Interactions of Candida albicans with epithelial cells

Cellular Microbiology

Volumn 12, Issue 3, 2010, Pages 273-282

  Zhu, Weidong ^a   Filler, Scott G ^a,b  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ASPARTIC PROTEINASE; ENHANCED ADHERENCE TO POLYSTYRENE 1 PROTEIN; FUNGAL PROTEIN; HYPAL WALL PROTEIN 1; IFF4 PROTEIN; INVASIN; PHOSPHOLIPASE; UNCLASSIFIED DRUG; UVOMORULIN;

CANDIDA ALBICANS; CELL ADHESION; CELL DAMAGE; CELL INVASION; CELL JUNCTION; ENDOCYTOSIS; EPITHELIUM CELL; FUNGAL COLONIZATION; HOST PATHOGEN INTERACTION; HUMAN; MICROBIAL ADHESION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW;

CANDIDA ALBICANS; CELL ADHESION; DESMOSOMAL CADHERINS; ENDOCYTOSIS; EPITHELIAL CELLS; FUNGAL PROTEINS; HUMANS; VIRULENCE FACTORS;

CANDIDA ALBICANS; FUNGI;

EID: 77950609407     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01412.x     Document Type: Review

References (89)

1. Alberti-Segui C, Morales AJ, Xing H, Kessler MM, Willins DA, Weinstock KG. Identification of potential cell-surface proteins in Candida albicans and investigation of the role of a putative cell-surface glycosidase in adhesion and virulence. Yeast 2004, 21:285-302.
2. Bates S, de la Rosa JM, MacCallum DM, Brown AJ, Gow NA, Odds FC. Candida albicans Iff11, a secreted protein required for cell wall structure and virulence. Infect Immun 2007, 75:2922-2928.
3. Braun BR, van Het Hoog M, d'Enfert C, Martchenko M, Dungan J, Kuo A. A human-curated annotation of the Candida albicans genome. PLoS Genet 2005, 1:e1.
4. Cawson RA, Rajasingham KC. Ultrastructural features of the invasive phase of Candida albicans. Br J Dermatol 1972, 87:435-443.
5. Chaffin WL. Candida albicans cell wall proteins. Microbiol Mol Biol Rev 2008, 72:495-544.
6. Chiang LY, Sheppard DC, Bruno VM, Mitchell AP, Edwards JE, Filler SG. Candida albicans protein kinase CK2 governs virulence during oropharyngeal candidiasis. Cell Microbiol 2007, 9:233-245.
7. Dalle F, Wachtler B, Coralie L, Holland G, Bannert N, Wilson D. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes: Cell Microbiol. 2009, 2009. Epub ahead of print. DOI 10.1111/j.1462-5822.2009.01394.x
8. Davis D, Wilson RB, Mitchell AP. RIM101-dependent and-independent pathways govern pH responses in Candida albicans. Mol Cell Biol 2000, 20:971-978.
9. De Bernardis F, Arancia S, Morelli L, Hube B, Sanglard D, Schafer W, Cassone A. Evidence that members of the secretory aspartyl proteinase gene family, in particular SAP2, are virulence factors for Candida vaginitis. J Infect Dis 1999, 179:201-208.
10. De Bernardis F, Liu H, O'Mahony R, La Valle R, Bartollino S, Sandini S. Human domain antibodies against virulence traits of Candida albicans inhibit fungus adherence to vaginal epithelium and protect against experimental vaginal candidiasis. J Infect Dis 2007, 195:149-157.
11. Dongari-Bagtzoglou A, Kashleva H, Villar CC. Bioactive interleukin-1alpha is cytolytically released from Candida albicans-infected oral epithelial cells. Med Mycol 2004, 42:531-541.
12. Drago L, Mombelli B, De Vecchi E, Bonaccorso C, Fassina MC, Gismondo MR. Candida albicans cellular internalization: a new pathogenic factor? Int J Antimicrob Agents 2000, 16:545-547.
13. El Barkani A, Kurzai O, Fonzi WA, Ramon A, Porta A, Frosch M, Muhlschlegel FA. Dominant active alleles of RIM101 (PRR2) bypass the pH restriction on filamentation of Candida albicans. Mol Cell Biol 2000, 20:4635-4647.
14. Enache E, Eskandari T, Borja L, Wadsworth E, Hoxter B, Calderone R. Candida albicans adherence to a human oesophageal cell line. Microbiology 1996, 142:2741-2746.
