The cervicovaginal mucus barrier to HIV-1 is diminished in bacterial vaginosis
Autoři:
Thuy Hoang aff001; Emily Toler aff001; Kevin DeLong aff001; Nomfuneko A. Mafunda aff004; Seth M. Bloom aff004; Hannah C. Zierden aff001; Thomas R. Moench aff008; Jenell S. Coleman aff009; Justin Hanes aff001; Douglas S. Kwon aff004; Samuel K. Lai aff011; Richard A. Cone aff008; Laura M. Ensign aff001
Působiště autorů:
The Center for Nanomedicine, The Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America
aff001; Department of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America
aff002; Department of Ophthalmology, The Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America
aff003; Ragon Institute of MGH, MIT, and Harvard, Massachusetts General Hospital, Cambridge, Massachusetts, United States of America
aff004; Division of Infectious Diseases, Massachusetts General Hospital, Boston, Massachusetts, United States of America
aff005; Harvard Medical School, Boston, Massachusetts, United States of America
aff006; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, Maryland, United States of America
aff007; Department of Biophysics, Johns Hopkins University, Baltimore, Maryland, United States of America
aff008; Department of Gynecology and Obstetrics, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America
aff009; The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins University, Baltimore, Maryland, United States of America
aff010; Division of Pharmacoengineering and Molecular Pharmaceutics, Eshelman School of Pharmacy, UNC/NCSU Joint Department of Biomedical Engineering, Department of Microbiology & Immunology, University of North Carolina-Chapel Hill, Chapel Hill, North Carolina,
aff011
Vyšlo v časopise:
The cervicovaginal mucus barrier to HIV-1 is diminished in bacterial vaginosis. PLoS Pathog 16(1): e32767. doi:10.1371/journal.ppat.1008236
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1008236
Souhrn
Bacterial vaginosis (BV), a condition in which the vaginal microbiota consists of community of obligate and facultative anaerobes rather than dominated by a single species of Lactobacillus, affects ~30% of women in the US. Women with BV are at 60% increased risk for HIV acquisition and are 3-times more likely to transmit HIV to an uninfected partner. As cervicovaginal mucus (CVM) is the first line of defense against mucosal pathogens and the home of the resident vaginal microbiota, we hypothesized the barrier function of CVM to HIV may be diminished in BV. Here, we characterized CVM properties including pH, lactic acid content, and Nugent score to correlate with the microbiota community composition, which was confirmed by 16S rDNA sequencing on a subset of samples. We then quantified the mobility of fluorescently-labeled HIV virions and nanoparticles to characterize the structural and adhesive barrier properties of CVM. Our analyses included women with Nugent scores categorized as intermediate (4–6) and BV (7–10), women that were either symptomatic or asymptomatic, and a small group of women before and after antibiotic treatment for symptomatic BV. Overall, we found that HIV virions had significantly increased mobility in CVM from women with BV compared to CVM from women with Lactobacillus crispatus-dominant microbiota, regardless of whether symptoms were present. We confirmed using nanoparticles and scanning electron microscopy that the impaired barrier function was due to reduced adhesive barrier properties without an obvious degradation of the physical CVM pore structure. We further confirmed a similar increase in HIV mobility in CVM from women with Lactobacillus iners-dominant microbiota, the species most associated with transitions to BV and that persists after antibiotic treatment for BV. Our findings advance the understanding of the protective role of mucus and highlight the interplay between vaginal microbiota and the innate barrier function mucus.
Klíčová slova:
Bacterial vaginosis – HIV – HIV clinical manifestations – Lactic acid – Lactobacillus – Microbiome – Mucus – Virions
Zdroje
1. Koumans EH, Sternberg M, Bruce C, McQuillan G, Kendrick J, Sutton M, et al. The prevalence of bacterial vaginosis in the United States, 2001–2004; associations with symptoms, sexual behaviors, and reproductive health. Sexually transmitted diseases. 2007;34(11):864–9. Epub 2007/07/11. doi: 10.1097/OLQ.0b013e318074e565 17621244.
2. Olson KM, Boohaker LJ, Schwebke JR, Aslibekyan S, Muzny CA. Comparisons of vaginal flora patterns among sexual behaviour groups of women: implications for the pathogenesis of bacterial vaginosis. Sexual health. 2017. Epub 2017/12/08. doi: 10.1071/SH17087 29212588.
