Dressed to impress: Impact of environmental adaptation on the Candidaalbicans cell wall

Molecular Microbiology

Volumn 97, Issue 1, 2015, Pages 7-17

  Hall, Rebecca A ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; PROTEOME; FUNGAL PROTEIN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; POLYSACCHARIDE;

ANTIGEN RECOGNITION; CANDIDA ALBICANS; CANDIDIASIS; CELL STRUCTURE; ENVIRONMENTAL PARAMETERS; EVOLUTIONARY ADAPTATION; FUNGAL CELL WALL; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS MUTANT; GLYCOSYLATION; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STRESS; ADAPTATION; ANIMAL; CELL WALL; CHEMISTRY; IMMUNOLOGY; MICROBIOLOGY; MUTATION; PATHOGENICITY; ULTRASTRUCTURE;

CANDIDA ALBICANS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CELL WALL; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MUTATION; PATHOGEN-ASSOCIATED MOLECULAR PATTERN MOLECULES; POLYSACCHARIDES;

EID: 84932194165     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13020     Document Type: Review

References (118)

1. Alsteens, D., Garcia, M.C., Lipke, P.N., and Dufrêne, Y.F. (2010) Force-induced formation and propagation of adhesion nanodomains in living fungal cells. PNAS 107: 20744-20749.
2. Bain, J.M., Louw, J., Lewis, L.E., Okai, B., Walls, C.A., Ballou, E.R., etal. (2014) Candida albicans hypha formation and mannan masking of β-glucan inhibit macrophage phagosome maturation. MBio 5: e01874-14.
3. Baker, L.G., Specht, C.A., Donlin, M.J., and Lodge, J.K. (2007) Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans. Eukaryot Cell 6: 855-867.
4. 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.
5. Bauters, T.G.M., Dhont, M.A., Temmerman, M.I.L., and Nelis, H.J. (2002) Prevalence of vulvovaginal candidiasis and susceptibility to fluconazole in women. Am J Obstet Gynecol 187: 569-574.
6. Bensen, E.S., Martin, S.J., Li, M., Berman, J., and Davis, D.A. (2004) Transcriptional profiling in Candida albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol Microbiol 54: 1335-1351.
7. Boon, C., Deng, Y., Wang, L.-H., He, Y., Xu, J.-L., Fan, Y., etal. (2007) A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J 2: 27-36.
8. Bowman, S.M., and Free, S.J. (2006) The structure and synthesis of the fungal cell wall. Bioessays 28: 799-808.
9. Brand, A., Barnes, J.D., Mackenzie, K.S., Odds, F.C., and Gow, N.A.R. (2008) Cell wall glycans and soluble factors determine the interactions between the hyphae of Candida albicans and Pseudomonas aeruginosa. 287: 48-55.
10. Brothers, K.M., Newman, Z.R., and Wheeler, R.T. (2011) Live imaging of disseminated candidiasis in zebrafish reveals role of phagocyte oxidase in limiting filamentous growth. Eukaryot Cell 10: 932-944.
11. Brown, G.D., and Gordon, S. (2001) Immune recognition: a new receptor for [beta]-glucans. Nature 413: 36-37.
12. Bruno, V.M., Wang, Z., Marjani, S.L., Euskirchen, G.M., Martin, J., Sherlock, G., and Snyder, M. (2010) Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res 20: 1451-1458.
13. Buffo, J., Herman, M., and Soll, D. (1984) A characterization of pH regulated dimorphism in Candida albicans. Mycopathologia 85: 21-30.
14. Cabral, V., Znaidi, S., Walker, L.A., Martin-Yken, H., Dague, E., Legrand, M., etal. (2014) Targeted changes of the cell wall proteome influence Candida albicans ability to form single- and multi-strain biofilms. PLoS Pathog 10: e1004542.
15. Chaffin, W.L., Lopez-Ribot, J.L., Casanova, M., Gozalbo, D., and MartÃnez, J.P. (1998) Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 62: 130-180.
16. Cheng, G., Yeater, K.M., and Hoyer, L.L. (2006) Cellular and molecular biology of Candida albicans estrogen response. Eukaryot Cell 5: 180-191.
17. Cheng, S.-C., van de Veerdonk, F.L., Lenardon, M., Stoffels, M., Plantinga, T., Smeekens, S., etal. (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.
