214-223.
37. Hessell AJ, Poignard P, Hunter M, Hangartner L, Tehrani DM, Bleeker WK, Parren PW, Marx PA, Burton DR: Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat Med 2009; 15:951-954.
38. Hild-Petito S, Veazey RS, Larner JM, Reel JR, Blye RP: Effects of two progestin-only contraceptives, Depo-Provera and Norplant-II, on the vaginal epithelium of rhesus monkeys. AIDS Res Hum Retroviruses 1998; 14(Suppl 1):S125-S130.
39. Klatt NR, Canary LA, Vanderford TH, Vinton CL, Engram JC, Dunham RM, Cronise HE, Swerczek JM, Lafont BA, Picker LJ, Silvestri G, Brenchley JM: Dynamics of simian immunodeficiency virus SIVmac239 infection in pigtail macaques. J Virol 2012; 86:1203-1213.
40. Livingston L, Sweeney E, Mitchell J, Luo W, Paul K, Powell N, Michael Hendry R, McNicholl J, Kersh E: Hormonal synchronization of the menstrual cycles of pigtail macaques to facilitate biomedical research including modeling HIV susceptibility. J Med Primatol 2011; 40:164-170.
41. Otten RA, Adams DR, Kim CN, Jackson E, Pullium JK, Lee K, Grohskopf LA, Monsour M, Butera S, Folks TM: Multiple vaginal exposures to low doses of R5 simian-human immunodeficiency virus: strategy to study HIV preclinical interventions in nonhuman primates. J Infect Dis 2005; 191:164-173.
42. Patton D, Butler K, Cosgrove-Sweeney YT, Tsai CC, Doncel G, Saifuddon M: Chlamydia trachomatis plus SHIV: co-infection model development in the pigtailed macaque. In Chlamydia Infections, M. Chernesky (ed). Ontario, Canada, Elsevier Biomedical Press, 2006, pp 412-424.
43. Patton DL, Sweeney YC, Rabe LK, Hillier SL: The vaginal microflora of pig-tailed macaques and the effects of chlorhexidine and benzalkonium on this ecosystem. Sex Transm Dis 1996; 23:489-493.
44. Patton DL, Sweeney YT, Balkus JE, Rohan LC, Moncla BJ, Parniak MA, Hillier SL: Preclinical safety assessments of UC781 anti-human immunodeficiency virus topical microbicide formulations. Antimicrob Agents Chemother 2007; 5:1608-1615.
45. Poonia B, Walter L, Dufour J, Harrison R, Marx PA, Veazey RS: Cyclic changes in the vaginal epithelium of normal rhesus macaques. J Endocrinol 2006; 190:829-835.
46. Promadej-Lanier N, Hanson DL, Srinivasan P, Luo W, Adams DR, Guenthner PC, Butera S, Otten RA, Kersh EN: Resistance to Simian HIV infection is associated with high plasma interleukin-8, RANTES and Eotaxin in a macaque model of repeated virus challenges. J Acquir Immune Defic Syndr 2010; 53:574-581.
47. Radzio J, Hanley K, Hanson DL, Mitchell J, Bachman S, Deyounks F, Heneine W, Garcia-Lerma JG: The injectable contraceptive Depo-Provera does not reduce the prophylactic efficacy of Truvada in pigtail macaques. Conference on Retroviruses and Opportunistic Infections Atlanta, GA, 2013.
48. Radzio J, Hanley K, Mitchell J, Ellis S, Deyounks F, Jenkins L, Hanson DL, Heneine W, Garcia-Lerma JG: Physiologic doses of depot-medroxyprogesterone acetate do not increase acute plasma SHIV viremia or mucosal virus shedding in pigtail macaques. AIDS, 2013 (submitted).
49. Riesen JW, Meyer RK, Wolf RC: The effect of season on occurrence of ovulation in the rhesus monkey. Biol Reprod 1971; 5:111-114.
50. Rowell TE: Behaviour and female reproductive cycles of rhesus macaques. J Reprod Fertil 1963; 6:193-203.
51. Schlievert PM, Strandberg KL, Brosnahan AJ, Peterson ML, Pambuccian SE, Nephew KR, Brunner KG, Schultz-Darken NJ, Haase AT: Glycerol monolaurate does not alter rhesus macaque (Macaca mulatta) vaginal lactobacilli and is safe for chronic use. Antimicrob Agents Chemother 2008; 52:4448-4454.
52. Spear GT, Gilbert D, Sikaroodi M, Doyle L, Green L, Gillevet PM, Landay AL, Veazey RS: Identification of rhesus macaque genital microbiota by 16S pyrosequencing shows similarities to human bacterial vaginosis: implications for use as an animal model for HIV vaginal infection. AIDS Res Hum Retroviruses 2010; 26:193-200.
53. Spear GT, Kersh E, Guenthner P, Vishwanathan SA, Gilbert D, Zariffard MR, Mirmonsef P, Landay A, Zheng L, Gillevet P: Longitudinal assessment of pigtailed macaque lower genital tract microbiota by pyrosequencing reveals dissimilarity to the genital microbiota of healthy humans. AIDS Res Hum Retroviruses 2012; 28:1244-1249.
