Understanding vulvovaginal candidiasis through a community genomics approach

Current Fungal Infection Reports

Volumn 7, Issue 2, 2013, Pages 126-131

  Bradford, L Latey ^a   Ravel, Jacques ^a   Bruno, Vincent ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Candida albicans; Genomics; Microbiome; Vagina; VVC

Indexed keywords

ARTICLE; CELLULAR IMMUNITY; GENE EXPRESSION; HOST RESISTANCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; LACTOBACILLUS CRISPATUS; LACTOBACILLUS GASSERI; METAGENOMICS; MICROBIAL COMMUNITY; PATHOGENESIS; SPECIES COMPOSITION; URINARY TRACT INFECTION; VAGINA CANDIDIASIS; VAGINA FLORA; VAGINITIS;

EID: 84882988860     PISSN: 19363761     EISSN: 1936377X     Source Type: Journal    
DOI: 10.1007/s12281-013-0135-0     Document Type: Article

References (69)

1. Sobel JD, Faro S, Force RW, Foxman B, Ledger WJ, et al. Vulvovaginal candidiasis: epidemiologic, diagnostic, and therapeutic considerations. YMOB. 1998;178:203-11.
2. Sobel JD. Vulvovaginal candidosis. Lancet. 2007;369:1961-71.
3. Geiger AM, Foxman B, Sobel JD. Chronic vulvovaginal candidiasis: characteristics of women with Candida albicans, C glabrata and no candida. Genitourin Med. 1995;71:304-7.
4. Nyirjesy P. Chronic vulvovaginal candidiasis. Am Fam Physician. 2001;63:697-702.
5. Anderson MR, Klink K, Cohrssen A. Evaluation of vaginal complaints. JAMA. 2004;291:1368-79.
6. Workowski KA, Berman SM. Sexually transmitted diseases treatment guidelines, 2010; 2010.
7. Sobel JD. Epidemiology and pathogenesis of recurrent vulvovaginal candidiasis. YMOB. 1985;152:924-35.
8. Sobel JD. Vaginitis. N Engl J Med. 1997;337:1896-903.
9. de Leon EM, Jacober SJ, Sobel JD, Foxman B. Prevalence and risk factors for vaginal Candida colonization in women with type 1 and type 2 diabetes. BMC Infect Dis. 2002;2:1.
10. Sobel JD. Pathogenesis of recurrent vulvovaginal Candidiasis. Curr Infect Dis Rep. 2002;4:514-9.
11. Hetticarachchi N, Ashbee HR, Wilson JD. Prevalence and management of non-albicans vaginal candidiasis. Sex Transm Infect. 2010;86:99-100.
12. • Babic M, Hukic M. Candida albicans and non-albicans species as etiological agent of vaginitis in pregnant and non-pregnant women. Bosnian J Basic Med Sci. 2010;10(1):89-97. This article examines the contribution of non-Â-albicans species of Candida to the burden of vaginal candidiasis.
13. Zeng J, Zong L-L, Mao T, Huang Y-X, Xu Z-M. Distribution of Candida albican genotype and Candida species is associated with the severity of vulvovagianl candidiasis. Nan Fang Yi Ke Da Xue Xue Bao. 2011;31:1649-53.
14. Zhu W, Filler SG. Interactions of Candida albicans with epithelial cells. Cell Microbiol. 2010;12:273-82.
15. Romani L, Bistoni F, Puccetti P. Adaptation of Candida albicans to the host environment: the role of morphogenesis in virulence and survival in mammalian hosts. Curr Opin Microbiol. 2003;6:338-43.
16. Staib P, Kretschmar M, Nichterlein T, Hof H, Morschhäuser J. Differential activation of a Candida albicans virulence gene family during infection. Proc Natl Acad Sci USA. 2000;97:6102-7.
17. Filler SG, Sheppard DC. Fungal invasion of normally non-phagocytic host cells. PLoS Pathog. 2006;2:e129.
18. Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev. 2003;67:400-28.
19. Ray TL, Payne CD. Scanning electron microscopy of epidermal adherence and cavitation in murine candidiasis: a role for Candida acid proteinase. Infect Immun. 1988;56:1942-9.
20. Park H, Myers CL, Sheppard DC, Phan QT, Sanchez AA, et al. Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell Microbiol. 2005;7:499-510.
21. Eversole LR, Reichart PA, Ficarra G. Oral keratinocyte immune responses in HIV-associated candidiasis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1997;84(4):372-80.
22. Farah CS, Ashman RB, Challacombe SJ. Oral candidosis. Clin Dermatol. 2000;18:553-62.
