Mannosylation in candida albicans: Role in cell wall function and immune recognition

Molecular Microbiology

Volumn 90, Issue 6, 2013, Pages 1147-1161

  Hall, Rebecca A ^a   Gow, Neil A R ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL POLYSACCHARIDE; MANNAN; MANNOPROTEIN; MANNOSIDE;

ANTIGEN RECOGNITION; BIOSYNTHESIS; CANDIDA ALBICANS; CELL WALL; CHEMICAL MODIFICATION; DISEASE MARKER; FUNGAL PHENOMENA AND FUNCTIONS; FUNGUS CELL INTERACTION; FUNGUS MUTANT; HOST; HUMAN; IMMUNE RESPONSE; MANNOSYLATION; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW;

CANDIDA ALBICANS; FUNGI;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CELL WALL; FUNGAL PROTEINS; GLYCOSYLATION; HUMANS; IMMUNITY, INNATE; MANNANS; MANNOSIDES; MEMBRANE GLYCOPROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRULENCE FACTORS;

EID: 84890116565     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12426     Document Type: Review

References (116)

1. Alam, F., Mustafa, A., and Khan, Z. (2007) Comparative evaluation of (1, 3)-beta-D-glucan, mannan and anti-mannan antibodies, and Candida species-specific snPCR in patients with candidemia. BMC Infect Dis 7: 103.
2. Almirante, B., Rodríguez, D., Park, B.J., Cuenca-Estrella, M., Planes, A.M., Almela, M., etal. (2005) Epidemiology and predictors of mortality in cases of Candida bloodstream infection: results from population-based surveillance, Barcelona, Spain, from 2002 to 2003. J Clin Microbiol 43: 1829-1835.
3. Arendrup, M.C., Bergmann, O.J., Larsson, L., Nielsen, H.V., Jarløv, J.O., and Christensson, B. (2010) Detection of candidaemia in patients with and without underlying haematological disease. Clin Microbiol Infect 16: 855-862.
4. Ariizumi, K., Shen, G.-L., Shikano, S., Xu, S., Ritter, R., Kumamoto, T., etal. (2000) Identification of a novel, dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning. J Biol Chem 275: 20157-20167.
5. Bai, C., Xu, X.-L., Chan, F.-Y., Lee, R.T.H., and Wang, Y. (2006) MNN5 encodes an iron-regulated alpha-1, 2-mannosyltransferase important for protein glycosylation, cell wall integrity, morphogenesis, and virulence in Candida albicans. Eukaryot Cell 5: 238-247.
6. Bailey, J.W., Sada, E., Brass, C., and Bennett, J.E. (1985) Diagnosis of systemic candidiasis by latex agglutination for serum antigen. J Clin Microbiol 21: 749-752.
7. 2+-ATPase, is required for glycosylation and virulence. J Biol Chem 280: 23408-23415.
8. Bates, S., Hughes, H.B., Munro, C.A., Thomas, W.P.H., MacCallum, D.M., Bertram, G., etal. (2006) Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem 281: 90-98.
9. Bates, S., Hall, R.A., Cheetham, J., Netea, M.G., MacCallum, D.M., Brown, A.J.P., etal. (2013) Role of the Candida albicans MNN1 gene family in cell wall structure and virulence. BMC Res Notes 6: 249.
10. Bowman, S.M., and Free, S.J. (2006) The structure and synthesis of the fungal cell wall. Bioessays 28: 799-808.
11. Brown, G.D., and Gordon, S. (2001) Immune recognition: a new receptor for [beta]-glucans. Nature 413: 36-37.
12. Buurman, E.T., Westwater, C., Hube, B., Brown, A.J.P., Odds, F.C., and Gow, N.A.R. (1998) Molecular analysis of CaMnt1p, a mannosyl transferase important for adhesion and virulence of Candida albicans. Proc Natl Acad Sci USA 95: 7670-7675.
13. Cambi, A., Gijzen, K., de Vries, I.J.M., Torensma, R., Joosten, B., Adema, G.J., etal. (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.
14. Cambi, A., Netea, M.G., Mora-Montes, H.M., Gow, N.A.R., Hato, S.V., Lowman, D.W., etal. (2008) Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J Biol Chem 283: 20590-20599.