18. Cottier, F., Raymond, M., Kurzai, O., Bolstad, M., Leewattanapasuk, W., Jiménez-López, C., etal. (2012) The bZIP transcription factor Rca1p is a central regulator of a novel CO2 sensing pathway in yeast. PLoS Pathog 8: e1002485.
19. Cruz, M.R., Graham, C.E., Gagliano, B.C., Lorenz, M.C., and Garsin, D.A. (2013) Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infect Immun 81: 189-200.
20. Daniels, K.J., Park, Y.-N., Srikantha, T., Pujol, C., and Soll, D.R. (2013) Impact of environmental conditions on the form and function of Candida albicans biofilms. Eukaryot Cell 12: 1389-1402.
21. Davidson, G.S., Joe, R.M., Roy, S., Meirelles, O., Allen, C.P., Wilson, M.R., etal. (2011) The proteomics of quiescent and nonquiescent cell differentiation in yeast stationary-phase cultures. Mol Biol Cell 22: 988-998.
22. Davies, A., Brailsford, S., and Beighton, D. (2006) Oral candidosis in patients with advanced cancer. Oral Oncol 42: 698-702.
23. Demuyser, L., Jabra-Rizk, M.A., and Van Dijck, P. (2014) Microbial cell surface proteins and secreted metabolites involved in multispecies biofilms. 70: 219-230.
24. Deveau, A., Piispanen, A.E., Jackson, A.A., and Hogan, D.A. (2010) Farnesol induces hydrogen peroxide resistance in Candida albicans yeast by inhibiting the Ras-cyclic AMP signaling pathway. Eukaryot Cell 9: 569-577.
25. Dutton, L., Nobbs, A., Jepson, K., Jepson, M., Vickerman, M., Aqeel Alawfi, A., etal. (2014) O-Mannosylation in Candida albicans enables development of interkingdom biofilm communities. MBio 5: 11-14.
26. Ene, I.V., Adya, A.K., Wehmeier, S., Brand, A.C., MacCallum, D.M., Gow, N.A.R., and Brown, A.J.P. (2012a) Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell Microbiol 14: 1319-1335.
27. Ene, I.V., Heilmann, C.J., Sorgo, A.G., Walker, L.A., de Koster, C.G., Munro, C.A., etal. (2012b) Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans. Proteomics 12: 3164-3179.
28. Ene, I.V., Cheng, S.-C., Netea, M.G., and Brown, A.J.P. (2013) Growth of Candida albicans cells on the physiologically relevant carbon source lactate affects their recognition and phagocytosis by immune cells. Infect Immun 81: 238-248.
29. Fradin, C., Jouault, T., Mallet, A., Mallet, J.M., Camus, D., Sinaÿ, P., and Poulain, D. (1996) Beta-1, 2-linked oligomannosides inhibit Candida albicans binding to murine macrophage. J Leukoc Biol 60: 81-87.
30. 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.
31. Free, S.J. (2013) Chapter two - fungal cell wall organization and biosynthesis. In Adv. Genet. Theodore Friedmann, J.C.D., and Stephen, F.G. (eds). Waltham MA, USA: Academic Press, pp. 33-82.
32. Ghosh, M., Fahey, J.V., Shen, Z., Lahey, T., Cu-Uvin, S., Wu, Z., etal. (2010) Anti-HIV activity in cervical-vaginal secretions from HIV-positive and -negative women correlate with innate antimicrobial levels and IgG antibodies. PLoS ONE 5: e11366.
33. Hall, R.A., and Gow, N.A.R. (2013) Mannosylation in Candida albicans: role in cell wall function and immune recognition. Mol Microbiol 90: 1147-1161.
34. Hall, R.A., Cottier, F., and Muhlschlegel, F.A. (2009) Molecular networks in the fungal pathogen Candida albicans. Adv Appl Microbiol 66: 191-212.
35. Hall, R.A., De Sordi, L., MacCallum, D.M., Topal, H., Eaton, R., Bloor, J.W., etal. (2010) CO2 acts as a signalling molecule in populations of the fungal pathogen Candida albicans. PLoS Pathog 6: e1001193.
36. Hall, R.A., Turner, K.J., Chaloupka, J., Cottier, F., De Sordi, L., Sanglard, D., etal. (2011) The quorum-sensing molecules farnesol/homoserine lactone and dodecanol operate via distinct modes of action in Candida albicans. Eukaryot Cell 10: 1034-1042.
