The evolving view of IL-17-mediated immunity in defense against mucocutaneous candidiasis in humans

International Reviews of Immunology

Volumn 34, Issue 4, 2015, Pages 348-363

  Soltész, Beáta ^a   Tóth, Beáta ^a   Sarkadi, Adrien Katalin ^a   Erdos, Melinda ^a   Maródi, Lászlo ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Candida; Interleukin 17; Interleukin 17 receptor mediated signaling; Mucocutaneous candidiasis disease; Pattern recognition receptors; Signal transducer and activator of transcription

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 9; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; CD4 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12 RECEPTOR BETA1; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; NUCLEAR FACTOR KAPPA B ACTIVATOR 1; PATTERN RECOGNITION RECEPTOR; STAT1 PROTEIN; STAT3 PROTEIN; UNCLASSIFIED DRUG;

AUTOIMMUNE POLYENDOCRINOPATHY CANDIDIASIS ECTODERMAL DYSTROPHY; CANDIDA; GERMLINE MUTATION; HOST RESISTANCE; HUMAN; IMMUNITY; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INNATE IMMUNITY; LYMPHOCYTE DIFFERENTIATION; MUCOCUTANEOUS CANDIDIASIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TH17 CELL; ANIMAL; GENETICS; IMMUNOLOGY; METABOLISM;

ANIMALS; CANDIDIASIS, CHRONIC MUCOCUTANEOUS; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-17; TH17 CELLS;

EID: 84953887296     PISSN: 08830185     EISSN: 15635244     Source Type: Journal    
DOI: 10.3109/08830185.2015.1049345     Document Type: Review

References (106)

