IL-22 and IDO1 Affect Immunity and Tolerance to Murine and Human Vaginal Candidiasis

PLoS Pathogens

Volumn 9, Issue 7, 2013, Pages

  De Luca, Antonella ^a,b   Carvalho, Agostinho ^a   Cunha, Cristina ^a   Iannitti, Rossana G ^a   Pitzurra, Lucia ^a,c   Giovannini, Gloria ^a   Mencacci, Antonella ^a,c   Bartolommei, Lorenzo ^a   Moretti, Silvia ^a   Massi Benedetti, Cristina ^a   Fuchs, Dietmar ^d   De Bernardis, Flavia ^b   Puccetti, Paolo ^a   Romani, Luigina ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c Ospedale S Maria della Misericordia   (Italy)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CALGRANULIN A; CALGRANULIN B; GAMMA INTERFERON; INDOLEAMINE 2, 3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 22; KYNURENINE; MYELOID DIFFERENTIATION FACTOR 88; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRYPTOPHAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANDIDA ALBICANS; CD4+ T LYMPHOCYTE; CELL ISOLATION; CONTROLLED STUDY; DNA ISOLATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FUNGUS GROWTH; GENE EXPRESSION; GENETIC VARIABILITY; GENOTYPE; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; MAJOR CLINICAL STUDY; MOUSE; NEUTROPHIL; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECURRENT INFECTION; SINGLE NUCLEOTIDE POLYMORPHISM; TH1 CELL; TH17 CELL; VAGINA CANDIDIASIS; WESTERN BLOTTING;

EID: 84884768609     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003486     Document Type: Article

References (69)

1. Fidel PL Jr, (2005) Immunity in vaginal candidiasis. Curr Opin Infect Dis 18: 107-111.
2. Sobel JD, (1988) Pathogenesis and epidemiology of vulvovaginal candidiasis. Ann N Y Acad Sci 544: 547-557.
3. Fidel PL Jr, Cutler JE, (2011) Prospects for development of a vaccine to prevent and control vaginal candidiasis. Curr Infect Dis Rep 13: 102-107.
4. De Bernardis F, Amacker M, Arancia S, Sandini S, Gremion C, et al. (2012) A virosomal vaccine against candidal vaginitis: immunogenicity, efficacy and safety profile in animal models. Vaccine 30: 4490-4498.
5. Fidel PL Jr, Barousse M, Lounev V, Espinosa T, Chesson RR, et al. (2003) Local immune responsiveness following intravaginal challenge with Candida antigen in adult women at different stages of the menstrual cycle. Med Mycol 41: 97-109.
6. LeBlanc DM, Barousse MM, Fidel PL Jr, (2006) Role for dendritic cells in immunoregulation during experimental vaginal candidiasis. Infect Immun 74: 3213-3221.
7. Cassone A, De Bernardis F, Santoni G, (2007) Anticandidal immunity and vaginitis: novel opportunities for immune intervention. Infect Immun 75: 4675-4686.
8. Yano J, Lilly E, Barousse M, Fidel PL Jr, (2010) Epithelial cell-derived S100 calcium-binding proteins as key mediators in the hallmark acute neutrophil response during Candida vaginitis. Infect Immun 78: 5126-5137.
9. Carvalho LP, Bacellar O, Neves N, de Jesus AR, Carvalho EM, (2002) Downregulation of IFN-gamma production in patients with recurrent vaginal candidiasis. J Allergy Clin Immunol 109: 102-105.
10. Fidel PL Jr, Lynch ME, Sobel JD, (1993) Candida-specific Th1-type responsiveness in mice with experimental vaginal candidiasis. Infect Immun 61: 4202-4207.
11. Fidel PL Jr, Ginsburg KA, Cutright JL, Wolf NA, Leaman D, et al. (1997) Vaginal-associated immunity in women with recurrent vulvovaginal candidiasis: evidence for vaginal Th1-type responses following intravaginal challenge with Candida antigen. J Infect Dis 176: 728-739.
