450
Views
11
CrossRef citations to date
0
Altmetric
REVIEW

The Evolving View of IL-17-Mediated Immunity in Defense Against Mucocutaneous Candidiasis in Humans

, , , &
Pages 348-363 | Received 02 Feb 2015, Accepted 03 Apr 2015, Published online: 08 Jul 2015

REFERENCES

  • Maródi L. Local and systemic host defense mechanisms against Candida: immunopathology of candidal infections. Pediatr Infect Dis J 1997;16:795–801.
  • Pfaller MA, Diekema DJ. Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 2010;36:1–53.
  • 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.
  • Fleischmann J, Church JA, Lehrer RI. Primary Candida meningitis and chronic granulomatous disease. Am J Med Sci 1986;291:334–341.
  • Donini M, 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.
  • Cassone A. Vulvovaginal Candida albicans infections: pathogenesis, immunity and vaccine prospects. BJOG-Int J Obstet GY 2014. doi:10.1111/1471-0528.12994.
  • Conti HR, Peterson AC, Brane L, et al. Oral-resident natural Th17 cells and γδ T cells control opportunistic Candida albicans infections. J Exp Med 2014;211:2075–2084.
  • de Repentigny L, Lewandowski D, Jolicoeur P. Immunopathogenesis of oropharyngeal candidiasis in human immunodeficiency virus infection. Clin Microbiol Rev 2004;17:729–759.
  • Maródi L. Mucocutaneous Candidiasis. In: Sullivan KE, Stiehm RE, editors. Stiehm's immunodeficiencies. Amsterdam: Elsevier Inc; 2014. pp. 775–802.
  • Mogensen TH. STAT3 and the Hyper-IgE syndrome: clinical presentation, genetic origin, pathogenesis, novel findings and remaining uncertainties. JAK-STAT 2013;2:e23435.
  • 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.
  • Prando C, Samarina A, Bustamante J, et al. Inherited IL-12p40 deficiency: genetic, immunologic, and clinical features of 49 patients from 30 kindreds. Med (Baltimore) 2013;92:109–122.
  • Meloni A, Willcox N, Meager A, et al. Autoimmune polyendocrine syndrome type 1: an extensive longitudinal study in Sardinian patients. J Clin Endocrinol Metab 2012;97:1114–1124.
  • Liu L, Okada S, Kong XF, et al. Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J Exp Med 2011;208:1635–1648.
  • van de Veerdonk FL, Plantinga TS, Hoischen A, et al. STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N Engl J Med 2011;365:54–61.
  • 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.
  • Tóth B, Méhes L, Taskó S, et al. Herpes in STAT1 mutation. The Lancet 2012;379:2500.
  • Hori T, Ohnishi H, Teramoto T, et al. Autosomal-dominant chronic mucocutaneous candidiasis with STAT1-mutation can be complicated with chronic active hepatitis and hypothyroidism. J Clin Immunol 2012;32:1213–1220.
  • Takezaki S, Yamada M, Kato M, et al. Chronic mucocutaneous candidiasis caused by a gain-of-function mutation in the STAT1 DNA-binding domain. J Immunol 2012;189:1521–1526.
  • Tsumura M, Okada S, Sakai H, et al. Dominant-negative STAT1 SH2 domain mutations in unrelated patients with Mendelian susceptibility to mycobacterial disease. Hum Mutat 2012;33:1377–1387.
  • Soltész B, Tóth B, Shabashova N, et al. New and recurrent gain-of-function STAT1 mutations in patients with chronic mucocutaneous candidiasis from Eastern and Central Europe. J Med Genet 2013;50:567–578.
  • Puel A, Cypowyj S, Bustamante J, et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011;332:65–68.
  • Boisson B, Wang C, Pedergnana V, et al. An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis. Immunity 2013;39:676–686.
  • Naglik JR, Moyes DL, Wächtler B, Hube B. Candida albicans interactions with epithelial cells and mucosal immunity. Microbes Infect 2011;13:963–976.
  • Kumamoto CA. Inflammation and gastrointestinal Candida colonization. Curr Opin Microbiol 2011;14:386–391.