1. Maródi L. Local and systemic host defense mechanisms against Candida: Immunopathology of candidal infections. Pediatr Infect Dis J 1997; 16: 795-801.
2. Pfaller MA, Diekema DJ. Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 2010; 36: 1-53.
3. Maródi L, Johnston RB Jr. Invasive Candida species disease in infants and children: Occurrence, risk factors, management, and innate host defense mechanisms. Curr Opin Pediatr 2007; 19: 693-697.
4. Fleischmann J,Church JA, LehrerRI. PrimaryCandida meningitis and chronic granulomatous disease. Am JMed Sci 1986; 291: 334-341.
5. DoniniM, Fontana S, Savoldi G, et al. G-CSF treatment of severe congenital neutropenia reverses neutropenia but does not correct the underlying functional deficiency of the neutrophil in defending against microorganisms. Blood 2007; 109: 4716-4723.
6. Cassone A. Vulvovaginal Candida albicans infections: Pathogenesis, immunity and vaccine prospects. BJOG-Int J Obstet GY 2014. doi: 10.1111/1471-0528.12994.
7. Conti HR, Peterson AC, Brane L, et al. Oral-resident natural Th17 cells and ? d T cells control opportunistic Candida albicans infections. J ExpMed 2014; 211: 2075-2084.
8. de Repentigny L, Lewandowski D, Jolicoeur P.Immunopathogenesis of oropharyngeal candidiasis in human immunodeficiency virus infection. ClinMicrobiol Rev 2004; 17: 729-759.
9. Maródi L. Mucocutaneous Candidiasis. In: Sullivan KE, Stiehm RE, editors. Stiehm's immunodeficiencies. Amsterdam: Elsevier Inc; 2014. pp. 775-802.
10. Mogensen TH. STAT3 and the Hyper-IgE syndrome: Clinical presentation, genetic origin, pathogenesis, novel findings and remaining uncertainties. JAK-STAT 2013; 2: E23435.
11. Ouederni M, Sanal O, Ikinciogullari A, et al. Clinical features of Candidiasis in patients with inherited interleukin 12 receptor β1 deficiency. Clin Infect Dis 2014; 58: 204-213.
12. Prando C, Samarina A, Bustamante J, et al. Inherited IL-12p40 deficiency: Genetic, immunologic, and clinical features of 49 patients from30 kindreds.Med (Baltimore) 2013; 92: 109-122.
13. Meloni A, Willcox N, Meager A, et al. Autoimmune polyendocrine syndrome type 1: An extensive longitudinal study in Sardinian patients. J Clin EndocrinolMetab 2012; 97: 1114-1124.
14. Liu L, Okada S, Kong XF, et al. Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronicmucocutaneous candidiasis. J ExpMed 2011; 208: 1635-1648.
15. van de Veerdonk FL, Plantinga TS, Hoischen A, et al. STAT1 mutations in autosomal dominant chronicmucocutaneous candidiasis. N Engl JMed 2011; 365: 54-61.
16. Smeekens SP, Plantinga TS, van de Veerdonk FL, et al. STAT1 hyperphosphorylation and defective IL12R/IL23R signaling underlie defective immunity in autosomal dominant chronic mucocutaneous candidiasis. PLoS One 2011; 6: E29248.
17. Tóth B,Méhes L, Taskó S, et al. Herpes in STAT1mutation. The Lancet 2012; 379: 2500.
18. Hori T, Ohnishi H, Teramoto T, et al. Autosomal-dominant chronic mucocutaneous candidiasis with STAT1-mutation can be complicatedwith chronic active hepatitis and hypothyroidism. J Clin Immunol 2012; 32: 1213-1220.
19. Takezaki S, Yamada M, Kato M, et al. Chronic mucocutaneous candidiasis caused by a gain-offunctionmutation in the STAT1 DNA-binding domain. J Immunol 2012; 189: 1521-1526.
20. TsumuraM,Okada S, SakaiH, et al.Dominant-negative STAT1 SH2domainmutations in unrelated patients withMendelian susceptibility tomycobacterial disease. HumMutat 2012; 33: 1377-1387.
21. Soltész B, Tóth B, Shabashova N, et al. New and recurrent gain-of-function STAT1 mutations in patients with chronicmucocutaneous candidiasis from Eastern and Central Europe. JMed Genet 2013; 50: 567-578.
22. Puel A,Cypowyj S,Bustamante J, et al. Chronicmucocutaneous candidiasis inhumanswith inborn errors of interleukin-17 immunity. Science 2011; 332: 65-68.
23. Boisson B, Wang C, Pedergnana V, et al. An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronicmucocutaneous candidiasis. Immunity 2013; 39: 676-686.
24. Naglik JR,Moyes DL, Wächtler B, Hube B. Candida albicans interactions with epithelial cells and mucosal immunity.Microbes Infect 2011; 13: 963-976.
