Functional studies of the Ssk1p response regulator protein of Candida albicans as determined by phenotypic analysis of receiver domain point mutants

Molecular Microbiology

Volumn 62, Issue 4, 2006, Pages 997-1013

  Menon, Veena ^a   Li, Dongmei ^a   Chauhan, Neeraj ^a   Rajnarayanan, Rajendram ^b   Dubrovska, Alla ^c   West, Ann H ^c   Calderone, Richard ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b TOUGALOO COLLEGE   (United States)

^c UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; HOG1 MAP KINASE ENZYME; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN; PROTEIN SSK1P; REGULATOR PROTEIN; TERT BUTYL HYDROPEROXIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CPH1; TRANSCRIPTION FACTOR EFG1; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CELL NUCLEUS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CORRELATION ANALYSIS; DOWN REGULATION; ENZYME PHOSPHORYLATION; FUNGUS HYPHAE; IN VITRO STUDY; IN VIVO STUDY; METAL BINDING; MORPHOGENESIS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SENSITIVITY ANALYSIS; WILD TYPE; YEAST;

AMINO ACID SEQUENCE; CANDIDA ALBICANS; FUNGAL PROTEINS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; OXIDATIVE STRESS; PHENOTYPE; PHOSPHORYLATION; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TRANSFORMATION, GENETIC;

CANDIDA ALBICANS; MURINAE;

EID: 33750484000     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05438.x     Document Type: Article

References (59)