15. Cantero, P.D., and Ernst, J.F. (2011) Damage to the glycoshield activates PMT-directed O-mannosylation via the Msb2-Cek1 pathway in Candida albicans. Mol Microbiol 80: 715-725.
16. Corbucci, C., Cenci, E., Skrzypek, F., Gabrielli, E., Mosci, P., Ernst, J.F., etal. (2007) Immune response to Candida albicans is preserved despite defect in O-mannosylation of secretory proteins. Med Mycol 45: 709-719.
17. Díaz-Jiménez, D.F., Mora-Montes, H.M., Hernández-Cervantes, A., Luna-Arias, J.P., Gow, N.A.R., and Flores-Carreón, A. (2012) Biochemical characterization of recombinant Candida albicans mannosyltransferases Mnt1, Mnt2 and Mnt5 reveals new functions in O- and N-mannan biosynthesis. Biochem Biophys Res Commun 419: 77-82.
18. Douglas, C.M., D'Ippolito, J.A., Shei, G.J., Meinz, M., Onishi, J., Marrinan, J.A., etal. (1997) Identification of the FKS1 gene of Candida albicans as the essential target of 1, 3-beta-D-glucan synthase inhibitors. Antimicrob Agents Chemother 41: 2471-2479.
19. Dünkler, A., Walther, A., Specht, C.A., and Wendland, J. (2005) Candida albicans CHT3 encodes the functional homolog of the Cts1 chitinase of Saccharomyces cerevisiae. Fungal Genet Biol 42: 935-947.
20. Ellis, M., Al-Ramadi, B., Bernsen, R., Kristensen, J., Alizadeh, H., and Hedstrom, U. (2009) Prospective evaluation of mannan and anti-mannan antibodies for diagnosis of invasive Candida infections in patients with neutropenic fever. J Med Microbiol 58: 606-615.
21. Ene, I.V., Adya, A.K., Wehmeier, S., Brand, A.C., MacCallum, D.M., Gow, N.A.R., and Brown, A.J.P. (2012) Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell Microbiol 14: 1319-1335.
22. Ernst, J.F., and Pla, J. (2011) Signaling the glycoshield: maintenance of the Candida albicans cell wall. Int J Med Microbiol 301: 378-383.
23. Fontaine, T., Simenel, C., Dubreucq, G., Adam, O., Delepierre, M., Lemoine, J., etal. (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem 275: 27594-27607.
24. Fradin, C., Poulain, D., and Jouault, T. (2000) beta -1, 2-linked oligomannosides from Candida albicans bind to a 32-Kilodalton macrophage membrane protein homologous to the mammalian lectin Galectin-3. Infect Immun 68: 4391-4398.
25. Fukazawa, Y. (1989) Antigenic structure of Candida albicans immunochemical basis of the serologic specificity of the mannans in yeasts. Immunol Ser 47: 37-62.
26. Garey, K.W., Rege, M., Pai, M.P., Mingo, D.E., Suda, K.J., Turpin, R.S., and Bearden, D.T. (2006) Time to initiation of fluconazole therapy impacts mortality in patients with candidemia: a multi-institutional study. Clin Infect Dis 43: 25-31.
27. Gasparoto, T.H., Tessarolli, V., Garlet, T.P., Torres, S.A., Garlet, G.P., da Silva, J.S., and Campanelli, A.P. (2010) Absence of functional TLR4 impairs response of macrophages after Candida albicans infection. Med Mycol 48: 1009-1017.
28. Gow, N.A., and Hube, B. (2012) Importance of the Candida albicans cell wall during commensalism and infection. Curr Opin Microbiol 15: 406-412.
29. Gregori, C., Glaser, W., Frohner, I.E., Reinoso-Martín, C., Rupp, S., Schüller, C., and Kuchler, K. (2011) Efg1 controls caspofungin-induced cell aggregation of Candida albicans through the adhesin Als1. Eukaryot Cell 10: 1694-1704.
30. Hall, R.A., Bates, S., Lenardon, M.D., MacCallum, D.M., Wagener, J., Lowman, D.W., etal. (2013) The Mnn2 mannosyltransferase family modulates mannoprotein fibril length, immune recognition and virulence of Candida albicans. PLoS Pathog 9: e1003276.
