Cervicovaginal Bacteria Are a Major Modulator of Host Inflammatory Responses in the Female Genital Tract

Immunity

Volumn 42, Issue 5, 2015, Pages 965-976

  Anahtar, Melis N ^a,b   Byrne, Elizabeth H ^a   Doherty, Kathleen E ^a   Bowman, Brittany A ^a   Yamamoto, Hidemi S ^b   Soumillon, Magali ^c   Padavattan, Nikita ^d   Ismail, Nasreen ^d   Moodley, Amber ^e   Sabatini, Mary E ^a   Ghebremichael, Musie S ^a   Nusbaum, Chad ^c   Huttenhower, Curtis ^f   Virgin, Herbert W ^g   Ndung'u, Thumbi ^a,d   Dong, Krista L ^a,e   Walker, Bruce D ^a,h   Fichorova, Raina N ^b   Kwon, Douglas S ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d UNIVERSITY OF KWAZULU NATAL   (South Africa)

^e and Health ^*  (South Africa)

^f HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TOLL LIKE RECEPTOR 4; RNA 16S;

ADULT; ANTIGEN PRESENTING CELL; ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ENZYME ACTIVATION; FEMALE; FEMALE GENITAL TRACT INFLAMMATION; GRAM NEGATIVE BACTERIUM; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LACTOBACILLUS; LONGITUDINAL STUDY; LYMPHOCYTE; MAJOR CLINICAL STUDY; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOUTH AFRICAN; VAGINA FLORA; ADOLESCENT; AFRICA; BACTERIUM; BIODIVERSITY; GENETICS; IMMUNOLOGY; MICROBIOLOGY; SEQUENCE ANALYSIS; SOUTH AFRICA; VAGINA; YOUNG ADULT;

ADOLESCENT; ADULT; AFRICA; BACTERIA; BIODIVERSITY; CYTOKINES; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; LACTOBACILLUS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS; SOUTH AFRICA; VAGINA; YOUNG ADULT;

EID: 84929688630     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.04.019     Document Type: Article

References (50)

