Host defence against Candida albicans and the role of pattern-recognition receptors

Acta Dermato-Venereologica

Volumn 92, Issue 3, 2012, Pages 291-298

  Gauglitz, Gerd G ^a   Callenberg, Helene ^a   Weindl, Günther ^b   Korting, Hans C ^b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

C type lectin receptor; Candida albicans; Pathogen associated molecular pattern; Pattern recognition receptor; Toll like receptor

Indexed keywords

CD209 ANTIGEN; COLLECTIN; COMPLEMENT RECEPTOR; COMPLEMENT RECEPTOR 3; DECTIN 1; DECTIN 2; GALECTIN; LANGERIN; LECTIN; MANNOSE RECEPTOR; MINCLE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; NUCLEOTIDE BINDING PROTEIN; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

CANDIDA ALBICANS; CANDIDIASIS; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; INTRACELLULAR SIGNALING; INVASIVE CANDIDIASIS; MEDICAL RESEARCH; NONHUMAN; PRIORITY JOURNAL; REVIEW;

CANDIDA ALBICANS; CANDIDIASIS; COLLECTINS; HUMANS; IMMUNITY, INNATE; LECTINS, C-TYPE; RECEPTORS, COMPLEMENT; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84859764944     PISSN: 00015555     EISSN: None     Source Type: Journal    
DOI: 10.2340/00015555-1250     Document Type: Review

References (93)