25. Kumamoto CA. Inflammation and gastrointestinal Candida colonization. Curr Opin Microbiol 2011; 14: 386-391.
26. Gow NA, Hube B. Importance of the Candida albicans cell wall during commensalism and infection. Curr OpinMicrobiol 2012; 15: 406-412.
27. Vazquez JA, Sobel JD.Mucosal candidiasis. Infect Dis Clin North Am2002; 16: 793-820.
28. Hebecker B,Naglik JR,Hube B, Jacobsen ID. Pathogenicity mechanisms and host response during oral Candida albicans infections. Expert Rev Anti InfectTher 2014; 12: 867-879.
29. Zhu W, Filler SG. Interactions of Candida albicans with epithelial cells. Cell Microbiol 2010; 12: 273-282.
30. Staab JF, Bradway SD, Fidel PL, Sundstrom P. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 1999; 283: 1535-1538.
31. Phan QT, Myers CL, Fu Y, et al. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 2007; 5: E64.
32. Gale CA, Bendel CM,McClellanM, et al. Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1. Science 1998; 279: 1355-1358.
33. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27: 485-517.
34. Cypowyj S, Picard C, Maródi L, et al. Immunity to infection in IL-17-deficient mice and humans. Eur J Immunol 2012; 42: 2246-2254.
35. Maródi L, Cypowyj S, Tóth B, et al. Molecular mechanisms of mucocutaneous immunity against Candida and Staphylococcus species. J Allergy Clin Immunol 2012; 130: 1019-1027.
36. Puel A, Cypowyj S,Maródi L, et al. Inborn errors of human IL-17 immunity underlie chronic mucocutaneous candidiasis. Curr Opin Allergy Clin Immunol 2012; 12: 616-622.
37. Maródi L, Cypowyj S, Casanova JL, Puel A. The role of human IL-17 immunity in fungal disease. Curr Fungal Infect Rep 2013. DOI: 10.1007/s12281-013-0131-4.
38. Ness-Schwickerath KJ, Jin C, Morita CT. Cytokine requirements for the differentiation and expansion of IL-17A- And IL-22-producing human Vgamma2Vdelta2 T cells. J Immunol 2010; 184: 7268-7280.
39. Cua DJ, Tato CM. Innate IL-17-producing cells: The sentinels of the immune system. Nat Rev Immunol 2010; 10: 479-489.
40. Aggarwal S, Gurney AL. IL-17: Prototype member of an emerging cytokine family. J Leukoc Biol 2002; 71: 1-8.
41. NeteaMG,Maródi L. Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol 2010; 31: 346-353.
42. Maródi L, Korchak HM, Johnston RB Jr. Mechanisms of host defense against Candida species. I. Phagocytosis by monocytes and monocyte-derivedmacrophages. JImmunol 1991; 146: 2783-2789.
43. Maródi L, Schreiber S, Anderson DC, et al. Enhancement of macrophage candidacidal activity by interferon-gamma. Increased phagocytosis, killing, and calcium signal mediated by a decreased number ofmannose receptors. J Clin Invest 1993; 91: 2596-2601.
44. Dambuza IM, Brown GD. C-type lectins in immunity: Recent developments. Curr Opin Immunol 2014; 32C: 21-27.
45. Hernández-Santos N, Gaffen SL. Th17 cells in immunity to Candida albicans. Cell Host Microbe 2012; 11: 425-435.
46. van de Veerdonk FL,Marijnissen RJ, Kullberg BJ, et al.Themacrophagemannose receptor induces IL-17 in response to Candida albicans. Cell HostMicrobe 2009; 5: 329-340.
47. BourgeoisC,Majer O, Frohner IE, et al. Fungal attacks onmammalian hosts: Pathogen elimination requires sensing and tasting. Curr OpinMicrobiol 2010; 13: 401-408.
48. Netea MG, Brown GD, Kullberg BJ, Gow NA. An integrated model of the recognition of Candida albicans by the innate immune system. Nat RevMicrobiol 2008; 6: 67-78.
49. NeteaMG, Van Der Graaf CA, Vonk AG, et al. The role of toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J Infect Dis 2002; 185: 1483-1489.
50. NeteaMG, Sutmuller R, Hermann C, et al. Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J Immunol 2004; 172: 3712-3718.
51. Martinez-Pomares L. Themannose receptor. J Leukoc Biol 2012; 92: 1177-1186.
52. Heinsbroek SE, Taylor PR, Martinez FO, et al. Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog 2008; 4: E1000218.
53. Szolnoky G, Bata-Csörgö Z, Kenderessy AS, et al. A mannose-binding receptor is expressed on human keratinocytes and mediates killing of Candida albicans. J Invest Dermatol 2001; 117: 205-213.
