Antifungal Th immunity: Growing up in family

Frontiers in Immunology

Volumn 5, Issue OCT, 2014, Pages

  Borghi, Monica ^a   Renga, Giorgia ^a   Puccetti, Matteo ^b   Oikonomou, Vasileios ^a   Palmieri, Melissa ^a   Galosi, Claudia ^a   Bartoli, Andrea ^a   Romani, Luigina ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b Polo GGB   (Italy)

Author keywords

Fungi; Immunity; Th cell subsets; Tolerance

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 22;

ANTIFUNGAL RESISTANCE; ATOPIC DERMATITIS; BIOME; BIOTA; CANDIDA ALBICANS; CYSTIC FIBROSIS; DENDRITIC CELL; DYSBIOSIS; HELPER CELL; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; MALASSEZIA; MUCOCUTANEOUS CANDIDIASIS; MYCOSIS; NONHUMAN; PNEUMOCYSTIS JIROVECI; REGULATORY T LYMPHOCYTE; REVIEW; TH1 CELL; TH17 CELL; TH2 CELL; TH22 CELL; TH9 CELL; TRYPTOPHAN METABOLISM;

EID: 84928744065     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00506     Document Type: Review

References (92)

1. Cui L, Morris A, Ghedin E. The human mycobiome in health and disease. Genome Med (2013) 5:63. doi: 10.1186/gm467
2. Romani L. Immunity to fungal infections. Nat Rev Immunol (2011) 11:275-88. doi:10.1038/nri2939
3. Segal BH, Herbrecht R, Stevens DA, Ostrosky-Zeichner L, Sobel J, Viscoli C, et al. Defining responses to therapy and study outcomes in clinical trials of invasive fungal diseases: Mycoses Study Group and European Organization for Research and Treatment of Cancer consensus criteria. Clin Infect Dis (2008) 47:674-83. doi:10.1086/590566
4. Pflughoeft KJ, Versalovic J. Human microbiome in health and disease. Annu Rev Pathol (2012) 7:99-122. doi:10.1146/annurev-pathol-011811-132421
5. Paulino LC, Tseng CH, Strober BE, Blaser MJ. Molecular analysis of fungal microbiota in samples from healthy human skin and psoriatic lesions. J Clin Microbiol (2006) 44:2933-41. doi:10.1128/JCM.00785-06
6. Wang ZK, Yang YS, Stefka AT, Sun G, Peng LH. Review article: fungal microbiota and digestive diseases. Aliment Pharmacol Ther (2014) 39:751-66. doi:10.1111/apt.12665
7. Huffnagle GB, Noverr MC. The emerging world of the fungal microbiome. Trends Microbiol (2013) 21:334-41. doi:10.1016/j.tim.2013.04.002
8. Underhill DM, Iliev ID. The mycobiota: interactions between commensal fungi and the host immune system. Nat Rev Immunol (2014) 14:405-16. doi:10.1038/nri3684
9. Delhaes L, Monchy S, Frealle E, Hubans C, Salleron J, Leroy S, et al. The airway microbiota in cystic fibrosis: a complex fungal and bacterial community - implications for therapeutic management. PLoS One (2012) 7:e36313. doi:10.1371/journal.pone.0036313
10. Ott SJ, Kuhbacher T, Musfeldt M, Rosenstiel P, Hellmig S, Rehman A, et al. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol (2008) 43:831-41. doi:10.1080/00365520801935434
11. Li Q, Wang C, Tang C, He Q, Li N, Li J. Dysbiosis of gut fungal microbiota is associated with mucosal inflammation in Crohn's disease. J Clin Gastroenterol (2014) 48:513-23. doi:10.1097/MCG.0000000000000035
12. Zhang E, Tanaka T, Tajima M, Tsuboi R, Nishikawa A, Sugita T. Characterization of the skin fungal microbiota in patients with atopic dermatitis and in healthy subjects. Microbiol Immunol (2011) 55:625-32. doi:10.1111/j.1348-0421.2011.00364.x