1. of tumor necrosis factor alpha by human monocytes in a CD14- and Toll-like receptor 4-dependent manner. Microbiol Immunol 2002; 46: 503-512.
2. Netea MG, Van der Graaf C, Van der Meer JW, Kullberg BJ. Recognition of fungal pathogens by Toll-like receptors. Eur J Clin Microbiol Infect Dis 2004; 23: 672-676.
3. Netea MG, Gow NA, Munro CA, Bates S, Collins C, Ferwerda G, et al. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 2006; 116: 1642-1650.
4. Poulain D, Jouault T. Candida albicans cell wall glycans, host receptors and responses: elements for a decisive crosstalk. Curr Opin Microbiol 2004; 7: 342-349.
5. Pietrella D, Bistoni G, Corbucci C, Perito S, Vecchiarelli A. Candida albicans mannoprotein influences the biological function of dendritic cells. Cell Microbiol 2006; 8: 602-612.
6. Underhill DM. Toll-like receptors: networking for success. Eur J Immunol 2003; 33: 1767-1775.
7. Netea MG, van der Graaf C, Van der Meer JW, Kullberg BJ. Toll-like receptors and the host defense against microbial pathogens: bringing specificity to the innate-immune system. J Leukoc Biol 2004; 75: 749-755.
8. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
9. Willment JA, Brown GD. C-type lectin receptors in antifungal immunity. Trends Microbiol 2008; 16: 27-32.
10. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004; 5: 987-995.
11. Weindl G, Naglik JR, Kaesler S, Biedermann T, Hube B, Korting HC, et al. Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J Clin Invest 2007; 117: 3664-3672.
12. Jouault T, Ibata-Ombetta S, Takeuchi O, Trinel PA, Sacchetti P, Lefebvre P, et al. Candida albicans phospholipomannan is sensed through toll-like receptors. J Infect Dis 2003; 188: 165-172.
13. Netea MG, Van Der Graaf CA, Vonk AG, Verschueren I, Van Der Meer JW, Kullberg BJ. The role of toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J Infect Dis 2002; 185: 1483-1489.
14. Blasi E, Mucci A, Neglia R, Pezzini F, Colombari B, Radzioch D, et al. Biological importance of the two Tolllike receptors, TLR2 and TLR4, in macrophage response to infection with Candida albicans. FEMS Immunol Med Microbiol 2005; 44: 69-79.
15. van der Graaf CA, Netea MG, Verschueren I, van der Meer JW, Kullberg BJ. Differential cytokine production and Toll-like receptor signaling pathways by Candida albicans blastoconidia and hyphae. Infect Immun 2005; 73: 7458-7464.
16. Netea MG, Sutmuller R, Hermann C, Van der Graaf CA, Van der Meer JW, van Krieken JH, 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.
17. Sutmuller RP, den Brok MH, Kramer M, Bennink EJ, Toonen LW, Kullberg BJ, et al. Toll-like receptor 2 controls expansion and function of regulatory T cells. J Clin Invest 2006; 116: 485-494.
18. Villamon E, Gozalbo D, Roig P, O'Connor JE, Fradelizi D, Gil ML. Toll-like receptor-2 is essential in murine defenses against Candida albicans infections. Microbes Infect 2004; 6: 1-7.
19. Ali A, Natah S, Konttinen Y. Differential expression of Toll-like receptors in chronic hyperplastic candidosis. Oral Microbiol Immunol 2008; 23: 299-307.
20. Roeder A, Kirschning CJ, Schaller M, Weindl G, Wagner H, Korting HC, et al. Induction of nuclear factor- kappa B and c-Jun/activator protein-1 via toll-like receptor 2 in macrophages by antimycotic-treated Candida albicans. J Infect Dis 2004; 190: 1318-1326.
21. Netea MG, van de Veerdonk F, Verschueren I, van der Meer JW, Kullberg BJ. Role of TLR1 and TLR6 in the host defense against disseminated candidiasis. FEMS Immunol Med Microbiol 2008; 52: 118-123.
22. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Scie 1998; 282: 2085-2088.
23. Netea MG, Marodi L. Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol 2010; 31: 346-353.
24. Van der Graaf CA, Netea MG, Morre SA, Den Heijer M, Verweij PE, Van der Meer JW, et al. Toll-like receptor 4 Asp299Gly/Thr399Ile polymorphisms are a risk factor for Candida bloodstream infection. Eur Cytokine Netw 2006; 17: 29-34.
25. d'Ostiani CF, Del Sero G, Bacci A, Montagnoli C, Spreca A, Mencacci A, et al. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J Exp Med 2000; 191: 1661-1674.
26. Netea MG, Gow NA, Joosten LA, Verschueren I, van der Meer JW, Kullberg BJ. Variable recognition of Candida albicans strains by TLR4 and lectin recognition receptors. Med Mycol 2010; 48: 897-903.