15. Eversole LR, Reichart PA, Ficarra G, Schmidt-Westhausen A, Romagnoli P, Pimpinelli N. Oral keratinocyte immune responses in HIV-associated candidiasis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997, 84:372-380.
16. Farah CS, Ashman RB, Challacombe SJ. Oral candidosis. Clin Dermatol 2000, 18:553-562.
17. Feng Z, Jiang B, Chandra J, Ghannoum M, Nelson S, Weinberg A. Human beta-defensins: differential activity against candidal species and regulation by Candida albicans. J Dent Res 2005, 84:445-450.
18. Frank CF, Hostetter MK. Cleavage of E-cadherin: a mechanism for disruption of the intestinal epithelial barrier by Candida albicans. Transl Res 2007, 149:211-222.
19. Fu Y, Rieg G, Fonzi WA, Belanger PH, Edwards JE, Filler SG. Expression of the Candida albicans gene ALS1 in Saccharomyces cerevisiae induces adherence to endothelial and epithelial cells. Infect Immun 1998, 66:1783-1786.
20. Fu Y, Ibrahim AS, Sheppard DC, Chen YC, French SW, Cutler JE. Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol Microbiol 2002, 44:61-72.
21. Fu Y, Luo G, Spellberg BJ, Edwards JE, Ibrahim AS. Gene overexpression/suppression analysis of candidate virulence factors of Candida albicans. Eukaryot Cell 2008, 7:483-492.
22. Garcia-Tamayo J, Castillo G, Martinez AJ. Human genital candidiasis: histochemistry, scanning and transmission electron microscopy. Acta Cytol 1982, 26:7-14.
23. Gaur NK, Klotz SA. Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect Immun 1997, 65:5289-5294.
24. Granger BL, Flenniken ML, Davis DA, Mitchell AP, Cutler JE. Yeast wall protein 1 of Candida albicans. Microbiology 2005, 151:1631-1644.
25. Hoyer LL. The ALS gene family of Candida albicans. Trends Microbiol 2001, 9:176-180.
26. Hoyer LL, Hecht JE. The ALS5 gene of Candida albicans and analysis of the Als5p N-terminal domain. Yeast 2001, 18:49-60.
27. Hoyer LL, Payne TL, Bell M, Myers AM, Scherer S. Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr Genet 1998, 33:451-459.
28. Kamai Y, Kubota M, Hosokawa T, Fukuoka T, Filler SG. Contribution of Candida albicans ALS1 to the pathogenesis of experimental oropharyngeal candidiasis. Infect Immun 2002, 70:5256-5258.
29. Kempf M, Apaire-Marchais V, Saulnier P, Licznar P, Lefrancois C, Robert R, Cottin J. Disruption of Candida albicans IFF4 gene involves modifications of the cell electrical surface properties. Colloids Surf B Biointerfaces 2007, 58:250-255.
30. Kleinegger CL, Lockhart SR, Vargas K, Soll DR. Frequency, intensity, species, and strains of oral Candida vary as a function of host age. J Clin Microbiol 1996, 34:2246-2254.
31. Leidich SD, Ibrahim AS, Fu Y, Koul A, Jessup C, Vitullo J. Cloning and disruption of caPLB1, a phospholipase B gene involved in the pathogenicity of Candida albicans. J Biol Chem 1998, 273:26078-26086.
32. Lermann U, Morschhauser J. Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albicans. Microbiology 2008, 154:3281-3295.
33. Li F, Palecek SP. EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot Cell 2003, 2:1266-1273.
34. Li F, Palecek SP. Distinct domains of the Candida albicans adhesin Eap1p mediate cell-cell and cell-substrate interactions. Microbiology 2008, 154:1193-1203.
35. Li F, Svarovsky MJ, Karlsson AJ, Wagner JP, Marchillo K, Oshel P. Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell 2007, 6:931-939.
36. Loza L, Fu Y, Ibrahim AS, Sheppard DC, Filler SG, Edwards JE. Functional analysis of the Candida albicans ALS1 gene product. Yeast 2004, 21:473-482. Jr