13. Smeekens SP, Huttenhower C, Riza A, van de Veerdonk FL, Zeeuwen PL, Schalkwijk J, et al. Skin microbiome imbalance in patients with STAT1/STAT3 defects impairs innate host defense responses. J Innate Immun (2014) 6:253-62. doi:10.1159/000351912
14. Peleg AY, Hogan DA, Mylonakis E. Medically important bacterial-fungal interactions. Nat Rev Microbiol (2010) 8:340-9. doi:10.1038/nrmicro2313
15. Krause R, Schwab E, Bachhiesl D, Daxbock F, Wenisch C, Krejs GJ, et al. Role of Candida in antibiotic-associated diarrhea. J Infect Dis (2001) 184:1065-9. doi:10.1086/323550
16. Kawamoto S, Maruya M, Kato LM, Suda W, Atarashi K, Doi Y, et al. Foxp3(+) T cells regulate immunoglobulin a selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity (2014) 41:152-65. doi:10.1016/j.immuni.2014.05.016
17. Noverr MC, Huffnagle GB. Does the microbiota regulate immune responses outside the gut? Trends Microbiol (2004) 12:562-8. doi:10.1016/j.tim.2004.10.008
18. Perfect JR. The impact of the host on fungal infections. Am J Med (2012) 125:S39-51. doi:10.1016/j.amjmed.2011.10.010
19. Romani L, Fallarino F, De Luca A, Montagnoli C, D'Angelo C, Zelante T, et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature (2008) 451:211-5. doi:10.1038/nature06471
20. Iannitti RG, Carvalho A, Cunha C, De Luca A, Giovannini G, Casagrande A, et al. Th17/Treg imbalance in murine cystic fibrosis is linked to indoleamine 2,3-dioxygenase deficiency but corrected by kynurenines. Am J Respir Crit Care Med (2013) 187:609-20. doi:10.1164/rccm.201207-1346OC
21. Singh N, Perfect JR. Immune reconstitution syndrome associated with opportunistic mycoses. Lancet Infect Dis (2007) 7:395-401. doi:10.1016/S1473-3099(07)70085-3
22. Legrand F, Lecuit M, Dupont B, Bellaton E, Huerre M, Rohrlich PS, et al. Adjuvant corticosteroid therapy for chronic disseminated candidiasis. Clin Infect Dis (2008) 46:696-702. doi:10.1086/527390
23. Casadevall A, Pirofski LA. The damage-response framework of microbial pathogenesis. Nat Rev Microbiol (2003) 1:17-24. doi:10.1038/nrmicro732
24. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol (2010) 10:170-81. doi:10.1038/nri2711
25. Wuthrich M, Deepe GS Jr, Klein B. Adaptive immunity to fungi. Annu Rev Immunol (2012) 30:115-48. doi:10.1146/annurev-immunol-020711-074958
26. Carvalho A, De Luca A, Bozza S, Cunha C, D'Angelo C, Moretti S, et al. TLR3 essentially promotes protective class I-restricted memory CD8(+) T-cell responses to Aspergillus fumigatus in hematopoietic transplanted patients. Blood (2012) 119:967-77. doi:10.1182/blood-2011-06-362582
27. De Luca A, Iannitti RG, Bozza S, Beau R, Casagrande A, D'Angelo C, et al. CD4(+) T cell vaccination overcomes defective cross-presentation of fungal antigens in a mouse model of chronic granulomatous disease. J Clin Invest (2012) 122:1816-31. doi:10.1172/JCI60862
28. Bozza S, Gaziano R, Spreca A, Bacci A, Montagnoli C, Di Francesco P, et al. Dendritic cells transport conidia and hyphae of Aspergillus fumigatus from the airways to the draining lymph nodes and initiate disparate Th responses to the fungus. J Immunol (2002) 168:1362-71. doi:10.4049/jimmunol.168.3.1362
29. Ersland K, Wuthrich M, Klein BS. Dynamic interplay among monocyte-derived, dermal, and resident lymph node dendritic cells during the generation of vaccine immunity to fungi. Cell Host Microbe (2010) 7:474-87. doi:10.1016/j.chom.2010.05.010