1. Alonso-Monge, R., Vararro-Garcia, F., Molero, G., Diez-Orejas, R., Gustin, M., Pla, J., et al. (1999) Role of mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J Bacteriol 181: 3058-3068.
2. Alonso-Monge, R., Navarro-Garcia, F., Roman, E., Negredo, A., Eximan, B., Nombela, C., and Pla, J. (2003) The Hog1 MAP kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot Cell 2: 351-361.
3. Andaluz, E., Cuidad, T., Gomez-Raja, J., Calderone, R., and Larriba, G. (2006) Rad52 depletion in Candida albicans triggers both the DNA-damage checkpoint and filamentation accompanied by but independent of expression of hyphal-specific genes. Mol Microbiol 59: 1452-1472.
4. Arana, D.M., Nombela, C., Alonso-Monge, R., and Pla, J. (2005) The Pbs2 MAP kinase kinase is essential for the oxidative stress response in the fungal pathogen Candida albicans. Microbiology 151: 1033-1049.
5. Armitage, J.P. (1999) Bacterial tactic responses. Adv Microb Physiol 41: 229-289.
6. Bernhardt, J., Herman, D., Sheridan, M., and Calderone, R. (2001) Adherence and invasion studies of Candida albicans strains utilizing in vitro models of esophageal candidiasis. J Infect Dis 184: 1170-1175.
7. Bourret, R.B., Hess, J.F., and Simon, M.I. (1990) Conserved aspartate residues and phosphorylation in signal transduction by the chemotaxis protein CheY. Proc Natl Acad Sci USA 87: 41-45.
8. Buck, V., Quinn, J., Soto Pino, T., Martin, H., Saldaña, J., Makino, K., et al. (2001) Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol Biol Cell 12: 407-419.
9. Calera, J.A., and Calderone, R. (1999) Identification of a putative response regulator, two-component phosphorelay gene (CaSSK1) from Candida albicans. Yeast 15: 1243-1254.
10. Calera, J.A., Zhao, X.-J., and Calderone, R. (2000a) Defective hyphal formation and avirulence caused by a deletion of the CSSK1 response regulator gene in Candida albicans. Infect Immun 68: 518-525.
11. Calera, J.A., Herman, D., and Calderone. R.A. (2000b) Identification of YPD1, a gene of Candida albicans which encodes a two-component phospho-histidine intermediate protein. Yeast 16: 1053-1059.
12. Catlett, N.L., Yoder, O.C., and Turgeon, B.G. (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2: 1151-1161.
13. Chauhan, N., Inglis, D., Roman, E., Pla, J., Li, D., Calera, J.A., Calderone, R. (2003) The SSK1 of Candida albicans is associated with oxidative stress adaptation and cell wall biosynthesis. Eukaryot Cell 2: 1018-1024.
14. Chauhan, N., Latge, J.-P., and Calderone, R. (2006) Oxidant adaptation in the human pathogenic fungi, Candida albicans and Aspergillus fumigatus. Nat Microbiol Rev 4: 435-444.
15. Chen, D., Calderone, R., Richert, J., and Li, D. (2005) Deletion of the SSK1 response regulator gene in Candida albicans contributes to enhanced killing by human polymorphonuclear neutrophils. Infect Immun 73: 865-871.
16. Chen, D., Sarfati, J., Latge, J.-P., and Calderone, R. (2006) The sakA (Hog1) and tscB (Sln1) two-component proteins in oxidant adaptation in Aspergillus fumigatus. Med Mycol 44: 211-218.
17. Enjalbert, B., Smith, D., Alam, I., Nicholls, S., Brown, A.J., and Quinn. J. (2006) Role of Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol Biol Cell 17: 1018-1032.
18. Ferrigno, P., Posas, F., Koepp, D., Saito, H., and Silver, P.A. (1998) Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin b homologs NMD5 and XPO1. EMBO J 17: 5606-5614.
19. Hohmann, S. (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300-372.
20. Hoyer, L. (2001) The ALS gene family of Candida albicans. Trends Microbiol 9: 176-180.
21. Janiak-Spens, F., and West, A.H. (2000) Functional roles of conserved amino acid residues surrounding the phosphorylatable histidine of the yeast phosphorelay protein Ypd1p. Mol Microbiol 37: 136-144.
22. Janiak-Spens, F., Sparling, J.M., Gurfinkel, M., and West, A.H. (1999) Differential stabilities of phosphorylated response regulator domains deflect functional roles other yeast osmoregulatory SLN1 and SSK1 proteins. J Bacteriol 181: 411-417.
23. Jiang, M., Bourret, R.B., Simon, M.I., and Volz, K. (1997) Uncoupled phosphorylation and activation in bacterial chemotaxis. J Biol Chem 272: 11850-11855.
24. Lee, S.-Y., Cho, H.S., Pelton, J.G., Yan, D., Berry, E.A., and Wemmer, D.E. (2001) Crystal structure of activated CheY. J Biol Chem 276: 16425-16431.
25. Li, S., Ault, A., Malone, C.L., Raitt, D., Dean, S., Johnston, L.H., et al. (1998) The yeast histidine protein kinase, Sln1p, mediates phosphotransfer to two response regulators, Ssk1p and Skn7p. EMBO J 17: 6952-6962.
26. Li, D., Bernhardt, J., and Calderone, R. (2002) Temporal expression of the Candida albicans genes CHK1 and CSSK1, adherence and morphogenesis in a model of reconstituted human esophageal epithelial candidiasis. Infect Immun 70: 1558-1565.
27. Lukat, G.S., Lee, B.H., Mottonen, J.M., Stock, A.M., and Stock, J.B. (1991) Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis. J Biol Chem 266: 8348-8354.