3. Bukusi EA, Cohen CR, Meier AS, Waiyaki PG, Nguti R, Njeri JN, et al. Bacterial Vaginosis: Risk factors among Kenyan women and their male partners. Sexually transmitted diseases. 2006;33(6):361–7. doi: 10.1097/01.olq.0000200551.07573.df ISI:000237876000005. 16547451
4. Atashili J, Poole C, Ndumbe PM, Adimora AA, Smith JS. Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS. 2008;22(12):1493–501. Epub 2008/07/11. doi: 10.1097/QAD.0b013e3283021a37 18614873; PubMed Central PMCID: PMC2788489.
5. Eschenbach DA. Bacterial vaginosis and anaerobes in obstetric-gynecologic infection. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 1993;16 Suppl 4:S282–7. Epub 1993/06/01. doi: 10.1093/clinids/16.supplement_4.s282 8324132.
6. Dingens AS, Fairfortune TS, Reed S, Mitchell C. Bacterial vaginosis and adverse outcomes among full-term infants: a cohort study. BMC pregnancy and childbirth. 2016;16(1):278. Epub 2016/09/24. doi: 10.1186/s12884-016-1073-y 27658456; PubMed Central PMCID: PMC5034665.
7. Nelson DB, Hanlon AL, Wu G, Liu C, Fredricks DN. First Trimester Levels of BV-Associated Bacteria and Risk of Miscarriage Among Women Early in Pregnancy. Maternal and child health journal. 2015;19(12):2682–7. Epub 2015/07/15. doi: 10.1007/s10995-015-1790-2 26156825.
8. Fredricks DN, Fiedler TL, Marrazzo JM. Molecular identification of bacteria associated with bacterial vaginosis. The New England journal of medicine. 2005;353(18):1899–911. Epub 2005/11/04. doi: 10.1056/NEJMoa043802 16267321.
9. Kim TK, Thomas SM, Ho M, Sharma S, Reich CI, Frank JA, et al. Heterogeneity of vaginal microbial communities within individuals. Journal of clinical microbiology. 2009;47(4):1181–9. Epub 2009/01/23. doi: 10.1128/JCM.00854-08 19158255; PubMed Central PMCID: PMC2668325.
10. McKinnon LR, Achilles SL, Bradshaw CS, Burgener A, Crucitti T, Fredricks DN, et al. The Evolving Facets of Bacterial Vaginosis: Implications for HIV Transmission. AIDS Res Hum Retroviruses. 2019;35(3):219–28. Epub 2019/01/15. doi: 10.1089/AID.2018.0304 30638028.
11. Kroon SJ, Ravel J, Huston WM. Cervicovaginal microbiota, women's health, and reproductive outcomes. Fertil Steril. 2018;110(3):327–36. Epub 2018/08/14. doi: 10.1016/j.fertnstert.2018.06.036 30098679.
12. Gosmann C, Anahtar MN, Handley SA, Farcasanu M, Abu-Ali G, Bowman BA, et al. Lactobacillus-Deficient Cervicovaginal Bacterial Communities Are Associated with Increased HIV Acquisition in Young South African Women. Immunity. 2017;46(1):29–37. Epub 2017/01/15. doi: 10.1016/j.immuni.2016.12.013 28087240; PubMed Central PMCID: PMC5270628.
13. Cohen CR, Lingappa JR, Baeten JM, Ngayo MO, Spiegel CA, Hong T, et al. Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: a prospective cohort analysis among African couples. PLoS medicine. 2012;9(6):e1001251. Epub 2012/06/30. doi: 10.1371/journal.pmed.1001251 22745608; PubMed Central PMCID: PMC3383741.
14. Thurman AR, Doncel GF. Innate immunity and inflammatory response to Trichomonas vaginalis and bacterial vaginosis: relationship to HIV acquisition. Am J Reprod Immunol. 2011;65(2):89–98. Epub 2010/08/04. doi: 10.1111/j.1600-0897.2010.00902.x 20678168.
15. Mitchell C, Marrazzo J. Bacterial vaginosis and the cervicovaginal immune response. Am J Reprod Immunol. 2014;71(6):555–63. Epub 2014/05/17. doi: 10.1111/aji.12264 24832618; PubMed Central PMCID: PMC4128638.
16. Sicard JF, Le Bihan G, Vogeleer P, Jacques M, Harel J. Interactions of Intestinal Bacteria with Components of the Intestinal Mucus. Front Cell Infect Microbiol. 2017;7:387. Epub 2017/09/21. doi: 10.3389/fcimb.2017.00387 28929087; PubMed Central PMCID: PMC5591952.