37. McNulty KM, Plianrungsi J, Leigh JE, Mercante D, Fidel PL. Characterization of CD8+ T cells and microenvironment in oral lesions of human immunodeficiency virus-infected persons with oropharyngeal candidiasis. Infect Immun 2005, 73:3659-3667. Jr
38. Marr KA, Seidel K, White TC, Bowden RA. Candidemia in allogeneic blood and marrow transplant recipients: evolution of risk factors after the adoption of prophylactic fluconazole. J Infect Dis 2000, 181:309-316.
39. Martinez-Lopez R, Monteoliva L, Diez-Orejas R, Nombela C, Gil C. The GPI-anchored protein CaEcm33p is required for cell wall integrity, morphogenesis and virulence in Candida albicans. Microbiology 2004, 150:3341-3354.
40. Martinez-Lopez R, Park H, Myers CL, Gil C, Filler SG. Candida albicans Ecm33p is important for normal cell wall architecture and interactions with host cells. Eukaryot Cell 2006, 5:140-147.
41. Montes LF, Wilborn WH. Ultrastructural features of host-parasite relationship in oral candidiasis. J Bacteriol 1968, 96:1349-1356.
42. Moreno-Ruiz E, Galan-Diez M, Zhu W, Fernandez-Ruiz E, d'Enfert C, Filler SG. Candida albicans internalization by host cells is mediated by a clathrin-dependent mechanism. Cell Microbiol 2009, 11:1179-1189.
43. Naglik JR, Rodgers CA, Shirlaw PJ, Dobbie JL, Fernandes-Naglik LL, Greenspan D. Differential expression of Candida albicans secreted aspartyl proteinase and phospholipase B genes in humans correlates with active oral and vaginal infections. J Infect Dis 2003, 188:469-479.
44. Naglik JR, Moyes D, Makwana J, Kanzaria P, Tsichlaki E, Weindl G. Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 2008, 154:3266-3280.
45. Nobile CJ, Schneider HA, Nett JE, Sheppard DC, Filler SG, Andes DR, Mitchell AP. Complementary adhesin function in C. albicans biofilm formation. Curr Biol 2008a, 18:1017-1024.
46. Nobile CJ, Solis N, Myers CL, Fay AJ, Deneault JS, Nantel A. Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions. Cell Microbiol 2008b, 10:2180-2196.
47. Otoo HN, Lee KG, Qiu W, Lipke PN. Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot Cell 2008, 7:776-782.
48. Pardini G, De Groot PW, Coste AT, Karababa M, Klis FM, de Koster CG, Sanglard D. The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. J Biol Chem 2006, 281:40399-40411.
49. Park H, Myers CL, Sheppard DC, Phan QT, Sanchez AA, Edwards JE, Filler SG. Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell Microbiol 2005, 7:499-510.
50. Perez-Torres M, Valle BL, Maihle NJ, Negron-Vega L, Nieves-Alicea R, Cora EM. Shedding of epidermal growth factor receptor is a regulated process that occurs with overexpression in malignant cells. Exp Cell Res 2008, 314:2907-2918.
51. Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 2007, 5:e64.
52. Ponniah G, Rollenhagen C, Bahn YS, Staab JF, Sundstrom P. State of differentiation defines buccal epithelial cell affinity for cross-linking to Candida albicans Hwp1. J Oral Pathol Med 2007, 36:456-467.
53. Rajasingham KC, Challacombe SJ, Tovey S. Ultrastructure and possible processes involved in the invasion of host epithelial cells by Candida albicans in vaginal candidosis. Cytobios 1989, 60:11-20.
54. Ramirez-Amador V, Silverman S, Mayer P, Tyler M, Quivey J. Candidal colonization and oral candidiasis in patients undergoing oral and pharyngeal radiation therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997, 84:149-153.
