Cultivated vaginal microbiomes alter HIV-1 infection and antiretroviral efficacy in colonized epithelial multilayer cultures

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Pyles, Richard B ^a   Vincent, Kathleen L ^a   Baum, Marc M ^b   Elsom, Barry ^a   Miller, Aaron L ^a   Maxwell, Carrie ^a   Eaves Pyles, Tonyia D ^a   Li, Guangyu ^c   Popov, Vsevolod L ^a   Nusbaum, Rebecca J ^d   Ferguson, Monique R ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b OAK CREST INSTITUTE OF SCIENCE   (United States)

^c East Tennessee State University   (United States)

^d UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TENOFOVIR; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; CYTOKINE;

ARTICLE; COCULTURE; CONTROLLED STUDY; CRYOPRESERVATION; CULTURE MEDIUM; DRUG EFFICACY; DRUG SAFETY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; MICROBIOME; PHENOTYPE; POLYMERASE CHAIN REACTION; VAGINA FLORA; VAGINA MUCOSA; VIRUS REPLICATION; VIRUS TITRATION; ADULT; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL LINE; CULTURE TECHNIQUE; DRUG EFFECTS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; MICROFLORA; MUCOSA; PHYSIOLOGY; SECRETION (PROCESS); VAGINA; VIROLOGY;

ADULT; ANTI-HIV AGENTS; CELL CULTURE TECHNIQUES; CELL LINE; CYTOKINES; EPITHELIAL CELLS; FEMALE; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROBIOTA; MODELS, BIOLOGICAL; MUCOUS MEMBRANE; VAGINA; VIRUS REPLICATION;

EID: 84899951788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093419     Document Type: Article

References (55)