37. 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.
38. Han, K.-H., Park, S.J., Choi, S.J., Park, J.Y., and Lee, K.-H. (2013) Immunological features of macrophages induced by various morphological structures of Candida albicans. J Microbiol Biotechnol 23: 1031-1040.
39. 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.
40. Hogan, D.A., and Kolter, R. (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296: 2229-2232.
41. Hogan, D.A., Vik, A., and Kolter, R. (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54: 1212-1223.
42. Hornby, J., Jensen, E., Lisec, A., Tasto, J., Jahnke, B., Shoemaker, R., etal. (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67: 2982-2992.
43. Hromatka, B.S., Noble, S.M., and Johnson, A.D. (2005) Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol Biol Cell 16: 4814-4826.
44. Jarosz, L.M., Deng, D.M., van der Mei, H.C., Crielaard, W., and Krom, B.P. (2009) Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation. Eukaryot Cell 8: 1658-1664.
45. John, M., Keller, M.J., Fam, E.H., Cheshenko, N., Hogarty, K., Kasowitz, A., etal. (2005) Cervicovaginal secretions contribute to innate resistance to herpes simplex virus infection. J Infect Dis 192: 1731-1740.
46. Kaloriti, D., Tillmann, A., Cook, E., Jacobsen, M., You, T., Lenardon, M., etal. (2012) Combinatorial stresses kill pathogenic Candida species. Med Mycol 50: 699-709.
47. Kaloriti, D., Jacobsen, M., Yin, Z., Patterson, M., Tillmann, A., Smith, D.A., etal. (2014) Mechanisms underlying the exquisite sensitivity of Candida albicans to combinatorial cationic and oxidative stress that enhances the potent fungicidal activity of phagocytes. MBio 5: e01334-14.
48. Klengel, T., Liang, W.-J., Chaloupka, J., Ruoff, C., Schroppel, K., Naglik, J.R., etal. (2005) Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15: 2021-2026.
49. Klis, F., de Groot, P., and Hellingwerf, K. (2001) Molecular organization of the cell wall of Candida albicans. Med Mycol 39: 1-8.
50. Klis, F.M. (1994) Review: cell wall assembly in yeast. Yeast 10: 851-869.
51. Kobayashi, H., Shibata, N., Mitobe, H., Ohkubo, Y., and Suzuki, S. (1989) Structural study of phosphomannan of yeast-form cells of Candida albicans J-1012 strain with special reference to application of mild acetolysis. Arch Biochem Biophys 272: 364-375.
52. Kobayashi, H., Giummelly, P., Takahashi, S., Ishida, M., Sato, J., Takaku, M., etal. (1991) Candida albicans serotype A strains grow in yeast extract-added Sabouraud liquid medium at pH 2.0, elaborating mannans without beta-1, 2 linkage and phosphate group. Biochem Biophys Res Commun 175: 1003-1009.
53. Kobayashi, H., Takahashi, S., Shibata, N., Miyauchi, M., Ishida, M., Sato, J., etal. (1994a) Structural modification of cell wall mannans of Candida albicans serotype A strains grown in yeast extract-Sabouraud liquid medium under acidic conditions. Infect Immun 62: 968-973.
54. Kobayashi, H., Shibata, N., Suzuki, A., Takahashi, S., Suzuki, M., Matsuda, K., etal. (1994b) Expression of alpha-1, 3 linkage-containing oligomannosyl residues in a cell-wall mannan of Candida tropicalis grown in yeast extract-Sabouraud liquid medium under acidic conditions. FEBS Lett 414: 338-342.
55. Kobayashi, H., Tanaka, S., Suzuki, J., Kiuchi, Y., Shibata, N., Suzuki, S., and Okawa, Y. (1997) Amended structure of side chains in a cell wall mannan from Candida albicans serotype A strain grown in yeast extract-Sabouraud liquid medium under acidic conditions: detection of the branched side chains corresponding to antigenic factor 4. FEMS Microbiol Lett 152: 235-242.
56. Koyama, T., Makita, M., Shibata, N., and Okawa, Y. (2009) Influence of oxidative and osmotic stresses on the structure of the cell wall mannan of Candida albicans serotype A. Carbohydr Res 344: 2195-2200.
