Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood

Molecular Microbiology

Volumn 56, Issue 2, 2005, Pages 397-415

  Fradin, Chantal ^a   De Groot, Piet ^b   MacCallum, Donna ^c   Schaller, Martin ^d   Klis, Frans ^b   Odds, Frank C ^c   Hube, Bernhard ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; GLYCOSYLPHOSPHATIDYLINOSITOL; NITROGEN; SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE 5; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANDIDA ALBICANS; CELL STRUCTURE; CELL SURFACE; CULTURE MEDIUM; ERYTHROCYTE; FEMALE; FUNGAL VIRULENCE; FUNGUS CULTURE; FUNGUS GROWTH; GENE EXPRESSION; GENE INDUCTION; GRANULOCYTE; GROWTH INHIBITION; MONONUCLEAR CELL; MOUSE; MOUSE STRAIN; MYCOSIS; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SURVIVAL RATE; TRANSCRIPTION REGULATION;

BLOOD; CANDIDA ALBICANS; CANDIDIASIS; CELL PROLIFERATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GRANULOCYTES; HUMANS; TRANSCRIPTION, GENETIC;

CANDIDA ALBICANS; FUNGI;

EID: 17144368786     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04557.x     Document Type: Article

References (58)

1. Alarco, A.M., and Raymond, M. (1999) The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J Bacteriol 181: 700-708.
2. Augstein, A., Barth, K., Gentsch, M., Kohlwein, S.D., and Barth, G. (2003) Characterization, localization and functional analysis of Gpr1p, a protein affecting sensitivity to acetic acid in the yeast Yarrowia lipolytica. Microbiology 149: 589-600.
3. Barelle, C.J., Manson, C.L., MacCallum, D.M., Odds, F.C., Gow, N.A., and Brown, A.J. (2004) GFP as a quantitative reporter of gene regulation in Candida albicans. Yeast 21: 333-340.
4. Berman, J., and Sudbery, P.E. (2002) Candida albicans: a molecular revolution built on lessons from budding yeast. Nat Rev Genet 3: 918-930.
5. Borg-von Zepelin, M., Beggah, S., Boggian, K., Sanglard, D., and Monod, M. (1998) The expression of the secreted aspartyl proteinases Sap4 to Sap6 from Candida albicans in murine macrophages. Mol Microbiol 28: 543-554.
6. Brand, A., MacCallum, D.M., Brown, A.J., Gow, N.A., and Odds, F.C. (2004) Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot Cell 3: 900-909.
7. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D.S., et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
8. Brown, A.J., and Gow, N.A. (1999) Regulatory networks controlling Candida albicans morphogenesis. Trends Microbiol 7: 333-338.
9. Busetto, S., Trevisan, E., Patriarca, P., and Menegazzi, R. (2004) A single-step, sensitive flow cytofluorometric assay for the simultaneous assessment of membrane-bound and ingested Candida albicans in phagocytosing neutrophils. Cytometry 58A: 201-206.
10. Calderone, R.A., and Fonzi, W.A. (2001) Virulence factors of Candida albicans. Trends Microbiol 9: 327-335.
11. Caro, L.H., Tettelin, H., Vossen, J.H., Ram, A.F., van den Ende, H., and Klis, F.M. (1997) In silicio identification of glycosyl-phosphatidylinositol- anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13: 1477-1489.
12. De Groot, P.W., Hellingwerf, K.J., and Klis, F.M. (2003) Genome-wide identification of fungal GPI proteins. Yeast 20: 781-796.
13. De Groot, P.W.J., De Boer, A.D., Cunningham, J., Dekker, H.L., De Jong, L., Hellingwerf, K.J., et al. (2004) Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Euk Cell 3: 955-965.
14. Diamond, R.D., Clark, R.A., and Haudenschild, C.C. (1980) Damage to Candida albicans hyphae and pseudohyphae by the myeloperoxidase system and oxidative products of neutrophil metabolism in vitro. J Clin Invest 66: 908-917.
15. Diamond, R.D., and Haudenschild, C.C. (1981) Monocyte-mediated serum-independent damage to hyphal and pseudohyphal forms of Candida albicans in vitro. J Clin Invest 67: 173-182.
16. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
17. Enjalbert, B., Mantel, A., and Whiteway, M. (2003) Stress-induced gene expression in Candida albicans: absence of a general stress response. Mol Biol Cell 14: 1460-1467.
18. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M., and Hinton, J.C. (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103-118.
19. Faurschou, M., and Borregaard, N. (2003) Neutrophil granules and secretory vesicles in inflammation. Microbes Infect 5: 1317-1327.
20. Felk, A., Kretschmar, M., Albrecht, A., Schaller, M., Beinhauer, S., Nichterlein, T., et al. (2002) 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 70: 3689-3700.
21. Fonzi, W.A., and Irwin, M.Y. (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717-728.
22. Fradin, C., Kretschmar, M., Nichterlein, T., Gaillardin, C., d'Enfert, C., and Hube, B. (2003) Stage-specific gene expression of Candida albicans in human blood. Mol Microbiol 47: 1523-1543.
23. Fu, Y., Ibrahim, A.S., Sheppard, D.C., Chen, Y.C., French, S.W., Cutler, J.E., et al. (2002) Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol Microbiol 44: 61-72.
24. Gietz, R.D., and Woods, R.A. (2001) Genetic transformation of yeast. Biotechniques 30: 816-820, 822-816, 828 passim.
25. Gillum, A.M., Tsay, E.Y., and Kirsch, D.R. (1984) 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 198: 179-182.
26. Hampton, M.B., Kettle, A.J., and Winterbourn, C.C. (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007-3017.
27. Henson, P., Henson, J., Fittschen, C., Kimani, G., Bratton, D., and Riches, D. (1988) Phagocytic cells: degranulation and secretion. In Inflammation: Basic Principles and Clinical Correlates. Ji Gallin, I.G., and Snyderman, R. (eds). New York: Raven Press, pp. 363-390.
28. Hwang, C.S., Rhie, G., Kim, ST., Kim, Y.R., Huh, W.K., Baek, Y.U., and Kang, S.O. (1999) Copper- and zinc-containing superoxide dismutase and its gene from Candida albicans. Biochim Biophys Acta 1427: 245-255.
29. Kullberg, B.J., and Oude Lashof, A.M. (2002) Epidemiology of opportunistic invasive mycoses. Eur J Med Res 7: 183-191.
30. Lamarre, C., LeMay, J.D., Deslauriers, N., and Bourbonnais, Y. (2001) Candida albicans expresses an unusual cytoplasmic manganese-containing superoxide dismutase (SOD3 gene product) upon the entry and during the stationary phase. J Biol Chem 276: 43784-43791.
31. Lane, S., Birse, C., Zhou, S., Matson, R., and Liu, H. (2001) DNA array studies demonstrate convergent regulation of virulence factors by Cph1, Cph2, and Efg1 in Candida albicans. J Biol Chem 276: 48988-48996.
32. Lehrer, R.I., Ladra, K.M., and Hake, R.B. (1975) Nonoxidative fungicidal mechanisms of mammalian granulocytes: demonstration of components with candidacidal activity in human, rabbit, and guinea pig leukocytes. Infect Immun 11: 1226-1234.
33. Liu, H., Kohler, J., and Fink, G.R. (1994) Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723-1726.
34. Liu, L., Kang, K., Takahara, M., Cooper, K.D., and Ghannoum, M.A. (2001) Hyphae and yeasts of Candida albicans differentially regulate interleukin-12 production by human blood monocytes: inhibitory role of C. albicans germination. Infect Immun 69: 4695-4697.
35. Lorenz, M.C., and Fink, G.R. (2001) The glyoxylate cycle is required for fungal virulence. Nature 412: 83-86.
36. Marini, A.M., Soussi-Boudekou, S., Vissers, S., and Andre, B. (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 17: 4282-4293.
37. Martchenko, M., Alarco, A.M., Marcus, D., and Whiteway, M. (2004) CuZn superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal induced SOD5 gene. Mol Biol Cell 15: 456-467.
38. Murad, A.M., Lee, P.R., Broadbent, I.D., Barelle, C.J., and Brown, A.J. (2000) Clp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16: 325-327.
39. Mantel, A., Dignard, D., Bachewich, C., Harcus, D., Marcil, A., Bouin, A.P., et al. (2002) Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol Biol Cell 13: 3452-3465.