55. Rauceo JM, Gaur NK, Lee KG, Edwards JE, Klotz SA, Lipke PN. Global cell surface conformational shift mediated by a Candida albicans adhesin. Infect Immun 2004, 72:4948-4955.
56. Rauceo JM, De Armond R, Otoo H, Kahn PC, Klotz SA, Gaur NK, Lipke PN. Threonine-rich repeats increase fibronectin binding in the Candida albicans adhesin Als5p. Eukaryot Cell 2006, 5:1664-1673.
57. Ray TL, Payne CD. Scanning electron microscopy of epidermal adherence and cavitation in murine candidiasis: a role for Candida acid proteinase. Infect Immun 1988, 56:1942-1949.
58. Richter SS, Galask RP, Messer SA, Hollis RJ, Diekema DJ, Pfaller MA. Antifungal susceptibilities of Candida species causing vulvovaginitis and epidemiology of recurrent cases. J Clin Microbiol 2005, 43:2155-2162.
59. Rollenhagen C, Wollert T, Langford GM, Sundstrom P. Stimulation of cell motility and expression of late markers of differentiation in human oral keratinocytes by Candida albicans. Cell Microbiol 2009, 11:946-966.
60. Sandini S, La Valle R, De Bernardis F, Macri C, Cassone A. The 65 kDa mannoprotein gene of Candida albicans encodes a putative beta-glucanase adhesin required for hyphal morphogenesis and experimental pathogenicity. Cell Microbiol 2007, 9:1223-1238.
61. Schaller M, Korting HC, Schafer W, Bastert J, Chen W, Hube B. Secreted aspartic proteinase (Sap) activity contributes to tissue damage in a model of human oral candidosis. Mol Microbiol 1999, 34:169-180.
62. Schaller M, Bein M, Korting HC, Baur S, Hamm G, Monod M. The secreted aspartyl proteinases Sap1 and Sap2 cause tissue damage in an in vitro model of vaginal candidiasis based on reconstituted human vaginal epithelium. Infect Immun 2003, 71:3227-3234.
63. Scherwitz C. Ultrastructure of human cutaneous candidosis. J Invest Dermatol 1982, 78:200-205.
64. Schofield DA, Westwater C, Warner T, Nicholas PJ, Paulling EE, Balish E. Hydrolytic gene expression during oroesophageal and gastric candidiasis in immunocompetent and immunodeficient gnotobiotic mice. J Infect Dis 2003, 188:591-599.
65. Sentandreu M, Elorza MV, Sentandreu R, Fonzi WA. Cloning and characterization of PRA1, a gene encoding a novel pH-regulated antigen of Candida albicans. J Bacteriol 1998, 180:282-289.
66. Sharkey LL, McNemar MD, Saporito-Irwin SM, Sypherd PS, Fonzi WA. HWP1 functions in the morphological development of Candida albicans downstream of EFG1, TUP1, and RBF1. J Bacteriol 1999, 181:5273-5279.
67. Sheppard DC, Yeaman MR, Welch WH, Phan QT, Fu Y, Ibrahim AS. Functional and structural diversity in the Als protein family of Candida albicans. J Biol Chem 2004, 279:30840-30849.
68. Singleton DR, Hazen KC. Differential surface localization and temperature-dependent expression of the Candida albicans CSH1 protein. Microbiology 2004, 150:285-292.
69. Singleton DR, Fidel PL, Wozniak KL, Hazen KC. Contribution of cell surface hydrophobicity protein 1 (Csh1p) to virulence of hydrophobic Candida albicans serotype A cells. FEMS Microbiol Lett 2005, 244:373-377.
70. Soloviev DA, Fonzi WA, Sentandreu R, Pluskota E, Forsyth CB, Yadav S, Plow EF. Identification of pH-regulated antigen 1 released from Candida albicans as the major ligand for leukocyte integrin alphaMbeta2. J Immunol 2007, 178:2038-2046.
71. Staab JF, Bradway SD, Fidel PL, Sundstrom P. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 1999, 283:1535-1538.
72. Staab JF, Bahn YS, Tai CH, Cook PF, Sundstrom P. Expression of transglutaminase substrate activity on Candida albicans germ tubes through a coiled, disulfide-bonded N-terminal domain of Hwp1 requires C-terminal glycosylphosphatidylinositol modification. J Biol Chem 2004, 279:40737-40747.
73. Steubesand N, Kiehne K, Brunke G, Pahl R, Reiss K, Herzig KH. The expression of the beta-defensins hBD-2 and hBD-3 is differentially regulated by NF-kappaB and MAPK/AP-1 pathways in an in vitro model of Candida esophagitis. BMC Immunol 2009, 10:36.
74. Sundstrom P, Balish E, Allen CM. Essential role of the Candida albicans transglutaminase substrate, hyphal wall protein 1, in lethal oroesophageal candidiasis in immunodeficient mice. J Infect Dis 2002, 185:521-530.
75. Takesue Y, Kakehashi M, Ohge H, Imamura Y, Murakami Y, Sasaki M. Combined assessment of beta-d-glucan and degree of candida colonization before starting empiric therapy for candidiasis in surgical patients. World J Surg 2004, 28:625-630.
76. Theiss S, Ishdorj G, Brenot A, Kretschmar M, Lan CY, Nichterlein T. Inactivation of the phospholipase B gene PLB5 in wild-type Candida albicans reduces cell-associated phospholipase A2 activity and attenuates virulence. Int J Med Microbiol 2006, 296:405-420.
77. Vazquez JA, Skiest DJ, Nieto L, Northland R, Sanne I, Gogate J. A multicenter randomized trial evaluating posaconazole versus fluconazole for the treatment of oropharyngeal candidiasis in subjects with HIV/AIDS. Clin Infect Dis 2006, 42:1179-1186.
78. Villar CC, Kashleva H, Mitchell AP, Dongari-Bagtzoglou A. Invasive phenotype of Candida albicans affects the host proinflammatory response to infection. Infect Immun 2005, 73:4588-4595.
79. Villar CC, Kashleva H, Nobile CJ, Mitchell AP, Dongari-Bagtzoglou A. Mucosal tissue invasion by Candida albicans is associated with E-cadherin degradation, mediated by transcription factor Rim101p and protease Sap5p. Infect Immun 2007, 75:2126-2135.
80. Watts HJ, Cheah FS, Hube B, Sanglard D, Gow NA. Altered adherence in strains of Candida albicans harbouring null mutations in secreted aspartic proteinase genes. FEMS Microbiol Lett 1998, 159:129-135.
81. Weindl G, Naglik JR, Kaesler S, Biedermann T, Hube B, Korting HC, Schaller M. Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J Clin Invest 2007, 117:3664-3672.
82. Willis AM, Coulter WA, Fulton CR, Hayes JR, Bell PM, Lamey PJ. Oral candidal carriage and infection in insulin-treated diabetic patients. Diabet Med 1999, 16:675-679.
83. Yano J, Lilly EA, Steele C, Fortenberry D, Fidel PL. Oral and vaginal epithelial cell anti-Candida activity is acid labile and does not require live epithelial cells. Oral Microbiol Immunol 2005, 20:199-205. Jr
84. Yu L, Lee KK, Sheth HB, Lane-Bell P, Srivastava G, Hindsgaul O. Fimbria-mediated adherence of Candida albicans to glycosphingolipid receptors on human buccal epithelial cells. Infect Immun 1994, 62:2843-2848.
85. Zakikhany K, Naglik JR, Schmidt-Westhausen A, Holland G, Schaller M, Hube B. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell Microbiol 2007, 9:2938-2954.
86. Zhao X, Oh SH, Cheng G, Green CB, Nuessen JA, Yeater K. ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 2004, 150:2415-2428.
87. Zhao X, Oh SH, Yeater KM, Hoyer LL. Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the Als family. Microbiology 2005, 151:1619-1630.
88. Zhao X, Oh SH, Hoyer LL. Unequal contribution of ALS9 alleles to adhesion between Candida albicans and human vascular endothelial cells. Microbiology 2007a, 153:2342-2350.
89. Zhao X, Oh SH, Hoyer LL. Deletion of ALS5, ALS6 or ALS7 increases adhesion of Candida albicans to human vascular endothelial and buccal epithelial cells. Med Mycol 2007b, 45:429-434.