27. Gil ML, Gozalbo D. TLR2, but not TLR4, triggers cytokine production by murine cells in response to Candida albicans yeasts and hyphae. Microbes Infect 2006; 8: 2299-2304.
28. Netea MG, van der Meer JW, Kullberg BJ. Both TLR2 and TLR4 are involved in the recognition of Candida albicans. Reply to "TLR2, but not TLR4, triggers cytokine production by murine cells in response to Candida albicans yeasts and hyphae" by Gil and Gozalbo, Microbes and Infection 8 (2006) 2823-2824. Microbes Infect 2006; 8: 2821-2822; author reply 2823-2824.
29. Bellocchio S, Montagnoli C, Bozza S, Gaziano R, Rossi G, Mambula SS, et al. The contribution of the Toll-like/ IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 2004; 172: 3059-3069.
30. van de Veerdonk FL, Netea MG, Jansen TJ, Jacobs L, Verschueren I, van der Meer JW, et al. Redundant role of TLR9 for anti-Candida host defense. Immunobiology 2008; 213: 613-620.
31. Miyazato A, Nakamura K, Yamamoto N, Mora-Montes HM, Tanaka M, Abe Y, et al. Toll-like receptor 9-dependent activation of myeloid dendritic cells by Deoxynucleic acids from Candida albicans. Infect Immun 2009; 77: 3056-3064.
32. Weis WI, Taylor ME, Drickamer K. The C-type lectin superfamily in the immune system. Immunol Rev 1998; 163: 19-34.
33. McKenzie EJ, Taylor PR, Stillion RJ, Lucas AD, Harris J, Gordon S, et al. Mannose receptor expression and function define a new population of murine dendritic cells. J Immunol 2007; 178: 4975-4983.
34. Taylor PR, Gordon S, Martinez-Pomares L. The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol 2005; 26: 104-110.
35. Romani L, Montagnoli C, Bozza S, Perruccio K, Spreca A, Allavena P, et al. The exploitation of distinct recognition receptors in dendritic cells determines the full range of host immune relationships with Candida albicans. Int Immunol 2004; 16: 149-161.
36. Le Cabec V, Emorine LJ, Toesca I, Cougoule C, Maridonneau-Parini I. The human macrophage mannose receptor is not a professional phagocytic receptor. J Leukoc Biol 2005; 77: 934-943.
37. Chieppa M, Bianchi G, Doni A, Del Prete A, Sironi M, Laskarin G, et al. Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an antiinflammatory immunosuppressive program. J Immunol 2003; 171: 4552-4560.
38. Yamamoto Y, Klein TW, Friedman H. Involvement of mannose receptor in cytokine interleukin-1beta (IL-1beta), IL-6, and granulocyte-macrophage colony-stimulating factor responses, but not in chemokine macrophage inflammatory protein 1beta (MIP-1beta), MIP-2, and KC responses, caused by attachment of Candida albicans to macrophages. Infect Immun 1997; 65: 1077-1082.
39. Heinsbroek SE, Taylor PR, Martinez FO, Martinez-Pomares L, Brown GD, Gordon S. Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog 2008; 4: e1000218.
40. Kery V, Krepinsky JJ, Warren CD, Capek P, Stahl PD. Ligand recognition by purified human mannose receptor. Arch Biochem Biophys 1992; 298: 49-55.
41. Lee SJ, Zheng NY, Clavijo M, Nussenzweig MC. Normal host defense during systemic candidiasis in mannose receptor- deficient mice. Infect Immun 2003; 71: 437-445.
42. Netea MG, Ferwerda G, van der Graaf CA, Van der Meer JW, Kullberg BJ. Recognition of fungal pathogens by tolllike receptors. Curr Pharm Des 2006; 12: 4195-4201.
43. Koppel EA, van Gisbergen KP, Geijtenbeek TB, van Kooyk Y. Distinct functions of DC-SIGN and its homologues L-SIGN (DC-SIGNR) and mSIGNR1 in pathogen recognition and immune regulation. Cell Microbiol 2005; 7: 157-165.
44. Cambi A, Gijzen K, de Vries JM, Torensma R, Joosten B, Adema GJ, et al. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur J Immunol 2003; 33: 532-538.
45. den Dunnen J, Gringhuis SI, Geijtenbeek TB. Innate signaling by the C-type lectin DC-SIGN dictates immune responses. Cancer Immunol Immunother 2009; 58: 1149-1157.
46. Caparros E, Munoz P, Sierra-Filardi E, Serrano-Gomez D, Puig-Kroger A, Rodriguez-Fernandez JL, et al. DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 2006; 107: 3950-3958.
47. Gringhuis SI, den Dunnen J, Litjens M, van Het Hof B, van Kooyk Y, Geijtenbeek TB. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinasedependent acetylation of transcription factor NF-kappaB. Immunity 2007; 26: 605-616.
48. Ferwerda G, Netea MG, Joosten LA, van der Meer JW, Romani L, Kullberg BJ. The role of Toll-like receptors and C-type lectins for vaccination against Candida albicans. Vaccine 2010; 28: 614-622.
49. Heinsbroek SE, Brown GD, Gordon S. Dectin-1 escape by fungal dimorphism. Trends Immunol 2005; 26: 352-354.
50. LeibundGut-Landmann S, Gross O, Robinson MJ, Osorio F, Slack EC, Tsoni SV, et al. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol 2007; 8: 630-638.
51. Hollmig ST, Ariizumi K, Cruz PD, Jr. Recognition of nonself- polysaccharides by C-type lectin receptors dectin-1 and dectin-2. Glycobiology 2009; 19: 568-575.
52. Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, Findon H, et al. Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol 2007; 8: 31-38.
53. Osorio F, LeibundGut-Landmann S, Lochner M, Lahl K, Sparwasser T, Eberl G, et al. DC activated via dectin-1 convert Treg into IL-17 producers. Eur J Immunol 2008; 38: 3274-3281.
54. 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: 773-776.
55. Eyerich K, Foerster S, Rombold S, Seidl HP, Behrendt H, Hofmann H, et al. Patients with chronic mucocutaneous candidiasis exhibit reduced production of Th17-associated cytokines IL-17 and IL-22. J Invest Dermatol 2008; 128: 2640-2645.
56. Sato K, Yang XL, Yudate T, Chung JS, Wu J, Luby-Phelps K, et al. Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor gamma chain to induce innate immune responses. J Biol Chem 2006; 281: 38854-38866.
57. Robinson MJ, Osorio F, Rosas M, Freitas RP, Schweighoffer E, Gross O, et al. Dectin-2 is a Syk-coupled pattern recognition receptor crucial for Th17 responses to fungal infection. J Exp Med 2009; 206: 2037-2051.
58. Bi L GS, Wu W, Hsu YM, Zhu J, Ariizumi K, Lin X. CARD9 mediates Dectin-2-induced IKK ubiquitination leading to activation of NF-kappaB in response to the stimulation by the hyphal form of Candida albicans. J Biol Chem 2010; 285: 25969-25977.
59. Wells CA, Salvage-Jones JA, Li X, Hitchens K, Butcher S, Murray RZ, et al. The macrophage-inducible C-type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J Immunol 2008; 180: 7404-7413.
60. Matsumoto M, Tanaka T, Kaisho T, Sanjo H, Copeland NG, Gilbert DJ, et al. A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J Immunol 1999; 163: 5039-5048.
61. Graham LM, Brown GD. The Dectin-2 family of C-type lectins in immunity and homeostasis. Cytokine 2009; 48: 148-155.
62. Truong MJ, Gruart V, Kusnierz JP, Papin JP, Loiseau S, Capron A, et al. Human neutrophils express immunoglobulin E (IgE)-binding proteins (Mac-2/epsilon BP) of the S-type lectin family: role in IgE-dependent activation. J Exp Med 1993; 177: 243-248.
63. Kohatsu L, Hsu DK, Jegalian AG, Liu FT, Baum LG. Galectin-3 induces death of Candida species expressing specific beta-1,2-linked mannans. J Immunol 2006; 177: 4718-4726.
64. Jouault T, El Abed-El Behi M, Martinez-Esparza M, Breuilh L, Trinel PA, Chamaillard M, et al. Specific recognition of Candida albicans by macrophages requires galectin-3 to discriminate Saccharomyces cerevisiae and needs association with TLR2 for signaling. J Immunol 2006; 177: 4679-4687.
65. Jawhara S, Thuru X, Standaert-Vitse A, Jouault T, Mordon S, Sendid B, et al. Colonization of mice by Candida albicans is promoted by chemically induced colitis and augments inflammatory responses through galectin-3. J Infect Dis 2008; 197: 972-980.
66. Takahara K, Omatsu Y, Yashima Y, Maeda Y, Tanaka S, Iyoda T, et al. Identification and expression of mouse Langerin (CD207) in dendritic cells. Int Immunol 2002; 14: 433-444.
67. Takahara K, Yashima Y, Omatsu Y, Yoshida H, Kimura Y, Kang YS, et al. Functional comparison of the mouse DCSIGN, SIGNR1, SIGNR3 and Langerin, C-type lectins. Int Immunol 2004; 16: 819-829.
68. Stambach NS, Taylor ME. Characterization of carbohydrate recognition by langerin, a C-type lectin of Langerhans cells. Glycobiology 2003; 13: 401-410.
69. de Jong MA, Vriend LE, Theelen B, Taylor ME, Fluitsma D, Boekhout T, et al. C-type lectin Langerin is a betaglucan receptor on human Langerhans cells that recognizes opportunistic and pathogenic fungi. Mol Immunol 2010; 47: 1216-1225.
70. Hogaboam CM, Takahashi K, Ezekowitz RA, Kunkel SL, Schuh JM. Mannose-binding lectin deficiency alters the development of fungal asthma: effects on airway response, inflammation, and cytokine profile. J Leukoc Biol 2004; 75: 805-814.
71. Kishore U, Greenhough TJ, Waters P, Shrive AK, Ghai R, Kamran MF, et al. Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol Immunol 2006; 43: 1293-1315.
72. Rosseau S, Hammerl P, Maus U, Gunther A, Seeger W, Grimminger F, et al. Surfactant protein A down-regulates proinflammatory cytokine production evoked by Candida albicans in human alveolar macrophages and monocytes. J Immunol 1999; 163: 4495-4502.
73. Rosseau S, Guenther A, Seeger W, Lohmeyer J. Phagocytosis of viable Candida albicans by alveolar macrophages: lack of opsonin function of surfactant protein A. J Infect Dis 1997; 175: 421-428.
74. van Rozendaal BA, van Spriel AB, van De Winkel JG, Haagsman HP. Role of pulmonary surfactant protein D in innate defense against Candida albicans. J Infect Dis 2000; 182: 917-922.
75. van Asbeck EC, Hoepelman AI, Scharringa J, Herpers BL, Verhoef J. Mannose binding lectin plays a crucial role in innate immunity against yeast by enhanced complement activation and enhanced uptake of polymorphonuclear cells. BMC Microbiol 2008; 8: 229.
76. Kitz DJ, Stahl PD, Little JR. The effect of a mannose binding protein on macrophage interactions with Candida albicans. Cell Mol Biol 1992; 38: 407-412.
77. Ghezzi MC, Raponi G, Angeletti S, Mancini C. Serummediated enhancement of TNF-alpha release by human monocytes stimulated with the yeast form of Candida albicans. J Infect Dis 1998; 178: 1743-1749.
78. Held K, Thiel S, Loos M, Petry F. Increased susceptibility of complement factor B/C2 double knockout mice and mannan- binding lectin knockout mice to systemic infection with Candida albicans. Mol Immunol 2008; 45: 3934-3941.
79. Babula O, Lazdane G, Kroica J, Ledger WJ, Witkin SS. Relation between recurrent vulvovaginal candidiasis, vaginal concentrations of mannose-binding lectin, and a mannose-binding lectin gene polymorphism in Latvian women. Clin Infect Dis 2003; 37: 733-737.
80. Liu F, Liao Q, Liu Z. Mannose-binding lectin and vulvovaginal candidiasis. Int J Gynaecol Obstet 2006; 92: 43-47.
81. Giraldo PC, Babula O, Goncalves AK, Linhares IM, Amaral RL, Ledger WJ, et al. Mannose-binding lectin gene polymorphism, vulvovaginal candidiasis, and bacterial vaginosis. Obstet Gynecol 2007; 109: 1123-1128.
82. Donders GG, Babula O, Bellen G, Linhares IM, Witkin SS. Mannose-binding lectin gene polymorphism and resistance to therapy in women with recurrent vulvovaginal candidiasis. BJOG 2008; 115: 1225-1231.
83. Milanese M, Segat L, De Seta F, Pirulli D, Fabris A, Morgutti M, et al. MBL2 genetic screening in patients with recurrent vaginal infections. Am J Reprod Immunol 2008; 59: 146-151.
84. Thornton BP, Vetvicka V, Pitman M, Goldman RC, Ross GD. Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J Immunol 1996; 156: 1235-1246.
85. Forsyth CB, Plow EF, Zhang L. Interaction of the fungal pathogen Candida albicans with integrin CD11b/CD18: recognition by the I domain is modulated by the lectinlike domain and the CD18 subunit. J Immunol 1998; 161: 6198-6205.
86. Forsyth CB, Mathews HL. Lymphocyte adhesion to Candida albicans. Infect Immun 2002; 70: 517-527.
87. Rubin-Bejerano I, Abeijon C, Magnelli P, Grisafi P, Fink GR. Phagocytosis by human neutrophils is stimulated by a unique fungal cell wall component. Cell Host Microbe 2007; 2: 55-67.
88. Brandhorst TT, Wuthrich M, Finkel-Jimenez B, Warner T, Klein BS. Exploiting type 3 complement receptor for TNF-alpha suppression, immune evasion, and progressive pulmonary fungal infection. J Immunol 2004; 173: 7444-7453.
89. Jabra-Rizk MA, Falkler WA, Jr, Merz WG, Kelley JI, Baqui AA, Meiller TF. Candida dubliniensis and Candida albicans display surface variations consistent with observed intergeneric coaggregation. Rev Iberoam Micol 1999; 16: 187-193.
90. Bryant C, Fitzgerald KA. Molecular mechanisms involved in inflammasome activation. Trends Cell Biol 2009; 19: 455-464.
91. Gross O, Poeck H, Bscheider M, Dostert C, Hannesschlager N, Endres S, et al. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 2009; 459: 433-436.
92. Hise AG, Tomalka J, Ganesan S, Patel K, Hall BA, Brown GD, et al. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 2009; 5: 487-497.
93. Joly S, Ma N, Sadler JJ, Soll DR, Cassel SL, Sutterwala FS. Cutting edge: Candida albicans hyphae formation triggers activation of the Nlrp3 inflammasome. J Immunol 2009; 183: 3578-3581.