The vaginal mycobiome: A contemporary perspective on fungi in women's health and diseases

Virulence

Volumn 8, Issue 3, 2017, Pages 342-351

  Bradford, L Latéy ^a   Ravel, Jacques ^a  

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

Author keywords

Candida albicans; fungal community; fungi; infectious diseases; microbial ecology; microbiome; microbiota; mycobiota; vagina; vulvovaginal candidiasis

Indexed keywords

ALLERGIC RHINITIS; CELL DIFFERENTIATION; COMMENSALISM; COMPARATIVE STUDY; ECOSYSTEM HEALTH; FUNGAL COMMUNITY; FUNGUS GROWTH; HUMAN; MYCOBIOME; NEUTROPHIL CHEMOTAXIS; NONHUMAN; REVIEW; VAGINA CANDIDIASIS; CLASSIFICATION; FEMALE; FUNGUS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; MYCOSIS; ORGANISMAL INTERACTION; VAGINA; VAGINITIS; WOMEN'S HEALTH;

FEMALE; FUNGI; HUMANS; MICROBIAL INTERACTIONS; MICROBIOTA; MYCOBIOME; MYCOSES; VAGINA; VAGINITIS; WOMEN'S HEALTH;

EID: 84990985710     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.1080/21505594.2016.1237332     Document Type: Review

References (130)

1. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, Gillevet PM. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathogens 2010; 6:e1000713; PMID:20072605; http://dx.doi.org/10.1371/journal.ppat.1000713
2. Gevers D, Knight R, Petrosino JF, Huang K, McGuire AL, Birren BW, Nelson KE, White O, Methe BA, Huttenhower C. The Human Microbiome Project:a community resource for the healthy human microbiome. PLoS Biol 2012; 10:e1001377; PMID:22904687; http://dx.doi.org/10.1371/journal.pbio.1001377
3. Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486:207-14; PMID:22699609; http://dx.doi.org/10.1038/nature11234
4. Markowitz VM, Chen IM, Chu K, Szeto E, Palaniappan K, Jacob B, Ratner A, Liolios K, Pagani I, Huntemann M, et al. IMG/M-HMP:a metagenome comparative analysis system for the Human Microbiome Project. PloS One 2012; 7:e40151; PMID:22792232; http://dx.doi.org/10.1371/journal.pone.0040151
5. Gevers D, Pop M, Schloss PD, Huttenhower C. Bioinformatics for the human microbiome project. PLoS Comput Biol 2012; 8:e1002779; PMID:23209389; http://dx.doi.org/10.1371/journal.pcbi.1002779
6. Huffnagle GB, Noverr MC. The emerging world of the fungal microbiome. Trends Microbiol 2013; 21:334-41; PMID:23685069; http://dx.doi.org/10.1016/j.tim.2013.04.002
7. Galask RP. Vaginal colonization by bacteria and yeast. Am J Obstet Gynecol 1988; 158:993-5; PMID:3284368; http://dx.doi.org/10.1016/0002-9378(88)90111-1
8. Carter BJC. A study of the vaginal flora in the normal female. South Med J 1937; 30:298-304; http://dx.doi.org/10.1097/00007611-193703000-00012
9. Carter B, Jones CP, Creadick RN, Parker RT, Turner V. The vaginal fungi. Ann N Y Acad Sci 1959; 83:265-79; PMID:13808012; http://dx.doi.org/10.1111/j.1749-6632.1960.tb40900.x
10. Barousse MM, Van Der Pol BJ, Fortenberry D, Orr D, Fidel PL, Jr. Vaginal yeast colonisation, prevalence of vaginitis, and associated local immunity in adolescents. Sex Transm Infect 2004; 80:48-53; PMID:14755036; http://dx.doi.org/10.1136/sti.2002.003855
11. Nowakowska D, Kurnatowska A, Stray-Pedersen B, Wilczynski J. Prevalence of fungi in the vagina, rectum and oral cavity in pregnant diabetic women:relation to gestational age and symptoms. Acta Obstet Gynecol Scand 2004; 83:251-6; PMID:14995920; http://dx.doi.org/10.1111/j.0001-6349.2004.0361.x
12. Goldacre MJ, Milne LJ, Watt B, Loudon N, Vessey MP. Prevalence of Yeast and fungi other than Candida albicans in the vagina of normal young women. Br J Obstet Gynaecol 1981; 88:596-600; PMID:7248216; http://dx.doi.org/10.1111/j.1471-0528.1981.tb01214.x
