The moonlighting protein Tsa1p is implicated in oxidative stress response and in cell wall biogenesis in Candida albicans

Molecular Microbiology

Volumn 57, Issue 5, 2005, Pages 1318-1341

  Urban, Constantin ^a,c   Xiong, Xin ^a   Sohn, Kai ^a   Schröppel, Klaus ^b   Brunner, Herwig ^a   Rupp, Steffen ^a  

^a FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GENE PRODUCT; MEMBRANE PROTEIN; PROTEIN EFG1P; PROTEIN TSA1P; PROTEIN TUP1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL CELL WALL; BIOGENESIS; CANDIDA ALBICANS; CONTROLLED STUDY; CORRELATION ANALYSIS; DELETION MUTANT; GENE TRANSLOCATION; HOST PATHOGEN INTERACTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; STATISTICAL SIGNIFICANCE;

CANDIDA ALBICANS; CELL NUCLEUS; CELL WALL; CYTOPLASM; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; NUCLEAR PROTEINS; OXIDATIVE STRESS; PEROXIDASES; PROTEIN TRANSPORT; REPRESSOR PROTEINS; THIOREDOXIN REDUCTASE (NADPH); TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VIRULENCE; VITAMIN K 3; WATER;

CANDIDA ALBICANS; SACCHAROMYCES CEREVISIAE;

EID: 23844556478     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04771.x     Document Type: Article

References (72)

