Interplay between Candida albicans and the mammalian innate host defense

Infection and Immunity

Volumn 80, Issue 4, 2012, Pages 1304-1313

  Cheng, Shih Chin ^a   Joosten, Leo A B ^a   Kullberg, Bart Jan ^a   Netea, Mihai G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FARNESOL; INTERLEUKIN 17; PATTERN RECOGNITION RECEPTOR;

CANDIDA ALBICANS; CANDIDIASIS; CELL TYPE; CYTOKINE PRODUCTION; EPITHELIUM CELL; FUNGAL COLONIZATION; HOST RESISTANCE; INNATE IMMUNITY; MAMMAL; MOLECULAR RECOGNITION; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; SHORT SURVEY; YEAST; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE EVASION; IMMUNOLOGY; MICROBIOLOGY; REVIEW;

CANDIDA ALBICANS; CANDIDIASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; RECEPTORS, PATTERN RECOGNITION;

EID: 84860244125     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.06146-11     Document Type: Short Survey

References (124)

1. Abe S, et al. 2009. Suppression of anti-Candida activity of macrophages by a quorum-sensing molecule, farnesol, through induction of oxidative stress. Microbiol. Immunol. 53:323-330.
2. Abiko Y, et al. 2002. Upregulation of human beta-defensin 2 peptide expression in oral lichen planus, leukoplakia and candidiasis. An immunohistochemical study. Pathol. Res. Pract. 198:537-542.
3. Aratani Y, et al. 1999. Severe impairment in early host defense against Candida albicans in mice deficient in myeloperoxidase. Infect. Immun. 67:1828-1836.
4. Bagasra O, Howeedy A, Kajdacsy-Balla A. 1988. Macrophage function in chronic experimental alcoholism. I. Modulation of surface receptors and phagocytosis. Immunology 65:405-409.
5. Bahri R, Curt S, Saidane-Mosbahi D, Rouabhia M. 2010. Normal human gingival epithelial cells sense C. parapsilosis by toll-like receptors and module its pathogenesis through antimicrobial peptides and proinflammatory cytokines. Mediators Inflamm. 2010:940383.
6. Bahri R, Saidane-Mosbahi D, Rouabhia M. 2010. Candida famata modulates toll-like receptor, beta-defensin, and proinflammatory cytokine expression by normal human epithelial cells. J. Cell. Physiol. 222: 209-218.
7. Balish E, et al. 1999. Mucosal and systemic candidiasis in IL-8Rh-/- BALB/c mice. J. Leukoc. Biol. 66:144-150.
8. Barousse MM, et al. 2001. Growth inhibition of Candida albicans by human vaginal epithelial cells. J. Infect. Dis. 184:1489-1493.
9. Braun BR, Kadosh D, Johnson AD. 2001. NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 20:4753-4761.
10. Brodsky IE, Monack D. 2009. NLR-mediated control of inflammasome assembly in the host response against bacterial pathogens. Semin. Immunol. 21:199-207.
11. Brouwer N, et al. 2008. Mannose-binding lectin (MBL) facilitates opsonophagocytosis of yeasts but not of bacteria despite MBL binding. J. Immunol. 180:4124-4132.
12. Brown GD, et al. 2002. Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 196:407-412.
13. Bugarcic A, et al. 2008. Human and mouse macrophage-inducible Ctype lectin (Mincle) bind Candida albicans. Glycobiology 18:679-685.
14. Calderone RA, Fonzi WA. 2001. Virulence factors of Candida albicans. Trends Microbiol. 9:327-335.
15. Cambi A, et al. 2003. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur. J. Immunol. 33:532-538.
16. Cambi A, et al. 2008. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J. Biol. Chem. 283:20590-20599.
17. Cheng SC, et al. 2010. Candida albicans releases soluble factors that potentiate cytokine production by human cells through a proteaseactivated receptor 1-and 2-independent pathway. Infect. Immun. 78: 393-399.
18. Cheng SC, et al. 4 January 2012, posting date. Complement plays a central role in Candida albicans-induced cytokine production by human PBMCs. Eur. J. Immunol. doi:10.1002/eji.201142057.