30. Rizzetto L, De Filippo C, Rivero D, Riccadonna S, Beltrame L, Cavalieri D. Systems biology of host-mycobiota interactions: dissecting dectin-1 and dectin-2 signalling in immune cells with DC-ATLAS. Immunobiology (2013) 218:1428-37. doi:10.1016/j.imbio.2013.07.002
31. Gringhuis SI, Den Dunnen J, Litjens M, Van Der Vlist M, Wevers B, Bruijns SC, et al. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat Immunol (2009) 10:203-13. doi:10.1038/ni.1692
32. Roy RM, Klein BS. Dendritic cells in antifungal immunity and vaccine design. Cell Host Microbe (2012) 11:436-46. doi:10.1016/j.chom.2012.04.005
33. Romani L, Bistoni F, Puccetti P. Fungi, dendritic cells and receptors: a host perspective of fungal virulence. Trends Microbiol (2002) 10:508-14. doi:10.1016/S0966-842X(02)02460-5
34. Muranski P, Restifo NP. Essentials of Th17 cell commitment and plasticity. Blood (2013) 121:2402-14. doi:10.1182/blood-2012-09-378653
35. Jarvis JN, Casazza JP, Stone HH, Meintjes G, Lawn SD, Levitz SM, et al. The phenotype of the Cryptococcus-specific CD4+ memory T-cell response is associated with disease severity and outcome in HIV-associated cryptococcal meningitis. J Infect Dis (2013) 207:1817-28. doi:10.1093/infdis/jit099
36. de Oliveira LL, Coltri KC, Cardoso CR, Roque-Barreira MC, Panunto-Castelo A. T helper 1-inducing adjuvant protects against experimental paracoccidioidomycosis. PLoS Negl Trop Dis (2008) 2:e183. doi:10.1371/journal.pntd.0000183
37. Spellberg B, Ibrahim AS, Lin L, Avanesian V, Fu Y, Lipke P, et al. Antibody titer threshold predicts anti-candidal vaccine efficacy even though the mechanism of protection is induction of cell-mediated immunity. J Infect Dis (2008) 197:967-71. doi:10.1086/529204
38. Ouederni M, Sanal O, Ikinciogullari A, Tezcan I, Dogu F, Sologuren I, et al. Clinical features of candidiasis in patients with inherited interleukin 12 receptor beta1 deficiency. Clin Infect Dis (2014) 58:204-13. doi:10.1093/cid/cit722
39. Moraes-Vasconcelos D, Grumach AS, Yamaguti A, Andrade ME, Fieschi C, De Beaucoudrey L, et al. Paracoccidioides brasiliensis disseminated disease in a patient with inherited deficiency in the beta1 subunit of the interleukin (IL)-12/IL-23 receptor. Clin Infect Dis (2005) 41:e31-7. doi:10.1086/432119
40. Puel A, Cypowyj S, Marodi L, Abel L, Picard C, Casanova JL. Inborn errors of human IL-17 immunity underlie chronic mucocutaneous candidiasis. Curr Opin Allergy Clin Immunol (2012) 12:616-22. doi:10.1097/ACI.0b013e328358cc0b
41. Milner JD, Brenchley JM, Laurence A, Freeman AF, Hill BJ, Elias KM, et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature (2008) 452:773-6. doi:10.1038/nature06764
42. Eyerich K, Rombold S, Foerster S, Behrendt H, Hofmann H, Ring J, et al. Altered, but not diminished specific T cell response in chronic mucocutaneous candidiasis patients. Arch Dermatol Res (2007) 299:475-81. doi:10.1007/s00403-007-0792-3
43. Ryan KR, Hong M, Arkwright PD, Gennery AR, Costigan C, Dominguez M, et al. Impaired dendritic cell maturation and cytokine production in patients with chronic mucocutanous candidiasis with or without APECED. Clin Exp Immunol (2008) 154:406-14. doi:10.1111/j.1365-2249.2008.03778.x
44. van de Veerdonk FL, Plantinga TS, Hoischen A, Smeekens SP, Joosten LA, Gilissen C, et al. STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N Engl J Med (2011) 365:54-61. doi:10.1056/NEJMoa1100102