54. Bi L,Gojestani S,Wu W, et al.CARD9 mediates dectin-2-induced IkappaBalpha kinase ubiquitination leading to activation of NF-kappaB in response to stimulation by the hyphal formof Candida albicans. J Biol Chem 2010; 285: 25969-25977.
55. Glocker EO, Hennigs A, Nabavi M, et al. A homozygous CARD9mutation in a family with susceptibility to fungal infections. N Engl JMed 2009; 361: 1727-1735.
56. Lanternier F, Pathan S, Vincent QB, et al. Deep dermatophytosis and inherited CARD9 deficiency. N Engl JMed 2013; 369: 1704-1714.
57. Wang X,Wang W, Lin Z, et al. CARD9mutations linked to subcutaneous phaeohyphomycosis and TH17 cell deficiencies. J Allergy Clin Immunol 2014; 133: 905-908.e3.
58. Lanternier F, Barbati E,Meinzer U, et al. Inherited CARD9 deficiency in 2 unrelated patients with invasive exophiala infection. J Infect Dis 2014 DOI: 10.1093/infdis/jiu412.
59. Davis SD, Schaller J, Wedgwood RJ. Job's syndrome. Recurrent, "cold", staphylococcal abscesses. Lancet 1966; 1: 1013-1015.
60. Grimbacher B, Holland SM, Puck JM. Hyper-IgE syndromes. Immunol Rev 2005; 203: 244-250.
61. Buckley RH. The hyper-IgE syndrome. Clin Rev Allergy Immunol 2001; 20: 139-154.
62. Minengishi Y, Saito M, Tsuchiya A, et al. Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 2007; 448: 1058-1062.
63. Holland SM, DeLeo FR, Elloumi HZ, et al. STAT3 mutations in the hyper-IgE syndrome. N Engl J Med 2007; 357: 1608-1619.
64. Jiao H,TóthB,ErdosM,et al.Novel and recurrent STAT3mutations inhyper-IgEsyndromepatients from different ethnic groups.Mol Immunol 2008; 46: 202-206.
65. Chandesris MO,Melki I, Natividad A, et al. Autosomal dominant STAT3 deficiency and hyper-IgE syndrome: Molecular, cellular, and clinical features froma French national survey.Medicine (Baltimore) 2012; 91: E1-e19.
66. MaCS,ChewGY, SimpsonN, et al.Deficiency ofTh17 cells inhyper IgE syndromedue tomutations in STAT3. J ExpMed 2008; 205: 1551-1557.
67. Milner JD, Brenchley JM, Laurence A, et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 2008; 452: 773-776.
68. Minegishi Y, Saito M, Nagasawa M, et al. Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J Exp Med 2009; 206: 1291-1301.
69. O'Shea JJ, Lahesmaa R, Vahedi G, et al. Genomic views of STAT function in CD4+ T helper cell differentiation. Nat Rev Immunol 2011; 11: 239-250.
70. O'Shea JJ, Holland SM, Staudt LM. JAKs and STATs in immunity, immunodeficiency, and cancer. N Engl JMed 2013; 368: 161-170.
71. Casanova JL, Holland SM, Notarangelo LD. Inborn errors of human JAKs and STATs. Immunity 2012; 36: 515-528.
72. Kane A, Deenick EK, Ma CS, et al. STAT3 is a central regulator of lymphocyte differentiation and function. Curr Opin Immunol 2014; 28: 49-57.
73. Ma CS, Avery DT, Chan A, et al. Functional STAT3 deficiency compromises the generation of human T follicular helper cells. Blood 2012; 119: 3997-4008.
74. Siegel AM, Heimall J, Freeman AF, et al. A critical role for STAT3 transcription factor signaling in the development andmaintenance of human T cellmemory. Immunity 2011; 35: 806-818.
75. Conti HR, Baker O, Freeman AF, et al. New mechanism of oral immunity to mucosal candidiasis in hyper-IgE syndrome.Mucosal Immunol 2011; 4: 448-455.
76. Tomalka J, Azodi E, Narra HP, et al. β-Defensin 1 Plays a Role in Acute Mucosal Defense against Candida albicans. J Immunol 2015 pii: 1203239 [Epub ahead of print]
77. Boisson-Dupuis S, Kong XF, Okada S, et al. Inborn errors of human STAT1: Allelic heterogeneity governs the diversity of immunological and infectious phenotypes. Curr Opin Immunol 2012; 24: 364-378.
78. Sampaio EP, Hsu AP, Pechacek J, et al. Signal transducer and activator of transcription 1 (STAT1) gain-of-function mutations and disseminated coccidioidomycosis and histoplasmosis. J Allergy Clin Immunol 2013; 131: 1624-1634.
79. KumarN,HanksME, Chandrasekaran P, et al. Gain-of-function signal transducer and activator of transcription 1 (STAT1) mutation-related primary immunodeficiency is associated with disseminatedmucormycosis. J Allergy Clin Immunol 2014; 134: 236-239.
80. Kilic SS,Puel A,Casanova JL.Orf Infection in aPatientwith Stat1Gain-of-Function. J ClinImmunol 2014 Nov 4. [Epub ahead of print]