31. Hashimoto, H., and Yoda, K. (1997) Novel membrane protein complexes for protein glycosylation in the yeast Golgi apparatus. Biochem Biophys Res Commun 241: 682-686.
32. Hazen, K.C., Singleton, D.R., and Masuoka, J. (2007) Influence of outer region mannosylphosphorylation on N-glycan formation by Candida albicans: normal acid-stable N-glycan formation requires acid-labile mannosylphosphate addition. Glycobiology 17: 1052-1060.
33. Hobson, R.P., Munro, C.A., Bates, S., MacCallum, D.M., Cutler, J.E., Heinsbroek, S.E.M., etal. (2004) Loss of cell wall mannosylphosphate in Candida albicans does not influence macrophage recognition. J Biol Chem 279: 39628-39635.
34. Hoyer, L.L. (2001) The ALS gene family of Candida albicans. Trends Microbiol 9: 176-180.
35. Jacquinot, P.M., Plancke, Y., Sendid, B., Strecker, G., and Poulain, D. (1998) Nature of Candida albicans-derived carbohydrate antigen recognized by a monoclonal antibody in patient sera and distribution over Candida species. FEMS Microbiol Lett 169: 131-138.
36. Jones, J.M. (1990) Laboratory diagnosis of invasive candidiasis. Clin Microbiol Rev 3: 32-45.
37. Jouault, T., Bernigaud, A., Lepage, G., Trinel, P.A., and Poulain, D. (1994) The Candida albicans phospholipomannan induces in vitro production of tumour necrosis factor-α from human and murine macrophages. Immunology 83: 268-273.
38. Jouault, T., Fradin, C., Trinel, P.-A., Bernigaud, A., and Poulain, D. (1998) Early signal transduction induced by Candida albicans in macrophages through shedding of a glycolipid. J Infect Dis 178: 792-802.
39. Jouault, T., Ibata-Ombetta, S., Takeuchi, O., Trinel, P.-A., Sacchetti, P., Lefebvre, P., etal. (2003) Candida albicans phospholipomannan is sensed through Toll-like receptors. J Infect Dis 188: 165-172.
40. Jouault, T., El Abed-El Behi, M., Martínez-Esparza, M., Breuilh, L., Trinel, P., Chamaillard, M., etal. (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.
41. Jungmann, J., and Munro, S. (1998) Multi-protein complexes in the cis Golgi of Saccharomyces cerevisiae with [alpha]-1, 6-mannosyltransferase activity. EMBO J 17: 423-434.
42. Karson, E.M., and Ballou, C.E. (1978) Biosynthesis of yeast mannan. Properties of a mannosylphosphate transferase in Saccharomyces cerevisiae. J Biol Chem 253: 6484-6492.
43. Kelleher, D.J., and Gillmore, R. (2006) An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16: 47-62.
44. Keppler-Ross, S., Douglas, L., Konopka, J.B., and Dean, N. (2010) Recognition of yeast by murine macrophages requires mannan but not glucan. Eukaryot Cell 9: 1776-1787.
45. Kéry, V., Krepinský, J.J., Warren, C.D., Capek, P., and Stahl, P. (1992) Ligand recognition by purified human mannose receptor. Arch Biochem Biophys 298: 49-55.
46. Klevay, M.J., Ernst, E.J., Hollanbaugh, J.L., Miller, J.G., Pfaller, M.A., and Diekema, D.J. (2008) Therapy and outcome of Candida glabrata versus Candida albicans bloodstream infection. Diagn Microbiol Infect Dis 60: 273-277.
47. Kohatsu, L., Hsu, D.K., Jegalian, A.G., Liu, F.-T., and Baum, L.G. (2006) Galectin-3 induces death of Candida species expressing specific beta1, 2-linked mannans. J Immunol 177: 4718-4726.
48. Kozel, T., and Bauman, S. (2012) CrAg lateral flow assay for cryptococcosis. Expert Opin Med Diagn 6: 245-251.
49. Kruppa, M., Greene, R.R., Noss, I., Lowman, D.W., and Williams, D.L. (2011) C. albicans increases cell wall mannoprotein, but not mannan, in response to blood, serum and cultivation at physiological temperature. Glycobiology 21: 1173-1180.
50. Latgé, J., Kobayashi, H., and Debeaupuis, J. (1994) Chemical and immunological characterization of the galactomannan secreted by Aspergillus fumigatus. Infect Immun 62: 5424-5433.
