Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes

Cellular Microbiology

Volumn 12, Issue 2, 2010, Pages 248-271

  Dalle, Frederic ^a,b,c   Wächtler, Betty ^a,d   L'Ollivier, Coralie ^b,c   Holland, Gudrun ^a   Bannert, Norbert ^a   Wilson, Duncan ^d   Labruère, Catherine ^f   Bonnin, Alain ^b,c   Hube, Bernhard ^a,d,e  

^a ROBERT KOCH INSTITUTE   (Germany)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c DIJON UNIVERSITY HOSPITAL   (France)

^d HANS KNÖLL INSTITUTE   (Germany)

^e FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^f UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CELL ADHESION; CELL DAMAGE; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; FUNGUS MUTANT; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTESTINE CELL; MOUTH MUCOSA; MUCOSA CELL; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; CELL STRAIN CACO 2; CYTOLOGY; EPITHELIUM CELL; MICROBIOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

CANDIDA ALBICANS; FUNGI;

CACO-2 CELLS; CANDIDA ALBICANS; CELL DIFFERENTIATION; CELL LINE, TUMOR; ENTEROCYTES; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE;

EID: 77649229368     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01394.x     Document Type: Article

References (82)

1. Allison AC, Davies P, De Petris S. Role of contractile microfilaments in macrophage movement and endocytosis. Nat New Biol 1971, 232:153-155.
2. Amyere M, Mettlen M, Van Der Smissen P, Platek A, Payrastre B, Veithen A, Courtoy PJ. Origin, originality, functions, subversions and molecular signalling of macropinocytosis. Int J Med Microbiol 2002, 291:487-494.
3. Antley PP, Hazen KC. Role of yeast cell growth temperature on Candida albicans virulence in mice. Infect Immun 1988, 56:2884-2890.
4. Bernhardt J, Herman D, Sheridan M, Calderone R. Adherence and invasion studies of Candida albicans strains, using in vitro models of esophageal candidiasis. J Infect Dis 2001, 184:1170-1175.
5. Brand A, Shanks S, Duncan VM, Yang M, Mackenzie K, Gow NA. Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr Biol 2007, 17:347-352.
6. Cole GT, Halawa AA, Anaissie EJ. The role of the gastrointestinal tract in hematogenous candidiasis: from the laboratory to the bedside. Clin Infect Dis 1996, 22(Suppl. 2):S73-S88.
7. Cossart P. Host/pathogen interactions. Subversion of the mammalian cell cytoskeleton by invasive bacteria. J Clin Invest 1997, 99:2307-2311.
8. Coyne CB, Shen L, Turner JR, Bergelson JM. Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2007, 2:181-192.
9. Dalle F, Jouault T, Trinel PA, Esnault J, Mallet JM, d'Athis P. Beta-1,2- and alpha-1,2-linked oligomannosides mediate adherence of Candida albicans blastospores to human enterocytes in vitro. Infect Immun 2003, 71:7061-7068.
10. Dieterich C, Schandar M, Noll M, Johannes FJ, Brunner H, Graeve T, Rupp S. In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion. Microbiology 2002, 148:497-506.
11. Enache E, Eskandari T, Borja L, Wadsworth E, Hoxter B, Calderone R. Candida albicans adherence to a human oesophageal cell line. Microbiology 1996, 142(Part 10):2741-2746.
12. Eto DS, Sundsbak JL, Mulvey MA. Actin-gated intracellular growth and resurgence of uropathogenic Escherichia coli. Cell Microbiol 2006, 8:704-717.
13. Eugene E, Hoffmann I, Pujol C, Couraud PO, Bourdoulous S, Nassif X. Microvilli-like structures are associated with the internalization of virulent capsulated Neisseria meningitidis into vascular endothelial cells. J Cell Sci 2002, 115:1231-1241.