57. Kraus, P.R., and Heitman, J. (2003) Coping with stress: calmodulin and calcineurin in model and pathogenic fungi. Biochem Biophys Res Commun 311: 1151-1157.
58. Kravtsov, E.G., I., Anokhina, V., Rybas, Y.A., Sachivkina, N.P., Ermolaev, A.V., and Brodskaya, S.B. (2014) Effects of female sex hormones on adhesion of Candida albicans yeast-like fungi to the buccal epithelium. Bull Exp Biol Med 157: 246-248.
59. 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.
60. Lee, K.K., MacCallum, D.M., Jacobsen, M.D., Walker, L.A., Odds, F.C., Gow, N.A.R., and Munro, C.A. (2012) Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob Agents Chemother 56: 208-217.
61. 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.
62. 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.
63. Lowman, D.W., Greene, R.R., Bearden, D.W., Kruppa, M.D., Pottier, M., Monteiro, M.A., etal. (2014) Novel structural features in Candida albicans hyphal glucan provide a basis for differential innate immune recognition of hyphae versus yeast. J Biol Chem 289: 3432-3443.
64. 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.
65. 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.
66. Marakalala, M.J., Vautier, S., Potrykus, J., Walker, L.A., Shepardson, K.M., Hopke, A., etal. (2013) Differential adaptation of Candida albicans in vivo modulates immune recognition by Dectin-1. PLoS Pathog 9: e1003315.
67. Monge, R.A., Román, E., Nombela, C., and Pla, J. (2006) The MAP kinase signal transduction network in Candida albicans. Microbiology 152: 905-912.
68. Mora-Montes, H.M., Netea, M.G., Ferwerda, G., Lenardon, M.D., Brown, G.D., Mistry, A.R., etal. (2011) Recognition and blocking of innate immunity cells by Candida albicans chitin. Infect Immun 79: 1961-1970.
69. Munro, C.A., Selvaggini, S., de Bruijn, I., Walker, L., Lenardon, M.D., Gerssen, B., etal. (2007) The PKC, HOG and Ca2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Mol Microbiol 63: 1399-1413.
70. Nash, E.E., Peters, B.M., Palmer, G.E., Fidel, P.L., and Noverr, M.C. (2014) Morphogenesis is not required for Candida albicans-Staphylococcus aureus intra-abdominal infection-mediated dissemination and lethal sepsis. Infect Immun 82: 3426-3435.
71. 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.
72. Nett, J.E., Marchillo, K., Spiegel, C.A., and Andes, D.R. (2010) Development and validation of an in vivo Candida albicans biofilm denture model. Infect Immun 78: 3650-3659.
73. Nobile, C.J., Solis, N., Myers, C.L., Fay, A.J., Deneault, J.-S., Nantel, A., etal. (2008) Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions. Cell Microbiol 10: 2180-2196.
74. Odds, F.C. (1988) Candida and candidosis. A review and bibliography.
75. Okawa, Y., and Goto, K. (2006) Antigenicity of cell wall mannans of Candida albicans and Candida stellatoidea cultured at high temperatures in BACTEC medium. Biol Pharm Bull 29: 1723-1727.
76. Ovchinnikova, E.S., Krom, B.P., Harapanahalli, A.K., Busscher, H.J., and van der Mei, H.C. (2013) Surface thermodynamic and adhesion force evaluation of the role of chitin-binding protein in the physical interaction between Pseudomonas aeruginosa and Candida albicans. Langmuir 29: 4823-4829.
77. Peleg, A.Y., Tampakakis, E., Fuchs, B.B., Eliopoulos, G.M., Moellering, R.C., and Mylonakis, E. (2008) Prokaryote-eukaryote interactions identified by using Caenorhabditis elegans. Proc Natl Acad Sci USA 105: 14585-14590.
78. Perlroth, J., Choi, B., and Spellberg, B. (2007) Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med Mycol 45: 321-346.
79. Persi, M.A., Burnham, J.C., and Duhring, J.L. (1985) Effects of carbon dioxide and pH on adhesion of Candida albicans to vaginal epithelial cells. Infect Immun 50: 82-90.
80. Peters, B.M., and Noverr, M.C. (2013) Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity. Infect Immun 81: 2178-2189.
81. Peters, B.M., Ovchinnikova, E.S., Krom, B.P., Schlecht, L.M., Zhou, H., Hoyer, L.L., etal. (2012) Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology 158: 2975-2986.
