Host-pathogen interactions and virulence-associated genes during Candida albicans oral infections

International Journal of Medical Microbiology

Volumn 301, Issue 5, 2011, Pages 417-422

  Martin, Ronny ^a,c   Wächtler, Betty ^a   Schaller, Martin ^b   Wilson, Duncan ^a   Hube, Bernhard ^a,c  

^a HANS KNÖLL INSTITUTE   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

C. albicans; Oral infections; Transcriptional profiling; Virulence associated genes

Indexed keywords

ADHESIN; ALS PROTEIN; CARBON; HWP1 PROTEIN; HYDROLASE; INVASIN; UNCLASSIFIED DRUG;

CANDIDIASIS; CARBON SOURCE; DISEASE ASSOCIATION; ENDOCYTOSIS; ENVIRONMENT; EPITHELIUM CELL; FUNGAL GENE; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; HOST; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MUTANT; NITROSATIVE STRESS; NONHUMAN; PH; PRESSURE; PSEUDOMEMBRANOUS CANDIDIASIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHORT SURVEY; THRUSH;

CANDIDA ALBICANS; CANDIDIASIS, ORAL; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HOST-PATHOGEN INTERACTIONS; HUMANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VIRULENCE; VIRULENCE FACTORS;

EID: 79956359929     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2011.04.009     Document Type: Short Survey

References (76)