14. Felk A, Kretschmar M, Albrecht A, Schaller M, Beinhauer S, Nichterlein T. Candida albicans hyphal formation and the expression of the Efg1-regulated proteinases Sap4 to Sap6 are required for the invasion of parenchymal organs. Infect Immun 2002, 70:3689-3700.
15. Finlay BB, Cossart P. Exploitation of mammalian host cell functions by bacterial pathogens. Science 1997, 276:718-725.
16. Fradin C, De Groot P, MacCallum D, Schaller M, Klis F, Odds FC, Hube B. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 2005, 56:397-415.
17. 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.
18. Gacser A, Stehr F, Kroger C, Kredics L, Schafer W, Nosanchuk JD. Lipase 8 affects the pathogenesis of Candida albicans. Infect Immun 2007, 75:4710-4718.
19. Gillum AM, Tsay EY, Kirsch DR. Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 1984, 198:179-182.
20. Gow NA, Brown AJ, Odds FC. Fungal morphogenesis and host invasion. Curr Opin Microbiol 2002, 5:366-371.
21. Harrison RE, Grinstein S. Phagocytosis and the microtubule cytoskeleton. Biochem Cell Biol 2002, 80:509-515.
22. Hazen KC. Participation of yeast cell surface hydrophobicity in adherence of Candida albicans to human epithelial cells. Infect Immun 1989, 57:1894-1900.
23. Hazen KC, Brawner DL, Riesselman MH, Jutila MA, Cutler JE. Differential adherence of hydrophobic and hydrophilic Candida albicans yeast cells to mouse tissues. Infect Immun 1991, 59:907-912.
24. Hewlett LJ, Prescott AR, Watts C. The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol 1994, 124:689-703.
25. Hube B, Naglik JR. Extracellular Hydrolases 2002, 107-122. Calderone RA, In: and Candidiasis, ed., Washington DC, USA, ASM Press, pp.
26. Hube B, Sanglard D, Odds FC, Hess D, Monod M, Schafer W. Disruption of each of the secreted aspartyl proteinase genes SAP1, SAP2, and SAP3 of Candida albicans attenuates virulence. Infect Immun 1997, 65:3529-3538.
27. Isberg RR, Voorhis DL, Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 1987, 50:769-778.
28. King RD, Lee JC, Morris AL. Adherence of Candida albicans and other Candida species to mucosal epithelial cells. Infect Immun 1980, 27:667-674.
29. Kunze D, Melzer I, Bennett D, Sanglard D, MacCallum D, Norskau J. Functional analysis of the phospholipase C gene CaPLC1 and two unusual phospholipase C genes, CaPLC2 and CaPLC3, of Candida albicans. Microbiology 2005, 151:3381-3394.
30. 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.
31. Mavor AL, Thewes S, Hube B. Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes. Curr Drug Targets 2005, 6:863-874.
32. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 1996, 84:923-932.
33. Molinari G, Rohde M, Guzman CA, Chhatwal GS. Two distinct pathways for the invasion of Streptococcus pyogenes in non-phagocytic cells. Cell Microbiol 2000, 2:145-154.
34. Mullin JM, Agostino N, Rendon-Huerta E, Thornton JJ. Keynote review: epithelial and endothelial barriers in human disease. Drug Discov Today 2005, 10:395-408.
35. Naglik J, Albrecht A, Bader O, Hube B. Candida albicans proteinases and host/pathogen interactions. Cell Microbiol 2004, 6:915-926.
36. Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 2003a, 67:400-428. table of contents.
37. 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 2003b, 188:469-479.
38. 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.
39. Nazli A, Wang A, Steen O, Prescott D, Lu J, Perdue MH. Enterocyte cytoskeleton changes are crucial for enhanced translocation of nonpathogenic Escherichia coli across metabolically stressed gut epithelia. Infect Immun 2006, 74:192-201.