23. Lian CH, Liu WD. Differential expression of Candida albicans secreted aspartyl proteinase in human vulvovaginal candidiasis. Mycoses. 2007;50:383-90.
24. Taylor BN, Staib P, Binder A, Biesemeier A, Sehnal M, et al. Profile of Candida albicans-secreted aspartic proteinase elicited during vaginal infection. Infect Immun. 2005;73:1828-35.
25. Paiva LCF, Vidigal PG, Donatti L, Svidzinski TIE, Consolaro MEL. Assessment of in vitro biofilm formation by Candida species isolates from vulvovaginal candidiasis and ultrastructural characteristics. Micron. 2012;43:497-502.
26. Harriott MM, Lilly EA, Rodriguez TE, Fidel PL, Noverr MC. Candida albicans forms biofilms on the vaginal mucosa. Microbiology (Reading, Engl). 2010;156:3635-44.
27. Cheng S, Clancy CJ, Checkley MA, Zhang Z, Wozniak KL, et al. The role of Candida albicans NOT5 in virulence depends upon diverse host factors in vivo. Infect Immun. 2005;73:7190-7.
28. De Bernardis F, Mühlschlegel FA, Cassone A. The pH of the host niche controls gene expression in and virulence of Candida albicans. Infect Immun. 1998;66(7):3317-25.
29. Fidel PL. History and update on host defense against vaginal Candidiasis. Am J Reprod Immunol. 2007;57:2-12.
30. Leigh JE, Barousse M, Swoboda RK, Myers T, Hager S, et al. Candida-specific systemic cell-mediated immune reactivities in human immunodeficiency virus-positive persons with mucosal candidiasis. J Infect Dis. 2001;183:277-85.
31. Schuman P, Sobel JD, Ohmit SE, Mayer KH, Carpenter CC, et al. Mucosal candidal colonization and candidiasis in women with or at risk for human immunodeficiency virus infection. HIV Epidemiology Research Study (HERS) Group. Clin Infect Dis. 1998;27:1161-7.
32. Steele C, Ozenci H, Luo W, Scott M, Fidel PL. Growth inhibition of Candida albicans by vaginal cells from naïve mice. Med Mycol. 1999;37:251-9.
33. Nomanbhoy F, Steele C, Yano J, Fidel PL. Vaginal and oral epithelial cell anti-Candida activity. Infect Immun. 2002;70:7081-8.
34. Barousse MM, Steele C, Dunlap K, Espinosa T, Boikov D, et al. Growth inhibition of Candida albicans by human vaginal epithelial cells. J Infect Dis. 2001;184:1489-93.
35. • Yano J, Noverr MC, Fidel PL. Cytokines in the host response to Candida vaginitis: Identifying a role for non-Â-classical immune mediators, S100 alarmins. Cytokine. 2012;58:118-28. This article discusses the innate immune response to Candida.
36. Chaim W, Foxman B, Sobel JD. Association of recurrent vaginal candidiasis and secretory ABO and Lewis phenotype. J Infect Dis. 1997;176:828-30.
37. Babula O, Lazdane G, Kroica J, Ledger WJ, Witkin SS. Relation between recurrent vulvovaginal candidiasis, vaginal concentrations of mannose-binding lectin, and a mannose-binding lectin gene polymorphism in Latvian women. Clin Infect Dis. 2003;37:733-7.
38. Fidel PL, Barousse M, Espinosa T, Ficarra M, Sturtevant J, et al. An intravaginal live Candida challenge in humans leads to new hypotheses for the immunopathogenesis of vulvovaginal candidiasis. Infect Immun. 2004;72:2939-46.
39. Fidel Jr P. Immunity in vaginal candidiasis. Curr Opin Infect Dis. 2005;18(2):107-11.
40. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, et al. The human microbiome project. Nature. 2007;449:804-10.
41. NIH HMP Working Group, Peterson J, Garges S, Giovanni M, McInnes P, et al. The NIH human microbiome project. Genome Res. 2009;19:2317-23.
42. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122:107-18.
43. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022-3.
44. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007;449:811-8.
45. •• Ma B, Forney LJ, Ravel J. Vaginal microbiome: rethinking health and disease. Annu Rev Microbiol. 2012;66:371-89. This review provides an evidence-Âbased argument for studying both the composition and function of the vaginal ecosystem as a means for understanding vaginal health and disease.
46. Sobel J. Is there a protective role for vaginal flora? Curr Infect Dis Rep. 1999;1:379-83.