1. Almeida R.S., Brunke S., Albrecht A., Thewes S., Laue M., Edwards J.E., Filler S.G., Hube B. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 2008, 4:e1000217.
2. Biswas S., Van Dijck P., Datta A. Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol. Mol. Biol. Rev. 2007, 71:348-376.
3. Butler G., Rasmussen M.D., Lin M.F., Santos M.A., Sakthikumar S., Munro C.A., Rheinbay E., Grabherr M., Forche A., Reedy J.L., Agrafioti I., Arnaud M.B., Bates S., Brown A.J., Brunke S., Costanzo M.C., Fitzpatrick D.A., de Groot P.W., Harris D., Hoyer L.L., Hube B., Klis F.M., Kodira C., Lennard N., Logue M.E., Martin R., Neiman A.M., Nikolaou E., Quail M.A., Quinn J., Santos M.C., Schmitzberger F.F., Sherlock G., Shah P., Silverstein K.A., Skrzypek M.S., Soll D., Staggs R., Stansfield I., Stumpf M.P., Sudbery P.E., Srikantha T., Zeng Q., Berman J., Berriman M., Heitman J., Gow N.A., Lorenz M.C., Birren B.W., Kellis M., Cuomo C.A. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 2009, 459:657-662.
4. Blankenship J.R., Mitchell A.P. How to build a biofilm: a fungal perspective. Curr. Opin. Microbiol. 2006, 9:588-594.
5. Caracuel-Rios Z., Talbot N.J. Cellular differentiation and host invasion by the rice blast fungus Magnaporthe grisea. Curr. Opin. Microbiol. 2007, 10:339-345.
6. Challacombe S.J., Naglik J.R. The effects of HIV infection on oral mucosal immunity. Adv. Dent. Res. 2006, 19:29-35.
7. Correira A., Lermann U., Teixeira L., Cerca F., Botelho S., Gil da Costa R.M., Sampaio P., Gärtner F., Morschhäuser J., Vilanova M., Pais C. Limited role of secreted aspartyl proteinases Sap1-6 in Candida albicans virulence and host immune response in murine hematogenously disseminated candidiasis. Infect. Immun. 2010, 10.1128/IAI. 00248-10.
8. Dalle F., Wächtler B., L'Ollivier C., Holland G., Bannert N., Wilson D., Labruere C., Bonnin A., Hube B. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell Microbiol. 2009, 12:248-271.
9. Edgerton M., Koshlukova S.E. Salivary histatin 5 and its similarities to the other antimicrobial proteins in human saliva. Adv. Dent. Res. 2000, 14:16-21.
10. Elahi S., Pang G., Ashman R., Clancy R. Enhanced clearance of Candida albicans from the oral cavities of mice following oral administration of Lactobacillus acidophilus. Clin. Exp. Immunol. 2005, 141:29-36.
11. Ferwerda G., Netea M.G., Joosten L.A., van der Meer J.W., Romani L., Kullberg B.J. The role of Toll-like receptors and C-type lectins for vaccination against Candida albicans. Vaccine 2010, 28:614-622.
12. Fidel P.L. Candida-host interactions in HIV disease: relationships in oropharyngeal candidiasis. Adv. Dent. Res. 2006, 19:80-84.
13. Filler S.G., Sheppard D.C. Fungal invasion of normally non-phagocytic host cells. PLoS Pathog. 2006, 2:e129.
14. Green C.B., Marretta S.M., Cheng G., Faddoul F.F., Ehrhart E.J., Hoyer L.L. RT-PCR analysis of Candida albicans ALS gene expression in a hyposalivatory rat model of oral candidiasis and in HIV-positive human patients. Med. Mycol. 2006, 44:103-111.
15. Hiller E., Heine S., Brunner H., Rupp S. Candida albicans Sun41p, a putative glycosidase, is involved in morphogenesis, cell wall biogenesis, and biofilm formation. Eukaryot. Cell 2007, 6:2056-2065.
16. Hogan D.A., Kolter R. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 2002, 296:2229-2232.
17. Ibrahim A.S., Spellberg B.J., Avenissian V., Fu Y., Filler S.G., Edwards J.E. Vaccination with recombinant N-terminal domain of Als1p improves survival during murine disseminated candidiasis by enhancing cell-mediated, not humoral, immunity. Infect. Immun. 2005, 73:999-1005.
18. Ibrahim A.S., Spellberg B.J., Avanesian V., Fu Y., Edwards J.E. The anti-Candida vaccine based on the recombinant N-terminal domain of Als1p is broadly active against disseminated candidiasis. Infect. Immun. 2006, 74:3039-3041.
19. Jainkittivong A., Johnson D.A., Yeh C.K. The relationship between salivary histatin levels and oral yeast carriage. Oral Microbiol. Immunol. 1998, 13:181-187.
20. Jouault T., Sarazin A., Martinez-Esparza M., Fradin C., Sendid B., Poulain D. Host responses to a versatile commensal: PAMPs and PRRs interplay leading to tolerance or infection by Candida albicans. Cell. Microbiol. 2009, 11:1007-1015.
21. LaFleur M.D., Kumamoto C.A., Lewis K. Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob. Agents Chemother. 2006, 50:3839-3846.
22. Leidich S.D., Ibrahim A.S., Fu Y., Koul A., Jessup C., Vitullo J., Fonzi W., Mirbod F., Nakashima S., Nozawa Y., Ghannoum M.A. Cloning and disruption of CaPLB1, aphospholipase B gene involved in the pathogenicity of Candida albicans. J. Biol. Chem. 1998, 270:26078-26086.
23. Leito J.T., Ligtenberg A.J., Nazmi K., Veerman E.C. Identification of salivary components that induce transition of hyphae to yeast in Candida albicans. FEMS Yeast Res. 2009, 9:1102-1110.