82. Poulain, D., Tronchin, G., Dubremetz, J.F., and Biguet, J. (1978) Ultrastructure of the cell wall of Candida albicans blastospores: study of its constitutive layers by the use of a cytochemical technique revealing polysaccharides. Ann Microbiol 129: 141-145.
83. Ravel, J., Gajer, P., Abdo, Z., Schneider, G.M., Koenig, S.S.K., McCulle, S.L., etal. (2011) Vaginal microbiome of reproductive-age women. PNAS 108: 4680-4687.
84. Rodaki, A., I., Bohovych, M., Enjalbert, B., Young, T., Odds, F.C., Gow, N.A.R., and Brown, A.J.P. (2009) Glucose promotes stress resistance in the fungal pathogen Candida albicans. Mol Biol Cell 20: 4845-4855.
85. Romanowski, K., Zaborin, A., Valuckaite, V., Rolfes, R.J., Babrowski, T., Bethel, C., etal. (2012) Candida albicans isolates from the gut of critically ill patients respond to phosphate limitation by expressing filaments and a lethal phenotype. PLoS ONE 7: e30119.
86. Rossignol, T., Ding, C., Guida, A., d'Enfert, C., Higgins, D.G., and Butler, G. (2009) Correlation between biofilm formation and the hypoxic response in Candida parapsilosis. Eukaryot Cell 8: 550-559.
87. 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.
88. Schlecht, L.M., Peters, B.M., Krom, B.P., Freiberg, J.A., Hänsch, G.M., Filler, S.G., etal. (2015) Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiology 161: 168-181.
89. Segata, N., Haake, S., Mannon, P., Lemon, K., Waldron, L., Gevers, D., etal. (2012) Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol 13: R42.
90. Shepardson, K.M., Ngo, L.Y., Aimanianda, V., Latge, J.-P., Barker, B.M., Blosser, S.J., etal. (2013) Hypoxia enhances innate immune activation to Aspergillus fumigates through cell wall modulation. Microbes Infect 15: 259-269.
91. 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.
92. Shibata, N., Fukasawa, S., Kobayashi, H., Tojo, M., Yonezu, T., Ambo, A., etal. (1989) Structural analysis of phospho-d-mannan-protein complexes isolated from yeast and mold form cells of Candida albicans NIH A-207 serotype a strain. Carbohydr Res 187: 239-253.
93. Shibata, N., Kobayashi, H., Takahashi, S., Okawa, Y., Hisamichi, K., Suzuki, S., and Suzuki, S. (1991) Structural study on a phosphorylated mannotetraose obtained from the phosphomannan of Candida albicans NIH B-792 strain by acetolysis. Arch Biochem Biophys 290: 535-542.
94. Shibata, N., Arai, M., Haga, E., Kikuchi, T., Najima, M., Satoh, T., etal. (1992a) Structural identification of an epitope of antigenic factor 5 in mannans of Candida albicans NIH B-792 (serotype B) and J-1012 (serotype A) as beta-1, 2-linked oligomannosyl residues. Infect Immun 60: 4100-4110.
95. Shibata, N., Arai, M., Haga, E., Kikuchi, T., Najima, M., Satoh, T., etal. (1992b) Structural identification of an epitope of antigenic factor 5 in mannans of Candida albicans NIH B-792 (serotype B) and J-1012 (serotype A) as beta-1, 2-linked oligomannosyl residues. Infect Immun 60: 4100-4110.
96. Shibata, N., Ikuta, K., Imai, T., Satoh, Y., Satoh, R., Suzuki, A., etal. (1995) Existence of branched side chains in the cell wall mannan of pathogenic yeast, Candida albicans. J Biol Chem 270: 1113-1122.
97. Shibata, N., Suzuki, A., Kobayashi, H., and Okawa, Y. (2007) Chemical structure of the cell-wall mannan of Candida albicans serotype A and its difference in yeast and hyphal forms. Biochem J 404: 365-372.
98. Silverman, R.J., Nobbs, A.H., Vickerman, M.M., Barbour, M.E., and Jenkinson, H.F. (2010) Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun 78: 4644-4652.