17. Robinson CV, Elkins MR, Bialkowski KM, Thornton DJ, Kertesz MA. Desulfurization of mucin by Pseudomonas aeruginosa: influence of sulfate in the lungs of cystic fibrosis patients. J Med Microbiol. 2012;61(Pt 12):1644–53. Epub 2012/08/25. doi: 10.1099/jmm.0.047167–0 22918866.
18. Ravcheev DA, Thiele I. Comparative Genomic Analysis of the Human Gut Microbiome Reveals a Broad Distribution of Metabolic Pathways for the Degradation of Host-Synthetized Mucin Glycans and Utilization of Mucin-Derived Monosaccharides. Front Genet. 2017;8:111. Epub 2017/09/16. doi: 10.3389/fgene.2017.00111 28912798; PubMed Central PMCID: PMC5583593.
19. Lai SK, Hida K, Shukair S, Wang YY, Figueiredo A, Cone R, et al. Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus. Journal of virology. 2009;83(21):11196–200. Epub 2009/08/21. doi: 10.1128/JVI.01899-08 19692470; PubMed Central PMCID: PMC2772788.
20. Nunn KL, Wang YY, Harit D, Humphrys MS, Ma B, Cone R, et al. Enhanced Trapping of HIV-1 by Human Cervicovaginal Mucus Is Associated with Lactobacillus crispatus-Dominant Microbiota. mBio. 2015;6(5):e01084–15. Epub 2015/10/08. doi: 10.1128/mBio.01084-15 26443453; PubMed Central PMCID: PMC4611035.
21. Lai SK, Wang YY, Hida K, Cone R, Hanes J. Nanoparticles reveal that human cervicovaginal mucus is riddled with pores larger than viruses. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(2):598–603. Epub 2009/12/19. doi: 10.1073/pnas.0911748107 20018745; PubMed Central PMCID: PMC2818964.
22. Wang YY, Kannan A, Nunn KL, Murphy MA, Subramani DB, Moench T, et al. IgG in cervicovaginal mucus traps HSV and prevents vaginal herpes infections. Mucosal immunology. 2014;7(5):1036–44. Epub 2014/02/06. doi: 10.1038/mi.2013.120 24496316; PubMed Central PMCID: PMC4122653.
23. Shukair SA, Allen SA, Cianci GC, Stieh DJ, Anderson MR, Baig SM, et al. Human cervicovaginal mucus contains an activity that hinders HIV-1 movement. Mucosal immunology. 2013;6(2):427–34. Epub 2012/09/20. doi: 10.1038/mi.2012.87 22990624; PubMed Central PMCID: PMC3732193.
24. Boukari H, Brichacek B, Stratton P, Mahoney SF, Lifson JD, Margolis L, et al. Movements of HIV-virions in human cervical mucus. Biomacromolecules. 2009;10(9):2482–8. Epub 2009/08/29. doi: 10.1021/bm900344q 19711976; PubMed Central PMCID: PMC2768114.
25. Carias AM, McCoombe S, McRaven M, Anderson M, Galloway N, Vandergrift N, et al. Defining the interaction of HIV-1 with the mucosal barriers of the female reproductive tract. Journal of virology. 2013;87(21):11388–400. Epub 2013/08/24. doi: 10.1128/JVI.01377-13 23966398; PubMed Central PMCID: PMC3807311.
26. Odeblad E. Intracavitary Circulation of Aqueous Material in the Human Vagina. Acta Obstet Gynecol Scand. 1964;43:360–8. Epub 1964/01/01. doi: 10.3109/00016346409162686 14286007.
27. Boskey ER, Moench TR, Hees PS, Cone RA. A self-sampling method to obtain large volumes of undiluted cervicovaginal secretions. Sexually transmitted diseases. 2003;30(2):107–9. Epub 2003/02/05. doi: 10.1097/00007435-200302000-00002 12567165.
28. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. Journal of clinical microbiology. 1991;29(2):297–301. Epub 1991/02/01. 1706728; PubMed Central PMCID: PMC269757.
29. Witkin SS, Mendes-Soares H, Linhares IM, Jayaram A, Ledger WJ, Forney LJ. Influence of vaginal bacteria and D- and L-lactic acid isomers on vaginal extracellular matrix metalloproteinase inducer: implications for protection against upper genital tract infections. mBio. 2013;4(4). Epub 2013/08/08. doi: 10.1128/mBio.00460-13 23919998; PubMed Central PMCID: PMC3735189.
30. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proceedings of the National Academy of Sciences of the United States of America. 2011;108 Suppl 1:4680–7. Epub 2010/06/11. doi: 10.1073/pnas.1002611107 20534435; PubMed Central PMCID: PMC3063603.
31. Lai SK, O'Hanlon DE, Harrold S, Man ST, Wang YY, Cone R, et al. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(5):1482–7. Epub 2007/01/25. doi: 10.1073/pnas.0608611104 17244708; PubMed Central PMCID: PMC1785284.
32. Wang YY, Lai SK, Ensign LM, Zhong W, Cone R, Hanes J. The microstructure and bulk rheology of human cervicovaginal mucus are remarkably resistant to changes in pH. Biomacromolecules. 2013;14(12):4429–35. Epub 2013/11/26. doi: 10.1021/bm401356q 24266646; PubMed Central PMCID: PMC3918948.
33. Wang YY, Lai SK, So C, Schneider C, Cone R, Hanes J. Mucoadhesive Nanoparticles May Disrupt the Protective Human Mucus Barrier by Altering Its Microstructure. Plos One. 2011;6(6). ARTN e21547 doi: 10.1371/journal.pone.0021547 WOS:000292290100035. 21738703
34. Wohlbold TJ, Krammer F. In the shadow of hemagglutinin: a growing interest in influenza viral neuraminidase and its role as a vaccine antigen. Viruses. 2014;6(6):2465–94. Epub 2014/06/25. doi: 10.3390/v6062465 24960271; PubMed Central PMCID: PMC4074938.
35. Lyczak JB, Cannon CL, Pier GB. Lung infections associated with cystic fibrosis. Clin Microbiol Rev. 2002;15(2):194–222. Epub 2002/04/05. doi: 10.1128/CMR.15.2.194-222.2002 11932230; PubMed Central PMCID: PMC118069.
36. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. Mucins in the mucosal barrier to infection. Mucosal immunology. 2008;1(3):183–97. Epub 2008/12/17. doi: 10.1038/mi.2008.5 19079178.
37. Cone RA. Barrier properties of mucus. Advanced drug delivery reviews. 2009;61(2):75–85. Epub 2009/01/13. doi: 10.1016/j.addr.2008.09.008 19135107.
38. Chappell CA, Rohan LC, Moncla BJ, Wang L, Meyn LA, Bunge K, et al. The effects of reproductive hormones on the physical properties of cervicovaginal fluid. American journal of obstetrics and gynecology. 2014;211(3):226 e1–7. Epub 2014/03/26. doi: 10.1016/j.ajog.2014.03.041 24662718; PubMed Central PMCID: PMC4149850.
39. Lai SK, Wang YY, Wirtz D, Hanes J. Micro- and macrorheology of mucus. Advanced drug delivery reviews. 2009;61(2):86–100. Epub 2009/01/27. doi: 10.1016/j.addr.2008.09.012 19166889; PubMed Central PMCID: PMC2736374.
40. Mlisana K, Naicker N, Werner L, Roberts L, van Loggerenberg F, Baxter C, et al. Symptomatic vaginal discharge is a poor predictor of sexually transmitted infections and genital tract inflammation in high-risk women in South Africa. J Infect Dis. 2012;206(1):6–14. Epub 2012/04/21. doi: 10.1093/infdis/jis298 22517910; PubMed Central PMCID: PMC3490689.
41. Bacterial vaginosis: Clinical manifestations and diagnosis [Internet]. 2018 [cited December 2018]. Available from: https://www.uptodate.com/contents/bacterial-vaginosis-clinical-manifestations-and-diagnosis.
42. Workowski KA, Bolan GA, Centers for Disease C, Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep. 2015;64(RR-03):1–137. Epub 2015/06/05. 26042815; PubMed Central PMCID: PMC5885289.
43. Schwebke JR, Desmond R. A randomized trial of metronidazole in asymptomatic bacterial vaginosis to prevent the acquisition of sexually transmitted diseases. American journal of obstetrics and gynecology. 2007;196(6):517 e1-6. Epub 2007/06/06. doi: 10.1016/j.ajog.2007.02.048 17547876; PubMed Central PMCID: PMC1993882.
44. Cauci S, Culhane JF, Di Santolo M, McCollum K. Among pregnant women with bacterial vaginosis, the hydrolytic enzymes sialidase and prolidase are positively associated with interleukin-1beta. American journal of obstetrics and gynecology. 2008;198(1):132 e1-7. Epub 2007/08/24. doi: 10.1016/j.ajog.2007.05.035 17714681.