13. Sobel JD. Epidemiology and pathogenesis of recurrent vulvovaginal candidiasis. YMOB 1985; 152:924-35
14. Sobel JD. Recurrent vulvovaginal candidiasis. A prospective study of the efficacy of maintenance ketoconazole therapy. N Engl J Med 1986; 315:1455-8; PMID:3537785; http://dx.doi.org/10.1056/NEJM19861204315-2305
15. Landers DV, Wiesenfeld HC, Heine RP, Krohn MA, Hillier SL. Predictive value of the clinical diagnosis of lower genital tract infection in women. Am J Obstet Gynecol 2004; 190:1004-10; PMID:15118630; http://dx.doi.org/10.1016/j.ajog.2004.02.015
16. Odds FC. Genital candidosis. Clin Exp Dermatol 1982; 7:345-54; PMID:7127883; http://dx.doi.org/10.1111/j.1365-2230.1982.tb02441.x
17. Odds FC. Ecology and epidemiology of Candida species. Zentralbl Bakteriol Mikrobiol Hyg A 1984; 257:207-12; PMID:6385559
18. Odds FC, Webster CE, Fisk PG, Riley VC, Mayuranathan P, Simmons PD. Candida species and C. albicans biotypes in women attending clinics in genitourinary medicine. J Med Microbiol 1989; 29:51-4; PMID:2657069; http://dx.doi.org/10.1099/00222615-29-1-51
19. Xu J, Boyd CM, Livingston E, Meyer W, Madden JF, Mitchell TG. Species and genotypic diversities and similarities of pathogenic yeasts colonizing women. J Clin Microbiol 1999; 37:3835-43; PMID:10565893
20. Guo R, Zheng N, Lu H, Yin H, Yao J, Chen Y. Increased diversity of fungal flora in the vagina of patients with recurrent vaginal candidiasis and allergic rhinitis. Microb Ecol 2012; 64:918-27; PMID:22767123; http://dx.doi.org/10.1007/s00248-012-0084-0
21. Ma B, Forney LJ, Ravel J. Vaginal microbiome:rethinking health and disease. Annu Rev Microbiol 2012; 66:371-89; PMID:22746335; http://dx.doi.org/10.1146/annurev-micro-092611-150157
22. Drell T, Lillsaar T, Tummeleht L, Simm J, Aaspollu A, Vain E, Saarma I, Salumets A, Donders GG, Metsis M. Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PloS One 2013; 8:e54379; PMID:23372716; http://dx.doi.org/10.1371/journal.pone.0054379
23. Cui L, Morris A, Ghedin E. The human mycobiome in health and disease. Genome Med 2013; 5:63; PMID:23899327; http://dx.doi.org/10.1186/gm467
24. Dollive S, Peterfreund GL, Sherrill-Mix S, Bittinger K, Sinha R, Hoffmann C, Nabel CS, Hill DA, Artis D, Bachman MA, et al. A tool kit for quantifying eukaryotic rRNA gene sequences from human microbiome samples. Genome Biol 2012; 13:R60; PMID:22759449
25. Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson KH, Koljalg U. Taxonomic reliability of DNA sequences in public sequence databases:a fungal perspective. PloS One 2006; 1:e59; PMID:17183689; http://dx.doi.org/10.1371/journal.pone.0000059
26. Witkin SS, Ledger WJ. Complexities of the Uniquely Human Vagina. Sci Transl Med 2012; 4:132fs11-fs11; PMID:22553249; http://dx.doi.org/10.1126/scitranslmed.3003944
27. Linhares IM, Summers PR, Larsen B, Giraldo PC, Witkin SS. Contemporary perspectives on vaginal pH and lactobacilli. Am J Obstet Gynecol 2011; 204:120-e1-5; PMID:20832044; http://dx.doi.org/10.1016/j.ajog.2010.07.010
28. Mirmonsef P, Gilbert D, Veazey RS, Wang J, Kendrick SR, Spear GT. A comparison of lower genital tract glycogen and lactic acid levels in women and macaques:implications for HIV and SIV susceptibility. AIDS Res Hum Retroviruses 2012; 28:76-81; PMID:21595610; http://dx.doi.org/10.1089/aid.2011.0071