19. Cheng SC, et al. 2011. The dectin-1/inflammasome pathway is responsible for the induction of protective T-helper 17 responses that discriminate between yeasts and hyphae of Candida albicans. J. Leukoc. Biol. 90:357-366.
20. Cheng SC, et al. 2010. Candida albicans dampens host defense by downregulating IL-17 production. J. Immunol. 185:2450-2457.
21. Conti HR, et al. 2011. New mechanism of oral immunity to mucosal candidiasis in hyper-IgE syndrome. Mucosal Immunol. 4:448-455.
22. Conti HR, et al. 2009. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med. 206: 299-311.
23. Decanis N, Savignac K, Rouabhia M. 2009. Farnesol promotes epithelial cell defense against Candida albicans through Toll-like receptor 2 expression, interleukin-6 and human beta-defensin 2 production. Cytokine 45:132-140.
24. De Luca A, et al. 2010. IL-22 defines a novel immune pathway of antifungal resistance. Mucosal Immunol. 3:361-373.
25. d'Ostiani CF, et al. 2000. 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. 191:1661-1674.
26. Eyerich S, 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.
27. Fernandez-Arenas E, et al. 2009. Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cell. Microbiol. 11:560-589.
28. Ferwerda B, et al. 2009. Human dectin-1 deficiency and mucocutaneous fungal infections. N. Engl. J. Med. 361:1760-1767.
29. Fidel PL, Jr. 2002. Distinct protective host defenses against oral and vaginal candidiasis. Med. Mycol. 40:359-375.
30. Fidel PL, Jr. 2011. Candida-host interactions in HIV disease: implications for oropharyngeal candidiasis. Adv. Dent. Res. 23:45-49.
31. Fidel PL, Jr, 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.
32. Filler SG. 2006. Candida-host cell receptor-ligand interactions. Curr. Opin. Microbiol. 9:333-339.
33. Fradin C, et al. 2005. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 56:397-415.
34. Frohner IE, Bourgeois C, Yatsyk K, Majer O, Kuchler K. 2009. Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 71:240-252.
35. Gantner BN, Simmons RM, Underhill DM. 2005. Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J. 24:1277-1286.
36. Ghosh S, et al. 2010. Candida albicans cell wall components and farnesol stimulate the expression of both inflammatory and regulatory cytokines in the murine RAW264.7 macrophage cell line. FEMS Immunol. Med. Microbiol. 60:63-73.
37. Ghosh S, et al. 2009. Arginine-induced germ tube formation in Candida albicans is essential for escape from murine macrophage lineRAW264.7. Infect. Immun. 77:1596-1605.
38. Glocker EO, et al. 2009. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N. Engl. J. Med. 361:1727-1735.
39. Gow NA, et al. 2007. Immune recognition of Candida albicans betaglucan by dectin-1. J. Infect. Dis. 196:1565-1571.
40. Gropp K, et al. 2009. The yeast Candida albicans evades human complement attack by secretion of aspartic proteases. Mol. Immunol. 47: 465-475.
41. Gross O, et al. 2009. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defense. Nature 459:433-436.
42. Hajjeh RA, et al. 2004. Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J. Clin. Microbiol. 42:1519-1527.
43. Hise AG, et al. 2009. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5:487-497.
44. Hornby JM, et al. 2001. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67: 2982-2992.
45. Huang W, Na L, Fidel PL, Schwarzenberger P. 2004. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190:624-631.
46. Joly S, et al. 2009. Cutting edge: Candida albicans hyphae formation triggers activation of the Nlrp3 inflammasome. J. Immunol. 183:3578-3581.
47. Jouault T, et al. 2006. Specific recognition of Candida albicans by macrophages requires galectin-3 to discriminate Saccharomyces cerevisiae and needs association with TLR2 for signaling. J. Immunol. 177:4679-4687.
48. Jouault T, et al. 2003. Candida albicans phospholipomannan is sensed through toll-like receptors. J. Infect. Dis. 188:165-172.
49. Kankkunen P, et al. 2010. (1,3)-Beta-glucans activate both dectin-1 and NLRP3 inflammasome in human macrophages. J. Immunol. 184:6335-6342.