45. Vinh DC. Insights into human antifungal immunity from primary immunodeficiencies. Lancet Infect Dis (2011) 11:780-92. doi:10.1016/S1473-3099(11)70217-1
46. Pandiyan P, Conti HR, Zheng L, Peterson AC, Mathern DR, Hernandez-Santos N, et al. CD4(+)CD25(+)Foxp3(+) regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity (2011) 34:422-34. doi:10.1016/j.immuni.2011.03.002
47. Zelante T, De Luca A, Bonifazi P, Montagnoli C, Bozza S, Moretti S, et al. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur J Immunol (2007) 37:2695-706. doi:10.1002/eji.200737409
48. Wuthrich M, Gern B, Hung CY, Ersland K, Rocco N, Pick-Jacobs J, et al. Vaccine-induced protection against 3 systemic mycoses endemic to North America requires Th17 cells in mice. J Clin Invest (2011) 121:554-68. doi:10.1172/JCI43984
49. Cheng SC, van de Veerdonk F, Smeekens S, Joosten LA, Van Der Meer JW, Kullberg BJ, et al. Candida albicans dampens host defense by downregulating IL-17 production. J Immunol (2010) 185:2450-7. doi:10.4049/jimmunol.1000756
50. Loures FV, Pina A, Felonato M, Calich VL. TLR2 is a negative regulator of Th17 cells and tissue pathology in a pulmonary model of fungal infection. J Immunol (2009) 183:1279-90. doi:10.4049/jimmunol.0801599
51. Romani L, Zelante T, De Luca A, Fallarino F, Puccetti P. IL-17 and therapeutic kynurenines in pathogenic inflammation to fungi. J Immunol (2008) 180:5157-62. doi:10.4049/jimmunol.180.8.5157
52. Zelante T, Iannitti RG, De Luca A, Arroyo J, Blanco N, Servillo G, et al. Sensing of mammalian IL-17A regulates fungal adaptation and virulence. Nat Commun (2012) 3:683. doi:10.1038/ncomms1685
53. Ahlgren KM, Moretti S, Ardesjö Lundgren B, Karlsson I, Åhlin E, Norling A, et al. Increased IL-17A secretion in response to Candida albicans in autoimmune polyendocrine syndrome type 1 and its animal model. Eur J Immunol (2011) 41:235-45. doi:10.1002/eji.200939883
54. Kisand K, Boe Wolff AS, Podkrajsek KT, Tserel L, Link M, Kisand KV, et al. Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J Exp Med (2010) 207:299-308. doi:10.1084/jem.20091669
55. Puel A, Doffinger R, Natividad A, Chrabieh M, Barcenas-Morales G, Picard C, et al. Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J Exp Med (2010) 207:291-7. doi:10.1084/jem.20091983
56. Wildbaum G, Nahir MA, Karin N. Beneficial autoimmunity to proinflammatory mediators restrains the consequences of self-destructive immunity. Immunity (2003) 19:679-88. doi:10.1016/S1074-7613(03)00291-7
57. Kreindler JL, Steele C, Nguyen N, Chan YR, Pilewski JM, Alcorn JF, et al. Vitamin D3 attenuates Th2 responses to Aspergillus fumigatus mounted by CD4+ T cells from cystic fibrosis patients with allergic bronchopulmonary aspergillosis. J Clin Invest (2010) 120:3242-54. doi:10.1172/JCI42388
58. Bhatia S, Fei M, Yarlagadda M, Qi Z, Akira S, Saijo S, et al. Rapid host defense against Aspergillus fumigatus involves alveolar macrophages with a predominance of alternatively activated phenotype. PLoS One (2011) 6:e15943. doi:10.1371/journal.pone.0015943
59. Nelson MP, Christmann BS, Werner JL, Metz AE, Trevor JL, Lowell CA, et al. IL-33 and M2a alveolar macrophages promote lung defense against the atypical fungal pathogen Pneumocystis murina. J Immunol (2011) 186:2372-81. doi:10.4049/jimmunol.1002558
