Lactobacillus-Deficient Cervicovaginal Bacterial Communities Are Associated with Increased HIV Acquisition in Young South African Women

Immunity

Volumn 46, Issue 1, 2017, Pages 29-37

  Gosmann, Christina ^a,b   Anahtar, Melis N ^a,b   Handley, Scott A ^c   Farcasanu, Mara ^a   Abu Ali, Galeb ^d   Bowman, Brittany A ^a   Padavattan, Nikita ^e   Desai, Chandni ^c   Droit, Lindsay ^c   Moodley, Amber ^f   Dong, Mary ^a,f   Chen, Yuezhou ^g   Ismail, Nasreen ^e   Ndung'u, Thumbi ^a,e   Ghebremichael, Musie S ^a,b   Wesemann, Duane R ^g   Mitchell, Caroline ^a   Dong, Krista L ^a,f   Huttenhower, Curtis ^d   Walker, Bruce D ^a,h,i   Virgin, Herbert W ^c   Kwon, Douglas S ^a,b   more..

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e UNIVERSITY OF KWAZULU NATAL   (South Africa)

^f Females Rising through Education   (South Africa)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

^h HOWARD HUGHES MEDICAL INSTITUTE   (United States)

ⁱ Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

female genital tract (FGT); HIV acquisition; HIV susceptibility; mucosal immunology; sub Saharan Africa; vaginal microbiome

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; RNA 16S; TUMOR NECROSIS FACTOR;

ADULT; AMPLICON; ARTICLE; ATOPOBIUM VAGINAE; BACTERIAL MICROBIOME; CD4+ T LYMPHOCYTE; CELL COUNT; CLOSTRIDIUM; COMMUNITY STRUCTURE; CONTROLLED STUDY; FEMALE; FOLLOW UP; GARDNERELLA VAGINALIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INCIDENCE; INFECTION RISK; LACTOBACILLUS CRISPATUS; LACTOBACILLUS INERS; MAJOR CLINICAL STUDY; MEGASPHAERA; MICROBIAL COMMUNITY; MYCOPLASMA; PREVOTELLA BIVIA; PREVOTELLA MELANINOGENICA; PRIORITY JOURNAL; PROSPECTIVE STUDY; SHUTTLEWORTHIA; SNEATHIA SANGUINEGENS; SOUTH AFRICAN; TARGET CELL; TH17 CELL; VEILLONELLA; VEILLONELLA MONTPELLIERENSIS; YOUNG ADULT; ANAEROBIC BACTERIUM; ANIMAL; COHORT ANALYSIS; FLOW CYTOMETRY; IMMUNOLOGY; LACTOBACILLUS; MICROBIOLOGY; MICROFLORA; MOUSE; PREVOTELLA; SOUTH AFRICA; UTERINE CERVIX; VAGINA;

ANIMALS; BACTERIA, ANAEROBIC; CD4-POSITIVE T-LYMPHOCYTES; CERVIX UTERI; COHORT STUDIES; FEMALE; FLOW CYTOMETRY; HIV INFECTIONS; HUMANS; LACTOBACILLUS; MICE; MICROBIOTA; PREVOTELLA; SOUTH AFRICA; VAGINA;

EID: 85009172894     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.12.013     Document Type: Article

References (34)