99. Sobel, J.D. (1992) Pathogenesis and treatment of recurrent vulvovaginal candidiasis. Clin Infect Dis 14: S148-S153.
100. Sobel, J.D. (2007) Vulvovaginal candidosis. Lancet 369: 1961-1971.
101. Sosinska, G.J., de Groot, P.W.J., Teixeira de Mattos, M.J., Dekker, H.L., de Koster, C.G., Hellingwerf, K.J., and Klis, F.M. (2008) Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 154: 510-520.
102. Spinillo, A., Capuzzo, E., Nicola, S., Baltaro, F., Ferrari, A., and Monaco, A. (1995) The impact of oral contraception on vulvovaginal candidiasis. Contraception 51: 293-297.
103. Srikantha, T., Daniels, K.J., Pujol, C., Sahni, N., Yi, S., and Soll, D.R. (2012) Nonsex genes in the mating type locus of Candida albicans play roles in a/α biofilm formation, including impermeability and fluconazole resistance. PLoS Pathog 8: e1002476.
104. Staniszewska, M., Bondaryk, M., Rabczenko, D., Smoleńska-Sym, G., and Kurzatkowski, W. (2013) Cell wall carbohydrates content of pathogenic Candida albicans strain morphological forms. Med Dosw Mikrobiol 65: 119-128.
105. - and Toll-like receptor 4-dependent manner. Microbiol Immunol 46: 503-512.
106. Tada, R., Nagi-Miura, N., Adachi, Y., and Ohno, N. (2008) The influence of culture conditions on vasculitis and anaphylactoid shock induced by fungal pathogen Candida albicans cell wall extract in mice. Microb Pathog 44: 379-388.
107. 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.
108. 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.
109. Traven, A., Jänicke, A., Harrison, P., Swaminathan, A., Seemann, T., and Beilharz, T.H. (2012) Transcriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities. PLoS ONE 7: e46243.
110. Trinel, P.A., Jouault, T., Cutler, J.E., and Poulain, D. (2002) β-1, 2-Mannosylation of Candida albicans mannoproteins and glycolipids differs with growth temperature and serotype. Infect Immun 70: 5274-5278.
111. Ueno, K., Okawara, A., Yamagoe, S., Naka, T., Umeyama, T., Utena-Abe, Y., etal. (2013) The mannan of Candida albicans lacking β-1, 2-linked oligomannosides increases the production of inflammatory cytokines by dendritic cells. Med Mycol 51: 385-395.
112. Vílchez, R., Lemme, A., Ballhausen, B., Thiel, V., Schulz, S., Jansen, R., etal. (2010) Streptococcus mutans inhibits Candida albicans hyphal formation by the fatty acid signaling molecule trans-2-decenoic acid (SDSF). Chembiochem 11: 1552-1562.
113. Weissman, Z., and Kornitzer, D. (2004) A family of Candida cell surface haem-binding proteins involved in haemin and haemoglobin-iron utilization. Mol Microbiol 53: 1209-1220.
114. West, L., Lowman, D.W., Mora-Montes, H.M., Grubb, S., Murdoch, C., Thornhill, M.H., etal. (2013) Differential virulence of Candida glabrata glycosylation mutants. J Biol Chem 288: 22006-22018.
115. Wira, C.R., Ghosh, M., Smith, J.M., Shen, L., Connor, R.I., Sundstrom, P., etal. (2011) Epithelial cell secretions from the human female reproductive tract inhibit sexually transmitted pathogens and Candida albicans but not Lactobacillus. Mucosal Immunol 4: 335-342.
116. Witkin, S.S., Mendes-Soares, H., Linhares, I.M., Jayaram, A., Ledger, W.J., and Forney, L.J. (2013) Influence of vaginal bacteria and d- and l-lactic acid isomers on vaginal extracellular matrix metalloproteinase inducer: implications for protection against upper genital tract infections. MBio 4: e00460-13.
117. Wu, C.J., Lee, H.C., Yang, Y.L., Chang, C.M., Chen, H.T., Lin, C.C., etal. (2012) Oropharyngeal yeast colonization in HIV-infected outpatients in southern Taiwan: CD4 count, efavirenz therapy and intravenous drug use matter. Clin Microbiol Infect 18: 485-490.
118. Yi, S., Sahni, N., Daniels, K.J., Lu, K.L., Srikantha, T., Huang, G., etal. (2011) Alternative mating type configurations (a/α versus a/a or α/α) of Candida albicans result in alternative biofilms regulated by different pathways. PLoS Biol 9: e1001117.