40. Okutomi, T., Abe, S., Tansho, S., Wakabayashi, H., Kawase, K., and Yamaguchi, H. (1997) Augmented inhibition of growth of Candida albicans by neutrophils in the presence of lactoferrin. FEMS Immunol Med Microbiol 18: 105-112.
41. Pfaller, M.A., Jones, R.N., Doern, G.V., Sader, H.S., Messer, S.A., Houston, A., et al. (2000) Bloodstream infections due to Candida species: SENTRY antimicrobial surveillance program in North America and Latin America, 1997-1998. Antimicrob Agents Chemother 44: 747-751.
42. Phan, Q.T., Belanger, P.M., and Filler, S.G. (2000) Role of hyphal formation in interactions of Candida albicans with endothelial cells. Infect Immun 68: 3485-3490.
43. Ramarao, N., Gray-Owen, S.D., and Meyer, T.F. (2000) Helicobacter pylori induces but survives the extracellular release of oxygen radicals from professional phagocytes using its catalase activity. Mol Microbiol 38: 103-113.
44. Rex, J.H., Bennett, J.E., Sugar, A.M., Pappas, P.G., van der Horst, C.M., Edwards, J.E., et al. (1994) A randomized trial comparing fluconazole with amphotericin B for the treatment of candidemia in patients without neutropenia. Candidemia Study Group and the National Institute. N Engl J Med 331: 1325-1330.
45. Rotrosen, D., Edwards, J.E., Jr, Gibson, T.R., Moore, J.C., Cohen, A.H., and Green, I. (1985) Adherence of Candida to cultured vascular endothelial cells: mechanisms of attachment and endothelial cell penetration. J Infect Dis 152: 1264-1274.
46. Rubin-Bejerano, I., Fraser, I., Grisafi, P., and Fink, G.R. (2003) Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc Natl Acad Sci USA 100: 11007-11012.
47. Sanglard, D., Hube, B., Monod, M., Odds, F.C., and Gow, N.A. (1997) A triple deletion of the secreted aspartyl proteinase genes SAP4, SAP5, and SAP6 of Candida albicans causes attenuated virulence. Infect Immun 65: 3539-3546.
48. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
49. Smail, E.H., Cronstein, B.N., Meshulam, T., Esposito, A.L., Ruggeri, R.W., and Diamond, R.D. (1992) In vitro, Candida albicans releases the immune modulator adenosine and a second, high-molecular weight agent that blocks neutrophil killing. J Immunol 148: 3588-3595.
50. Staudinger, B.J., Oberdoerster, M.A., Lewis, P.J., and Rosen, H. (2002) mRNA expression profiles for Escherichia coli ingested by normal and phagocyte oxidase-deficient human neutrophils. J Clin Invest 110: 1151-1163.
51. Stoldt, V.R., Sonneborn, A., Leuker, C.E., and Ernst, J.F. (1997) Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J 16: 1982-1991.
52. Torosantucci, A., Chiani, P., and Cassone, A. (2000) Differential chemokine response of human monocytes to yeast and hyphal forms of Candida albicans and its relation to the beta-1,6 glucan of the fungal cell wall. J Leukoc Biol 68: 923-932.
53. Tripathi, G., Wiltshire, C., Macaskill, S., Tournu, H., Budge, S., and Brown, A.J. (2002) Gcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans. EMBO J 21: 5448-5456.
54. Velasco, E., Thuler, L.C., Martins, C.A., Nucci, M., Dias, L.M., and Goncalves, V.M. (2000) Epidemiology of bloodstream infections at a cancer center. Sao Paulo Med J 118: 131-138.
55. Vossen, J.H., Muller, W.H., Lipke, P.M., and Klis, F.M. (1997) Restrictive glycosylphosphatidylinositol anchor synthesis in cwh6/gpi3 yeast cells causes aberrant biogenesis of cell wall proteins. J Bacteriol 179: 2202-2209.
56. Wakabayashi, H., Abe, S., Teraguchi, S., Hayasawa, H., and Yamaguchi, H. (1998) Inhibition of hyphal growth of azole-resistant strains of Candida albicans by triazole antifungal agents in the presence of lactoferrin-related compounds. Antimicrob Agents Chemother 42: 1587-1591.
57. Zink, S., Nass, T., Rosen, P., and Ernst, J.F. (1996) Migration of the fungal pathogen Candida albicans across endothelial monolayers. Infect Immun 64: 5085-5091.
58. Zubenko, G.S., and Jones, E.W. (1981) Protein degradation, meiosis and sporulation in proteinase-deficient mutants of Saccharomyces cerevisiae. Genetics 97: 45-64.