60. Guimaraes AJ, Frases S, Gomez FJ, Zancope-Oliveira RM, Nosanchuk JD. Monoclonal antibodies to heat shock protein 60 alter the pathogenesis of Histoplasma capsulatum. Infect Immun (2009) 77:1357-67. doi:10.1128/IAI.01443-08
61. Casadevall A, Pirofski LA. A reappraisal of humoral immunity based on mechanisms of antibody-mediated protection against intracellular pathogens. Adv Immunol (2006) 91:1-44. doi:10.1016/S0065-2776(06)91001-3
62. McClelland EE, Nicola AM, Prados-Rosales R, Casadevall A. Ab binding alters gene expression in Cryptococcus neoformans and directly modulates fungal metabolism. J Clin Invest (2010) 120:1355-61. doi:10.1172/JCI38322
63. Subramaniam KS, Datta K, Quintero E, Manix C, Marks MS, Pirofski LA. The absence of serum IgM enhances the susceptibility of mice to pulmonary challenge with Cryptococcus neoformans. J Immunol (2010) 184:5755-67. doi:10.4049/jimmunol.0901638
64. Kaplan MH. Th9 cells: differentiation and disease. Immunol Rev (2013) 252:104-15. doi:10.1111/imr.12028
65. Schlapbach C, Gehad A, Yang C, Watanabe R, Guenova E, Teague JE, et al. Human TH9 cells are skin-tropic and have autocrine and paracrine proinflammatory capacity. Sci Transl Med (2014) 6:219ra218. doi:10.1126/scitranslmed.3007828
66. Wilhelm C, Hirota K, Stieglitz B, Van Snick J, Tolaini M, Lahl K, et al. An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat Immunol (2011) 12:1071-7. doi:10.1038/ni.2133
67. Wilhelm C, Turner JE, Van Snick J, Stockinger B. The many lives of IL-9: a question of survival? Nat Immunol (2012) 13:637-41. doi:10.1038/ni.2303
68. Trifari S, Spits H. IL-22-producing CD4+ T cells: middle-men between the immune system and its environment. Eur J Immunol (2010) 40:2369-71. doi:10.1002/eji.201040848
69. Duhen T, Geiger R, Jarrossay D, Lanzavecchia A, Sallusto F. Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat Immunol (2009) 10:857-63. doi:10.1038/ni.1767
70. Kagami S, Rizzo HL, Lee JJ, Koguchi Y, Blauvelt A. Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J Invest Dermatol (2010) 130:1373-83. doi:10.1038/jid.2009.399
71. Liu Y, Yang B, Zhou M, Li L, Zhou H, Zhang J, et al. Memory IL-22-producing CD4+ T cells specific for Candida albicans are present in humans. Eur J Immunol (2009) 39:1472-9. doi:10.1002/eji.200838811
72. De Luca A, Zelante T, D'Angelo C, Zagarella S, Fallarino F, Spreca A, et al. IL-22 defines a novel immune pathway of antifungal resistance. Mucosal Immunol (2010) 3:361-73. doi:10.1038/mi.2010.22
73. Zelante T, Iannitti R, De Luca A, Romani L. IL-22 in antifungal immunity. Eur J Immunol (2011) 41:270-5. doi:10.1002/eji.201041246
74. De Luca A, Carvalho A, Cunha C, Iannitti RG, Pitzurra L, Giovannini G, et al. IL-22 and IDO1 affect immunity and tolerance to murine and human vaginal candidiasis. PLoS Pathog (2013) 9:e1003486. doi:10.1371/journal.ppat.1003486
75. Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity (2013) 39:372-85. doi:10.1016/j.immuni.2013.08.003
76. Romani L, Puccetti P. Protective tolerance to fungi: the role of IL-10 and tryptophan catabolism. Trends Microbiol (2006) 14:183-9. doi:10.1016/j.tim.2006.02.003
77. Roncarolo MG, Gregori S, Bacchetta R, Battaglia M. Tr1 cells and the counter-regulation of immunity: natural mechanisms and therapeutic applications. Curr Top Microbiol Immunol (2014) 380:39-68. doi:10.1007/978-3-662-43492-5_3