40. Nucci M, Anaissie E. Revisiting the source of candidemia: skin or gut? Clin Infect Dis 2001, 33:1959-1967.
41. Odds FC. Ecology of Candida and epidemiology of Candidiasis. 1988, 68-92. Odds FC. In: and Candidiasis, ed., London, UK, Bailliere Tindall, pp.
42. Odds FC. Secreted proteinases and Candida albicans virulence. Microbiology 2008, 154:3245-3246.
43. Oelschlaeger TA, Guerry P, Kopecko DJ. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc Natl Acad Sci USA 1993, 90:6884-6888.
44. 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.
45. 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.
46. Pietiainen V, Marjomaki V, Upla P, Pelkmans L, Helenius A, Hyypia T. Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol Biol Cell 2004, 15:4911-4925.
47. Pinto M, Robine-Leon S, Appay M, Kedinger M, Triadou N, Dussaulx E. Enterocyte-like diiferentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol Cell 1983, 47:323-330.
48. Pittet D, Monod M, Suter PM, Frenk E, Auckenthaler R. Candida colonization and subsequent infections in critically ill surgical patients. Ann Surg 1994, 220:751-758.
49. Pizarro-Cerda J, Cossart P. Bacterial adhesion and entry into host cells. Cell 2006, 124:715-727.
50. 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.
51. Rosenshine I, Donnenberg MS, Kaper JB, Finlay BB. Signal transduction between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induces tyrosine phosphorylation of host cell proteins to initiate cytoskeletal rearrangement and bacterial uptake. EMBO J 1992, 11:3551-3560.
52. Ruhnke M. Skin and mucous membrane infections. 2002, 307-325. Calderone RA. In: Candida and Candidosis, ed., Washington DC, USA, ASM Press, pp.
53. Rupniak HT, Rowlatt C, Lane EB, Steele JG, Trejdosiewicz LK, Laskiewicz B. Characteristics of four new human cell lines derived from squamous cell carcinomas of the head and neck. J Natl Cancer Inst 1985, 75:621-635.
54. Sanglard D, Hube B, Monod M, Odds FC, Gow NA. A triple deletion of the secreted aspartyl proteinase genes SAP4, SAP5, and SAP6 of Candida albicans causes attenuated virulence. Infect Immun 1997, 65:3539-3546.
55. Sansonetti P. Host-pathogen interactions: the seduction of molecular cross talk. Gut 2002, 50(Suppl. 3):III2-III8.
56. Schaller M, Hube B, Ollert MW, Schafer W, Borg-von Zepelin M, Thoma-Greber E, Korting HC. In vivo expression and localization of Candida albicans secreted aspartyl proteinases during oral candidiasis in HIV-infected patients. J Invest Dermatol 1999, 112:383-386.
57. Schaller M, Mailhammer R, Grassl G, Sander CA, Hube B, Korting HC. Infection of human oral epithelia with Candida species induces cytokine expression correlated to the degree of virulence. J Invest Dermatol 2002, 118:652-657.
58. Schaller M, Boeld U, Oberbauer S, Hamm G, Hube B, Korting HC. Polymorphonuclear leukocytes (PMNs) induce protective Th1-type cytokine epithelial responses in an in vitro model of oral candidosis. Microbiology 2004, 150:2807-2813.
59. Schaller M, Borelli C, Korting HC, Hube B. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 2005, 48:365-377.
60. Schaller M, Zakikhany K, Naglik JR, Weindl G, Hube B. Models of oral and vaginal candidiasis based on in vitro reconstituted human epithelia. Nat Protoc 2006, 1:2767-2773.
61. Schofield DA, Westwater C, Warner T, Balish E. Differential Candida albicans lipase gene expression during alimentary tract colonization and infection. FEMS Microbiol Lett 2005, 244:359-365.
62. Silva TM, Glee PM, Hazen KC. Influence of cell surface hydrophobicity on attachment of Candida albicans to extracellular matrix proteins. J Med Vet Mycol 1995, 33:117-122.
63. Slevogt H, Seybold J, Tiwari KN, Hocke AC, Jonatat C, Dietel S. Moraxella catarrhalis is internalized in respiratory epithelial cells by a trigger-like mechanism and initiates a TLR2- and partly NOD1-dependent inflammatory immune response. Cell Microbiol 2007, 9:694-707.
64. Sohn K, Senyurek I, Fertey J, Konigsdorfer A, Joffroy C, Hauser N. An in vitro assay to study the transcriptional response during adherence of Candida albicans to different human epithelia. FEMS Yeast Res 2006, 6:1085-1093.
65. Soldati T. Unconventional myosins, actin dynamics and endocytosis: a menage a trois? Traffic 2003, 4:358-366.
66. Sousa S, Cabanes D, El-Amraoui A, Petit C, Lecuit M, Cossart P. Unconventional myosin VIIa and vezatin, two proteins crucial for Listeria entry into epithelial cells. J Cell Sci 2004, 117:2121-2130.
67. Southern P, Horbul J, Maher D, Davis DA. C. albicans colonization of human mucosal surfaces. PLoS ONE 2008, 3:e2067.
68. Stehr F, Felk A, Gacser A, Kretschmar M, Mahnss B, Neuber K. Expression analysis of the Candida albicans lipase gene family during experimental infections and in patient samples. FEMS Yeast Res 2004, 4:401-408.
69. Swanson JA, Baer SC. Phagocytosis by zippers and triggers. Trends Cell Biol 1995, 5:89-93.
70. Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol 1995, 5:424-428.
71. Tang P, Rosenshine I, Finlay BB. Listeria monocytogenes, an invasive bacterium, stimulates MAP kinase upon attachment to epithelial cells. Mol Biol Cell 1994, 5:455-464.
72. Voss A, Hollis RJ, Pfaller MA, Wenzel RP, Doebbeling BN. Investigation of the sequence of colonization and candidemia in nonneutropenic patients. J Clin Microbiol 1994, 32:975-980.
73. Wain WH, Price MF, Cawson RA. Factors affecting plaque formation by Candida albicans infecting the chick chorio-allantoic membrane. Sabouraudia 1976, 14:149-151.
74. Weide MR, Ernst JF. Caco-2 monolayer as a model for transepithelial migration of the fungal pathogen Candida albicans. Mycoses 1999, 42(Suppl. 2):61-67.
75. Wendland J, Hellwig D, Walther A, Sickinger S, Shadkchan Y, Martin R. Use of the Porcine Intestinal Epithelium (PIE)-Assay to analyze early stages of colonization by the human fungal pathogen Candida albicans. J Basic Microbiol 2006, 46:513-523.
76. Wiesner SM, Bendel CM, Hess DJ, Erlandsen SL, Wells CL. Adherence of yeast and filamentous forms of Candida albicans to cultured enterocytes. Crit Care Med 2002, 30:677-683.
77. Wooldridge KG, Williams PH, Ketley JM. Host signal transduction and endocytosis of Campylobacter jejuni. Microb Pathog 1996, 21:299-305.
78. Wurzner R, Langgartner M, Spotl L, Eder A, Bujdakova H, Schroppel K, Dierich MP. Temperature-dependent surface expression of the beta-2-integrin analogue of Candida albicans and its role in adhesion to the human endothelium. Exp Clin Immunogenet 1996, 13:161-172.
79. Yang YL, Lo HJ, Hung CC, Li Y. Effect of prolonged HAART on oral colonization with Candida and candidiasis. BMC Infect Dis 2006, 6:8.
80. Yordanov M, Dimitrova P, Patkar S, Falcocchio S, Xoxi E, Saso L, Ivanovska N. Ibogaine reduces organ colonization in murine systemic and gastrointestinal Candida albicans infections. J Med Microbiol 2005, 54:647-653.
81. 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.
82. Zink S, Nass T, Rosen P, Ernst JF. Migration of the fungal pathogen Candida albicans across endothelial monolayers. Infect Immun 1996, 64:5085-5091.