29. Spear GT, French AL, Gilbert D, Zariffard MR, Mirmonsef P, Sullivan TH, Spear WW, Landay A, Micci S, Lee BH, et al. Human α-amylase present in lower-genital-tract mucosal fluid processes glycogen to support vaginal colonization by Lactobacillus. J Infect Dis 2014; 210:1019-28; PMID:24737800; http://dx.doi.org/10.1093/infdis/jiu231
30. Larsen B, Markovetz AJ, Galask RP. Spatial relationship of the vaginal microflora to the vaginal epithelium of female rats:scanning electron microscopy. App Environ Microbiol 1977; 34:80-7; PMID:889330
31. Mirmonsef P, Hotton AL, Gilbert D, Burgad D, Landay A, Weber KM, Cohen M, Ravel J, Spear GT. Free glycogen in vaginal fluids is associated with Lactobacillus colonization and low vaginal pH. PloS One 2014; 9:e102467; PMID:25033265; http://dx.doi.org/10.1371/journal.pone.0102467
32. Amjadi F, Salehi E, Mehdizadeh M, Aflatoonian R. Role of the innate immunity in female reproductive tract. Adv Biomed Res 2014; 3:1; PMID:24592358; http://dx.doi.org/10.4103/2277-9175.124626
33. Brock M. Fungal metabolism in host niches. Curr Opin Microbiol 2009; 12:371-6; PMID:19535285; http://dx.doi.org/10.1016/j.mib.2009.05.004
34. Goplerud CP, Ohm MJ, Galask RP. Aerobic and anaerobic flora of the cervix during pregnancy and the puerperium. Am J Obstet Gynecol 1976; 126:858-68; PMID:793391; http://dx.doi.org/10.1016/0002-9378(76)90674-8
35. Larsen B, Galask RP. Influence of estrogen and normal flora on vaginal candidiasis in the rat. J Reprod Med 1984; 29:863-8; PMID:6394756
36. Cassone A, Sobel JD. Experimental Models of Vaginal Candidiasis and Their Relevance to Human Candidiasis. Infect Immun 2016; 84:1255-61; PMID:26883592; http://dx.doi.org/10.1128/IAI.01544-15
37. Fidel PL, Jr., Cutright J, Steele C. Effects of reproductive hormones on experimental vaginal candidiasis. Infect Immun 2000; 68:651-7; PMID:10639429; http://dx.doi.org/10.1128/IAI.68.2.651-657.2000
38. Skowronski R, Feldman D. Characterization of an estrogen-binding protein in the yeast Candida albicans. Endocrinology 1989; 124:1965-72; PMID:2647470; http://dx.doi.org/10.1210/endo-124-4-1965
39. Lasarte S, Samaniego R, Salinas-Munoz L, Guia-Gonzalez MA, Weiss LA, Mercader E, Ceballos-Garcia E, Navarro-Gonzalez T, Moreno-Ochoa L, Perez-Millan F, et al. Sex Hormones Coordinate Neutrophil Immunity in the Vagina by Controlling Chemokine Gradients. J Infect Dis 2016; 213:476-84; PMID:26238687; http://dx.doi.org/10.1093/infdis/jiv402
40. Chen RY, Fan YM, Zhang Q, Liu S, Li Q, Ke GL, Li C, You Z. Estradiol inhibits Th17 cell differentiation through inhibition of RORgammaT transcription by recruiting the ERalpha/REA complex to estrogen response elements of the RORgammaT promoter. J Immunol 2015; 194:4019-28; http://dx.doi.org/10.4049/jimmunol.1400806
41. Tarry W, Fisher M, Shen S, Mawhinney M. Candida albicans:the estrogen target for vaginal colonization. J Surg Res 2005; 129:278-82; PMID:16111702; http://dx.doi.org/10.1016/j.jss.2005.05.019
42. McCourtie J, Douglas LJ. Relationship between cell surface composition of Candida albicans and adherence to acrylic after growth on different carbon sources. Infect Immun 1981; 32:1234-41; PMID:7019091
43. Ene IV, Heilmann CJ, Sorgo AG, Walker LA, de Koster CG, Munro CA, Klis FM, Brown AJ. Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans. Proteomics 2012; 12:3164-79; PMID:22997008; http://dx.doi.org/10.1002/pmic.201200228
44. Ene IV, Adya AK, Wehmeier S, Brand AC, MacCallum DM, Gow NAR, Brown AJP. Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell Microbiol 2012; 14:1319-35; PMID:22587014; http://dx.doi.org/10.1111/j.1462-5822.2012.01813.x