24. Lermann U., Morschhäuser J. Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albicans. Microbiology 2008, 154:3281-3295.
25. Li F., Palecek S.P. EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot. Cell 2003, 2:1266-1273.
26. Li F., Svarovsky M.J., Karlsson A.J., Wagner J.P., Marchillo K., Oshel P., Andes D., Palecek S.P. Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot. Cell 2007, 6:931-939.
27. Malic S., Hill K.E., Ralphs J.R., Hayes A., Thomas D.W., Potts A.J., Williams D.W. Characterization of Candida albicans infection of an in vitro oral epithelial model using confocal laser scanning microscopy. Oral Microbiol. Immunol. 2007, 22:188-194.
28. Martin G.S., Mannino D.M., Eaton S., Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 2003, 348:1546-1554.
29. Martin R., Moran G.P., Jacobsen I.D., Heyken A., Domey J., Sullivan D.J., Kurzai O., Hube B. The Candida albicans-specific gene EED1 encodes a key regulator of hyphal extension. PLoS One 2011, 6:e18394.
30. Meiller T.F., Hube B., Schild L., Shirtliff M.E., Scheper M.A., Winkler R., Ton A., Jabra-Rizk M.A. A novel immune evasion strategy of Candida albicans: proteolytic cleavage of a salivary antimicrobial peptide. PLoS One 2009, 4:e5039.
31. Mühlschlegel F.A., Fonzi W.A. PHR2 of Candida albicans encodes a functional homolog of the pH-regulated gene PHR1 with an inverted pattern of pH-dependent expression. Mol. Cell Biol. 1997, 17:5960-5967.
32. Mukherjee P.K., Zhou G., Munyon R., Ghannoum M.A. Candida biofilm: a well-designed protected environment. Med. Mycol. 2005, 43:191-208.
33. Naglik J.R., Scott J., Rahman D., Mistry M., Challacombe S.J. Serum and saliva antibodies do not inhibit Candida albicans Sap2 proteinase activity using a BSA hydrolysis assay. Med. Mycol. 2005, 43:73-77.
34. Naglik J.R., Fostira F., Ruprai J., Staab J.F., Challacombe S.J., Sundstrom P. Candida albicans HWP1 gene expression and host antibody responses in colonization and disease. J. Med. Microbiol. 2006, 55:1323-1327.
35. Naglik J.R., Fidel P.L., Odds F.C. Animal models of mucosal Candida infection. FEMS Microbiol. Lett. 2008, 283:129-139.
36. Naglik J.R., Moyes D., Makwana J., Kanzaria P., Tsichlaki E., Weindl G., Tappuni A.R., Rodgers C.A., Woodman A.J., Challacombe S.J., Schaller M., Hube B. Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 2008, 154:3266-3280.
37. Netea M.G., Brown G.D., Kullberg B.J., Gow N.A. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 2008, 6:67-78.
38. Nobile C.J., Andes D.R., Nett J.E., Smith F.J., Yue F., Phan Q.T., Edwards J.E., Filler S.G., Mitchell A.P. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2006, 2:e63.
39. Nobile C.J., Schneider H.A., Nett J.E., Sheppard D.C., Filler S.G., Andes D.R., Mitchell A.P. Complementary adhesin function in C. albicans biofilm formation. Curr. Biol. 2008, 18:1017-1024.
40. Nobile C.J., Solis N., Myers C.L., Fay A.J., Deneault J.S., Nantel A., Mitchell A.P., Filler S.G. Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions. Cell Microbiol. 2008, 10:2180-2196.
41. Norice C.T., Smith F.J., Solis N., Filler S.G., Mitchell A.P. Requirement for Candida albicans Sun41 in biofilm formation and virulence. Eukaryot. Cell 2007, 6:2046-2055.
42. Park H., Myers C.L., Sheppard D.C., Phan Q.T., Sanchez A.A., Edwards J.E., Filler S.G. Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell Microbiol. 2005, 7:499-510.
43. Park H., Liu Y., Solis N., Spotkov J., Hamaker J., Blankenship J.R., Yeaman M.R., Mitchell A.P., Liu H., Filler S.G. Transcriptional responses of Candida albicans to epithelial and endothelial cells. Eukaryot. Cell 2009, 8:1498-1510.
44. Perlroth J., Choi B., Spellberg B. Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 2007, 45:321-346.
45. Pfaller M.A., Diekema D.J. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 2007, 20:133-163.
46. Phan Q.T., Myers C.L., Fu Y., Sheppard D.C., Yeaman M.R., Welch W.H., Ibrahim A.S., Edwards J.E., Filler S.G. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 2007, 5:e64.
47. Pierce G.E. Pseudomonas aeruginosa, Candida albicans, and device-related nosocomial infections: implications, trends, and potential approaches for control. J. Ind. Microbiol. Biotechnol. 2005, 32:309-318.
48. Pollock J.J., Denepitiya L., MacKay B.J., Iacono V.J. Fungistatic and fungicidal activity of human parotid salivary histidine-rich polypeptides on Candida albicans. Infect. Immun. 1984, 44:702-707.
49. Rahman D., Mistry M., Thavaraj S., Challacombe S.J., Naglik J.R. Murine model of concurrent oral and vaginal Candida albicans colonization to study epithelial host-pathogen interactions. Microb. Infect. 2007, 9:615-622.
50. Ruhnke M., Maschmeyer G. Management of mycoses in patients with hematologic disease and cancer-review of the literature. Eur. J. Med. Res. 2002, 7:227-235.