54. Veazey RS: Microbicide safety/efficacy studies in animals: macaques and small animal models. Curr Opin HIV AIDS 2008; 3:567-573.
55. Veazey RS, Shattock RJ, Klasse PJ, Moore JP: Animal models for microbicide studies. Curr HIV Res 2012; 10:79-87.
56. Hadzic S, Wang X, Dufour J, Doyle L, Marx PA, Lackner AA, Paulsen DB, Veazey R: Comparison of the vaginal environment of Macaca mulatta and Macaca nemestrina throughout the menstrual cycle. Am J Reprod Immunol 2014; 71:322-329.
57. Chen Z, Huang Y, Zhao X, Skulsky E, Lin D, Ip J, Gettie A, Ho DD: Enhanced infectivity of an R5-tropic simian/human immunodeficiency virus carrying human immunodeficiency virus type 1 subtype C envelope after serial passages in pig-tailed macaques (Macaca nemestrina). J Virol 2000; 74:6501-6510.
58. Mirmonsef P, Gilbert D, Veazey RS, Wang J, Kendrick SR, Spear GT: A comparison of lower genital tract glycogen and lactic acid levels in women and macaques: implications for HIV and SIV susceptibility. AIDS Res Hum Retroviruses 2012; 28:76-81.
59. Hanna NF, Taylor-Robinson D, Kalodiki-Karamanoli M, Harris JR, McFadyen IR: The relation between vaginal pH and the microbiological status in vaginitis. Br J Obstet Gynaecol 1985; 92:1267-1271.
60. Carias AM, McCoombe S, McRaven M, Anderson M, Galloway N, Vandergrift N, Fought AJ, Lurain J, Duplantis M, Veazey RS, Hope TJ: Defining the interaction of HIV-1 with the mucosal barriers of the female reproductive tract. J Virol 2013; 87:11388-11400.
61. Howell AL, Edkins RD, Rier SE, Yeaman GR, Stern JE, Fanger MW, Wira CR: Human immunodeficiency virus type 1 infection of cells and tissues from the upper and lower human female reproductive tract. J Virol 1997; 71:3498-3506.
62. Kaushic C, Ferreira VH, Kafka JK, Nazli A: HIV infection in the female genital tract: discrete influence of the local mucosal microenvironment. Am J Reprod Immunol 2010; 63:566-575.
63. Ma Z, Lu FX, Torten M, Miller CJ: The number and distribution of immune cells in the cervicovaginal mucosa remain constant throughout the menstrual cycle of rhesus macaques. Clin Immunol 2001; 100:240-249.
64. Parakkal PF, Gregoire AT: Differentiation of vaginal epithelium in the normal and hormone-treated rhesus monkey. Biol Reprod 1972; 6:117-130.
65. Mauck CK, Callahan MM, Baker J, Arbogast K, Veazey R, Stock R, Pan Z, Morrison CS, Chen-Mok M, Archer DF, Gabelnick HL: The effect of one injection of Depo-Provera on the human vaginal epithelium and cervical ectopy. Contraception 1999; 60:15-24.
66. Miller L, Patton DL, Meier A, Thwin SS, Hooton TM, Eschenbach DA: Depomedroxyprogesterone-induced hypoestrogenism and changes in vaginal flora and epithelium. Obstet Gynecol 2000; 96:431-439.
67. Nanda K, Amaral E, Hays M, Viscola MA, Mehta N, Bahamondes L: Pharmacokinetic interactions between depot medroxyprogesterone acetate and combination antiretroviral therapy. Fertil Steril 2008; 90:965-971.
68. Veazey RS, Ketas TJ, Dufour J, Moroney-Rasmussen T, Green LC, Klasse PJ, Moore JP: Protection of rhesus macaques from vaginal infection by vaginally delivered maraviroc, an inhibitor of HIV-1 entry via the CCR5 co-receptor. J Infect Dis 2010; 202:739-744.
69. Vishwanathan SA, Burgener A, Mogk K, Westmacott GR, Guenthner P, Henning T, Ball TB, Garber D, McNicholl J, Kersh E: Upregulation of innate immune factors in vaginal secretions of pig-tailed macaques during the follicular phase of the menstrual cycle when susceptibility to SHIV infection is lower compared to the luteal phase. International Society for Immunology Reproduction (ISIR), hosted by the American Society for Reproductive Immunology (ASRI), Boston, MA, 2013.
70. Lifson JD, Haigwood NL: Lessons in nonhuman primate models for AIDS vaccine research: from minefields to milestones. Cold Spring Harb Perspect Med 2012; 2:a007310.
71. Pereira LE, Srinivasan P, Smith J: Simian-human immunodeficiency viruses and their impact on non-human primate models for AIDS. In Immunodeficiency. K Metodiev (ed). Rijeka, Croatia, InTech, 2013, pp 311-356.