45. Sosinska GJ, de Groot PW, Teixeira de Mattos MJ, Dekker HL, de Koster CG, Hellingwerf KJ, Klis FM. Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 2008; 154:510-20; PMID:18227255; http://dx.doi.org/10.1099/mic.0.2007/012617-0
46. Ene IV, Cheng SC, Netea MG, Brown AJP. Growth of Candida albicans Cells on the Physiologically Relevant Carbon Source Lactate Affects Their Recognition and Phagocytosis by Immune Cells. Infect Immun 2012; 81:238-48; PMID:23115042; http://dx.doi.org/10.1128/IAI.01092-12
47. Masson L, Salkinder AL, Olivier AJ, McKinnon LR, Gamieldien H, Mlisana K, Scriba TJ, Lewis DA, Little F, Jaspan HB, et al. Relationship between female genital tract infections, mucosal interleukin-17 production and local T helper type 17 cells. Immunology 2015; 146:557-67; PMID:26302175; http://dx.doi.org/10.1111/imm.12527
48. Noverr MC, Phare SM, Toews GB, Coffey MJ, Huffnagle GB. Pathogenic yeasts Cryptococcus neoformans and Candida albicans produce immunomodulatory prostaglandins. Infect Immun 2001; 69:2957-63; PMID:11292712; http://dx.doi.org/10.1128/IAI.69.5.2957-2963.2001
49. Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, Zecchi R, D'Angelo C, Massi-Benedetti C, Fallarino F, et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 2013; 39:372-85; PMID:23973224; http://dx.doi.org/10.1016/j.immuni.2013.08.003
50. De Luca A, Carvalho A, Cunha C, Iannitti RG, Pitzurra L, Giovannini G, Mencacci A, Bartolommei L, Moretti S, Massi-Benedetti C, et al. IL-22 and IDO1 affect immunity and tolerance to murine and human vaginal candidiasis. PLoS Pathog 2013; 9:e1003486
51. Chaffin WL. Candida albicans cell wall proteins. Microbiol Mol Biol Rev 2008; 72:495-544; PMID:18772287; http://dx.doi.org/10.1128/MMBR.00032-07
52. Moyes DL, Richardson JP, Naglik JR. Candida albicans-epithelial interactions and pathogenicity mechanisms:scratching the surface. Virulence 2015; 6:338-46; PMID:25714110; http://dx.doi.org/10.1080/21505594.2015.1012981
53. Mayer FL, Wilson D, Hube B. Candida albicans pathogenicity mechanisms. Virulence 2013; 4:119-28; PMID:23302789; http://dx.doi.org/10.4161/viru.22913
54. Sobel JD, Muller G, Buckley HR. Critical role of germ tube formation in the pathogenesis of candidal vaginitis. Infect Immun 1984; 44:576-80; PMID:6327527
55. Iliev ID, Underhill DM. Striking a balance:fungal commensalism versus pathogenesis. Curr Opin Microbiol 2013; 16:366-73; PMID:23756050; http://dx.doi.org/10.1016/j.mib.2013.05.004
56. King RD, Lee JC, Morris AL. Adherence of Candida albicans and other Candida species to mucosal epithelial cells. Infect Immun 1980; 27:667-74; PMID:6991423
57. Sobel JD, Myers PG, Kaye D, Levison ME. Adherence of Candida albicans to human vaginal and buccal epithelial cells. J Infect Dis 1981; 143:76-82; PMID:7012245; http://dx.doi.org/10.1093/infdis/143.1.76
58. Trumbore DJ, Sobel JD. Recurrent vulvovaginal candidiasis:vaginal epithelial cell susceptibility to Candida albicans adherence. Obstet Gynecol 1986; 67:810-2; PMID:3517722; http://dx.doi.org/10.1097/00006250-198606000-00012
59. Fleury FJ. Adult vaginitis. Clin Obstet Gynecol 1981; 24:407-38; PMID:7307366; http://dx.doi.org/10.1097/00003081-198106000-00008
60. Sobel JD. Pathogenesis of Candida vulvovaginitis. Curr Topics Med Mycol 1989; 3:86-108; PMID:2688924; http://dx.doi.org/10.1007/978-1-4612-3624-5_5
61. Hurley R, De Louvois J. Candida vaginitis. Postgrad Med J 1979; 55:645-7; PMID:523355; http://dx.doi.org/10.1136/pgmj.55.647.645