1. Angiolella, L., Micocci, M.M., D'Alessio, S., Girolamo, A., Maras, B., and Cassone, A. (2002) Identification of major glucan-associated cell wall proteins of Candida albicans and their role in fluconazole resistance. Antimicrob Agents Chemother 46: 1688-1694.
2. Biteau, B., Labarre, J., and Toledano, M.B. (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425: 980-984.
3. Bjellqvist, B., Pasquali, C., Ravier, F., Sanchez, J.C., and Hochstrasser, D. (1993) A nonlinear wide-range immobilized pH gradient for two-dimensional electrophoresis and its definition in a relevant pH scale. Electrophoresis 14: 1357-1365.
4. Boeke, J.D., LaCroute, F., and Fink, G.R. (1984) A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 197: 345-346.
5. Braun, B.R., and Johnson, A.D. (1997) Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277: 105-109. [See comments 277: 52-53; 278: 20-21.]
6. Braun, B.R., and Johnson, A.D. (2000) TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans. Genetics 155: 57-67.
7. Braun, B.R., Head, W.S., Wang, M.X., and Johnson, A.D. (2000) Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156: 31-44. [In process citation.]
8. Care, R.S., Trevethick, J., Binley, K.M., and Sudbery, P.E. (1999) The MET3 promoter: a new tool for Candida albicans molecular genetics. Mol Microbiol 34: 792-798.
9. Cha, M.K., Yun, C.H., and Kim, I.H. (2000) Interaction of human thiol-specific antioxidant protein 1 with erythrocyte plasma membrane. Biochemistry 39: 6944-6950.
10. Chae, H.Z., and Rhee, S.G. (1994) A thiol-specific antioxidant and sequence homology to various proteins of unknown function. Biofactors 4: 177-180.
11. Chae, H.Z., Uhm, T.B., and Rhee, S.G. (1994) Dimerization of thiol-specific antioxidant and the essential role of cysteine 47. Proc Natl Acad Sci USA 91: 7022-7026.
12. Chaffin, W.L., Lopez-Ribot, J.L., Casanova, M., Gozalbo, D., and Martinez, J.P. (1998) Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 62: 130-180.
13. Chen, J.W., Dodia, C., Feinstein, S.I., Jain, M.K., and Fisher, A.B. (2000) 1-Cys peroxiredoxin, a bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. J Biol Chem 275: 28421-28427.
14. Choi, W., Yoo, Y.J., Kim, M., Shin, D., and Jeon, H.B. (2003) Identification of proteins highly expressed in the hyphae of Candida albicans by two-dimensional electrophoresis. Yeast 20: 1053-1060.
15. Cole, S.R., Ashman, L.K., and Ey, P.L. (1987) Biotinylation: an alternative to radioiodination for the identification of cell surface antigens in immunoprecipitates. Mol Immunol 24: 699-705.
16. Cutler, J.E. (1991) Putative virulence factors of Candida albicans. Annu Rev Microbiol 45: 187-218.
17. d'Enfert, C., Goyard, S., Rodriguez-Arnaveilhe, S., Frangeul, L., Jones, L., Tekaia, F., et al. (2005) CandidaDB: a genome database for Candida albicans pathogenomics. Nucleic Acids Res 33: D353-357.
18. De Groot, P.W., Hellingwerf, K.J., and Klis, F.M. (2003) Genome-wide identification of fungal GPI proteins. Yeast 20: 781-796.
19. Dieterich, C., Schandar, M., Noll, M., Johannes, F.J., Brunner, H., Graeve, T., and Rupp, S. (2002) In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion. Microbiology 148: 497-506.
20. Enjalbert, B., Nantel, A., and Whiteway, M. (2003) Stress-induced gene expression in Candida albicans: absence of a general stress response. Mol Biol Cell 14: 1460-1467.
21. Fonzi, W.A., and Irwin, M.Y. (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717-728.
22. Garrido, E.O., and Grant, C.M. (2002) Role of thioredoxins in the response of Saccharomyces cerevisiae to oxidative stress induced by hydroperoxides. Mol Microbiol 43: 993-1003.
23. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
24. Gerami-Nejad, M., Berman, J., and Gale, C.A. (2001) Cassettes for PCR-mediated construction of green, yellow, and cyan fluorescent protein fusions in Candida albicans. Yeast 18: 859-864.
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. Granato, D., Bergonzelli, G.E., Pridmore, R.D., Marvin, L., Rouvet, M., and Corthesy-Theulaz, I.E. (2004) Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun 72: 2160-2169.
27. 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 cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukariotic Cell 3: 955-965.
28. Hofmann, B., Hecht, H.J., and Flohe, L. (2002) Peroxiredoxins. Biol Chem 383: 347-364.
29. Hong, S.K., Cha, M.K., Choi, Y.S., Kim, W.C., and Kim, I.H. (2002) Msn2p/Msn4p act as a key transcriptional activator of yeast cytoplasmic thiol peroxidase II. J Biol Chem 277: 12109-12117.
30. Huang, M.E., Rio, A.G., Nicolas, A., and Kolodner, R.D. (2003) A genomewide screen in Saccharomyces cerevisiae for genes that suppress the accumulation of mutations. Proc Natl Acad Sci USA 100: 11529-11534.
31. Hughes, R.C. (1999) Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1473: 172-185.
32. Jang, H.H., Lee, K.O., Chi, Y.H., Jung, B.G., Park, S.K., Park, J.H., et al. (2004) Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117: 625-635.
33. Jeffery, C.J. (1999) Moonlighting proteins. Trends Biochem Sci 24: 8-11.
34. Jeffery, C.J. (2003) Moonlighting proteins: old proteins learning new tricks. Trends Genet 19: 415-417.
35. Jitsurong, S., Kiamsiri, S., and Pattararangrong, N. (1993) New milk medium for germ tube and chlamydoconidia production by Candida albicans. Mycopathologia 123: 95-98.
36. Klis, F.M., de Groot, P., and Hellingwerf, K. (2001) Molecular organization of the cell wall of Candida albicans. Med Mycol 39: 1-8.
37. Kohler, J.R., and Fink, G.R. (1996) Candida albicans strains heterozygous and homozygous for mutations in mitogen-activated protein kinase signaling components have defects in hyphal development. Proc Natl Acad Sci USA 93: 13223-13228.