72. von Bubnoff A: Looking for the perfect challenge. IAVI Rep 2009; 13.
73. Reynolds MR, Sacha JB, Weiler AM, Borchardt GJ, Glidden CE, Sheppard NC, Norante FA, Castrovinci PA, Harris JJ, Robertson HT, Friedrich TC, McDermott AB, Wilson NA, Allison DB, Koff WC, Johnson WE, Watkins DI: The TRIM5{alpha} genotype of rhesus macaques affects acquisition of simian immunodeficiency virus SIVsmE660 infection after repeated limiting-dose intrarectal challenge. J Virol 2011; 85:9637-9640.
74. Letvin NL, Miller MD, Shen L, Chen ZW, Yasutomi Y: Simian immunodeficiency virus-specific cytotoxic T lymphocytes in rhesus monkeys: characterization and vaccine induction. Semin Immunol 1993; 5:215-223.
75. Newman RM, Hall L, Kirmaier A, Pozzi LA, Pery E, Farzan M, O'Neil SP, Johnson W: Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog 2008; 4:e1000003.
76. Hudgens MG, Gilbert PB, Mascola JR, Wu CD, Barouch DH, Self SG: Power to detect the effects of HIV vaccination in repeated low-dose challenge experiments. J Infect Dis 2009; 200:609-613.
77. Keele BF, Li H, Learn GH, Hraber P, Giorgi EE, Grayson T, Sun C, Chen Y, Yeh WW, Letvin NL, Mascola JR, Nabel GJ, Haynes BF, Bhattacharya T, Perelson AS, Korber BT, Hahn BH, Shaw GM: Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J Exp Med 2009; 206:1117-1134.
78. Regoes RR: The role of exposure history on HIV acquisition: insights from repeated low-dose challenge studies. PLoS Comput Biol 2012; 8:e1002767.
79. Sweeney YT, Angeles RO, Cummings PK, Smith AD, Patton DL: Pigtailed macaque model refinement: topical microbicide safety in the presence of coitus. J Med Primatol 2011; 40:327-334.
80. Wira CR, Fahey JV: A new strategy to understand how HIV infects women: identification of a window of vulnerability during the menstrual cycle. AIDS 2008; 22:1909-1917.
81. Hel Z, Stringer E, Mestecky J: Sex steroid hormones, hormonal contraception, and the immunobiology of human immunodeficiency virus-1 infection. Endocr Rev 2010; 31:79-97.
82. Smith J, Srinivasan P, Rastogi R, Teller R, Pereira LE, McNicholl J, Hendry RM, Mesquita P, Kiser P, Herold B: Pigtailed macaques under high doses of depot medroxyprogesterone are protected from multiple SHIV exposures with a tenofovir disoproxil fumarate intravaginal ring. Interscience Conference on Antimicrobial Agents and Chemotherapy, Seattle, WA, 2013.
83. Heffron R, Donnell D, Rees H, Celum C, Mugo N, Were E, de Bruyn G, Nakku-Joloba E, Ngure K, Kiarie J, Coombs RW, Baeten JM, Partners in Prevention HSVHIVTST: Use of hormonal contraceptives and risk of HIV-1 transmission: a prospective cohort study. Lancet Infect Dis 2012; 12:19-26.
84. Morrison CS, Richardson BA, Mmiro F, Chipato T, Celentano DD, Luoto J, Mugerwa R, Padian N, Rugpao S, Brown JM, Cornelisse P, Salata RA, Hormonal C, the Risk of HIVASG: Hormonal contraception and the risk of HIV acquisition. AIDS 2007; 21:85-95.
85. Plummer FA: Heterosexual transmission of human immunodeficiency virus type 1 (HIV): interactions of conventional sexually transmitted diseases, hormonal contraception and HIV-1. AIDS Res Hum Retroviruses 1998; 14(Suppl 1):S5-S10.
86. Division of STD Prevention, National Center for HIV/AIDS Viral Hepatitis, STD, and Tuberculosis Prevention: CDC Fact Sheet: The Role of STD Detection and Treatment in HIV Prevention. Atlanta, Centers for Disease Control and Prevention, U. S. Department of Health and Human Services, 2007. Available at http://www.cdc.gov/std/hiv/stdfact-std-hiv.htm.
87. Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, Hayes RJ: Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 2006; 20:73-83.
88. Laga M, Manoka A, Kivuvu M, Malele B, Tuliza M, Nzila N, Goeman J, Behets F, Batter V, Alary M, Heyward WL, Ryder RW, Piot P: Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS 1993; 7:95-102.
89. Cohen MS: Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet 1998; 351(Suppl 3):5-7.
90. Tsuiki A, Luo W, Henning T, Vishwanathan S, Dinh C, Adams D, Sweeney E, Mitchell J, Bachman S, Sharma P, Powell N, Hendry M, McNicholl J, Kersh E: Evaluation of the lymphocyte trafficking drug FTY720 in vaginal tissues. J Med Primatol 2013; 42:89-100.