50. Kasperkovitz PV, et al. 2011. Toll-like receptor 9 modulates macrophage antifungal effector function during innate recognition of Candida albicans and Saccharomyces cerevisiae. Infect. Immun. 79:4858-4867.
51. Kullberg BJ, Netea MG, Vonk AG, Van der Meer JW. 1999. Modulation of neutrophil function in host defense against disseminated Candida albicans infection in mice. FEMS Immunol. Med. Microbiol. 26:299-307.
52. Kumar H, et al. 2009. Involvement of the NLRP3 inflammasome in innate and humoral adaptive immune responses to fungal beta-glucan. J. Immunol. 183:8061-8067.
53. Li M, Chen Q, Tang R, Shen Y, Liu WD. 2011. The expression of beta-defensin-2,3 and LL-37 induced by Candida albicans phospholipomannan in human keratinocytes. J. Dermatol. Sci. 61:72-75.
54. Lieschke GJ, Burgess AW. 1992. Granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor. N. Engl. J. Med. 327:99-106.
55. Lilly EA, Leigh JE, Joseph SH, Fidel PL, Jr. 2006. Candida-induced oral epithelial cell responses. Mycopathologia 162:25-32.
56. Lo HJ, et al. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90:939-949.
57. Lu Q, Jayatilake JA, Samaranayake LP, Jin L. 2006. Hyphal invasion of Candida albicans inhibits the expression of human beta-defensins in experimental oral candidiasis. J. Invest. Dermatol. 126:2049-2056.
58. Luo S, et al. 2011. The pH-regulated antigen 1 of Candida albicans binds the human complement inhibitor C4b-binding protein and mediates fungal complement evasion. J. Biol. Chem. 286:8021-8029.
59. Luo S, Hartmann A, Dahse HM, Skerka C, Zipfel PF. 2010. Secreted pH-regulated antigen 1 of Candida albicans blocks activation and conversion of complement C3. J. Immunol. 185:2164-2173.
60. Luo S, Poltermann S, Kunert A, Rupp S, Zipfel PF. 2009. Immune evasion of the human pathogenic yeast Candida albicans: Pra1 is a Factor H, FHL-1 and plasminogen binding surface protein. Mol. Immunol. 47:541-550.
61. Marcil A, Harcus D, Thomas DY, Whiteway M. 2002. Candida albicans killing by RAW 264.7 mouse macrophage cells: effects of Candida genotype, infection ratios, and gamma interferon treatment. Infect. Immun. 70:6319-6329.
62. Marodi L, Korchak HM, Johnston RB, Jr. 1991. Mechanisms of host defense against Candida species. I. Phagocytosis by monocytes and monocyte-derived macrophages. J. Immunol. 146:2783-2789.
63. McGreal EP, et al. 2006. The carbohydrate-recognition domain of dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 16:422-430.
64. McKenzie CG, et al. 2010. Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect. Immun. 78:1650-1658.
65. Means TK, et al. 2009. Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J. Exp. Med. 206:637-653.
66. Medzhitov R, Janeway CA, Jr. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295-298.
67. Mencacci A, et al. 2000. Interleukin 18 restores defective Th1 immunity to Candida albicans in caspase 1-deficient mice. Infect. Immun. 68:5126-5131.
68. Meri T, et al. 2004. The hyphal and yeast forms of Candida albicans bind the complement regulator C4b-binding protein. Infect. Immun. 72: 6633-6641.
69. Meri T, et al. 2002. The yeast Candida albicans binds complement regulators factor H and FHL-1. Infect. Immun. 70:5185-5192.
70. Miyazato A, et al. 2009. Toll-like receptor 9-dependent activation of myeloid dendritic cells by deoxynucleic acids from Candida albicans. Infect. Immun. 77:3056-3064.
71. Moretti S, et al. 2008. The contribution of PARs to inflammation and immunity to fungi. Mucosal Immunol. 1:156-168.
72. Moyes DL, et al. 2010. A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of Candida albicans in epithelial cells. Cell Host Microbe 8:225-235.
73. Mullick A, et al. 2004. Dysregulated inflammatory response to Candida albicans in a C5-deficient mouse strain. Infect. Immun. 72:5868-5876.