38. Lee, J., Godon, C., Lagniel, G., Spector, D., Garin, J., Labarre, J., and Toledano, M.B. (1999) Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Biol Chem 274: 16040-16046.
39. Lee, S.M., and Park, J.W. (1998) Thermosensitive phenotype of yeast mutant lacking thioredoxin peroxidase. Arch Biochem Biophys 359: 99-106.
40. 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.
41. [Published erratum: Science 1995, 267: 17.]
42. Lo, H.J., Kohler, J.R., Di Domenico, B., Loebenberg, D., Cacciapuoti, A., and Fink, G.R. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
43. Lotz, H., Sohn, K., Brunner, H., Muhlschlegel, F.A., and Rupp, S. (2004) RBR1, a novel pH-regulated cell wall gene of Candida albicans, is repressed by RIM101 and activated by NRG1. Eukaryot Cell 3: 776-784.
44. Martchenko, M., Alarco, A.M., Marcus, D., and Whiteway, M. (2004) Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol Biol Cell 15: 456-467.
45. Missall, T.A., Pusateri, M.E., and Lodge, J.K. (2004) Thiol peroxidase is critical for virulence and resistance to nitric oxide and peroxide in the fungal pathogen, Cryptococcus neoformans. Mol Microbiol 51: 1447-1458.
46. Modun, B., and Williams, P. (1999) The staphylococcal transferrin-binding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. Infect Immun 67: 1086-1092.
47. Morschhauser, J., Michel, S., and Staib, P. (1999) Sequential gene disruption in Candida albicans by FLP-mediated site-specific recombination. Mol Microbiol 32: 547-556.
48. Navarro-Garcia, F., Sanchez, M., Nombela, C., and Pla, J. (2001) Virulence genes in the pathogenic yeast Candida albicans. FEMS Microbiol Rev 25: 245-268.
49. Netto, L.E.S., Chae, H.Z., Kang, S.W., Rhee, S.G., and Stadtman, E.R. (1996) Removal of hydrogen peroxide by thiol-specific antioxidant enzyme (TSA) is involved with its antioxidant properties. TSA possesses thiol peroxidase activity. J Biol Chem 271: 15315-15321.
50. Nickel, W. (2003) The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 270: 2109-2119.
51. Odds, F.C. (1994) Pathogenesis of Candida infections. J Am Acad Dermatol 31: S2-S5.
52. Park, S.G., Cha, M.K., Jeong, W., and Kim, I.H. (2000) Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J Biol Chem 275: 5723-5732.
53. Park, J.W., and Floyd, R.A. (1994) Generation of strand breaks and formation of 8-hydroxy-2′-deoxyguanosine in DNA by a Thiol/Fe3+/O2- catalyzed oxidation system. Arch Biochem Biophys 312: 285-291.
54. Phan, Q.T., Belanger, P.H., and Filler, S.G. (2000) Role of hyphal formation in interactions of Candida albicans with endothelial cells. Infect Immun 68: 3485-3490.
55. Pitarch, A., Sanchez, M., Nombela, C., and Gil, C. (2002) Sequential fractionation and two-dimensional gel analysis unravels the complexity of the dimorphic fungus Candida albicans cell wall proteome. Mol Cell Proteomics 1: 967-982.
56. Poole, L.B., Chae, H.Z., Flores, B.M., Reed, S.L., Rhee, S.G., and Torian, B.E. (1997) Peroxidase activity of a TSA-like antioxidant protein from a pathogenic amoeba. Free Radic Biol Med 23: 955-959.
57. Ross, S.J., Findlay, V.J., Malakasi, P., and Morgan, B.A. (2000) Thioredoxin peroxidase is required for the transcriptional response to oxidative stress in budding yeast. Mol Biol Cell 11: 2631-2642.
58. Rupp, S. (2004) Proteomics on its way to study host-pathogen interaction. Curr Opin Microbiol 7: 330-335.
59. Schweizer, A., Rupp, S., Taylor, B.N., Rollinghoff, M., and Schroppel, K. (2000) The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans. Mol Microbiol 38: 435-445.
60. Shepherd, M.G. (1987) Cell envelope of Candida albicans. Crit Rev Microbiol 15: 7-25.
61. Shibutani, S., Takeshita, M., and Grollman, A.P. (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349: 431-434.
62. Singh, P., Chauhan, N., Ghosh, A., Dixon, F., and Calderone, R. (2004) SKN7 of Candida albicans: mutant construction and phenotype analysis. Infect Immun 72: 2390-2394.
63. Sohn, K., Urban, C., Brunner, H., and Rupp, S. (2003) EFG1 is a major regulator of cell wall dynamics in Candida albicans as shown by DNA-microarrays. Mol Microbiol 47: 89-102.
64. Sundstrom, P. (2002) Adhesion in Candida spp. Cell Microbiol 4: 461-469.
65. Trotter, E.W., and Grant, C.M. (2002) Thioredoxins are required for protection against a reductive stress in the yeast Saccharomyces cerevisiae. Mol Microbiol 46: 869-878.
66. Urban, C., Sohn, K., Lottspeich, F., Brunner, H., and Rupp, S. (2003) Identification of surface determinants in C. albicans reveals Tsa1p, a protein differentially localized in the cell. FEBS Lett 544: 229-236.
67. Wong, C.M., Zhou, Y., Ng, R.W., Kung, H.F., and Jin, D.Y. (2002) Cooperation of yeast peroxiredoxins Tsa1p and Tsa2p in the cellular defense against oxidative and nitrosative stress. J Biol Chem 277: 5385-5394.
68. Wong, C.M., Ching, Y.P., Zhou, Y., Kung, H.F., and Jin, D.Y. (2003) Transcriptional regulation of yeast peroxiredoxin gene TSA2 through Hap1 p, Rox1 p, and Hap2/3/5p. Free Radic Biol Med 34: 585-597.
69. Wong, C.M., Siu, K.L., and Jin, D.Y. (2004) Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J Biol Chem 279: 23207-23213.
70. Wood, Z.A., Schroder, E., Robin Harris, J., and Poole, L.B. (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28: 32-40.
71. Yim, M.B., Chae, H.Z., Rhee, S.G., Chock, P.B., and Stadtman, E.R. (1994) On the protective mechanism of the thiol-specific antioxidant enzyme against the oxidative damage of biomacromolecules. J Biol Chem 269: 1621-1626.
72. Zhang, X., De Micheli, M., Coleman, S.T., Sanglard, D., and Moye-Rowley, W.S. (2000) Analysis of the oxidative stress regulation of the Candida albicans transcription factor, Cap1p. Mol Microbiol 36: 618-629.