1. Abubucker S., Segata N., Goll J., Schubert A.M., Izard J., Cantarel B.L., Rodriguez-Mueller B., Zucker J., Thiagarajan M., Henrissat B., et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput. Biol. 2012, 8:e1002358.
2. Aroutcheva A., Gariti D., Simon M., Shott S., Faro J., Simoes J.A., Gurguis A., Faro S. Defense factors of vaginal lactobacilli. Am. J. Obstet. Gynecol. 2001, 185:375-379.
3. Atashili J., Poole C., Ndumbe P.M., Adimora A.A., Smith J.S. Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS 2008, 22:1493-1501.
4. Bradshaw C.S., Vodstrcil L.A., Hocking J.S., Law M., Pirotta M., Garland S.M., De Guingand D., Morton A.N., Fairley C.K. Recurrence of bacterial vaginosis is significantly associated with posttreatment sexual activities and hormonal contraceptive use. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 2013, 56:777-786.
5. Bradshaw C.S., Walker J., Fairley C.K., Chen M.Y., Tabrizi S.N., Donovan B., Kaldor J.M., McNamee K., Urban E., Walker S., et al. Prevalent and incident bacterial vaginosis are associated with sexual and contraceptive behaviours in young Australian women. PLoS ONE 2013, 8:e57688.
6. Brotman R.M., Klebanoff M.A., Nansel T.R., Yu K.F., Andrews W.W., Zhang J., Schwebke J.R. Bacterial vaginosis assessed by gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. J.Infect. Dis. 2010, 202:1907-1915.
7. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K., Gordon J.I., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7:335-336.
8. Caporaso J.G., Lauber C.L., Walters W.A., Berg-Lyons D., Huntley J., Fierer N., Owens S.M., Betley J., Fraser L., Bauer M., et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012, 6:1621-1624.
9. Chaban B., Links M.G., Jayaprakash T.P., Wagner E.C., Bourque D.K., Lohn Z., Albert A.Y., van Schalkwyk J., Reid G., Hemmingsen S.M., et al. Characterization of the vaginal microbiota of healthy Canadian women through the menstrual cycle. Microbiome 2014, 2:23.
10. Cohen C.R., Moscicki A.B., Scott M.E., Ma Y., Shiboski S., Bukusi E., Daud I., Rebbapragada A., Brown J., Kaul R. Increased levels of immune activation in the genital tract of healthy young women from sub-Saharan Africa. AIDS 2010, 24:2069-2074.
11. Cule E., De Iorio M. Ridge regression in prediction problems: automatic choice of the ridge parameter. Genet. Epidemiol. 2013, 37:704-714.
12. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S., Collini S., Pieraccini G., Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 2010, 107:14691-14696.
13. Delaney M.L., Onderdonk A.B. Nugent score related to vaginal culture in pregnant women. Obstet. Gynecol. 2001, 98:79-84.
14. Doerflinger S.Y., Throop A.L., Herbst-Kralovetz M.M. Bacteria in the vaginal microbiome alter the innate immune response and barrier properties of the human vaginal epithelia in a species-specific manner. J.Infect. Dis. 2014, 209:1989-1999.
15. Drell T., Lillsaar T., Tummeleht L., Simm J., Aaspõllu A., Väin E., Saarma I., Salumets A., Donders G.G., Metsis M. Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PLoS ONE 2013, 8:e54379.
16. El Aila N.A., Tency I., Claeys G., Verstraelen H., Saerens B., Santiago G.L., De Backer E., Cools P., Temmerman M., Verhelst R., Vaneechoutte M. Identification and genotyping of bacteria from paired vaginal and rectal samples from pregnant women indicates similarity between vaginal and rectal microflora. BMC Infect. Dis. 2009, 9:167.
17. Eren A.M., Zozaya M., Taylor C.M., Dowd S.E., Martin D.H., Ferris M.J. Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. PLoS ONE 2011, 6:e26732.
18. Fichorova R.N., Yamamoto H.S., Delaney M.L., Onderdonk A.B., Doncel G.F. Novel vaginal microflora colonization model providing new insight into microbicide mechanism of action. mBiol. 2011, 2. e00168-00111.
19. Ghartey J.P., Smith B.C., Chen Z., Buckley N., Lo Y., Ratner A.J., Herold B.C., Burk R.D. Lactobacillus crispatus dominant vaginal microbiome is associated with inhibitory activity of female genital tract secretions against Escherichia coli. PLoS ONE 2014, 9:e96659.
20. Haase A.T. Targeting early infection to prevent HIV-1 mucosal transmission. Nature 2010, 464:217-223.
21. Hedges S.R., Sibley D.A., Mayo M.S., Hook E.W., Russell M.W. Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections. J.Infect. Dis. 1998, 178:742-751.
22. Hickey D.K., Patel M.V., Fahey J.V., Wira C.R. Innate and adaptive immunity at mucosal surfaces of the female reproductive tract: stratification and integration of immune protection against the transmission of sexually transmitted infections. J.Reprod. Immunol. 2011, 88:185-194.
23. Huttenhower C. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214. Human Microbiome Project Consortium.
24. Iijima N., Mattei L.M., Iwasaki A. Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc. Natl. Acad. Sci. USA 2011, 108:284-289.
25. Inglis S.R., Jeremias J., Kuno K., Lescale K., Peeper Q., Chervenak F.A., Witkin S.S. Detection of tumor necrosis factor-alpha, interleukin-6, and fetal fibronectin in the lower genital tract during pregnancy: relation to outcome. Am. J. Obstet. Gynecol. 1994, 171:5-10.