62. Drake TE, Maibach HI. Candida and candidiasis. One. Cultural conditions, epidemiology and pathogenesis. Postgrad Med 1973; 53:83-7; PMID:4569505; http://dx.doi.org/10.1080/00325481.1973.11713368
63. Rane HS, Hardison S, Botelho C, Bernardo SM, Wormley F, Jr., Lee SA. Candida albicans VPS4 contributes differentially to epithelial and mucosal pathogenesis. Virulence 2014; 5:810-8; PMID:25483774; http://dx.doi.org/10.4161/21505594.2014.956648
64. Luna-Tapia A, Peters BM, Eberle KE, Kerns ME, Foster TP, Marrero L, Noverr MC, Fidel PL, Jr., Palmer GE. ERG2 and ERG24 Are Required for Normal Vacuolar Physiology as Well as Candida albicans Pathogenicity in a Murine Model of Disseminated but Not Vaginal Candidiasis. Eukaryot Cell 2015; 14:1006-16; PMID:26231054; http://dx.doi.org/10.1128/EC.00116-15
65. Fidel PL, Jr. Distinct protective host defenses against oral and vaginal candidiasis. Medical Mycol 2002; 40:359-75; PMID:12230215; http://dx.doi.org/10.1080/714031126
66. Yano J, Noverr MC, Fidel PL, Jr. Cytokines in the host response to Candida vaginitis:Identifying a role for non-classical immune mediators, S100 alarmins. Cytokine 2012; 58:118-28; PMID:22182685; http://dx.doi.org/10.1016/j.cyto.2011.11.021
67. Fidel PL, Jr., Sobel JD. Immunopathogenesis of recurrent vulvovaginal candidiasis. Clin Microbiol Rev 1996; 9:335-48; PMID:8809464
68. Fidel PL, Jr. Immunity in vaginal candidiasis. Curr Opin Infect Dis 2005; 18:107-11; PMID:15735412; http://dx.doi.org/10.1097/01.qco.0000160897.74492.a3
69. Fidel PL, Jr. History and update on host defense against vaginal candidiasis. Am J Reprod Immunol 2007; 57:2-12; PMID:17156186; http://dx.doi.org/10.1111/j.1600-0897.2006.00450.x
70. Peeters F, Snauwaert R, Segers J, Amery W, van Cutsem J. Observations on candidal vaginitis. Vaginal pH, microbiology, and cytology. Am J Obstet Gynecol 1972; 112:80-6; PMID:4621407; http://dx.doi.org/10.1016/0002-9378(72)90533-9
71. Jacobsen ID, Wilson D, Wachtler B, Brunke S, Naglik JR, Hube B. Candida albicans dimorphism as a therapeutic target. Expert Rev Anti Infect Ther 2012; 10:85-93; PMID:22149617; http://dx.doi.org/10.1586/eri.11.152
72. Biswas S, Van Dijck P, Datta A. Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol Mol Biol Rev 2007; 71:348-76; PMID:17554048; http://dx.doi.org/10.1128/MMBR.00009-06
73. Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell 2003; 2:1053-60; PMID:14555488; http://dx.doi.org/10.1128/EC.2.5.1053-1060.2003
74. Kimura LH, Pearsall NN. Relationship between germination of Candida albicans and increased adherence to human buccal epithelial cells. Infect Immun 1980; 28:464-8; PMID:6995309
75. Sobel JD, Muller G. Ketoconazole in the prevention of experimental candidal vaginitis. Antimicrob Agents Chemother 1984; 25:281-2; PMID:6324671; http://dx.doi.org/10.1128/AAC.25.2.281
76. Peters BM, Palmer GE, Nash AK, Lilly EA, Fidel PL, Jr., Noverr MC. Fungal morphogenetic pathways are required for the hallmark inflammatory response during Candida albicans vaginitis. Infect Immun 2014; 82:532-43; PMID:24478069; http://dx.doi.org/10.1128/IAI.01417-13
77. Albuquerque P, Casadevall A. Quorum sensing in fungi–a review. Med Mycol 2012; 50:337-45; PMID:22268493; http://dx.doi.org/10.3109/13693786.2011.652201
78. Cassone A, De Bernardis F, Mondello F, Ceddia T, Agatensi L. Evidence for a correlation between proteinase secretion and vulvovaginal candidosis. J Infect Dis 1987; 156:777-83; PMID:3309073; http://dx.doi.org/10.1093/infdis/156.5.777