1. Anahtar, M.N., Byrne, E.H., Doherty, K.E., Bowman, B.A., Yamamoto, H.S., Soumillon, M., Padavattan, N., Ismail, N., Moodley, A., Sabatini, M.E., et al. Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity 42 (2015), 965–976.
2. Anahtar, M.N., Bowman, B.A., Kwon, D.S., Efficient Nucleic Acid Extraction and 16S rRNA Gene Sequencing for Bacterial Community Characterization. J. Vis. Exp., 110, 2016, 53939.
3. Bradshaw, C.S., Pirotta, M., De Guingand, D., Hocking, J.S., Morton, A.N., Garland, S.M., Fehler, G., Morrow, A., Walker, S., Vodstrcil, L.A., Fairley, C.K., Efficacy of oral metronidazole with vaginal clindamycin or vaginal probiotic for bacterial vaginosis: randomised placebo-controlled double-blind trial. PLoS ONE, 7, 2012, e34540.
4. Byrne, E.H., Anahtar, M.N., Cohen, K.E., Moodley, A., Padavattan, N., Ismail, N., Bowman, B.A., Olson, G.S., Mabhula, A., Leslie, A., et al. Association between injectable progestin-only contraceptives and HIV acquisition and HIV target cell frequency in the female genital tract in South African women: a prospective cohort study. Lancet Infect. Dis. 16 (2016), 441–448.
5. Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J., Holmes, S.P., DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13 (2016), 581–583.
6. Christensen-Quick, A., Lafferty, M., Sun, L., Marchionni, L., DeVico, A., Garzino-Demo, A., Human Th17 cells lack HIV-inhibitory RNases and are highly permissive to productive HIV infection. J. Virol. 90 (2016), 7833–7847.
7. Faith, J.J., Ahern, P.P., Ridaura, V.K., Cheng, J., Gordon, J.I., Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice. Sci. Transl. Med., 6, 2014, 220ra11.
8. Gorgos, L.M., Sycuro, L.K., Srinivasan, S., Fiedler, T.L., Morgan, M.T., Balkus, J.E., McClelland, S.R., Fredricks, D.N., Marrazzo, J.M., Relationship of Specific Bacteria in the Cervical and Vaginal Microbiotas With Cervicitis. Sex. Transm. Dis. 42 (2015), 475–481.
9. Gosmann, C., Mattarollo, S.R., Bridge, J.A., Frazer, I.H., Blumenthal, A., IL-17 suppresses immune effector functions in human papillomavirus-associated epithelial hyperplasia. J. Immunol. 193 (2014), 2248–2257.
10. Haase, A.T., Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu. Rev. Med. 62 (2011), 127–139.
11. Handley, S.A., Desai, C., Zhao, G., Droit, L., Monaco, C.L., Schroeder, A.C., Nkolola, J.P., Norman, M.E., Miller, A.D., Wang, D., et al. SIV Infection-Mediated Changes in Gastrointestinal Bacterial Microbiome and Virome Are Associated with Immunodeficiency and Prevented by Vaccination. Cell Host Microbe 19 (2016), 323–335.
12. Hay, P.E., Lamont, R.F., Taylor-Robinson, D., Morgan, D.J., Ison, C., Pearson, J., Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. BMJ 308 (1994), 295–298.
13. Ivanov, I.I., Atarashi, K., Manel, N., Brodie, E.L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K.C., Santee, C.A., Lynch, S.V., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139 (2009), 485–498.
14. Koning, F.A., Otto, S.A., Hazenberg, M.D., Dekker, L., Prins, M., Miedema, F., Schuitemaker, H., Low-level CD4+ T cell activation is associated with low susceptibility to HIV-1 infection. J. Immunol. 175 (2005), 6117–6122.
15. Lamont, R.F., Nhan-Chang, C.L., Sobel, J.D., Workowski, K., Conde-Agudelo, A., Romero, R., Treatment of abnormal vaginal flora in early pregnancy with clindamycin for the prevention of spontaneous preterm birth: a systematic review and metaanalysis. Am. J. Obstet. Gynecol. 205 (2011), 177–190.
16. Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550.
17. Low, N., Chersich, M.F., Schmidlin, K., Egger, M., Francis, S.C., van de Wijgert, J.H., Hayes, R.J., Baeten, J.M., Brown, J., Delany-Moretlwe, S., et al. Intravaginal practices, bacterial vaginosis, and HIV infection in women: individual participant data meta-analysis. PLoS Med., 8, 2011, e1000416.
18. Marchesi, J.R., Adams, D.H., Fava, F., Hermes, G.D., Hirschfield, G.M., Hold, G., Quraishi, M.N., Kinross, J., Smidt, H., Tuohy, K.M., et al. The gut microbiota and host health: a new clinical frontier. Gut 65 (2016), 330–339.
19. Martin, H.L., Richardson, B.A., Nyange, P.M., Lavreys, L., Hillier, S.L., Chohan, B., Mandaliya, K., Ndinya-Achola, J.O., Bwayo, J., Kreiss, J., Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J. Infect. Dis. 180 (1999), 1863–1868.
20. 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. 61 (2015), 260–269.
21. McKinnon, L.R., Karim, Q.A., Factors Driving the HIV Epidemic in Southern Africa. Curr. HIV/AIDS Rep. 13 (2016), 158–169.
22. 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 in vivo. J. Virol. 85 (2011), 10189–10200.
23. Monaco, C.L., Gootenberg, D.B., Zhao, G., Handley, S.A., Ghebremichael, M.S., Lim, E.S., Lankowski, A., Baldridge, M.T., Wilen, C.B., Flagg, M., et al. Altered Virome and Bacterial Microbiome in Human Immunodeficiency Virus-Associated Acquired Immunodeficiency Syndrome. Cell Host Microbe 19 (2016), 311–322.
24. Morgan, X.C., Tickle, T.L., Sokol, H., Gevers, D., Devaney, K.L., Ward, D.V., Reyes, J.A., Shah, S.A., LeLeiko, N., Snapper, S.B., et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol., 13, 2012, R79.
25. Myer, L., Kuhn, L., Stein, Z.A., Wright, T.C. Jr., Denny, L., Intravaginal practices, bacterial vaginosis, and women's susceptibility to HIV infection: epidemiological evidence and biological mechanisms. Lancet Infect. Dis. 5 (2005), 786–794.
26. Nunn, K.L., Wang, Y.Y., Harit, D., Humphrys, M.S., Ma, B., Cone, R., Ravel, J., Lai, S.K., Enhanced Trapping of HIV-1 by Human Cervicovaginal Mucus Is Associated with Lactobacillus crispatus-Dominant Microbiota. MBio, 6, 2015 e01084–e15.
27. 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 108:Suppl 1 (2011), 4680–4687.
28. Rodriguez-Garcia, M., Barr, F.D., Crist, S.G., Fahey, J.V., Wira, C.R., Phenotype and susceptibility to HIV infection of CD4+ Th17 cells in the human female reproductive tract. Mucosal Immunol. 7 (2014), 1375–1385.
29. Spurbeck, R.R., Arvidson, C.G., Lactobacilli at the front line of defense against vaginally acquired infections. Future Microbiol. 6 (2011), 567–582.
30. Stevenson, M., Stanwick, T.L., Dempsey, M.P., Lamonica, C.A., HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J. 9 (1990), 1551–1560.
31. Stieh, D.J., Matias, E., Xu, H., Fought, A.J., Blanchard, J.L., Marx, P.A., Veazey, R.S., Hope, T.J., Th17 Cells Are Preferentially Infected Very Early after Vaginal Transmission of SIV in Macaques. Cell Host Microbe 19 (2016), 529–540.
32. UNAIDS, U.J.P.o.H.A. (2014). The gap report 2014: Adolescent girls and young women.
33. Ward, H., Rönn, M., Contribution of sexually transmitted infections to the sexual transmission of HIV. Curr. Opin. HIV AIDS 5 (2010), 305–310.
34. Woodman, Z., Can one size fit all? Approach to bacterial vaginosis in sub-Saharan Africa. Ann. Clin. Microbiol. Antimicrob., 15, 2016, 16.