12. Pietrella D, Rachini A, Pines M, Pandey N, Mosci P, et al. (2011) Th17 cells and IL-17 in protective immunity to vaginal candidiasis. PLoS One 6: e22770.
13. De Luca A, Zelante T, D'Angelo C, Zagarella S, Fallarino F, et al. (2010) IL-22 defines a novel immune pathway of antifungal resistance. Mucosal Immunol 3: 361-373.
14. Gessner MA, Werner JL, Lilly LM, Nelson MP, Metz AE, et al. (2012) Dectin-1-dependent interleukin-22 contributes to early innate lung defense against Aspergillus fumigatus. Infect Immun 80: 410-417.
15. Eyerich S, Wagener J, Wenzel V, Scarponi C, Pennino D, et al. (2011) IL-22 and TNF-alpha represent a key cytokine combination for epidermal integrity during infection with Candida albicans. Eur J Immunol 41: 1894-1901.
16. Eyerich K, Foerster S, Rombold S, Seidl HP, Behrendt H, et al. (2008) Patients with chronic mucocutaneous candidiasis exhibit reduced production of Th17-associated cytokines IL-17 and IL-22. J Invest Dermatol 128: 2640-2645.
17. Browne SK, Holland SM, (2010) Anti-cytokine autoantibodies explain some chronic mucocutaneous candidiasis. Immunol Cell Biol 88: 614-615.
18. Kisand K, Boe Wolff AS, Podkrajsek KT, Tserel L, Link M, et al. (2010) Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J Exp Med 207: 299-308.
19. Puel A, Doffinger R, Natividad A, Chrabieh M, Barcenas-Morales G, et al. (2010) Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J Exp Med 207: 291-297.
20. Yano J, Kolls JK, Happel KI, Wormley F, Wozniak KL, et al. (2012) The acute neutrophil response mediated by S100 alarmins during vaginal Candida infections is independent of the Th17-pathway. PLoS One 7: e46311.
21. Read AF, Graham AL, Raberg L, (2008) Animal defenses against infectious agents: is damage control more important than pathogen control. PLoS Biol 6: e4.
22. Schneider DS, Ayres JS, (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 8: 889-895.
23. Restif O, Koella JC, (2004) Concurrent evolution of resistance and tolerance to pathogens. Am Nat 164: E90-102.
24. Romani L, (2011) Immunity to fungal infections. Nat Rev Immunol 11: 275-288.
25. Piccinni MP, Vultaggio A, Scaletti C, Livi C, Gomez MJ, et al. (2002) Type 1 T helper cells specific for Candida albicans antigens in peripheral blood and vaginal mucosa of women with recurrent vaginal candidiasis. J Infect Dis 186: 87-93.
26. Fidel PL Jr, (2007) History and update on host defense against vaginal candidiasis. Am J Reprod Immunol 57: 2-12.
27. Yano J, Noverr MC, Fidel PL Jr, (2012) Cytokines in the host response to Candida vaginitis: Identifying a role for non-classical immune mediators, S100 alarmins. Cytokine 58: 118-128.
28. Fidel PL Jr, Barousse M, Espinosa T, Ficarra M, Sturtevant J, et al. (2004) An intravaginal live Candida challenge in humans leads to new hypotheses for the immunopathogenesis of vulvovaginal candidiasis. Infect Immun 72: 2939-2946.
29. Cobbold SP, Adams E, Nolan KF, Regateiro FS, Waldmann H, (2010) Connecting the mechanisms of T-cell regulation: dendritic cells as the missing link. Immunol Rev 236: 203-218.
30. Saraiva M, O'Garra A, (2010) The regulation of IL-10 production by immune cells. Nat Rev Immunol 10: 170-181.
31. Wormley FL Jr, Chaiban J, Fidel PL Jr, (2001) Cell adhesion molecule and lymphocyte activation marker expression during experimental vaginal candidiasis. Infect Immun 69: 5072-5079.
32. Wormley FL Jr, Steele C, Wozniak K, Fujihashi K, McGhee JR, et al. (2001) Resistance of T-cell receptor delta-chain-deficient mice to experimental Candida albicans vaginitis. Infect Immun 69: 7162-7164.