45. Howe L, Wiggins R, Soothill PW, Millar MR, Horner PJ, Corfield AP. Mucinase and sialidase activity of the vaginal microflora: implications for the pathogenesis of preterm labour. International journal of STD & AIDS. 1999;10(7):442–7. Epub 1999/08/24. doi: 10.1258/0956462991914438 10454178.
46. Smayevsky J, Canigia LF, Lanza A, Bianchini H. Vaginal microflora associated with bacterial vaginosis in nonpregnant women: reliability of sialidase detection. Infectious diseases in obstetrics and gynecology. 2001;9(1):17–22. Epub 2001/05/23. doi: 10.1155/S1064744901000047 11368254; PubMed Central PMCID: PMC1784631.
47. Wiggins R, Hicks SJ, Soothill PW, Millar MR, Corfield AP. Mucinases and sialidases: their role in the pathogenesis of sexually transmitted infections in the female genital tract. Sex Transm Infect. 2001;77(6):402–8. Epub 2001/11/21. doi: 10.1136/sti.77.6.402 11714935; PubMed Central PMCID: PMC1744407.
48. Gilbert NM, Lewis WG, Lewis AL. Clinical features of bacterial vaginosis in a murine model of vaginal infection with Gardnerella vaginalis. Plos One. 2013;8(3):e59539. Epub 2013/03/26. doi: 10.1371/journal.pone.0059539 23527214; PubMed Central PMCID: PMC3602284.
49. Lewis WG, Robinson LS, Gilbert NM, Perry JC, Lewis AL. Degradation, foraging, and depletion of mucus sialoglycans by the vagina-adapted Actinobacterium Gardnerella vaginalis. The Journal of biological chemistry. 2013;288(17):12067–79. Epub 2013/03/13. doi: 10.1074/jbc.M113.453654 23479734; PubMed Central PMCID: PMC3636892.
50. Olmsted SS, Meyn LA, Rohan LC, Hillier SL. Glycosidase and proteinase activity of anaerobic gram-negative bacteria isolated from women with bacterial vaginosis. Sexually transmitted diseases. 2003;30(3):257–61. Epub 2003/03/05. doi: 10.1097/00007435-200303000-00016 12616147.
51. Olmsted SS, Khanna KV, Ng EM, Whitten ST, Johnson ON, 3rd, Markham RB, et al. Low pH immobilizes and kills human leukocytes and prevents transmission of cell-associated HIV in a mouse model. BMC infectious diseases. 2005;5:79. Epub 2005/10/01. doi: 10.1186/1471-2334-5-79 16194280; PubMed Central PMCID: PMC1262719.
52. Aldunate M, Tyssen D, Johnson A, Zakir T, Sonza S, Moench T, et al. Vaginal concentrations of lactic acid potently inactivate HIV. The Journal of antimicrobial chemotherapy. 2013;68(9):2015–25. Epub 2013/05/10. doi: 10.1093/jac/dkt156 23657804; PubMed Central PMCID: PMC3743514.
53. Tyssen D, Wang YY, Hayward JA, Agius PA, DeLong K, Aldunate M, et al. Anti-HIV-1 Activity of Lactic Acid in Human Cervicovaginal Fluid. mSphere. 2018;3(4). Epub 2018/07/07. doi: 10.1128/mSphere.00055-18 29976641; PubMed Central PMCID: PMC6034077.
54. Hearps AC, Tyssen D, Srbinovski D, Bayigga L, Diaz DJD, Aldunate M, et al. Vaginal lactic acid elicits an anti-inflammatory response from human cervicovaginal epithelial cells and inhibits production of pro-inflammatory mediators associated with HIV acquisition. Mucosal immunology. 2017;10(6):1480–90. Epub 2017/04/13. doi: 10.1038/mi.2017.27 28401934.
55. O'Hanlon DE, Cone RA, Moench TR. Vaginal pH measured in vivo: lactobacilli determine pH and lactic acid concentration. BMC Microbiol. 2019;19(1):13. Epub 2019/01/16. doi: 10.1186/s12866-019-1388-8 30642259; PubMed Central PMCID: PMC6332693.
56. Boily MC, Baggaley RF, Wang L, Masse B, White RG, Hayes RJ, et al. Heterosexual risk of HIV-1 infection per sexual act: systematic review and meta-analysis of observational studies. Lancet Infect Dis. 2009;9(2):118–29. Epub 2009/01/31. doi: 10.1016/S1473-3099(09)70021-0 19179227; PubMed Central PMCID: PMC4467783.