1. Thomas S (1928) Doderlein's bacillus - Lactobacillus acidophilus. Journal of Infectious Diseases 43: 218-227.
2. Weinstein L, Howard JH (1937) The Incidence of the Doderlein Vaginal Bacillus During the Post-Climacterium. Yale J Biol Med 10: 185-190.
3. Sobel JD (2005) What's new in bacterial vaginosis and trichomoniasis? Infect Dis Clin North Am 19: 387-406.
4. Koumans EH, Sternberg M, Bruce C, McQuillan G, Kendrick J, et al. (2007) The prevalence of bacterial vaginosis in the United States, 2001-2004; associations with symptoms, sexual behaviors, and reproductive health. Sex Transm Dis 34: 864-869. (Pubitemid 350287499)
5. Kenyon C, Colebunders R, Crucitti T (2013) The global epidemiology of bacterial vaginosis: a systematic review. Am J Obstet Gynecol.
6. Pennock JW, Stegall R, Bell B, Vargas G, Motamedi M, et al. (2009) Estradiol improves genital herpes vaccine efficacy in mice. Vaccine 27: 5830-5836.
7. Fethers KA, Fairley CK, Hocking JS, Gurrin LC, Bradshaw CS (2008) Sexual risk factors and bacterial vaginosis: a systematic review and meta-analysis. Clin Infect Dis 47: 1426-1435.
8. Verstraelen H, Swidsinski A (2013) The biofilm in bacterial vaginosis: implications for epidemiology, diagnosis and treatment. Curr Opin Infect Dis 26: 86-89.
9. Verstraelen H, Verhelst R, Vaneechoutte M, Temmerman M (2010) The epidemiology of bacterial vaginosis in relation to sexual behaviour. BMC Infect Dis 10: 81.
10. Vincent KL, Vargas G, Wei J, Bourne N, Motamedi M (2013) Monitoring vaginal epithelial thickness changes noninvasively in sheep using optical coherence tomography. Am J Obstet Gynecol 208: 282 e281-287.
11. Milligan GN, Meador MG, Chu CF, Young CG, Martin TL, et al. (2005) Long-term presence of virus-specific plasma cells in sensory ganglia and spinal cord following intravaginal inoculation of herpes simplex virus type 2. J Virol 79: 11537-11540. (Pubitemid 41170698)
12. Brotman RM, Klebanoff MA, Nansel TR, Andrews WW, Schwebke JR, et al. (2008) A longitudinal study of vaginal douching and bacterial vaginosis-a marginal structural modeling analysis. Am J Epidemiol 168: 188-196. (Pubitemid 351951592)
13. Bird MD, Chu CF, Johnson AJ, Milligan GN (2007) Early resolution of herpes simplex virus type 2 infection of the murine genital tract involves stimulation of genital parenchymal cells by gamma interferon. J Virol 81: 423-426. (Pubitemid 44975182)
14. Petrova MI, van den Broek M, Balzarini J, Vanderleyden J, Lebeer S (2013) Vaginal microbiota and its role in HIV transmission and infection. FEMS Microbiol Rev 37: 762-792.
15. Martin HL, Richardson BA, Nyange PM, Lavreys L, Hillier SL, et al. (1999) Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J Infect Dis 180: 1863-1868.
16. Sha BE, Zariffard MR, Wang QJ, Chen HY, Bremer J, et al. (2005) Female genital-tract HIV load correlates inversely with Lactobacillus species but positively with bacterial vaginosis and Mycoplasma hominis. J Infect Dis 191: 25-32. (Pubitemid 40041396)
17. Cohen CR, Lingappa JR, Baeten JM, Ngayo MO, Spiegel CA, et al. (2012) Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: a prospective cohort analysis among African couples. PLoS Med 9: e1001251.
18. Hemelaar J, Gouws E, Ghys PD, Osmanov S (2011) Global trends in molecular epidemiology of HIV-1 during 2000-2007. AIDS 25: 679-689.
19. Wahren B, Biswas P, Borggren M, Coleman A, Da Costa K, et al. (2010) Rational design of HIV vaccine and microbicides: report of the EUROPRISE annual conference. J Transl Med 8: 72.
20. Ravel J, Gajer P, Fu L, Mauck CK, Koenig SS, et al. (2012) Twice-daily application of HIV microbicides alter the vaginal microbiota. MBio 3.
21. Schellenberg JJ, Plummer FA (2012) The Microbiological Context of HIV Resistance: Vaginal Microbiota and Mucosal Inflammation at the Viral Point of Entry. Int J Inflam 2012: 131243.
22. Shattock RJ, Rosenberg Z (2012) Microbicides: topical prevention against HIV. Cold Spring Harb Perspect Med 2: a007385.
23. Ramjee G, Morar NS, Braunstein S, Friedland B, Jones H, et al. (2007) Acceptability of Carraguard, a candidate microbicide and methyl cellulose placebo vaginal gels among HIV-positive women and men in Durban, South Africa. AIDS Res Ther 4: 20.
24. Van Damme L, Govinden R, Mirembe FM, Guedou F, Solomon S, et al. (2008) Lack of effectiveness of cellulose sulfate gel for the prevention of vaginal HIV transmission. N Engl J Med 359: 463-472.
25. Cone RA, Hoen T, Wong X, Abusuwwa R, Anderson DJ, et al. (2006) Vaginal microbicides: detecting toxicities in vivo that paradoxically increase pathogen transmission. BMC Infect Dis 6: 90.
26. Keller MJ, Carpenter CA, Lo Y, Einstein MH, Liu C, et al. (2012) Phase I randomized safety study of twice daily dosing of acidform vaginal gel: candidate antimicrobial contraceptive. PLoS One 7: e46901.
27. Mirmonsef P, Gilbert D, Zariffard MR, Hamaker BR, Kaur A, et al. (2011) The effects of commensal bacteria on innate immune responses in the female genital tract. Am J Reprod Immunol 65: 190-195.
28. Fichorova RN, Tucker LD, Anderson DJ (2001) The molecular basis of nonoxynol-9-induced vaginal inflammation and its possible relevance to human immunodeficiency virus type 1 transmission. J Infect Dis 184: 418-428. (Pubitemid 32718505)