33. Mellor AL, Munn DH, (2004) IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 4: 762-774.
34. Zelante T, Fallarino F, Bistoni F, Puccetti P, Romani L, (2009) Indoleamine 2,3-dioxygenase in infection: the paradox of an evasive strategy that benefits the host. Microbes Infect 11: 133-141.
35. Romani L, Fallarino F, De Luca A, Montagnoli C, D'Angelo C, et al. (2008) Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451: 211-215.
36. De Luca A, Montagnoli C, Zelante T, Bonifazi P, Bozza S, et al. (2007) Functional yet balanced reactivity to Candida albicans requires TRIF, MyD88, and IDO-dependent inhibition of Rorc. J Immunol 179: 5999-6008.
37. Zelante T, Iannitti RG, De Luca A, Arroyo J, Blanco N, et al. (2012) Sensing of mammalian IL-17A regulates fungal adaptation and virulence. Nat Commun 3: 683.
38. Dai X, Zhu BT, (2010) Indoleamine 2,3-dioxygenase tissue distribution and cellular localization in mice: implications for its biological functions. J Histochem Cytochem 58: 17-28.
39. Roth A, Konig P, van Zandbergen G, Klinger M, Hellwig-Burgel T, et al. (2010) Hypoxia abrogates antichlamydial properties of IFN-gamma in human fallopian tube cells in vitro and ex vivo. Proc Natl Acad Sci U S A 107: 19502-19507.
40. Simonian PL, Wehrmann F, Roark CL, Born WK, O'Brien RL, et al. (2010) gammadelta T cells protect against lung fibrosis via IL-22. J Exp Med 207: 2239-2253.
41. Sonnenberg GF, Fouser LA, Artis D, (2011) Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 12: 383-390.
42. Montagnoli C, Fallarino F, Gaziano R, Bozza S, Bellocchio S, et al. (2006) Immunity and tolerance to Aspergillus involve functionally distinct regulatory T cells and tryptophan catabolism. J Immunol 176: 1712-1723.
43. Widner B, Werner ER, Schennach H, Wachter H, Fuchs D, (1997) Simultaneous measurement of serum tryptophan and kynurenine by HPLC. Clin Chem 43: 2424-2426.
44. Fallarino F, Grohmann U, You S, McGrath BC, Cavener DR, et al. (2006) The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J Immunol 176: 6752-6761.
45. Belladonna ML, Puccetti P, Orabona C, Fallarino F, Vacca C, et al. (2007) Immunosuppression via tryptophan catabolism: the role of kynurenine pathway enzymes. Transplantation 84: S17-20.
46. Carvalho A, Giovannini G, De Luca A, D'Angelo C, Casagrande A, et al. (2012) Dectin-1 isoforms contribute to distinct Th1/Th17 cell activation in mucosal candidiasis. Cell Mol Immunol 9: 276-286.
47. Ferwerda B, Ferwerda G, Plantinga TS, Willment JA, van Spriel AB, et al. (2009) Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 361: 1760-1767.
48. Bonifazi P, Zelante T, D'Angelo C, De Luca A, Moretti S, et al. (2009) Balancing inflammation and tolerance in vivo through dendritic cells by the commensal Candida albicans. Mucosal Immunol 2: 362-374.
49. Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, et al. (2013) Innate lymphoid cells-a proposal for uniform nomenclature. Nat Rev Immunol 13: 145-149.
50. Cherrier M, Ohnmacht C, Cording S, Eberl G, (2012) Development and function of intestinal innate lymphoid cells. Curr Opin Immunol 24: 277-283.
51. Qiu J, Heller JJ, Guo X, Chen ZM, Fish K, et al. (2012) The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36: 92-104.
52. Glocker EO, Hennigs A, Nabavi M, Schaffer AA, Woellner C, et al. (2009) A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med 361: 1727-1735.
53. Liu L, Okada S, Kong XF, Kreins AY, Cypowyj S, et al. (2011) Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J Exp Med 208: 1635-1648.