81. Lee PP, Mao H, Yang W, et al. Penicillium marneffei infection and impaired IFN-? immunity in humans with autosomal-dominant gain-of-phosphorylation STAT1 mutations. J Allergy Clin Immunol 2014; 133: 894-896.
82. Wang X, Lin Z, Gao L, et al. Exome sequencing reveals a signal transducer and activator of transcription 1 (STAT1) mutation in a child with recalcitrant cutaneous fusariosis. J Allergy Clin Immunol 2013; 131: 1242-1243.
83. Ives ML,MaCS, PalendiraU, et al. Signal transducer and activator of transcription 3 (STAT3)mutations underlying autosomal dominant hyper-IgE syndrome impair human CD8(+) T-cellmemory formation and function. J Allergy Clin Immunol 2013; 132: 400-411.
84. Zerbe CS, Holland SM. Disseminated histoplasmosis in persons with interferon-gamma receptor 1 deficiency. Clin Infect Dis 2005; 41: E38-e41.
85. Vinh DC, Masannat F, Dzioba RB, et al. Refractory disseminated coccidioidomycosis and mycobacteriosis in interferon-gamma receptor 1 deficiency. Clin Infect Dis 2009; 49: E62-65.
86. Kobayashi M, Fitz L, Ryan M, et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 1989; 170: 827-845.
87. Stern AS, Podlaski FJ,Hulmes JD, et al. Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells. Proc Natl Acad Sci USA 1990; 87: 6808-6812.
88. Trinchieri G. Interleukin-12: A cytokine at the interface of inflammation and immunity. Adv Immunol 1998; 70: 83-243.
89. Airoldi I, Guglielmino R, Carra G, et al. The interleukin-12 and interleukin-12 receptor system in normal and transformed human B lymphocytes. Haematologica 2002; 87: 434-442.
90. Oppmann B, Lesley R, Blom B, et al.Novel p19 protein engages IL-12p40 to forma cytokine, IL-23, with biological activities similar as well as distinct fromIL-12. Immunity 2000; 13: 715-725.
91. WatfordWT,Hissong BD, Bream JH, et al. Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4. Immunol Rev 2004; 202: 139-156.
92. McGeachy MJ, Cua DJ. Th17 cell differentiation: The long and winding road. Immunity 2008; 28: 445-453.
93. Filipe-Santos O, Bustamante J, Chapgier A, et al. Inborn errors of IL-12/23- And IFN-gammamediated immunity: Molecular, cellular, and clinical features. Semin Immunol 2006; 18: 347-361. Erratum in: Semin Immunol 2007; 19: 136-137.
94. Picard C, Fieschi C, Altare F, et al. Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients fromsix kindreds. AmJ HumGenet 2002; 70: 336-348.
95. Altare F, Lammas D, Revy P, et al. Inherited interleukin 12 deficiency in a child with bacille Calmette-Guérin and Salmonella enteritidis disseminated infection. J Clin Invest 1998; 102: 2035-2040.
96. de Jong R, Altare F, Haagen IA, et al. Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 1998; 280: 1435-1438.
97. Altare F, Durandy A, Lammas D, et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 1998; 280: 1432-1435.
98. Pedraza S, Lezana JL,Samarina A, et al.Clinical disease caused byKlebsiella in 2 unrelated patients with interleukin 12 receptor beta1 deficiency. Pediatrics 2010; 126: E971-e976.
99. Toy D, Kugler D, Wolfson M, et al. Cutting edge: Interleukin 17 signals through a heteromeric receptor complex. J Immunol 2006; 177: 36-39.
100. Bulek K, Liu C, Swaidani S, et al.The inducible kinase IKKi is required for IL-17-dependent signaling associated with neutrophilia and pulmonary inflammation. Nat Immunol 2011; 12: 844-852.
101. Chang SH, Dong C. Signaling of interleukin-17 family cytokines in immunity and inflammation. Cell Signal 2011; 23: 1069-1075.
102. MayMJ. IL-17R signaling: New players get in on the Act1. Nat Immunol 2011; 12: 813-815.
103. Shen F, Gaffen SL. Structure-function relationships in the IL-17 receptor: Implications for signal transduction and therapy. Cytokine 2008; 41: 92-104.
104. Qian Y, Liu C, Hartupee J, Altuntas CZ, et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 2007; 8: 247-256.
105. NovatchkovaM, Leibbrandt A,Werzowa J, et al.TheSTIR-domain superfamily in signal transduction, development and immunity. Trends Biochem Sci 2003; 28: 226-229.
106. Boisson B, Wang C, Pedergnana V, et al. An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronicmucocutaneous candidiasis. Immunity 2013; 39: 676-686.