51. Latgé, J.-P. (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66: 279-290.
52. Leitão, E.A., Bittencourt, V.C.B., Haido, R.M.T., Valente, A.P., Peter-Katalinic, J., Letzel, M., etal. (2003) β-Galactofuranose-containing O-linked oligosaccharides present in the cell wall peptidogalactomannan of Aspergillus fumigatus contain immunodominant epitopes. Glycobiology 13: 681-692.
53. Lemieux, C., St-Germain, G., Vincelette, J., Kaufman, L., and de Repentigny, L. (1990) Collaborative evaluation of antigen detection by a commercial latex agglutination test and enzyme immunoassay in the diagnosis of invasive candidiasis. J Clin Microbiol 28: 249-253.
54. Leroy, O., Gangneux, J.-P., Montravers, P., Mira, J.-P., Gouin, F., Sollet, J.-P., etal. (2009) Epidemiology, management, and risk factors for death of invasive Candida infections in critical care: a multicenter, prospective, observational study in France (2005-2006). Crit Care Med 37: 1612-1618.
55. Lewis, L.E., Bain, J.M., Lowes, C., Gillespie, C., Rudkin, F.M., Gow, N.A.R., and Erwig, L.-P. (2012) Stage specific assessment of Candida albicans phagocytosis by macrophages identifies cell wall composition and morphogenesis as key determinants. PLoS Pathog 8: e1002578.
56. Li, M., Chen, Q., Shen, Y., and Liu, W. (2009) Candida albicans phospholipomannan triggers inflammatory responses of human keratinocytes through Toll-like receptor 2. Exp Dermatol 18: 603-610.
57. Linden, J.R., Kunkel, D., Laforce-Nesbitt, S.S., and Bliss, J.M. (2013) The role of galectin-3 in phagocytosis of Candida albicans and Candida parapsilosis by human neutrophils. Cell Microbiol 15: 1127-1142.
58. Lowman, D.W., Ensley, H.E., Greene, R.R., Knagge, K.J., Williams, D.L., and Kruppa, M.D. (2011) Mannan structural complexity is decreased when Candida albicans is cultivated in blood or serum at physiological temperature. Carbohydr Res 346: 2752-2759.
59. McGreal, E.P., Rosas, M., Brown, G.D., Zamze, S., Wong, S.Y.C., Gordon, S., etal. (2006) The carbohydrate-recognition domain of Dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 16: 422-430.
60. McKenzie, C.G.J., Koser, U., Lewis, L.E., Bain, J.M., Mora-Montes, H.M., Barker, R.N., etal. (2010) Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect Immun 78: 1650-1658.
61. Martínez-Pomares, L., Mahoney, J.A., Káposzta, R., Linehan, S.A., Stahl, P.D., and Gordon, S. (1998) A functional soluble form of the murine mannose receptor is produced by macrophages in vitro and is present in mouse serum. J Biol Chem 273: 23376-23380.
62. Medzhitov, R., Preston-Hurlburt, P., and Janeway, C.J. (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
63. Mikulska, M., Calandra, T., Sanguinetti, M., Poulain, D., Viscoli, C., and the Third European Conference on Infections in Leukemia Group (2010) The use of mannan antigen and anti-mannan antibodies in the diagnosis of invasive candidiasis: recommendations from the Third European Conference on Infections in Leukemia. Crit Care 14: R222.
64. Mille, C., Janbon, G., Delplace, F., Ibata-Ombetta, S., Gaillardin, C., Strecker, G., etal. (2004) Inactivation of CaMIT1 inhibits Candida albicans phospholipomannan beta-mannosylation, reduces virulence, and alters cell wall protein beta-mannosylation. J Biol Chem 279: 47952-47960.
65. Mille, C., Bobrowicz, P., Trinel, P.A., Li, H., Maes, E., Guerardel, Y., etal. (2008) Identification of a new family of genes involved in beta-1, 2-mannosylation of glycans in Pichia pastoris and Candida albicans. J Biol Chem 283: 9724-9736.
66. Mille, C., Fradin, C., Delplace, F., Trinel, P.-A., Masset, A., François, N., etal. (2012) Members 5 and 6 of the Candida albicans BMT family encode enzymes acting specifically on β-mannosylation of the phospholipomannan cell-wall glycosphingolipid. Glycobiology 22: 1332-1342.