79. De Bernardis F, Agatensi L, Ross IK, Emerson GW, Lorenzini R, Sullivan PA, Cassone A. Evidence for a role for secreted aspartate proteinase of Candida albicans in vulvovaginal candidiasis. J Infect Dis 1990; 161:1276-83; PMID:2189009; http://dx.doi.org/10.1093/infdis/161.6.1276
80. Al- Hedaithy SS. Spectrum and proteinase production of yeasts causing vaginitis in Saudi Arabian women. Med Sci Monitor 2002; 8:CR498-501
81. Taylor BN, Staib P, Binder A, Biesemeier A, Sehnal M, Rollinghoff M, Morschhauser J, Schroppel K. Profile of Candida albicans-secreted aspartic proteinase elicited during vaginal infection. Infect Immun 2005; 73:1828-35; PMID:15731084; http://dx.doi.org/10.1128/IAI.73.3.1828-1835.2005
82. Naglik JR, Rodgers CA, Shirlaw PJ, Dobbie JL, Fernandes-Naglik LL, Greenspan D, Agabian N, Challacombe SJ. Differential expression of Candida albicans secreted aspartyl proteinase and phospholipase B genes in humans correlates with active oral and vaginal infections. J Infect Dis 2003; 188:469-79; PMID:12870130; http://dx.doi.org/10.1086/376536
83. Schaller M, Bein M, Korting HC, Baur S, Hamm G, Monod M, Beinhauer S, Hube B. The secreted aspartyl proteinases Sap1 and Sap2 cause tissue damage in an in vitro model of vaginal candidiasis based on reconstituted human vaginal epithelium. Infect Immun 2003; 71:3227-34; PMID:12761103; http://dx.doi.org/10.1128/IAI.71.6.3227-3234.2003
84. Robertson WH. Mycology of vulvovaginitis. Am J Obstet Gynecol 1988; 158:989-91; PMID:3284367; http://dx.doi.org/10.1016/0002-9378(88)90109-3
85. Cutler JE, Friedman L, Milner KC. Biological and chemical characterization of toxic substances from Candida albicans. Infect Immun 1972; 6:616-27; PMID:4564290
86. Moyes DL, Wilson D, Richardson JP, Mogavero S, Tang SX, Wernecke J, Hofs S, Gratacap RL, Robbins J, Runglall M, et al. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature 2016; 532:64-8; PMID:27027296; http://dx.doi.org/10.1038/nature17625
87. Bruno VM, Shetty AC, Yano J, Fidel PL, Jr., Noverr MC, Peters BM. Transcriptomic analysis of vulvovaginal candidiasis identifies a role for the NLRP3 inflammasome. mBio 2015; 6; PMID:25900651; http://dx.doi.org/10.1128/mBio.00182-15
88. Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J. Biofilms of non-Candida albicans Candida species:quantification, structure and matrix composition. Med Mycol 2009; 47:681-9; PMID:19888800; http://dx.doi.org/10.3109/13693780802549594
89. Paiva LC, Vidigal PG, Donatti L, Svidzinski TI, Consolaro ME. Assessment of in vitro biofilm formation by Candida species isolates from vulvovaginal candidiasis and ultrastructural characteristics. Micron 2012; 43:497-502; PMID:22001373; http://dx.doi.org/10.1016/j.micron.2011.09.013
90. Fanning S, Mitchell AP. Fungal biofilms. PLoS Pathogens 2012; 8:e1002585; PMID:22496639; http://dx.doi.org/10.1371/journal.ppat.1002585
91. Kumamoto CA. Molecular mechanisms of mechanosensing and their roles in fungal contact sensing. Nat Rev Microbiol 2008; 6:667-73; PMID:18679170; http://dx.doi.org/10.1038/nrmicro1960
92. Wachtler B, Wilson D, Haedicke K, Dalle F, Hube B. From attachment to damage:defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PloS One 2011; 6:e17046; PMID:21407800; http://dx.doi.org/10.1371/journal.pone.0017046
93. Dalle F, Wachtler B, L'Ollivier C, Holland G, Bannert N, Wilson D, Labruere C, Bonnin A, Hube B. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell Microbiol 2010; 12:248-71; PMID:19863559; http://dx.doi.org/10.1111/j.1462-5822.2009.01394.x
94. Finkel JS, Mitchell AP. Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 2011; 9:109-18; PMID:21189476; http://dx.doi.org/10.1038/nrmicro2475
95. Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR, Johnson AD. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 2012; 148:126-38; PMID:22265407; http://dx.doi.org/10.1016/j.cell.2011.10.048
96. Harriott MM, Lilly EA, Rodriguez TE, Fidel PL, Jr., Noverr MC. Candida albicans forms biofilms on the vaginal mucosa. Microbiology 2010; 156:3635-44; PMID:207056-67; http://dx.doi.org/10.1099/mic.0.039354-0
97. Muzny CA, Schwebke JR. Biofilms:An Underappreciated Mechanism of Treatment Failure and Recurrence in Vaginal Infections. Clin Infect Dis 2015; 61:601-6; PMID:25935553; http://dx.doi.org/10.1093/cid/civ353
98. Ramage G, Rajendran R, Sherry L, Williams C. Fungal biofilm resistance. Int J Microbiol 2012; 2012:528521; PMID:22518145; http://dx.doi.org/10.1155/2012/528-521
99. Diogo D, Bouchier C, d'Enfert C, Bougnoux ME. Loss of heterozygosity in commensal isolates of the asexual diploid yeast Candida albicans. Fungal Genet Biol 2009; 46:159-68; http://dx.doi.org/10.1016/j.fgb.2008.11.005
100. Coste A, Selmecki A, Forche A, Diogo D, Bougnoux ME, d'Enfert C, Berman J, Sanglard D. Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot Cell 2007; 6:1889-904; PMID:17693596; http://dx.doi.org/10.1128/EC.00151-07
101. Cruickshank R. Doderlein's Vaginal Bacillus:A Contribution to the Study of the Lacto-Bacilli. J Hygiene 1931; 31:375-81; PMID:20475100; http://dx.doi.org/10.1017/S0022172400010901
102. Auger P, Joly J. Microbial flora associated with Candida albicans vulvovaginitis. Obstet Gynecol 1980; 55:397-401; PMID:7360441
103. Donders GG, Bosmans E, Dekeersmaecker A, Vereecken A, Van Bulck B, Spitz B. Pathogenesis of abnormal vaginal bacterial flora. Am J Obstet Gynecol 2000; 182:872-8; PMID:10764465; http://dx.doi.org/10.1016/S0002-9378(00)70338-3
104. Pybus V, Onderdonk AB. Microbial interactions in the vaginal ecosystem, with emphasis on the pathogenesis of bacterial vaginosis. Microbes Infect 1999; 1:285-92; PMID:10602662; http://dx.doi.org/10.1016/S1286-4579(99)80024-0
105. Lai SK, Hida K, Shukair S, Wang YY, Figueiredo A, Cone R, Hope TJ, Hanes J. Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus. J Virol 2009; 83:11196-200; PMID:19692470; http://dx.doi.org/10.1128/JVI.01899-08
106. Gupta K, Stapleton AE, Hooton TM, Roberts PL, Fennell CL, Stamm WE. 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; PMID:9697725; http://dx.doi.org/10.1086/515635
107. Odds FC. Candida and candidosis. Baltimore:University Park Press, 1979
108. Segal E, Savage DC. Adhesion of Candida albicans to mouse intestinal mucosa in vitro:development of the assay and test of inhibitors. J Med Veterinary Mycol 1986; 24:477-9; PMID:3553522; http://dx.doi.org/10.1080/02681218680000751
109. Noverr MC, Huffnagle GB. Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect Immun 2004; 72:6206-10; PMID:15501745; http://dx.doi.org/10.1128/IAI.72.11.6206-6210.2004
110. Pirotta MV, Gunn JM, Chondros P. “Not thrush again!” Women's experience of post-antibiotic vulvovaginitis. Med J Aust 2003; 179:43-6; PMID:12831384
111. Bluestein D, Rutledge C, Lumsden L. Predicting the occurrence of antibiotic-induced candidal vaginitis (AICV). Fam Pract Res J 1991; 11:319-26; PMID:1755351
112. Sobel JD. Vulvovaginal candidosis. Lancet 2007; 369:1961-71; PMID:17560449; http://dx.doi.org/10.1016/S0140-6736(07)60917-9
113. Glover DD, Larsen B. Relationship of fungal vaginitis therapy to prior antibiotic exposure. Infect Dis Obstet Gynecol 2003; 11:157-60; PMID:15022876; http://dx.doi.org/10.1080/10647440300025514