51. Sandovsky-Losica H., Chauhan N., Calderone R., Segal E. Gene transcription studies of Candida albicans following infection of HEp2 epithelial cells. Med. Mycol. 2006, 44:329-334.
52. Schaller M., Schafer W., Korting H.C., Hube B. Differential expression of secreted aspartyl proteinases in a model of human oral candidosis and in patient samples from the oral cavity. Mol. Microbiol. 1998, 29:605-615.
53. Schaller M., Korting H.C., Schäfer 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.
54. Schaller M., Borelli C., Korting H.C., Hube B. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 2005, 48:365-377.
55. Schaller M., Zakikhany K., Naglik J.R., Weindl G., Hube B. Models of oral and vaginal candidiasis based on in vitro reconstituted human epithelia. Nat. Protoc. 2006, 1:2767-2773.
56. Shen S., Samaranayake L.P., Yip H.K., Dyson J.E. Bacterial and yeast flora of root surface caries in elderly, ethnic Chinese. Oral. Dis. 2002, 8:207-217.
57. Sobel J.D. Pathogenesis and epidemiology of vulvovaginal candidiasis. Ann. N.Y. Acad. Sci. 1988, 544:547-557.
58. Spellberg B., Ibrahim A.S., Edwards J.E., Filler S.G. Mice with disseminated candidiasis die of progressive sepsis. J. Infect. Dis. 2005, 192:336-343.
59. Spellberg B.J., Ibrahim A.S., Avenissian V., Filler S.G., Myers C.L., Fu Y., Edwards J.E. The anti-Candida albicans vaccine composed of the recombinant N terminus of Als1p reduces fungal burden and improves survival in both immunocompetent and immunocompromised mice. Infect. Immun. 2005, 73:6191-6193.
60. Spellberg B.J., Ibrahim A.S., Avanesian V., Fu Y., Myers C., Phan Q.T., Filler S.G., Yeaman M.R., Edwards J.E. Efficacy of the anti-Candida rAls3p-N or rAls1p-N vaccines against disseminated and mucosal candidiasis. J. Infect. Dis. 2006, 194:256-260.
61. Spellberg B., Ibrahim A.S., Yeaman M.R., Lin L., Fu Y., Avanesian V., Bayer A.S., Filler S.G., Lipke P., Otoo H., Edwards J.E. The antifungal vaccine derived from the recombinant N terminus of Als3p protects mice against the bacterium Staphylococcus aureus. Infect. Immun. 2008, 76:4574-4580.
62. Spiering M.J., Moran G.P., Chauvel M., Maccallum D.M., Higgins J., Hokamp K., Yeomans T., d'Enfert C., Coleman D.C., Sullivan D.J. Comparative transcript profiling of Candida albicans and Candida dubliniensis identifies SFL2, a C. albicans gene required for virulence in a reconstituted epithelial infection model. Eukaryot. Cell 2009, 9:251-265.
63. Staab J.F., Bahn Y.S., Tai C.H., Cook P.F., 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.
64. Taylor B.N., Fichtenbaum C., Saavedra M., Slavinsky I.J., Swoboda R., Wozniak K., Arribas A., Powderly W., Fidel P.L. In vivo virulence of Candida albicans isolates causing mucosal infections in people infected with the human immunodeficiency virus. J. Infect. Dis. 2000, 182:955-959.
65. ten Cate J.M., Klis F.M., Pereira-Cenci T., Crielaard W., de Groot P.W. Molecular and cellular mechanisms that lead to Candida biofilm formation. J. Dent. Res. 2009, 88:105-115.
66. Villar C.C., Kashleva H., Nobile C.J., Mitchell A.P., 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.
67. Villar C.C., Dongari-Bagtzoglou A. Immune defence mechanisms and immunoenhancement strategies in oropharyngeal candidiasis. Expert Rev. Mol. Med. 2008, 10:e29.
68. Wächtler B., Wilson D., Haedicke K., Dalle F., Hube B. From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS One 2011, 6:e17046.
69. Wargo M.J., Hogan D.A. Examination of Pseudomonas aeruginosa lasI regulation and 3-oxo-C12-homoserine lactone production using a heterologous Escherichia coli system. FEMS Microbiol. Lett. 2007, 273:38-44.
70. Weindl G., Naglik J.R., Kaesler S., Biedermann T., Hube B., Korting H.C., Schaller M. Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J. Clin. Invest. 2007, 117:3664-3672.
71. White S.J., Rosenbach A., Lephart P., Nguyen D., Benjamin A., Tzipori S., Whiteway M., Mecsas J., Kumamoto C.A. Self-regulation of Candida albicans population size during GI colonization. PLoS Pathog. 2007, 3:e184.
72. Wilson D., Thewes S., Zakikhany K., Fradin C., Albrecht A., Almeida R., Brunke S., Grosse K., Martin R., Mayer F., Leonhardt I., Schild L., Seider K., Skibbe M., Slesiona S., Waechtler B., Jacobsen I., Hube B. Identifying infection-associated genes of Candida albicans in the postgenomic era. FEMS Yeast Res. 2009, 9:688-700.
73. Zakikhany K., Naglik J.R., 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.
74. Zaremba M.L., Stokowska W., Klimiuk A., Daniluk T., Rozkiewicz D., Cylwik-Rokicka D., Waszkiel D., Tokajuk G., Kierklo A., Abdelrazek S. Microorganisms in root carious lesions in adults. Adv. Med. Sci. 2006, 51(Suppl 1):237-240.
75. Zhu W., Filler S.G. Interactions of Candida albicans with epithelial cells. Cell Microbiol. 2010, 12:273-282.
76. Zijnge V., van Leeuwen M.B., Degener J.E., Abbas F., Thurnheer T., Gmür R., Harmsen H.J. Oral biofilm architecture on natural teeth. PLoS One 2010, 5:e9321.