74. Murad AM, et al. 2001. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20: 4742-4752.
75. Murciano C, et al. 2011. Candida albicans cell wall glycosylation may be indirectly required for activation of epithelial cell proinflammatory responses. Infect. Immun. 79:4902-4911.
76. Nakagawa Y, Kanbe T, Mizuguchi I. 2003. Disruption of the human pathogenic yeast Candida albicans catalase gene decreases survival in mouse-model infection and elevates susceptibility to higher temperature and to detergents. Microbiol. Immunol. 47:395-403.
77. Navarathna DH, Nickerson KW, Duhamel GE, Jerrels TR, Petro TM. 2007. Exogenous farnesol interferes with the normal progression of cytokine expression during candidiasis in a mouse model. Infect. Immun. 75:4006-4011.
78. Netea MG, Brown GD, Kullberg BJ, Gow NA. 2008. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6:67-78.
79. Netea MG, et al. 2006. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J. Clin. Invest. 116:1642-1650.
80. Netea MG, Marodi L. 2010. Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol. 31:346-353.
81. Netea MG, van de Veerdonk F, Verschueren I, Van der Meer JW, Kullberg BJ. 2008. Role of TLR1 and TLR6 in the host defense against disseminated candidiasis. FEMS Immunol. Med. Microbiol. 52:118-123.
82. Netea MG, et al. 1999. Increased susceptibility of TNF-alpha lymphotoxin-alpha double knockout mice to systemic candidiasis through impaired recruitment of neutrophils and phagocytosis of Candida albicans. J. Immunol. 163:1498-1505.
83. Newman SL, Bhugra B, Holly A, Morris RE. 2005. Enhanced killing of Candida albicans by human macrophages adherent to type 1 collagen matrices via induction of phagolysosomal fusion. Infect. Immun. 73: 770-777.
84. Palmer GE. 2011. Vacuolar trafficking and Candida albicans pathogenesis. Commun. Integr. Biol. 4:240-242.
85. Palmer GE, Kelly MN, Sturtevant JE. 2005. The Candida albicans vacuole is required for differentiation and efficient macrophage killing. Eukaryot. Cell 4:1677-1686.
86. Peltz G, et al. 2011. Next-generation computational genetic analysis: multiple complement alleles control survival after Candida albicans infection. Infect. Immun. 79:4472-4479.
87. Phan QT, et al. 2007. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 5:e64.
88. Poltermann S, et al. 2007. Gpm1p is a factor H-, FHL-1-, and plasminogen-binding surface protein of Candida albicans. J. Biol. Chem. 282: 37537-37544.
89. Puel A, et al. 2011. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332:65-68.
90. Qian Q, Jutila MA, Van Rooijen N, Cutler JE. 1994. Elimination of mouse splenic macrophages correlates with increased susceptibility to experimental disseminated candidiasis. J. Immunol. 152:5000-5008.
91. Ray TL, Payne CD. 1988. Scanning electron microscopy of epidermal adherence and cavitation in murine candidiasis: a role for Candida acid proteinase. Infect. Immun. 56:1942-1949.
92. Romani L, et al. 1996. Impaired neutrophil response and CD4+ T helper cell 1 development in interleukin 6-deficient mice infected with Candida albicans. J. Exp. Med. 183:1345-1355.
93. Saijo S, et al. 2010. Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32:681-691.
94. Sasada M, et al. 1987. Candidacidal activity of monocyte-derived human macrophages: relationship between Candida killing and oxygen radical generation by human macrophages. J. Leukoc. Biol. 41:289-294.
95. Sato K, et al. 2006. 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. 281:38854-38866.
96. Schaller M, et al. 2004. Polymorphonuclear leukocytes (PMNs) induce protective Th1-type cytokine epithelial responses in an in vitro model of oral candidosis. Microbiology 150:2807-2813.
97. Schwarzenberger P, et al. 1998. IL-17 stimulates granulopoiesis in mice: use of an alternate, novel gene therapy-derived method for in vivo evaluation of cytokines. J. Immunol. 161:6383-6389.