54. Puel A, Cypowyj S, Bustamante J, Wright JF, Liu L, et al. (2011) Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332: 65-68.
55. Giraldo PC, Babula O, Goncalves AK, Linhares IM, Amaral RL, et al. (2007) Mannose-binding lectin gene polymorphism, vulvovaginal candidiasis, and bacterial vaginosis. Obstet Gynecol 109: 1123-1128.
56. Milanese M, Segat L, De Seta F, Pirulli D, Fabris A, et al. (2008) MBL2 genetic screening in patients with recurrent vaginal infections. Am J Reprod Immunol 59: 146-151.
57. Wojitani MD, de Aguiar LM, Baracat EC, Linhares IM, (2012) Association between mannose-binding lectin and interleukin-1 receptor antagonist gene polymorphisms and recurrent vulvovaginal candidiasis. Arch Gynecol Obstet 285: 149-153.
58. Babula O, Lazdane G, Kroica J, Linhares IM, Ledger WJ, et al. (2005) Frequency of interleukin-4 (IL-4)-589 gene polymorphism and vaginal concentrations of IL-4, nitric oxide, and mannose-binding lectin in women with recurrent vulvovaginal candidiasis. Clin Infect Dis 40: 1258-1262.
59. Lev-Sagie A, Prus D, Linhares IM, Lavy Y, Ledger WJ, et al. (2009) Polymorphism in a gene coding for the inflammasome component NALP3 and recurrent vulvovaginal candidiasis in women with vulvar vestibulitis syndrome. Am J Obstet Gynecol 200: e301-306, 303, e301-306.
60. Logters TT, Laryea MD, Altrichter J, Sokolowski J, Cinatl J, et al. (2009) Increased plasma kynurenine values and kynurenine-tryptophan ratios after major trauma are early indicators for the development of sepsis. Shock 32: 29-34.
61. Suzuki Y, Suda T, Furuhashi K, Suzuki M, Fujie M, et al. (2010) Increased serum kynurenine/tryptophan ratio correlates with disease progression in lung cancer. Lung Cancer 67: 361-365.
62. Arefayene M, Philips S, Cao D, Mamidipalli S, Desta Z, et al. (2009) Identification of genetic variants in the human indoleamine 2,3-dioxygenase (IDO1) gene, which have altered enzyme activity. Pharmacogenet Genomics 19: 464-476.
63. Soichot M, Hennart B, Al Saabi A, Leloire A, Froguel P, et al. (2011) Identification of a variable number of tandem repeats polymorphism and characterization of LEF-1 response elements in the promoter of the IDO1 gene. PLoS One 6: e25470.
64. Foxman B, Barlow R, D'Arcy H, Gillespie B, Sobel JD, (2000) Candida vaginitis: self-reported incidence and associated costs. Sex Transm Dis 27: 230-235.
65. Romani L, Mocci S, Bietta C, Lanfaloni L, Puccetti P, et al. (1991) Th1 and Th2 cytokine secretion patterns in murine candidiasis: association of Th1 responses with acquired resistance. Infect Immun 59: 4647-4654.
66. Iijima N, Mattei LM, Iwasaki A, (2011) Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc Natl Acad Sci U S A 108: 284-289.
67. Moretti S, Bozza S, D'Angelo C, Casagrande A, Della Fazia MA, et al. (2012) Role of innate immune receptors in paradoxical caspofungin activity in vivo in preclinical aspergillosis. Antimicrob Agents Chemother 56: 4268-4276.
68. Carvalho A, Marques A, Maciel P, Rodrigues F, (2007) Study of disease-relevant polymorphisms in the TLR4 and TLR9 genes: a novel method applied to the analysis of the Portuguese population. Mol Cell Probes 21: 316-320.
69. Cunha C, Di Ianni M, Bozza S, Giovannini G, Zagarella S, et al. (2010) Dectin-1 Y238X polymorphism associates with susceptibility to invasive aspergillosis in hematopoietic transplantation through impairment of both recipient- and donor-dependent mechanisms of antifungal immunity. Blood 116: 5394-5402.