67. Miyazato, A., Nakamura, K., Yamamoto, N., Mora-Montes, H.M., Tanaka, M., Abe, Y., etal. (2009) Toll-like receptor 9-dependent activation of myeloid dendritic cells by deoxynucleic acids from Candida albicans. Infect Immun 77: 3056-3064.
68. Mokaddas, E., Burhamah, M., Khan, Z., and Ahmad, S. (2010) Levels of (1-3)-beta-D-glucan, Candida mannan and Candida DNA in serum samples of pediatric cancer patients colonized with Candida species. BMC Infect Dis 10: 292.
69. Mokaddas, E., Khan, Z.U., Ahmad, S., Nampoory, M.R.N., and Burhamah, M. (2011) Value of (1-3)-β-D-glucan, Candida mannan and Candida DNA detection in the diagnosis of candidaemia. Clin Microbiol Infect 17: 1549-1553.
70. Mora-Montes, H.M., Bates, S., Netea, M.G., Diaz-Jimenez, D.F., Lopez-Romero, E., Zinker, S., etal. (2007) Endoplasmic Reticulum alpha-glycosidases of Candida albicans are required for N-glycosylation, cell wall integrity, and normal host-fungus interaction. Eukaryot. Cell 6: 2184-2193.
71. Mora-Montes, H.M., Ponce-Noyola, P., Villagómez-Castro, J.C., Gow, N.A.R., Flores-Carreón, A., and López-Romero, E. (2009) Protein glucosylation in Candida. Future Microbiol 4: 1167-1183.
72. Mora-Montes, H.M., Bates, S., Netea, M.G., Castillo, L., Brand, A., Buurman, E.T., etal. (2010) A multifunctional mannosyltransferase family in Candida albicans determines cell wall mannan structure and host-fungus interactions. J Biol Chem 285: 12087-12095.
73. Morelle, W., Bernard, M., Debeaupuis, J.-P., Buitrago, M., Tabouret, M., and Latgé, J.-P. (2005) Galactomannoproteins of Aspergillus fumigatus. Eukaryot Cell 4: 1308-1316.
74. Munro, C.A., Bates, S., Buurman, E.T., Hughes, H.B., MacCallum, D.M., Bertram, G., etal. (2005) Mnt1p and Mnt2p of Candida albicans are partially redundant alpha-1, 2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. J Biol Chem 280: 1051-1060.
75. Murciano, C., Moyes, D.L., Runglall, M., Islam, A., Mille, C., Fradin, C., etal. (2011) Candida albicans cell wall glycosylation may be indirectly required for activation of epithelial cell proinflammatory responses. Infect Immun 79: 4902-4911.
76. Nakayama, K., Feng, Y., Tanaka, A., and Jigami, Y. (1998) The involvement of mnn4 and mnn6 mutations in mannosylphosphorylation of O-linked oligosaccharide in yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1425: 255-262.
77. Netea, M.G., Gow, N.A.R., Munro, C.A., Bates, S., Collins, C., Ferwerda, G., etal. (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.
78. Netea, M.G., Brown, G.D., Kullberg, B.J., and Gow, N.A.R. (2008) An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 6: 67-78.
79. Netea, M.G., Gow, N.A.R., Joosten, L.A.B., Verschueren, I., van der Meer, J.W.M., and Kullberg, B.J. (2010) Variable recognition of Candida albicans strains by TLR4 and lectin recognition receptors. Med Mycol 48: 897-903.
80. Nihtinen, A., Anttila, V.J., Richardson, M., Ruutu, T., Juvonen, E., Meri, T., and Volin, L. (2011) Factors influencing the performance level of Candida mannan antigen testing in allogeneic stem cell transplant recipients not receiving fluconazole prophylaxis. Transpl Infect Dis 13: 266-272.
81. Nobile, C.J., Nett, J.E., Andes, D.R., and Mitchell, A.P. (2006) Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot Cell 5: 1604-1610.
82. O'Meara, T.R., and Alspaugh, J.A. (2012) The Cryptococcus neoformans capsule: a sword and a shield. Clin Microbiol Rev 25: 387-408.
