A proteomic view of Candida albicans yeast cell metabolism in exponential and stationary growth phases

International Journal of Medical Microbiology

Volumn 298, Issue 3-4, 2008, Pages 291-318

  Kusch, Harald ^a,b   Engelmann, Susanne ^b   Bode, Rüdiger ^b   Albrecht, Dirk ^b   Morschhäuser, Joachim ^a   Hecker, Michael ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Candida albicans; Exponential growth; Proteome signature; Reference map; Stationary phase

Indexed keywords

GLUCOSE; GLUTAMIC ACID; GLYOXYLIC ACID; PURINE; PYRIMIDINE; RIBOSOME PROTEIN;

ADAPTATION; ANIMAL CELL; ARTICLE; BACTERIUM CULTURE; CANDIDA ALBICANS; CARBON SOURCE; CELL METABOLISM; DNA SYNTHESIS; GLUCONEOGENESIS; GROWTH CURVE; HEAT STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT LIMITATION; OXIDATIVE STRESS; PROTEIN INDUCTION; PROTEIN SYNTHESIS; PROTEOMICS; RNA SYNTHESIS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UNINDEXED SEQUENCE; UPREGULATION; YEAST CELL;

EID: 39849102492     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2007.03.020     Document Type: Article

References (78)

1. F.J. Alvarez-Peral O. Zaragoza Y. Pedreno J.C. Arguelles Protective role of trehalose during severe oxidative stress caused by hydrogen peroxide and the adaptive oxidative stress response in Candida albicans Microbiology 148 2002 2599 2606
2. M.B. Arnaud M.C. Costanzo M.S. Skrzypek G. Binkley C. Lane S.R. Miyasato G. Sherlock The Candida Genome Database (CGD), a community resource for Candida albicans gene and protein information Nucleic Acids Res. 33 2005 D358 D363
3. M.B. Arnaud M.C. Costanzo M.S. Skrzypek P. Shah G. Binkley C. Lane S.R. Miyasato G. Sherlock Sequence resources at the Candida Genome Database Nucleic Acids Res. 35 2007 D452 D456
4. C.J. Barelle C.L. Priest D.M. Maccallum N.A. Gow F.C. Odds A.J. Brown Niche-specific regulation of central metabolic pathways in a fungal pathogen Cell. Microbiol. 8 2006 961 971
5. J. Becker F. Melchior V. Gerke F.R. Bischoff H. Ponstingl A. Wittinghofer RNA1 encodes a GTPase-activating protein specific for Gsp1p, the Ran/TC4 homologue of Saccharomyces cerevisiae J. Biol. Chem. 270 1995 11860 11865
6. H. Blum H. Beier H.J. Gross Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels