The role of dendritic cells in the innate recognition of pathogenic fungi (A. fumigatus, C. neoformans and C. albicans)

Virulence

Volumn 3, Issue 7, 2012, Pages

  Ramirez Ortiz, Zaida G ^a   Means, Terry K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Conventional dendritic cells; Fungi; Plasmacytoid dendritic cells; Scavenger receptors; Toll like receptors

Indexed keywords

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CELL FUNCTION; DENDRITIC CELL; HUMAN; INNATE IMMUNITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; REVIEW; T LYMPHOCYTE ACTIVATION; TUBERCULOSIS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CANDIDIASIS; CONVENTIONAL DENDRITIC CELLS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FUNGUS; IMMUNOCOMPROMISED PATIENT; IMMUNOLOGY; MICROBIOLOGY; PLASMACYTOID DENDRITIC CELL;

SCAVENGER RECEPTOR; TOLL LIKE RECEPTOR;

CONVENTIONAL DENDRITIC CELLS; FUNGI; PLASMACYTOID DENDRITIC CELLS; SCAVENGER RECEPTORS; TOLL-LIKE RECEPTORS;

ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CANDIDIASIS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DENDRITIC CELLS; HUMANS; IMMUNOCOMPROMISED HOST;

EID: 84870946492     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.4161/viru.22295     Document Type: Review

References (96)

1. Perfect JR. The impact of the host on fungal infections. Am J Med 2012; 125(Suppl):S39-51; PMID: 22196208; http://dx.doi.org/10.1016/j.amjmed.2011.10.010
2. Perfect JR. Invasive mycoses: evolving challenges and opportunities in antifungal therapy. Introduction. Am J Med 2012; 125(Suppl):S1-2; PMID:22196204; http://dx.doi.org/10.1016/j.amjmed.2011.10.007
3. Roy RM, Klein BS. Dendritic cells in antifungal immunity and vaccine design. Cell Host Microbe 2012; 11:436-46; PMID:22607797; http://dx.doi.org/10.1016/j.chom.2012.04.005
4. Latgé JP. Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 1999; 12:310-50; PMID:10194462
5. Cramer RA, Rivera A, Hohl TM. Immune responses against Aspergillus fumigatus: what have we learned? Curr Opin Infect Dis 2011; 24:315-22; PMID: 21666456; http://dx.doi.org/10.1097/QCO. 0b013e328348b159
6. Perfect JR, Casadevall A. Cryptococcosis. [v-vi.]. Infect Dis Clin North Am 2002; 16:837-74, v-vi; PMID: 12512184; http://dx.doi.org/10.1016/S0891-5520(02) 00036-3
7. Vonk AG, Netea MG, van der Meer JW, Kullberg BJ. Host defence against disseminated Candida albicans infection and implications for antifungal immunotherapy. Expert Opin Biol Ther 2006; 6:891-903; PMID: 16918256; http://dx.doi.org/10.1517/14712598.6.9. 891
8. Gow NA, van de Veerdonk FL, Brown AJ, Netea MG. Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 2012; 10:112-22; PMID:22158429
9. 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; PMID:18079743; http://dx.doi.org/10. 1038/nrmicro1815
10. Hage CA, Knox KS, Wheat LJ. Endemic mycoses: overlooked causes of community acquired pneumonia. Respir Med 2012; 106:769-76; PMID:22386326; http://dx.doi.org/10.1016/j.rmed.2012.02.004
11. Bonifaz A, Vázquez-González D, Perusquía-Ortiz AM. Endemic systemic mycoses: coccidioidomycosis, histoplasmosis, paracoccidioidomycosis and blastomycosis. J Dtsch Dermatol Ges 2011; 9:705-14, quiz 715; PMID: 21722309; http://dx.doi.org/10.1111/j.1610-0387. 2011.07731.x
12. Wüthrich M, Deepe GS, Jr., Klein B. Adaptive immunity to fungi. Annu Rev Immunol 2012; 30: 115-48; PMID:22224780; http://dx.doi.org/10.1146/annurev-immunol-020711-074958
13. Borchers AT, Gershwin ME. The immune response in Coccidioidomycosis. Autoimmun Rev 2010; 10:94-102; PMID:20728582; http://dx.doi.org/10.1016/j. autrev.2010.08.010
14. Edwards JA, Rappleye CA. Histoplasma mechanisms of pathogenesis-one portfolio doesn't fit all. FEMS Microbiol Lett 2011; 324:1-9; PMID:22092757; http://dx.doi.org/10.1111/j.1574-6968.2011.02363.x
15. Steinman RM. Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 2012; 30: 1-22; PMID:22136168; http://dx.doi.org/10.1146/annurev-immunol-100311-102839
16. Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V. Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol 2011; 29:163-83; PMID: 21219184; http://dx.doi.org/10.1146/annurev-immunol-031210-101345
17. Benko S, Magyarics Z, Szabó A, Rajnavölgyi E. Dendritic cell subtypes as primary targets of vaccines: the emerging role and cross-talk of pattern recognition receptors. Biol Chem 2008; 389:469-85; PMID: 18953714; http://dx.doi.org/10.1515/BC.2008.054
18. Rivera A, Ro G, Van Epps HL, Simpson T, Leiner I, Sant'Angelo DB, et al. Innate immune activation and CD4+ T cell priming during respiratory fungal infection. Immunity 2006; 25:665-75; PMID: 17027299; http://dx.doi.org/10.1016/j.immuni.2006.08.016
19. Brown GD. Innate antifungal immunity: the key role of phagocytes. Annu Rev Immunol 2011; 29:1-21; PMID: 20936972; http://dx.doi.org/10.1146/annurev-immunol-030409-101229
20. Romani L. Immunity to fungal infections. Nat Rev Immunol 2011; 11:275-88; PMID:21394104; http://dx.doi.org/10.1038/nri2939
21. Brummer E, Stevens DA. Collectins and fungal pathogens: roles of surfactant proteins and mannose binding lectin in host resistance. Med Mycol 2010; 48: 16-28; PMID:19639514; http://dx.doi.org/10.3109/13693780903117473
22. Cheng SC, Sprong T, Joosten LA, van der Meer JW, Kullberg BJ, Hube B, et al. Complement plays a central role in Candida albicans-induced cytokine production by human PBMCs. Eur J Immunol 2012; 42:993-1004; PMID:22531923; http://dx.doi.org/10.1002/eji. 201142057
23. Sudbery PE. Growth of Candida albicans hyphae. Nat Rev Microbiol 2011; 9:737-48; PMID:21844880; http://dx.doi.org/10.1038/nrmicro2636
24. Bernard M, Latgé JP. Aspergillus fumigatus cell wall: composition and biosynthesis. Med Mycol 2001; 39 (Suppl 1):9-17; PMID:11800273
25. Bose I, Reese AJ, Ory JJ, Janbon G, Doering TL. A yeast under cover: the capsule of Cryptococcus neoformans. Eukaryot Cell 2003; 2:655-63; PMID: 12912884; http://dx.doi.org/10.1128/EC.2.4.655-663.2003
26. Shoham S, Huang C, Chen JM, Golenbock DT, Levitz SM. Toll-like receptor 4 mediates intracellular signaling without TNF-alpha release in response to Cryptococcus neoformans polysaccharide capsule. J Immunol 2001; 166:4620-6; PMID:11254720
27. Nakamura K, Miyagi K, Koguchi Y, Kinjo Y, Uezu K, Kinjo T, et al. Limited contribution of Toll-like receptor 2 and 4 to the host response to a fungal infectious pathogen, Cryptococcus neoformans. FEMS Immunol Med Microbiol 2006; 47:148-54; PMID: 16706798; http://dx.doi.org/10.1111/j.1574-695X.2006.00078.x
28. Bellocchio S, Montagnoli C, Bozza S, Gaziano R, Rossi G, Mambula SS, et al. The contribution of the Tolllike/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 2004; 172:3059-69; PMID:14978111
29. Pietrella D, Bistoni G, Corbucci C, Perito S, Vecchiarelli A. Candida albicans mannoprotein influences the biological function of dendritic cells. Cell Microbiol 2006; 8:602-12; PMID:16548886; http://dx.doi.org/10.1111/j.1462-5822.2005.00651.x
30. Plantinga TS, Johnson MD, Scott WK, van de Vosse E, Velez Edwards DR, Smith PB, et al. Toll-like receptor 1 polymorphisms increase susceptibility to candidemia. J Infect Dis 2012; 205:934-43; PMID:22301633; http://dx.doi.org/10.1093/infdis/jir867
31. Kesh S, Mensah NY, Peterlongo P, Jaffe D, Hsu K, VAN DEN Brink M, et al. TLR1 and TLR6 polymorphisms are associated with susceptibility to invasive aspergillosis after allogeneic stem cell transplantation. Ann NY Acad Sci 2005; 1062:95-103; PMID:16461792; http://dx.doi.org/10.1196/annals. 1358.012
32. Rubino I, Coste A, Le Roy D, Roger T, Jaton K, Boeckh M, et al. Species-specific recognition of Aspergillus fumigatus by Toll-like receptor 1 and Toll-like receptor 6. J Infect Dis 2012; 205:944-54; PMID:22315281; http://dx.doi.org/10.1093/infdis/jir882
33. Van der Graaf CA, Netea MG, Morré 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; PMID:16613760
34. 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; 52:118-23; PMID: 18036178; http://dx.doi.org/10.1111/j.1574-695X.2007.00353.x
35. + T cell responses to Aspergillus fumigatus in hematopoietic transplanted patients. Blood 2012; 119:967-77; PMID: 22147891; http://dx.doi.org/10.1182/blood-2011-06-362582
36. Ariizumi K, Shen GL, Shikano S, Xu S, Ritter R, 3rd, Kumamoto T, et al. Identification of a novel, dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning. J Biol Chem 2000; 275:20157-67; PMID: 10779524; http://dx.doi.org/10.1074/jbc. M909512199
37. Brown GD, Gordon S. Immune recognition. A new receptor for beta-glucans. Nature 2001; 413:36-7; PMID:11544516; http://dx.doi.org/10.1038/35092620
38. Mezger M, Kneitz S, Wozniok I, Kurzai O, Einsele H, Loeffler J. Proinflammatory response of immature human dendritic cells is mediated by dectin-1 after exposure to Aspergillus fumigatus germ tubes. J Infect Dis 2008; 197:924-31; PMID:18279049; http://dx. doi.org/10.1086/528694
39. Saijo S, Iwakura Y. Dectin-1 and Dectin-2 in innate immunity against fungi. Int Immunol 2011; 23:467-72; PMID:21677049; http://dx.doi.org/10.1093/intimm/dxr046
40. McGreal EP, Rosas M, Brown GD, Zamze S, Wong SY, Gordon S, et al. The carbohydrate-recognition domain of Dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 2006; 16:422-30; PMID:16423983; http://dx.doi.org/10.1093/glycob/cwj077
41. 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; 281:38854-66; PMID:17050534; http://dx.doi.org/10.1074/jbc.M606542200
42. Robinson MJ, Osorio F, Rosas M, Freitas RP, Schweighoffer E, Gross O, et al. Dectin-2 is a Sykcoupled pattern recognition receptor crucial for Th17 responses to fungal infection. J Exp Med 2009; 206: 2037-51; PMID:19703985; http://dx.doi.org/10. 1084/jem.20082818
43. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A, et al. Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 2010; 32:681-91; PMID:20493731; http://dx.doi.org/10.1016/j.immuni.2010.05.001
44. Mansour MK, Schlesinger LS, Levitz SM. Optimal T cell responses to Cryptococcus neoformans mannoprotein are dependent on recognition of conjugated carbohydrates by mannose receptors. J Immunol 2002; 168:2872-9; PMID:11884457
45. Mansour MK, Latz E, Levitz SM. Cryptococcus neoformans glycoantigens are captured by multiple lectin receptors and presented by dendritic cells. J Immunol 2006; 176:3053-61; PMID:16493064
46. Takahara K, Yashima Y, Omatsu Y, Yoshida H, Kimura Y, Kang YS, et al. Functional comparison of the mouse DC-SIGN, SIGNR1, SIGNR3 and Langerin, C-type lectins. Int Immunol 2004; 16:819-29; PMID: 15096474; http://dx.doi.org/10.1093/intimm/dxh084
47. Levitz SM, Specht CA. The molecular basis for the immunogenicity of Cryptococcus neoformans mannoproteins. FEMS Yeast Res 2006; 6:513-24; PMID: 16696647; http://dx.doi.org/10.1111/j.1567-1364. 2006.00071.x
48. Pietrella D, Corbucci C, Perito S, Bistoni G, Vecchiarelli A. Mannoproteins from Cryptococcus neoformans promote dendritic cell maturation and activation. Infect Immun 2005; 73:820-7; PMID: 15664921; http://dx.doi.org/10.1128/IAI.73.2.820-827.2005
49. Dan JM, Wang JP, Lee CK, Levitz SM. Cooperative stimulation of dendritic cells by Cryptococcus neoformans mannoproteins and CpG oligodeoxynucleotides. PLoS One 2008; 3:e2046; PMID:18446192; http://dx. doi.org/10.1371/journal.pone.0002046
50. Dan JM, Kelly RM, Lee CK, Levitz SM. Role of the mannose receptor in a murine model of Cryptococcus neoformans infection. Infect Immun 2008; 76:2362-7; PMID:18391001; http://dx.doi.org/10.1128/IAI. 00095-08
51. Donini M, Zenaro E, Tamassia N, Dusi S. NADPH oxidase of human dendritic cells: role in Candida albicans killing and regulation by interferons, dectin-1 and CD206. Eur J Immunol 2007; 37:1194-203; PMID:17407098; http://dx.doi.org/10.1002/eji. 200636532
52. Serrano-Gómez D, Domínguez-Soto A, Ancochea J, Jimenez-Heffernan JA, Leal JA, Corbí AL. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol 2004; 173:5635-43; PMID: 15494514
53. Sainz J, Lupiáñez CB, Segura-Catena J, Vazquez L, Ríos R, Oyonarte S, et al. Dectin-1 and DC-SIGN polymorphisms associated with invasive pulmonary Aspergillosis infection. PLoS One 2012; 7:e32273; PMID:22384201; http://dx.doi.org/10.1371/journal. pone.0032273
54. 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: 532-8; PMID:12645952; http://dx.doi.org/10.1002/immu.200310029
55. Cambi A, Netea MG, Mora-Montes HM, Gow NA, Hato SV, Lowman DW, et al. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J Biol Chem 2008; 283:20590-9; PMID: 18482990; http://dx.doi.org/10.1074/jbc. M709334200
56. Lam JS, Huang H, Levitz SM. Effect of differential Nlinked and O-linked mannosylation on recognition of fungal antigens by dendritic cells. PLoS One 2007; 2: e1009; PMID:17925857; http://dx.doi.org/10.1371/journal.pone.0001009
57. 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; PMID:11801677
58. Park SJ, Burdick MD, Brix WK, Stoler MH, Askew DS, Strieter RM, et al. Neutropenia enhances lung dendritic cell recruitment in response to Aspergillus via a cytokine-to-chemokine amplification loop. J Immunol 2010; 185:6190-7; PMID:20926800; http://dx.doi.org/10.4049/jimmunol.1002064
59. Zelante T, Bozza S, De Luca A, D'Angelo C, Bonifazi P, Moretti S, et al. Th17 cells in the setting of Aspergillus infection and pathology. Med Mycol 2009; 47(Suppl 1):S162-9; PMID:18608926; http://dx.doi. org/10.1080/13693780802140766
60. Rivera A, Hohl TM, Collins N, Leiner I, Gallegos A, Saijo S, et al. Dectin-1 diversifies Aspergillus fumigatusspecific T cell responses by inhibiting T helper type 1 CD4 T cell differentiation. J Exp Med 2011; 208:369-81; PMID:21242294; http://dx.doi.org/10.1084/jem. 20100906
61. Fei M, Bhatia S, Oriss TB, Yarlagadda M, Khare A, Akira S, et al. TNF-alpha from inflammatory dendritic cells (DCs) regulates lung IL-17A/IL-5 levels and neutrophilia versus eosinophilia during persistent fungal infection. Proc Natl Acad Sci USA 2011; 108:5360-5; PMID:21402950; http://dx.doi.org/10.1073/pnas. 1015476108
62. Wozniak KL, Vyas JM, Levitz SM. In vivo role of dendritic cells in a murine model of pulmonary cryptococcosis. Infect Immun 2006; 74:3817-24; PMID:16790753; http://dx.doi.org/10.1128/IAI. 00317-06
63. Wozniak KL, Levitz SM. Cryptococcus neoformans enters the endolysosomal pathway of dendritic cells and is killed by lysosomal components. Infect Immun 2008; 76:4764-71; PMID:18678670; http://dx.doi.org/10. 1128/IAI.00660-08
64. Colonna M, Trinchieri G, Liu YJ. Plasmacytoid dendritic cells in immunity. Nat Immunol 2004; 5: 1219-26; PMID:15549123; http://dx.doi.org/10. 1038/ni1141
65. Kadowaki N, Ho S, Antonenko S, Malefyt RW, Kastelein RA, Bazan F, et al. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J Exp Med 2001; 194:863-9; PMID:11561001; http://dx.doi.org/10.1084/jem.194.6.863
66. Ramirez-Ortiz ZG, Specht CA, Wang JP, Lee CK, Bartholomeu DC, Gazzinelli RT, et al. Toll-like receptor 9-dependent immune activation by unmethylated CpG motifs in Aspergillus fumigatus DNA. Infect Immun 2008; 76:2123-9; PMID:18332208; http://dx. doi.org/10.1128/IAI.00047-08
67. Ramaprakash H, Ito T, Standiford TJ, Kunkel SL, Hogaboam CM. Toll-like receptor 9 modulates immune responses to Aspergillus fumigatus conidia in immunodeficient and allergic mice. Infect Immun 2009; 77:108-19; PMID:18936185; http://dx.doi.org/10.1128/IAI.00998-08
68. Romani L, Bistoni F, Gaziano R, Bozza S, Montagnoli C, Perruccio K, et al. Thymosin alpha 1 activates dendritic cells for antifungal Th1 resistance through toll-like receptor signaling. Blood 2004; 103:4232-9; PMID:14982877; http://dx.doi.org/10.1182/blood-2003-11-4036
69. Montagnoli C, Perruccio K, Bozza S, Bonifazi P, Zelante T, De Luca A, et al. Provision of antifungal immunity and concomitant alloantigen tolerization by conditioned dendritic cells in experimental hematopoietic transplantation. Blood Cells Mol Dis 2008; 40:55-62; PMID:17827038; http://dx.doi.org/10.1016/j. bcmd.2007.06.016
70. Ramirez-Ortiz ZG, Lee CK, Wang JP, Boon L, Specht CA, Levitz SM. A nonredundant role for plasmacytoid dendritic cells in host defense against the human fungal pathogen Aspergillus fumigatus. Cell Host Microbe 2011; 9:415-24; PMID:21575912; http://dx.doi.org/10.1016/j.chom.2011.04.007
71. Ang DK, Oates CV, Schuelein R, Kelly M, Sansom FM, Bourges D, et al. Cutting edge: pulmonary Legionella pneumophila is controlled by plasmacytoid dendritic cells but not type I IFN. J Immunol 2010; 184:5429-33; PMID:20400697; http://dx.doi.org/10. 4049/jimmunol.1000128
72. 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; 213:613-20; PMID:18950591; http://dx.doi.org/10.1016/j.imbio.2008.05.002
73. 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; 77:3056-64; PMID:19433551; http://dx.doi.org/10.1128/IAI.00840-08
74. Biondo C, Signorino G, Costa A, Midiri A, Gerace E, Galbo R, et al. Recognition of yeast nucleic acids triggers a host-protective type I interferon response. Eur J Immunol 2011; 41:1969-79; PMID:21480215; http://dx.doi.org/10.1002/eji.201141490
75. MacDonald AS, Straw AD, Bauman B, Pearce EJ. CD8-dendritic cell activation status plays an integral role in influencing Th2 response development. J Immunol 2001; 167:1982-8; PMID:11489979
76. Bauman SK, Nichols KL, Murphy JW. Dendritic cells in the induction of protective and nonprotective anticryptococcal cell-mediated immune responses. J Immunol 2000; 165:158-67; PMID:10861048
77. LeBlanc DM, Barousse MM, Fidel PL, Jr. Role for dendritic cells in immunoregulation during experimental vaginal candidiasis. Infect Immun 2006; 74: 3213-21; PMID:16714548; http://dx.doi.org/10. 1128/IAI.01824-05
78. Edwards L, Williams AE, Krieg AM, Rae AJ, Snelgrove RJ, Hussell T. Stimulation via Toll-like receptor 9 reduces Cryptococcus neoformans-induced pulmonary inflammation in an IL-12-dependent manner. Eur J Immunol 2005; 35:273-81; PMID:15597328; http://dx.doi.org/10.1002/eji.200425640
79. Nakamura K, Miyazato A, Xiao G, Hatta M, Inden K, Aoyagi T, et al. Deoxynucleic acids from Cryptococcus neoformans activate myeloid dendritic cells via a TLR9-dependent pathway. J Immunol 2008; 180:4067-74; PMID:18322216
80. Wang JP, Lee CK, Akalin A, Finberg RW, Levitz SM. Contributions of the MyD88-dependent receptors IL-18R, IL-1R, and TLR9 to host defenses following pulmonary challenge with Cryptococcus neoformans. PLoS One 2011; 6:e26232; PMID:22039448; http://dx.doi.org/10.1371/journal.pone.0026232
81. Zhang Y, Wang F, Bhan U, Huffnagle GB, Toews GB, Standiford TJ, et al. TLR9 signaling is required for generation of the adaptive immune protection in Cryptococcus neoformans-infected lungs. Am J Pathol 2010; 177:754-65; PMID:20581055; http://dx.doi. org/10.2353/ajpath.2010.091104
82. Pamer EG. TLR polymorphisms and the risk of invasive fungal infections. N Engl J Med 2008; 359: 1836-8; PMID:18946070; http://dx.doi.org/10.1056/NEJMe0806412
83. Bochud PY, Chien JW, Marr KA, Leisenring WM, Upton A, Janer M, et al. Toll-like receptor 4 polymorphisms and aspergillosis in stem-cell transplantation. N Engl J Med 2008; 359:1766-77; PMID: 18946062; http://dx.doi.org/10.1056/NEJMoa0802629
84. Van Der Veer J, Lewis RJ, Emtiazjoo AM, Allen SD, Wheat LJ, Hage CA. Cross-reactivity in the PlateliaTM Aspergillus enzyme immunoassay caused by blastomycosis. Med Mycol 2012; 50:396-8; PMID:21939346
85. Tirado-Sánchez A, Bonifaz A, Ponce-Olivera RM. IgM in lesional skin is indicative of renal involvement in adults with Henoch-Schönlein purpura but not children. J Am Acad Dermatol 2011; 64:1183-4; PMID:21571181; http://dx.doi.org/10.1016/j.jaad. 2010.12.044
86. Bonifaz A, Vázquez-González D. Tinea imbricata in the Americas. Curr Opin Infect Dis 2011; 24:106-11; PMID:21169831; http://dx.doi.org/10.1097/QCO. 0b013e328342cbc1
87. Borchers AT, Naguwa SM, Shoenfeld Y, Gershwin ME. The geoepidemiology of systemic lupus erythematosus. Autoimmun Rev 2010; 9:A277-87; PMID: 20036343; http://dx.doi.org/10.1016/j.autrev.2009.12.008
88. Mansour MK, Vyas JM, Levitz SM. Dynamic virulence: real-time assessment of intracellular pathogenesis links Cryptococcus neoformans phenotype with clinical outcome. MBio 2011; 2:e00217-11.
89. Lam JS, Mansour MK, Specht CA, Levitz SM. A model vaccine exploiting fungal mannosylation to increase antigen immunogenicity. J Immunol 2005; 175:7496-503; PMID:16301657
90. Carvalho A, Pasqualotto AC, Pitzurra L, Romani L, Denning DW, Rodrigues F. Polymorphisms in toll-like receptor genes and susceptibility to pulmonary aspergillosis. J Infect Dis 2008; 197:618-21; PMID: 18275280; http://dx.doi.org/10.1086/526500
91. Ferwerda B, Ferwerda G, Plantinga TS, Willment JA, van Spriel AB, Venselaar H, et al. Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 2009; 361:1760-7; PMID:19864674; http://dx.doi.org/10.1056/NEJMoa0901053
92. Glocker EO, Hennigs A, Nabavi M, Schäffer AA, Woellner C, Salzer U, et al. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med 2009; 361:1727-35; PMID: 19864672; http://dx.doi.org/10.1056/NEJMoa0810719
93. Cunha C, Di Ianni M, Bozza S, Giovannini G, Zagarella S, Zelante T, et al. 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 2010; 116: 5394-402; PMID:20807886; http://dx.doi.org/10. 1182/blood-2010-04-279307
94. Mezger M, Steffens M, Beyer M, Manger C, Eberle J, Toliat MR, et al. Polymorphisms in the chemokine (CX-C motif) ligand 10 are associated with invasive aspergillosis after allogeneic stem-cell transplantation and influence CXCL10 expression in monocyte-derived dendritic cells. Blood 2008; 111:534-6; PMID: 17957030; http://dx.doi.org/10.1182/blood-2007-05-090928
95. Plantinga TS, Hamza OJ, Willment JA, Ferwerda B, van de Geer NM, Verweij PE, et al. Genetic variation of innate immune genes in HIV-infected african patients with or without oropharyngeal candidiasis. J Acquir Immune Defic Syndr 2010; 55:87-94; PMID: 20577092; http://dx.doi.org/10.1097/QAI. 0b013e3181e53c64
96. Carvalho A, Cunha C, Carotti A, Aloisi T, Guarrera O, Di Ianni M, et al. Polymorphisms in Toll-like receptor genes and susceptibility to infections in allogeneic stem cell transplantation. Exp Hematol 2009; 37:1022-9; PMID:19539691; http://dx.doi.org/10.1016/j.exphem. 2009.06.004