  • Gow NA, Hube B. Importance of the Candida albicans cell wall during commensalism and infection. Curr Opin Microbiol 2012;15:406–412.
  • Vazquez JA, Sobel JD. Mucosal candidiasis. Infect Dis Clin North Am 2002;16:793–820.
  • Hebecker B, Naglik JR, Hube B, Jacobsen ID. Pathogenicity mechanisms and host response during oral Candida albicans infections. Expert Rev Anti Infect Ther 2014;12:867–879.
  • Zhu W, Filler SG. Interactions of Candida albicans with epithelial cells. Cell Microbiol 2010;12:273–282.
  • Staab JF, Bradway SD, Fidel PL, Sundstrom P. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 1999;283:1535–1538.
  • 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.
  • Gale CA, Bendel CM, McClellan M, et al. Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1. Science 1998;279:1355–1358.
  • Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009;27:485–517.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Cua DJ, Tato CM. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 2010;10:479–489.
  • Aggarwal S, Gurney AL. IL-17: prototype member of an emerging cytokine family. J Leukoc Biol 2002;71:1–8.
  • Netea MG, Maródi L. Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol 2010;31:346–353.
  • Maródi L, Korchak HM, Johnston RB Jr. Mechanisms of host defense against Candida species. I. Phagocytosis by monocytes and monocyte-derived macrophages. J Immunol 1991;146:2783–2789.
  • 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 of mannose receptors. J Clin Invest 1993;91:2596–2601.
  • Dambuza IM, Brown GD. C-type lectins in immunity: recent developments. Curr Opin Immunol 2014;32C:21-27.
  • Hernández-Santos N, Gaffen SL. Th17 cells in immunity to Candida albicans. Cell Host Microbe 2012;11:425–435.
  • van de Veerdonk FL, Marijnissen RJ, Kullberg BJ, et al. The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 2009;5:329–340.
  • Bourgeois C, Majer O, Frohner IE, et al. Fungal attacks on mammalian hosts: pathogen elimination requires sensing and tasting. Curr Opin Microbiol 2010;13:401–408.
  • Netea MG, Brown GD, Kullberg BJ, Gow NA. An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 2008;6:67–78.
  • Netea MG, 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.
  • Netea MG, 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.
  • Martinez-Pomares L. The mannose receptor. J Leukoc Biol 2012;92:1177–1186.
  • Heinsbroek SE, Taylor PR, Martinez FO, et al. Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog 2008;4:e1000218.
  • 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.
  • 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 form of Candida albicans. J Biol Chem 2010;285:25969–25977.
  • Glocker EO, Hennigs A, Nabavi M, et al. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med 2009;361:1727–1735.
  • Lanternier F, Pathan S, Vincent QB, et al. Deep dermatophytosis and inherited CARD9 deficiency. N Engl J Med 2013;369:1704–1714.
  • Wang X, Wang W, Lin Z, et al. CARD9 mutations linked to subcutaneous phaeohyphomycosis and TH17 cell deficiencies. J Allergy Clin Immunol 2014;133:905–908.e3.
  • 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.
  • Davis SD, Schaller J, Wedgwood RJ. Job's syndrome. Recurrent, “cold”, staphylococcal abscesses. Lancet 1966;1:1013–1015.
  • Grimbacher B, Holland SM, Puck JM. Hyper-IgE syndromes. Immunol Rev 2005;203:244–250.
  • Buckley RH. The hyper-IgE syndrome. Clin Rev Allergy Immunol 2001;20:139–154.
  • 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.
  • Holland SM, DeLeo FR, Elloumi HZ, et al. STAT3 mutations in the hyper-IgE syndrome. N Engl J Med 2007;357:1608–1619.
  • Jiao H, Tóth B, Erdos M, et al. Novel and recurrent STAT3 mutations in hyper-IgE syndrome patients from different ethnic groups. Mol Immunol 2008;46:202–206.
  • Chandesris MO, Melki I, Natividad A, et al. Autosomal dominant STAT3 deficiency and hyper-IgE syndrome: molecular, cellular, and clinical features from a French national survey. Medicine (Baltimore) 2012;91:e1–e19.