98. Sealy PI, Garner B, Swiatlo E, Chapman SW, Cleary JD. 2008. The interaction of mannose binding lectin (MBL) with mannose containing glycopeptides and the resultant potential impact on invasive fungal infection. Med. Mycol. 46:531-539.
99. Soloviev DA, Jawhara S, Fonzi WA. 2011. Regulation of innate immune response to Candida albicans infections by αMβ2-Pra1p interaction. Infect. Immun. 79:1546-1558.
100. Steele C, Leigh J, Swoboda R, Fidel PL, Jr. 2000. Growth inhibition of Candida by human oral epithelial cells. J. Infect. Dis. 182:1479-1485.
101. Tada H, et al. 2002. Saccharomyces cerevisiae-and Candida albicansderived mannan induced production of tumor necrosis factor alpha by human monocytes in a CD14-and Toll-like receptor 4-dependent manner. Microbiol. Immunol. 46:503-512.
102. Tang N, et al. 2004. Inhibition of monocytic interleukin-12 production by Candida albicans via selective activation of ERK mitogen-activated protein kinase. Infect. Immun. 72:2513-2520.
103. Tavanti A, et al. 2006. Candida albicans isolates with different genomic backgrounds display a differential response to macrophage infection. Microbes Infect. 8:791-800.
104. Urban CF, et al. 2009. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5:e1000639.
105. van de Veerdonk FL, et al. 2009. The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5:329-340.
106. van de Veerdonk F, et al. 2008. Redundant role of TLR9 for anti-Candida host defense. Immunobiology 213:613-620.
107. van de Veerdonk F, et al. 2011. STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N. Engl. J. Med. 365:54-61.
108. van Enckevort FH, et al. 1999. Increased susceptibility to systemic candidiasis in interleukin-6 deficient mice. Med. Mycol. 37:419-426.
109. van 't Wout JW, Linde I, Leijh PC, van Furth R. 1988. Contribution of granulocytes and monocytes to resistance against experimental disseminated Candida albicans infection. Eur. J. Clin. Microbiol. Infect. Dis. 7:736-741.
110. Vazquez-Torres A, Jones-Carson J, Balish E. 1996. Peroxynitrite contributes to the candidacidal activity of nitric oxide-producing macrophages. Infect. Immun. 64:3127-3133.
111. Wachtler B, Wilson D, Haedicke K, Dalle F, Hube B. 2011. From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS One 6:e17046.
112. Wang M, et al. 2008. Characterization and partial purification of Candida albicans secretory IL-12 inhibitory factor. BMC Microbiol. 8:31.
113. Weindl G, et al. 2007. Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J. Clin. Invest. 117:3664-3672.
114. Wellington M, Dolan K, Krysan DJ. 2009. Live Candida albicans suppresses production of reactive oxygen species in phagocytes. Infect. Immun. 77:405-413.
115. Westwater C, Balish E, Schofield DA. 2005. Candida albicansconditioned medium protects yeast cells from oxidative stress: a possible link between quorum sensing and oxidative stress resistance. Eukaryot. Cell 4:1654-1661.
116. Wheeler RT, Kombe D, Agarwala SD, Fink GR. 2008. Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog. 4:e1000227.
117. Whiteway M, Bachewich C. 2007. Morphogenesis in Candida albicans. Annu. Rev. Microbiol. 61:529-553.
118. Wisplinghoff H, et al. 2004. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39:309-317.
119. Xiong J, et al. 2000. Candida albicans and Candida krusei differentially induce human blood mononuclear cell interleukin-12 and gamma interferon production. Infect. Immun. 68:2464-2469.
120. 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.
121. Ye P, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194:519-527.
122. Zakikhany K, et al. 2007. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell. Microbiol. 9:2938-2954.
123. Zhang MX, Kozel TR. 1998. Mannan-specific immunoglobulin G antibodies in normal human serum accelerate binding of C3 to Candida albicans via the alternative complement pathway. Infect. Immun. 66: 4845-4850.
124. Zhang MX, Lupan DM, Kozel TR. 1997. Mannan-specific immunoglobulinGantibodies in normal human serum mediate classical pathway initiation of C3 binding to Candida albicans. Infect. Immun. 65:3822-3827.