114. Gajer P, Brotman RM, Bai G, Sakamoto J, Schutte UM, Zhong X, Koenig SS, Fu L, Ma ZS, Zhou X, et al. Temporal dynamics of the human vaginal microbiota. Sci Transl Med 2012; 4:132ra52; PMID:22553250; http://dx.doi.org/10.1126/scitranslmed.3003605
115. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011; 108 Suppl 1:4680-7
116. Pirotta MV, Garland SM. Genital Candida species detected in samples from women in Melbourne, Australia, before and after treatment with antibiotics. J Clin Microbiol 2006; 44:3213-7; PMID:16954250; http://dx.doi.org/10.1128/JCM.00218-06
117. McClelland RS, Richardson BA, Hassan WM, Graham SM, Kiarie J, Baeten JM, Mandaliya K, Jaoko W, Ndinya-Achola JO, Holmes KK. Prospective study of vaginal bacterial flora and other risk factors for vulvovaginal candidiasis. J Infect Dis 2009; 199:1883-90; PMID:19456235; http://dx.doi.org/10.1086/599213
118. Shirtliff ME, Peters BM, Jabra-Rizk MA. Cross-kingdom interactions:Candida albicans and bacteria. FEMS Microbiol Lett 2009; 299:1-8; PMID:19552706; http://dx.doi.org/10.1111/j.1574-6968.2009.01668.x
119. Domingue PA, Sadhu K, Costerton JW, Bartlett K, Chow AW. The human vagina:normal flora considered as an in situ tissue-associated, adherent biofilm. Genitourin Med 1991; 67:226-31; PMID:2071125
120. Park SJ, Han KH, Park JY, Choi SJ, Lee KH. Influence of bacterial presence on biofilm formation of Candida albicans. Yonsei Med J 2014; 55:449-58; PMID:24532517; http://dx.doi.org/10.3349/ymj.2014.55.2.449
121. Peleg AY, Hogan DA, Mylonakis E. Medically important bacterial-fungal interactions. Nat Rev Microbiol 2010; 8:340-9; PMID:20348933; http://dx.doi.org/10.1038/nrmicro2313
122. Klotz SA, Gaur NK, De Armond R, Sheppard D, Khardori N, Edwards JE, Jr., Lipke PN, El-Azizi M. Candida albicans Als proteins mediate aggregation with bacteria and yeasts. Med Mycol 2007; 45:363-70; PMID:17510860; http://dx.doi.org/10.1080/1369378070129-9333
123. Holmes AR, McNab R, Jenkinson HF. Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect Immun 1996; 64:4680-5; PMID:8890225
124. Boris S, Barbes C. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect 2000; 2:543-6; PMID:10865199; http://dx.doi.org/10.1016/S1286-4579(00)00313-0
125. Romani L, Zelante T, De Luca A, Iannitti RG, Moretti S, Bartoli A, Aversa F, Puccetti P. Microbiota control of a tryptophan-AhR pathway in disease tolerance to fungi. Euro J Immunol 2014; 44:3192-200; PMID:25256754; http://dx.doi.org/10.1002/eji.201344406
126. Rizzetto L, De Filippo C, Cavalieri D. Richness and diversity of mammalian fungal communities shape innate and adaptive immunity in health and disease. Euro J Immunol 2014; 44:3166-81; PMID:25257052; http://dx.doi.org/10.1002/eji.201344403
127. Underhill DM, Lliev LD. The mycobiota:interactions between commensal fungi and the host immune system. Nat Rev Immunol 2014; 14:405-16; PMID:24854590; http://dx.doi.org/10.1038/nri3684
128. Seed PC. The human mycobiome. Cold Spring Harbor Perspectives Med 2015; 5:a019810; http://dx.doi.org/10.1101/cshperspect.a019810
129. Tati S, Davidow P, McCall A, Hwang-Wong E, Rojas IG, Cormack B, Edgerton M. Candida glabrata Binding to Candida albicans Hyphae Enables Its Development in Oropharyngeal Candidiasis. PLoS Pathogens 2016; 12:e1005522; PMID:27029023; http://dx.doi.org/10.1371/journal.ppat.1005522
130. d'Enfert C. Hidden killers:persistence of opportunistic fungal pathogens in the human host. Curr Opin Microbiol 2009; 12:358-64; PMID:19541532; http://dx.doi.org/10.1016/j.mib.2009.05.008