26. Jaspers E., Overmann J. Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl. Environ. Microbiol. 2004, 70:4831-4839.
27. Jespers V., Crucitti T., Menten J., Verhelst R., Mwaura M., Mandaliya K., Ndayisaba G.F., Delany-Moretlwe S., Verstraelen H., Hardy L., et al. Prevalence and correlates of bacterial vaginosis in different sub-populations of women in sub-Saharan Africa: a cross-sectional study. PLoS ONE 2014, 9:e109670. Vaginal Biomarkers Study Group.
28. Kostic A.D., Chun E., Robertson L., Glickman J.N., Gallini C.A., Michaud M., Clancy T.E., Chung D.C., Lochhead P., Hold G.L., et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013, 14:207-215.
29. Lajoie J., Juno J., Burgener A., Rahman S., Mogk K., Wachihi C., Mwanjewe J., Plummer F.A., Kimani J., Ball T.B., Fowke K.R. A distinct cytokine and chemokine profile at the genital mucosa is associated with HIV-1 protection among HIV-exposed seronegative commercial sex workers. Mucosal Immunol. 2012, 5:277-287.
30. Littman D.R., Pamer E.G. Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe 2011, 10:311-323.
31. Lockwood C.J., Ghidini A., Wein R., Lapinski R., Casal D., Berkowitz R.L. Increased interleukin-6 concentrations in cervical secretions are associated with preterm delivery. Am. J. Obstet. Gynecol. 1994, 171:1097-1102.
32. Macklaim J.M., Fernandes A.D., Di Bella J.M., Hammond J.A., Reid G., Gloor G.B. Comparative meta-RNA-seq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis. Microbiome 2013, 1:12.
33. Madara J.L., Stafford J. Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J.Clin. Invest. 1989, 83:724-727.
34. Masson L., Passmore J.A., Liebenberg L.J., Werner L., Baxter C., Arnold K.B., Williamson C., Little F., Mansoor L.E., Naranbhai V., et al. Genital inflammation and the risk of HIV acquisition in women. Clin Infect Dis. 2015, Published online April 21, 2015. 10.1093/cid/civ298.
35. McGee Z.A., Clemens C.M., Jensen R.L., Klein J.J., Barley L.R., Gorby G.L. Local induction of tumor necrosis factor as a molecular mechanism of mucosal damage by gonococci. Microb. Pathog. 1992, 12:333-341.
36. Meditz A.L., Haas M.K., Folkvord J.M., Melander K., Young R., McCarter M., Mawhinney S., Campbell T.B., Lie Y., Coakley E., et al. HLA-DR+ CD38+ CD4+ T lymphocytes have elevated CCR5 expression and produce the majority of R5-tropic HIV-1 RNA invivo. J.Virol. 2011, 85:10189-10200.
37. Morrison C., Fichorova R.N., Mauck C., Chen P.L., Kwok C., Chipato T., Salata R., Doncel G.F. Cervical inflammation and immunity associated with hormonal contraception, pregnancy, and HIV-1 seroconversion. J.Acquir. Immune Defic. Syndr. 2014, 66:109-117.
38. Myer L., Denny L., Telerant R., Souza Md., Wright T.C., Kuhn L. Bacterial vaginosis and susceptibility to HIV infection in South African women: a nested case-control study. J.Infect. Dis. 2005, 192:1372-1380.
39. Ochiel D.O., Ghosh M., Fahey J.V., Guyre P.M., Wira C.R. Human uterine epithelial cell secretions regulate dendritic cell differentiation and responses to TLR ligands. J.Leukoc. Biol. 2010, 88:435-444.
40. Rampersaud R., Planet P.J., Randis T.M., Kulkarni R., Aguilar J.L., Lehrer R.I., Ratner A.J. Inerolysin, a cholesterol-dependent cytolysin produced by Lactobacillus iners. J.Bacteriol. 2011, 193:1034-1041.
41. Rasmussen S.J., Eckmann L., Quayle A.J., Shen L., Zhang Y.X., Anderson D.J., Fierer J., Stephens R.S., Kagnoff M.F. Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. J.Clin. Invest. 1997, 99:77-87.
42. Ravel J., Gajer P., Abdo Z., Schneider G.M., Koenig S.S., McCulle S.L., Karlebach S., Gorle R., Russell J., Tacket C.O., et al. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. USA 2011, 108(1):4680-4687.
43. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
44. Rodriguez A., Vigorito E., Clare S., Warren M.V., Couttet P., Soond D.R., van Dongen S., Grocock R.J., Das P.P., Miska E.A., et al. Requirement of bic/microRNA-155 for normal immune function. Science 2007, 316:608-611.
45. Segata N., Waldron L., Ballarini A., Narasimhan V., Jousson O., Huttenhower C. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat. Methods 2012, 9:811-814.
46. Soumillon M., Cacchirelli D., Semrau S., van Oudenaarden A., Mikkelsen T.S. Characterization of directed differentiation by high-throughput single-cell RNA-Seq. bioRxiv 2014, Published online March 5, 2014. 10.1101/003236.
47. Wiesenfeld H.C., Hillier S.L., Krohn M.A., Landers D.V., Sweet R.L. Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 2003, 36:663-668.
48. Wira C.R., Grant-Tschudy K.S., Crane-Godreau M.A. Epithelial cells in the female reproductive tract: a central role as sentinels of immune protection. Am. J. Reprod. Immunol. 2005, 53:65-76.
49. Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Magris M., Hidalgo G., Baldassano R.N., Anokhin A.P., et al. Human gut microbiome viewed across age and geography. Nature 2012, 486:222-227.
50. Zhou X., Brown C.J., Abdo Z., Davis C.C., Hansmann M.A., Joyce P., Foster J.A., Forney L.J. Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J. 2007, 1:121-133.