29. Pirrone V, Wigdahl B, Krebs FC (2011) The rise and fall of polyanionic inhibitors of the human immunodeficiency virus type 1. Antiviral Res 90: 168-182.
30. 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.
31. Hummelen R, Fernandes AD, Macklaim JM, Dickson RJ, Changalucha J, et al. (2010) Deep sequencing of the vaginal microbiota of women with HIV. PLoS One 5: e12078.
32. Lambert JA, Kalra A, Dodge CT, John S, Sobel JD, et al. (2013) Novel PCR-based methods enhance characterization of vaginal microbiota in a bacterial vaginosis patient before and after treatment. Appl Environ Microbiol 79: 4181-4185.
33. Gajer P, Brotman RM, Bai G, Sakamoto J, Schutte UM, et al. (2012) Temporal dynamics of the human vaginal microbiota. Sci Transl Med 4: 132ra152.
34. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, et al. (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 108 Suppl 1: 4680-4687.
35. Srinivasan S, Hoffman NG, Morgan MT, Matsen FA, Fiedler TL, et al. (2012) Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS One 7: e37818.
36. Rose WA Jr, McGowin CL, Spagnuolo RA, Eaves-Pyles TD, Popov VL, et al. (2012) Commensal bacteria modulate innate immune responses of vaginal epithelial cell multilayer cultures. PLoS One 7: e32728.
37. Moss JA, Malone AM, Smith TJ, Butkyavichene I, Cortez C, et al. (2012) Safety and pharmacokinetics of intravaginal rings delivering tenofovir in pig-tailed macaques. Antimicrob Agents Chemother 56: 5952-5960.
38. Eaves-Pyles T, Patel J, Arigi E, Cong Y, Cao A, et al. (2013) Immunomodulatory and Antibacterial Effects of Cystatin 9 against Francisella tularensis. Mol Med 19: 263-275.
39. Takeuchi Y, McClure MO, Pizzato M (2008) Identification of gammaretroviruses constitutively released from cell lines used for human immunodeficiency virus research. J Virol 82: 12585-12588.
40. Givan AL, White HD, Stern JE, Colby E, Gosselin EJ, et al. (1997) Flow cytometric analysis of leukocytes in the human female reproductive tract: comparison of fallopian tube, uterus, cervix, and vagina. Am J Reprod Immunol 38: 350-359. (Pubitemid 27427398)
41. Johnson AJ, Chu CF, Milligan GN (2008) Effector CD4+ T-cell involvement in clearance of infectious herpes simplex virus type 1 from sensory ganglia and spinal cords. J Virol 82: 9678-9688.
42. Abdool Karim Q, Abdool Karim SS, 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.
43. Mayer KH, Maslankowski LA, Gai F, El-Sadr WM, Justman J, et al. (2006) Safety and tolerability of tenofovir vaginal gel in abstinent and sexually active HIV-infected and uninfected women. AIDS 20: 543-551. (Pubitemid 43731598)
44. Hickey RJ, Zhou X, Pierson JD, Ravel J, Forney LJ (2012) Understanding vaginal microbiome complexity from an ecological perspective. Transl Res 160: 267-282.
45. Chu CF, Meador MG, Young CG, Strasser JE, Bourne N, et al. (2008) Antibody-mediated protection against genital herpes simplex virus type 2 disease in mice by Fc gamma receptor-dependent and -independent mechanisms. J Reprod Immunol 78: 58-67. (Pubitemid 351609115)
46. Yeoman CJ, Thomas SM, Miller ME, Ulanov AV, Torralba M, et al. (2013) A multi-omic systems-based approach reveals metabolic markers of bacterial vaginosis and insight into the disease. PLoS One 8: e56111.
47. Boily MC, Baggaley RF, Wang L, Masse B, White RG, et al. (2009) Heterosexual risk of HIV-1 infection per sexual act: systematic review and meta-analysis of observational studies. Lancet Infect Dis 9: 118-129.
48. Spear GT, St John E, Zariffard MR (2007) Bacterial vaginosis and human immunodeficiency virus infection. AIDS Res Ther 4: 25.
49. Nies AT, Damme K, Schaeffeler E, Schwab M (2012) Multidrug and toxin extrusion proteins as transporters of antimicrobial drugs. Expert Opin Drug Metab Toxicol 8: 1565-1577.
50. Losikoff P, Fichorova R, Snyder B, Rodriguez I, Cu-Uvin S, et al. (2007) Genital tract interleukin-8 but not interleukin-1beta or interleukin-6 concentration is associated with bacterial vaginosis and its clearance in HIV-infected and HIV-uninfected women. Infect Dis Obstet Gynecol 2007: 92307.
51. Baum MM, Butkyavichene I, Gilman J, Kennedy S, Kopin E, et al. (2012) An intravaginal ring for the simultaneous delivery of multiple drugs. J Pharm Sci 101: 2833-2843.
52. Moss JA, Malone AM, Smith TJ, Kennedy S, Kopin E, et al. (2012) Simultaneous delivery of tenofovir and acyclovir via an intravaginal ring. Antimicrob Agents Chemother 56: 875-882.
53. Bell BA, Vincent KL, Bourne N, Vargas G, Motamedi M (2013) Optical coherence tomography for assessment of microbicide safety in a small animal model. J Biomed Opt 18: 046010.
54. Palmer S, Margot N, Gilbert H, Shaw N, Buckheit R Jr, et al. (2001) Tenofovir, adefovir, and zidovudine susceptibilities of primary human immunodeficiency virus type 1 isolates with non-B subtypes or nucleoside resistance. AIDS Res Hum Retroviruses 17: 1167-1173. (Pubitemid 32881583)
55. Pyles RB, Thompson RL (1994) Mutations in accessory DNA replicating functions alter the relative mutation frequency of herpes simplex virus type 1 strains in cultured murine cells. J Virol 68: 4514-4524. (Pubitemid 24183048)