83. Odani, T., Shimma, Y., Tanaka, A., and Jigami, Y. (1996) Cloning and analysis of the MNN4 gene required for phosphorylation of N-linked oligosaccharides in Saccharomyces cerevisiae. Glycobiology 6: 805-810.
84. Odani, T., Shimma, Y., Wang, X.H., and Jigami, Y. (1997) Mannosylphosphate transfer to cell wall mannan is regulated by the transcriptional level of the MNN4 gene in Saccharomyces cerevisiae. FEBS Lett 420: 186-190.
85. Odds, F.C., and Evans, E.G. (1980) Distribution of pathogenic yeasts and humoral antibodies to candida among hospital inpatients. J Clin Pathol 33: 750-756.
86. Peltroche-Llacsahuanga, H., Goyard, S., d'Enfert, C., Prill, S.K.H., and Ernst, J.F. (2006) Protein O-mannosyltransferase isoforms regulate biofilm formation in Candida albicans. Antimicrob Agents Chemother 50: 3488-3491.
87. Porcaro, I., Vidal, M., Jouvert, S., Stahl, P.D., and Giaimis, J. (2003) Mannose receptor contribution to Candida albicans phagocytosis by murine E-clone J774 macrophages. J Leukoc Biol 74: 206-215.
88. Prill, S.K.H., Klinkert, B., Timpel, C., Gale, C.A., Schröppel, K., and Ernst, J.F. (2005) PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol Microbiol 55: 546-560.
89. Rohrlich, P., Sarfati, J., Mariani, P., Duval, M., Carol, A., Saint-Martin, C., etal. (1996) Prospective sandwich enzyme-linked immunosorbent assay for serum galactomannan: early predictive value and clinical use in invasive aspergillosis. Pediatr Infect Dis J 15: 232-237.
90. Romero, P.A., Lussier, M., Veronneau, S., Sdicu, A.-M., Herscovics, A., and Bussey, H. (1999) Mnt2p and Mnt3p of Saccharomyces cerevisiae are members of the Mnn1p family of α-1, 3-mannosyltransferases responsible for adding the terminal mannose residues of O-linked oligosaccharides. Glycobiology 9: 1045-1051.
91. Rouabhia, M., Schaller, M., Corbucci, C., Vecchiarelli, A., Prill, S.K.-H., Giasson, L., and Ernst, J.F. (2005) Virulence of the fungal pathogen Candida albicans requires the five isoforms of protein mannosyltransferases. Infect Immun 73: 4571-4580.
92. Saijo, S., Ikeda, S., Yamabe, K., Kakuta, S., Ishigame, H., Akitsu, A., etal. (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.
93. Sendid, B., Tabouret, M., Poirot, J.L., Mathieu, D., Fruit, J., and Poulain, D. (1999) New enzyme immunoassays for sensitive detection of circulating Candida albicans mannan and antimannan antibodies: useful combined test for diagnosis of systemic candidiasis. J Clin Microbiol 37: 1510-1517.
94. Sheth, C.C., Hall, R., Lewis, L., Brown, A.J.P., Odds, F.C., Erwig, L.P., and Gow, N.A.R. (2011) Glycosylation status of the C. albicans cell wall affects the efficiency of neutrophil phagocytosis and killing but not cytokine signaling. Med Mycol 49: 513-524.
95. Shibata, N., Saitoh, T., Tadokoro, Y., and Okawa, Y. (2009) The cell wall galactomannan antigen from Malassezia furfur and Malassezia pachydermatis contains beta-1, 6-linked linear galactofuranosyl residues and its detection has diagnostic potential. Microbiology 155: 3420-3429.
96. Singleton, D.R., Masuoka, J., and Hazen, K.C. (2005) Surface hydrophobicity changes of two Candida albicans serotype B mnn4Δ mutants. Eukaryot Cell 4: 639-648.
97. Smeekens, S.P., van de Veerdonk, F.L., van der Meer, J.W.M., Kullberg, B.J., Joosten, L.A.B., and Netea, M.G. (2010) The Candida Th17 response is dependent on mannan- and beta-glucan-induced prostaglandin E2. Int Immunol 22: 889-895.
98. + monocytes, promote Th17 responses to Candida albicans. Eur J Immunol 41: 2915-2924.