28. Maeda, T., Wurgler-Murphy, S.M., and Saito, H. (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242-245.
29. Moye-Rowley, S. (2003) Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences. Eukaryot Cell 2: 381-389.
30. Nagahashi, S., Mio, T., Nagahashi, S., Kokado, M., Ariswawa, M., and Aoki, Y. (1998) Isolation of CaSLN1 and CaNIK1, the genes for osmosensing histidine kinase homologues, from the pathogenic fungus, Candida albicans. Microbiology 144: 425-432.
31. Parkinson, J.S., and Kofoid, E.C. (1992) Communication modules in bacterial signaling proteins. Annu Rev Genet 26: 71-112.
32. Porter, S.W., and West, A.H. (2005) A common docking site for response regulators on the yeast phosphorelay protein YPD1. Biochim Biophys Acta 1748: 138-145.
33. Porter, S.W., Xu, Q., and West, A.H. (2003) Ssk1p response regulator binding surface on histidine containing phosphotransfer protein Ypd1p. Eukaryot Cell 2: 27-33.
34. Posas, F., and Saito, H. (1998) Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J 17: 1385-1394.
35. Posas, F., Wurgler-Murphy, S.M., Maeda, T., Witten, E.A., Thai, T.C., and Saito, H. (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 'two-component' osmosensor. Cell 86: 865-875.
36. Roman, E., Nombela, C., and Pla, J. (2005) The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans. Mol Cell Biol 25: 10611-10627.
37. Saito, H. (2001) Histidine phosphorylation and two-component signaling in eukaryotic cells. Chem Rev 101: 2497-2509.
38. San Jose, C., Monge, R., Perez-Diaz, R., Pla, J., and Nombela, C. (1996) The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus, Candida albicans. J Bacteriol 178: 5850-5852.
39. Singh, P., Chauhan, N., and Calderone, R. (2004) SKN7 of Candida albicans: mutant construction and phenotype analysis. Infect Immun 72: 2390-2394.
40. Smith, D.A., Nicholls, S., Morgan, B., Brown, A.J., and Quinn, J. (2004) A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol Biol Cell 14: 1460-1467.
41. Stock, A.M., and West, A.H. (2002) Response regulators and their interactions with histidine protein kinases. In Histidine Kinases in Signal Transduction. Inouye, M., and Dutta, R. (eds)., cp. 12, pp. 237-271. New York: Academic Press.
42. Stock, A., Koshland, D.E., Jr, and Stock, J. (1985) Homologies between the Salmonella typhimurium CheY protein and proteins involved in the regulation of chemotaxis, membrane protein synthesis, and sporulation. Proc Natl Acad Sci USA 82: 7989-7993.
43. Stock, J.B., Ninfa, A.J., and Stock, A.M. (1989) Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev 53: 450-490.
44. Stock, A.M., Robinson, V.L., and Goudreau, P.N. (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215.
45. Szurmant, H., and Ordal, G.W. (2004) Diversity of chemotaxis mechanisms among bacteria and Archaea. Microbiol Mol Biol Rev 68: 301-319.
46. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
47. Thomason, P., and Kay, R. (2000) Eukaryotic signal transduction via histidine-aspartate phosphorelay. J Cell Sci 113: 3141-3150.
48. Volz, K. (1993) Structural conservation in the CheY superfamily. Biochemistry 32: 11741-11753.
49. Wadhams, G.H., and Armitage, J.P. (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5: 1024-1037.
50. Webre, D.J., Wolanin, P.M., and Stock, J.B. (2003) Bacterial chemotaxis. Curr Biol 13: R47-R49.
51. West, A.H., and Stock, A.M. (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26: 369-376.
52. Wisplinghoff, H., Bischoff, T., Tallent, S., Seifert, H., Wenzel, R., and Edmond, M. (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24 179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39: 309-317.
53. Wolanin, P.M., Webre, D.J., and Stock, J.B. (2003) Mechanism of phosphatase activity in the chemotaxis response regulator CheY. Biochemistry 42: 14075-14082.
54. Wormley, F.L., Heinrich, G., Miller, J.L., Perfect, J.R., and Cox, G.M. (2005) Identification and characterization of an SKN7 homologue from Cryptococcus neoformans. Infect Immun 73: 5022-5030.
55. Wurgler-Murphy, S.M., and Saito, H. (1997) Two-component signal transducers and MAPK cascades. Trends Biochem Sci 22: 172-176.
56. Xu, Q., Nguyen, V., and West, A.H. (1999) Purification, crystallization, and preliminary X-ray diffraction analysis of the yeast phosphorelay protein YPD1. Acta Crystallogr D Biol Crystallogr D55: 291-293.
57. Xue, T., Nguyen, C., Romans, A., Kontoyiannis, D., and May, G.S. (2004) A mitogen-activated protein kinase that senses nitrogen regulates conidial germination and growth in Aspergillus fumigatus. Eukaryot Cell 3: 557-560.
58. Yale, J., and Bohnert, H.J. (2001) Transcript expression in Saccharomyces cerevisiae at high salinity. J Biol Chem 276: 15996-16007.
59. Yamada-Okabe, T., Mio, T., Ono, N., Kashima, Y., Matsui, M., Arisawa, A., and Yamada-Okabe, H. (1999) Roles of three histidine kinase genes in hyphal development and virulence of the pathogenic fungus, Candida albicans. J Bacteriol 181: 7243-7247.