78. Bedke T, Iannitti RG, De Luca A, Giovannini G, Fallarino F, Berges C, et al. Distinct and complementary roles for Aspergillus fumigatus-specific Tr1 and Foxp3 regulatory T cells in humans and mice. Immunol Cell Biol (2014) 92:659-70. doi:10.1038/icb.2014.34
79. Zelante T, Fallarino F, Bistoni F, Puccetti P, Romani L. Indoleamine 2,3-dioxygenase in infection: the paradox of an evasive strategy that benefits the host. Microbes Infect (2009) 11:133-41. doi:10.1016/j.micinf.2008.10.007
80. Grohmann U, Volpi C, Fallarino F, Bozza S, Bianchi R, Vacca C, et al. Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat Med (2007) 13:579-86. doi:10.1038/nm1563
81. Harrington L, Srikanth CV, Antony R, Rhee SJ, Mellor AL, Shi HN, et al. Deficiency of indoleamine 2,3-dioxygenase enhances commensal-induced antibody responses and protects against Citrobacter rodentium-induced colitis. Infect Immun (2008) 76:3045-53. doi:10.1128/IAI.00193-08
82. Trifari S, Kaplan CD, Tran EH, Crellin NK, Spits H. Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from T(H)-17, T(H)1 and T(H)2 cells. Nat Immunol (2009) 10:864-71. doi:10.1038/ni.1770
83. Heath-Pagliuso S, Rogers WJ, Tullis K, Seidel SD, Cenijn PH, Brouwer A, et al. Activation of the Ah receptor by tryptophan and tryptophan metabolites. Biochemistry (1998) 37:11508-15. doi:10.1021/bi980087p
84. Bjeldanes LF, Kim JY, Grose KR, Bartholomew JC, Bradfield CA. Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc Natl Acad Sci U S A (1991) 88:9543-7. doi:10.1073/pnas.88.21.9543
85. Esser C, Bargen I, Weighardt H, Haarmann-Stemmann T, Krutmann J. Functions of the aryl hydrocarbon receptor in the skin. Semin Immunopathol (2013) 35:677-91. doi:10.1007/s00281-013-0394-4
86. Di Meglio P, Duarte JH, Ahlfors H, Owens ND, Li Y, Villanova F, et al. Activation of the aryl hydrocarbon receptor dampens the severity of inflammatory skin conditions. Immunity (2014) 40:989-1001. doi:10.1016/j.immuni.2014.04.019
87. Vlachos C, Schulte BM, Magiatis P, Adema GJ, Gaitanis G. Malassezia-derived indoles activate the aryl hydrocarbon receptor and inhibit toll-like receptor-induced maturation in monocyte-derived dendritic cells. Br J Dermatol (2012) 167:496-505. doi:10.1111/j.1365-2133.2012.11014.x
88. Gaitanis G, Magiatis P, Stathopoulou K, Bassukas ID, Alexopoulos EC, Velegraki A, et al. AhR ligands, malassezin, and indolo[3,2-b]carbazole are selectively produced by Malassezia furfur strains isolated from seborrheic dermatitis. J Invest Dermatol (2008) 128:1620-5. doi:10.1038/sj.jid.5701252
89. Faber F, Baumler AJ. The impact of intestinal inflammation on the nutritional environment of the gut microbiota. Immunol Lett (2014) S0165-2478(14):83-82. doi:10.1016/j.imlet.2014.04.014
90. Kalo-Klein A, Witkin SS. Prostaglandin E2 enhances and gamma interferon inhibits germ tube formation in Candida albicans. Infect Immun (1990) 58:260-2.
91. Bonifazi P, Zelante T, D'Angelo C, De Luca A, Moretti S, Bozza S, et al. Balancing inflammation and tolerance in vivo through dendritic cells by the commensal Candida albicans. Mucosal Immunol (2009) 2:362-74. doi:10.1038/mi.2009.17
92. Bonifazi P, D'Angelo C, Zagarella S, Zelante T, Bozza S, De Luca A, et al. Intranasally delivered siRNA targeting PI3K/Akt/mTOR inflammatory pathways protects from aspergillosis. Mucosal Immunol (2010) 3:193-205. doi:10.1038/mi.2009.130