Microbiome Composition and Function Drives Wound-Healing Impairment in the Female Genital Tract

PLoS Pathogens

Volumn 12, Issue 9, 2016, Pages

  Zevin, Alexander S ^a   Xie, Irene Y ^b,c   Birse, Kenzie ^b,c   Arnold, Kelly ^d   Romas, Laura ^b,c   Westmacott, Garrett ^e   Novak, Richard M ^f   McCorrister, Stuart ^e   McKinnon, Lyle R ^c   Cohen, Craig R ^g   Mackelprang, Romel ^a   Lingappa, Jairam ^a,h   Lauffenburger, Doug A ⁱ   Klatt, Nichole R ^a   Burgener, Adam D ^b,c,j  

^a UNIVERSITY OF WASHINGTON   (United States)

^b PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^c UNIVERSITY OF MANITOBA   (Canada)

^d UNIVERSITY OF MICHIGAN   (United States)

^e PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^f UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

ⁱ Massachusetts Institute of Technology Cambridge   (United States)

^j KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; DYSBIOSIS; ENERGY METABOLISM; FEMALE; FEMALE GENITAL SYSTEM; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MASS SPECTROMETRY; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIOME; MIDDLE AGED; PREVALENCE; SEQUENCE ANALYSIS; VAGINITIS; WOUND HEALING IMPAIRMENT;

EID: 84989878256     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005889     Document Type: Article

References (43)

1. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R, Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–7. doi: 10.1126/science.117748619892944
2. Human Microbiome Project CStructure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–14. doi: 10.1038/nature1123422699609
3. Aroutcheva A, Gariti D, Simon M, Shott S, Faro J, Simoes JA, et al. Defense factors of vaginal lactobacilli. Am J Obstet Gynecol. 2001;185(2):375–9. 11518895
4. Fredricks DN, Fiedler TL, Marrazzo JM, Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med. 2005;353(18):1899–911. 16267321
5. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci. 2011;108(suppl. 1):4680–7. doi: 10.1073/pnas.100261110720534435
6. Kenyon C, Colebunders R, Crucitti T, The global epidemiology of bacterial vaginosis: a systematic review. Am J Obstet Gynecol. 2013;209(6):505–23. doi: 10.1016/j.ajog.2013.05.00623659989
7. Srinivasan S, Hoffman NG, Morgan MT, Matsen FA, Fiedler TL, Hall RW, et al. Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PloS one. 2012;7(6):e37818. doi: 10.1371/journal.pone.003781822719852
8. Fethers KA, Fairley CK, Hocking JS, Gurrin LC, Bradshaw CS, Sexual risk factors and bacterial vaginosis: a systematic review and meta-analysis. Clin Infect Dis. 2008;47(11):1426–35. doi: 10.1086/59297418947329
9. Shin LY, Kaul R, Stay it with flora: maintaining vaginal health as a possible avenue for prevention of human immunodeficiency virus acquisition. The Journal of infectious diseases. 2008;197(10):1355–7. doi: 10.1086/58749118444792
10. Buvé A, Jespers V, Crucitti T, Fichorova RN, The vaginal microbiota and susceptibility to HIV. Aids. 2014;28(16):2333–44. 25389548
11. 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. doi: 10.1097/QAD.0b013e3283021a3718614873
12. Burgener A, McGowan I, Klatt NR, HIV and mucosal barrier interactions: consequences for transmission and pathogenesis. Current opinion in immunology. 2015;36:22–30. doi: 10.1016/j.coi.2015.06.00426151777
13. 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. doi: 10.1016/j.immuni.2015.04.01925992865
14. Mitchell C, Marrazzo J, Bacterial vaginosis and the cervicovaginal immune response. Am J Reprod Immunol. 2014;71(6):555–63. doi: 10.1111/aji.1226424832618
15. McClelland RS, Balkus JE, Lee J, Anzala O, Kimani J, Schwebke J, et al. Randomized Trial of Periodic Presumptive Treatment With High-Dose Intravaginal Metronidazole and Miconazole to Prevent Vaginal Infections in HIV-negative Women. The Journal of infectious diseases. 2015;211(12):1875–82. doi: 10.1093/infdis/jiu81825526757
16. McClelland RS, Richardson BA, Hassan WM, Chohan V, Lavreys L, Mandaliya K, et al. Improvement of vaginal health for Kenyan women at risk for acquisition of human immunodeficiency virus type 1: results of a randomized trial. The Journal of infectious diseases. 2008;197(10):1361–8. doi: 10.1086/58749018444793
17. Wilson J, Managing recurrent bacterial vaginosis. Sexually Transmitted Infections. 2004;80(1):8–11. 14755028
18. Mathewson ND, Jenq R, Mathew AV, Koenigsknecht M, Hanash A, Toubai T, et al. Gut microbiome-derived metabolites modulate intestinal epithelial cell damage and mitigate graft-versus-host disease. Nat Immunol. 2016;17(5):505–13. doi: 10.1038/ni.340026998764
19. 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. doi: 10.1111/j.1600-0897.2010.00902.x20678168
20. Petrova MI, van den Broek M, Balzarini J, Vanderleyden J, Lebeer S, Vaginal microbiota and its role in HIV transmission and infection. FEMS microbiology reviews. 2013;37(5):762–92. doi: 10.1111/1574-6976.1202923789590
21. Tanca A, Palomba A, Salvatore P, Deligios M, Fraumene C, Manghina V, et al. A straightforward and efficient analytical pipeline for metaproteome characterization. Microbiome. 2014;2(49).
22. Zhou X, Brown CJ, Abdo Z, Davis CC, Hansmann MA, Joyce P, et al. Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. The ISME journal. 2007;1(2):121–33. 18043622
23. Brotman RM, Klebanoff MA, Nansel TR, Yu KF, Andrews WW, Zhang J, et al. Bacterial vaginosis assessed by gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. The Journal of infectious diseases. 2010;202(12):1907–15. doi: 10.1086/65732021067371
24. 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 Med. 2012;9(6):e1001251. doi: 10.1371/journal.pmed.100125122745608
25. Candi E, Schmidt R, Melino G, The cornified envelope: a model of cell death in the skin. Nature reviews Molecular cell biology. 2005;6(4):328–40. 15803139
26. Smith JL, The physiological role of ferritin-like compounds in bacteria. Crit Rev Microbiol. 2004;30(3):173–85. 15490969
27. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–4. doi: 10.1038/nature0754019043404
28. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65. doi: 10.1038/nature0882120203603
29. Srinivasan S, Morgan MT, Fiedler TL, Djukovic D, Hoffman NG, Raftery D, et al. Metabolic signatures of bacterial vaginosis. mBio. 2015;6(2).
30. Arnold KB, Burgener A, Birse K, Romas L, Dunphy LJ, Shahabi K, et al. Increased levels of inflammatory cytokines in the female reproductive tract are associated with altered expression of proteases, mucosal barrier proteins, and an influx of HIV-susceptible target cells. Mucosal immunology. 2015;9(1):194–205. doi: 10.1038/mi.2015.5126104913
31. Burian M, Schittek B, The secrets of dermcidin action. Int J Med Microbiol. 2015;305(2):283–6. doi: 10.1016/j.ijmm.2014.12.01225596890
32. Cruciani F, Wasinger V, Turroni S, Calanni F, Donders G, Brigidi P, et al. Proteome profiles of vaginal fluids from women affected by bacterial vaginosis and healthy controls: outcomes of rifaximin treatment. J Antimicrob Chemother. 2013;68(11):2648–59. doi: 10.1093/jac/dkt24423798671
33. Borgdorff H, Gautam R, Armstrong SD, Xia D, Ndayisaba GF, van Teijlingen NH, et al. Cervicovaginal microbiome dysbiosis is associated with proteome changes related to alterations of the cervicovaginal mucosal barrier. Mucosal immunology. 2015;9(3):621–33. doi: 10.1038/mi.2015.8626349657
34. Srinivasan S, Morgan MT, Fiedler TL, Djukovic D, Hoffman NG, Raftery D, et al. Metabolic Signatures of Bacterial Vaginosis. mBio. 2015;6(2):e00204–15. doi: 10.1128/mBio.00204-1525873373
35. Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic Analysis of the Human Distal Gut Microbiome. Science. 2006;312(5778):1355–59. 16741115
36. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature biotechnology. 2013;31(9):814–21. doi: 10.1038/nbt.267623975157
37. Baeten JM, Donnell D, Ndase P, Mugo NR, Campbell JD, Wangisi J, et al. Antiretroviral prophylaxis for HIV prevention in heterosexual men and women. N Engl J Med. 2012;367(5):399–410. doi: 10.1056/NEJMoa110852422784037
38. Birse K, Arnold KB, Novak RM, McCorrister S, Shaw S, Westmacott GR, et al. Molecular signatures of immune activation and epithelial barrier remodeling are enhanced during the luteal phase of the menstrual cycle: implications for HIV susceptibility. Journal of virology. 2015;89(17):8793–805. doi: 10.1128/JVI.00756-1526085144
39. Zevin AS, Rittmann BE, Krajmalnik-Brown R, The source of inoculum drives bacterial community structure in Synechocystis sp. PCC6803-based photobioreactors. Algal Research. 2016;13:109–15.
40. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high- throughput community sequencing data. Nature methods. 2010;7(5):335–6. doi: 10.1038/nmeth.f.30320383131
41. Huang da W, Sherman BT, Lempicki RA, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2009;4(1):44–57. doi: 10.1038/nprot.2008.21119131956
42. Liang CC, Park AY, Guan JL, In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nature protocols. 2007;2(2):329–33. 17406593
43. Benjamini Y, Hochberg Y, Controlling the False Discovery Rate- a Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society. 1995;57(1):289–300.