57. McKinley SA, Chen A, Shi F, Wang S, Mucha PJ, Forest MG, et al. Modeling neutralization kinetics of HIV by broadly neutralizing monoclonal antibodies in genital secretions coating the cervicovaginal mucosa. Plos One. 2014;9(6):e100598. Epub 2014/06/27. doi: 10.1371/journal.pone.0100598 24967706; PubMed Central PMCID: PMC4072659.
58. Masters WH JV. Human sexual response.: Little Brown, Boston, MA; 1966.
59. Boskey ER, Telsch KM, Whaley KJ, Moench TR, Cone RA. Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun. 1999;67(10):5170–5. Epub 1999/09/25. 10496892; PubMed Central PMCID: PMC96867.
60. Barreto-de-Souza V, Arakelyan A, Margolis L, Vanpouille C. HIV-1 vaginal transmission: cell-free or cell-associated virus? Am J Reprod Immunol. 2014;71(6):589–99. Epub 2014/04/16. doi: 10.1111/aji.12240 24730358; PubMed Central PMCID: PMC4517939.
61. Wessman M, Thorsteinsson K, Jensen JS, Storgaard M, Ronsholt FF, Johansen IS, et al. Bacterial vaginosis, human papilloma virus and herpes viridae do not predict vaginal HIV RNA shedding in women living with HIV in Denmark. BMC infectious diseases. 2017;17(1):376. Epub 2017/06/02. doi: 10.1186/s12879-017-2477-7 28569142; PubMed Central PMCID: PMC5452403.
62. Dinh MH, Anderson MR, McRaven MD, Cianci GC, McCoombe SG, Kelley ZL, et al. Visualization of HIV-1 interactions with penile and foreskin epithelia: clues for female-to-male HIV transmission. PLoS pathogens. 2015;11(3):e1004729. Epub 2015/03/10. doi: 10.1371/journal.ppat.1004729 25748093; PubMed Central PMCID: PMC4352059.
63. Amsel R, Totten PA, Spiegel CA, Chen KC, Eschenbach D, Holmes KK. Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. The American journal of medicine. 1983;74(1):14–22. Epub 1983/01/01. doi: 10.1016/0002-9343(83)91112-9 6600371.
64. Nance EA, Woodworth GF, Sailor KA, Shih TY, Xu Q, Swaminathan G, et al. A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Sci Transl Med. 2012;4(149):149ra19. Epub 2012/08/31. doi: 10.1126/scitranslmed.3003594 22932224; PubMed Central PMCID: PMC3718558.
65. Schuster BS, Ensign LM, Allan DB, Suk JS, Hanes J. Particle tracking in drug and gene delivery research: State-of-the-art applications and methods. Advanced drug delivery reviews. 2015;91:70–91. Epub 2015/04/11. doi: 10.1016/j.addr.2015.03.017 25858664; PubMed Central PMCID: PMC4813524.
66. Suh J, Dawson M, Hanes J. Real-time multiple-particle tracking: applications to drug and gene delivery. Advanced drug delivery reviews. 2005;57(1):63–78. Epub 2004/11/03. doi: 10.1016/j.addr.2004.06.001 15518921.
67. Anahtar MN, Byrne EH, Doherty KE, Bowman BA, Yamamoto HS, Soumillon M, et al. Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity. 2015;42(5):965–76. Epub 2015/05/21. doi: 10.1016/j.immuni.2015.04.019 25992865; PubMed Central PMCID: PMC4461369.
68. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6(8):1621–4. Epub 2012/03/10. doi: 10.1038/ismej.2012.8 22402401; PubMed Central PMCID: PMC3400413.
69. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. Epub 2010/04/13. doi: 10.1038/nmeth.f.303 20383131; PubMed Central PMCID: PMC3156573.
70. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3. Epub 2016/05/24. doi: 10.1038/nmeth.3869 27214047; PubMed Central PMCID: PMC4927377.
71. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. Plos One. 2013;8(4):e61217. Epub 2013/05/01. doi: 10.1371/journal.pone.0061217 23630581; PubMed Central PMCID: PMC3632530.
72. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10. Epub 1990/10/05. doi: 10.1016/S0022-2836(05)80360-2 2231712.
73. DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, et al. Temporal and spatial variation of the human microbiota during pregnancy. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(35):11060–5. Epub 2015/08/19. doi: 10.1073/pnas.1502875112 26283357; PubMed Central PMCID: PMC4568272.
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- Modular Mimicry and Engagement of the Hippo Pathway by Marburg Virus VP40: Implications for Filovirus Biology and Budding