47. Donders GGG, Bosmans E, Dekeersmaecker A, Vereecken A, Van Bulck B, et al. Pathogenesis of abnormal vaginal bacterial flora. Am J Obstet Gynecol. 2000;182:872-8.
48. Pybus V, Onderdonk AB. Microbial interactions in the vaginal ecosystem, with emphasis on the pathogenesis of bacterial vaginosis. Microbes Infect. 1999;1:285-92.
49. Lai SK, Hida K, Shukair S, Wang Y-Y, Figueiredo A, et al. Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus. J Virol. 2009;83:11196-200.
50. Gupta K, Stapleton AE, Hooton TM, Roberts PL, Fennell CL, et al. Inverse association of H2O2-producing lactobacilli and vaginal Escherichia coli colonization in women with recurrent urinary tract infections. J Infect Dis. 1998;178:446-50.
51. Taha TE, Hoover DR, Dallabetta GA, Kumwenda NI, Mtimavalye LA, et al. Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS. 1998;12:1699-706.
52. Gray RH, Wawer MJ, Sewankambo N, Serwadda D. HIV-1 infection associated with abnormal vaginal flora morphology and bacterial vaginosis. Lancet. 1997;350(9093):1780.
53. van De Wijgert JH, Mason PR, Gwanzura L, Mbizvo MT, Chirenje ZM, et al. Intravaginal practices, vaginal flora disturbances, and acquisition of sexually transmitted diseases in Zimbabwean women. J Infect Dis. 2000;181:587-94.
54. Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL. Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin Infect Dis. 2003;36:663-8.
55. Boskey ER, Cone RA, Whaley KJ, Moench TR. Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum Reprod. 2001.
56. Tomás M, Ocaña VS, Wiese B. Growth and lactic acid production by vaginal Lactobacillus acidophilus CRL 1259, and inhibition of uropathogenic Escherichia coli. J Med Microbiol. 2003;52(Pt 12):1117-24.
57. Antonio MA, Hawes SE, Hillier SL. The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis. 1999;180:1950-6.
58. Kaewsrichan J, Peeyananjarassri K, Kongprasertkit J. Selection and identification of anaerobic lactobacilli producing inhibitory compounds against vaginal pathogens. FEMS Immunol Med Microbiol. 2006;48:75-83.
59. Klebanoff SJ, Hillier SL, Eschenbach DA, Waltersdorph AM. Control of the microbial flora of the vagina by H2O2-generating lactobacilli. J Infect Dis. 1991;164:94-100.
60. Voravuthikunchai SP, Bilasoi S, Supamala O. Antagonistic activity against pathogenic bacteria by human vaginal lactobacilli. Anaerobe. 2006;12:221-6.
61. Zhou X, Bent SJ, Schneider MG, Davis CC, Islam MR, et al. Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods. Microbiology (Reading, Engl). 2004;150:2565-73.
62. Brotman RM, Ravel J. Ready or not: the molecular diagnosis of bacterial vaginosis. Clin Infect Dis. 2008;47(1):44-6.
63. Fredricks DN, Fiedler TL. Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med. 2005;353(18):1899-911.
64. Verstraelen H, Verhelst R, Claeys G, Temmerman M, Vaneechoutte M. Culture-independent analysis of vaginal microflora: the unrecognized association of Atopobium vaginae with bacterial vaginosis. YMOB. 2004;191:1130-2.
65. Linhares IM, Giraldo PC, Baracat EC. New findings about vaginal bacterial flora. Rev Assoc Med Bras. 2010;56:370-4.
66. •• Ravel J, Gajer P, Abdo Z. Vaginal microbiome of reproductive-Âage women. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4680-7. This article presents the first comprehensive description of the human vaginal microbiome using high-Âthroughput sequencing technologies.
67. •• Gajer P, Brotman RM, Bai G, Sakamoto J, Schütte UME, et al. Temporal dynamics of the human vaginal microbiota. Sci Trans Med. 2012;4:132ra52. This article reveals that while some bacterial communities within the human vagina are relatively stable, others change in correlation with menstrual cycle, sexual activity, etc.
68. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207-14.
69. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Publ Group. 2009;10:57-63.