99. Sobel, J.D. (2007) Vulvovaginal candidosis. Lancet 369: 1961-1971.
100. Southard, S.B., Specht, C.A., Mishra, C., Chen-Weiner, J., and Robbins, P.W. (1999) Molecular analysis of the Candida albicans homolog of Saccharomyces cerevisiae MNN9, required for glycosylation of cell wall mannoproteins. J Bacteriol 181: 7439-7448.
101. Suram, S., Gangelhoff, T.A., Taylor, P.R., Rosas, M., Brown, G.D., Bonventre, J.V., etal. (2010) Pathways regulating cytosolic phospholipase A2 activation and eicosanoid production in macrophages by Candida albicans. J Biol Chem 285: 30676-30685.
102. Tada, H., Nemoto, E., Shimauchi, H., Watanabe, T., Mikami, T., Matsumoto, T., etal. (2002) Saccharomyces cerevisiae and Candida albicans-derived 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.
103. Takahara, K., Tokieda, S., Nagaoka, K., Takeda, T., Kimura, Y., and Inaba, K. (2011) C-type lectin SIGNR1 enhances cellular oxidative burst response against C. albicans in cooperation with Dectin-1. Eur J Immunol 41: 1435-1444.
104. Takahara, K., Arita, T., Tokieda, S., Shibata, N., Okawa, Y., Tateno, H., etal. (2012) Difference in fine specificity to polysaccharides of C. albicans mannoprotein between mouse SIGNR1 and human DC-SIGN. Infect Immun 80: 1699-1706.
105. Taylor, P.R., Brown, G.D., Herre, J., Williams, D.L., Willment, J.A., and Gordon, S. (2004) The role of SIGNR1 and the beta-glucan receptor (Dectin-1) in the nonopsonic recognition of yeast by specific macrophages. J Immunol 172: 1157-1162.
106. Thornton, B.P., Větvicka, V., Pitman, M., Goldman, R.C., and Ross, G.D. (1996) Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J Immunol 156: 1235-1246.
107. Timpel, C., Strahl-Bolsinger, S., Ziegelbauer, K., and Ernst, J.F. (1998) Multiple functions of Pmt1p-mediated protein O-mannosylation in the fungal pathogen Candida albicans. J Biol Chem 273: 20837-20846.
108. Timpel, C., Zink, S., Strahl-Bolsinger, S., Schroppel, K., and Ernst, J. (2000) Morphogenesis, adhesive properties, and antifungal resistance depend on the Pmt6 protein mannosyltransferase in the fungal pathogen Candida albicans. J Bacteriol 182: 3063-3071.
109. Wagener, J., Weindl, G., de Groot, P.W.J., de Boer, A.D., Kaesler, S., Thavaraj, S., etal. (2012) Glycosylation of Candida albicans cell wall proteins is critical for induction of innate immune responses and apoptosis of epithelial cells. PLoS ONE 7: e50518.
110. Walker, L.A., Munro, C.A., Bruijn, I., Lenardon, M.D., McKinnon, A., and Gow, N.A. (2008) Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4: e1000040.
111. Wells, C.A., Salvage-Jones, J.A., Li, X., Hitchens, K., Butcher, S., Murray, R.Z., etal. (2008) The macrophage-inducible C-type lectin, Mincle, is an essential component of the innate immune response to Candida albicans. J Immunol 180: 7404-7413.
112. Wheeler, R.T., Kombe, D., Agarwala, S.D., and Fink, G.R. (2008) Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog 4: e1000227.
113. Yamasaki, S., Matsumoto, M., Takeuchi, O., Matsuzawa, T., Ishikawa, E., Sakuma, M., etal. (2009) C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc Natl Acad Sci USA 106: 1897-1902.
114. Yang, R.-B., Mark, M.R., Gray, A., Huang, A., Xie, M.H., Zhang, M., etal. (1998) Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 395: 284-288.
115. Yip, C.L., Welch, S.K., Klebl, F., Gilbert, T., Seidel, P., Grant, F.J., etal. (1994) Cloning and analysis of the Saccharomyces cerevisiae MNN9 and MNN1 genes required for complex glycosylation of secreted proteins. Proc Natl Acad Sci USA 91: 2723-2727.
116. Zhao, X., Daniels, K.J., Oh, S.-H., Green, C.B., Yeater, K.M., Soll, D.R., and Hoyer, L.L. (2006) Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152: 2287-2299.