  • Ma CS, Chew GY, Simpson N, et al. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J Exp Med 2008;205:1551–1557.
  • 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.
  • 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.
  • 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.
  • O'Shea JJ, Holland SM, Staudt LM. JAKs and STATs in immunity, immunodeficiency, and cancer. N Engl J Med 2013;368:161–170.
  • Casanova JL, Holland SM, Notarangelo LD. Inborn errors of human JAKs and STATs. Immunity 2012;36:515–528.
  • 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.
  • 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.
  • Siegel AM, Heimall J, Freeman AF, et al. A critical role for STAT3 transcription factor signaling in the development and maintenance of human T cell memory. Immunity 2011;35:806–818.
  • 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.
  • 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]
  • 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.
  • 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.
  • Kumar N, Hanks ME, Chandrasekaran P, et al. Gain-of-function signal transducer and activator of transcription 1 (STAT1) mutation-related primary immunodeficiency is associated with disseminated mucormycosis. J Allergy Clin Immunol 2014;134:236–239.
  • Kilic SS, Puel A, Casanova JL. Orf Infection in a Patient with Stat1 Gain-of-Function. J Clin Immunol 2014 Nov 4. [Epub ahead of print]
  • Lee PP, Mao H, Yang W, et al. Penicillium marneffei infection and impaired IFN-γ immunity in humans with autosomal-dominant gain-of-phosphorylation STAT1 mutations. J Allergy Clin Immunol 2014;133:894–896.
  • 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.
  • Ives ML, Ma CS, Palendira U, et al. Signal transducer and activator of transcription 3 (STAT3) mutations underlying autosomal dominant hyper-IgE syndrome impair human CD8(+) T-cell memory formation and function. J Allergy Clin Immunol 2013;132:400–411.
  • Zerbe CS, Holland SM. Disseminated histoplasmosis in persons with interferon-gamma receptor 1 deficiency. Clin Infect Dis 2005;41:e38–e41.
  • 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.
  • 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.
  • 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.
  • Trinchieri G. Interleukin-12: a cytokine at the interface of inflammation and immunity. Adv Immunol 1998;70:83-243.
  • 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.
  • Oppmann B, Lesley R, Blom B, et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000;13:715–725.
  • Watford WT, 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.
  • McGeachy MJ, Cua DJ. Th17 cell differentiation: the long and winding road. Immunity 2008;28:445–453.
  • Filipe-Santos O, Bustamante J, Chapgier A, et al. Inborn errors of IL-12/23- and IFN-gamma-mediated immunity: molecular, cellular, and clinical features. Semin Immunol 2006;18:347–361. Erratum in: Semin Immunol 2007;19:136-137.
  • Picard C, Fieschi C, Altare F, et al. Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds. Am J Hum Genet 2002;70:336–348.
  • 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.
  • 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.
  • Altare F, Durandy A, Lammas D, et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 1998;280:1432–1435.
  • Pedraza S, Lezana JL, Samarina A, et al. Clinical disease caused by Klebsiella in 2 unrelated patients with interleukin 12 receptor beta1 deficiency. Pediatrics 2010;126:e971–e976.
  • Toy D, Kugler D, Wolfson M, et al. Cutting edge: interleukin 17 signals through a heteromeric receptor complex. J Immunol 2006;177:36–39.
  • 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.
  • Chang SH, Dong C. Signaling of interleukin-17 family cytokines in immunity and inflammation. Cell Signal 2011;23:1069–1075.
  • May MJ. IL-17R signaling: new players get in on the Act1. Nat Immunol 2011;12:813–815.
  • Shen F, Gaffen SL. Structure-function relationships in the IL-17 receptor: implications for signal transduction and therapy. Cytokine 2008;41:92–104.
  • 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.
  • Novatchkova M, Leibbrandt A, Werzowa J, et al. The STIR-domain superfamily in signal transduction, development and immunity. Trends Biochem Sci 2003;28:226-229.
  • Boisson B, Wang C, Pedergnana V, et al. An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis. Immunity 2013;39:676–686.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.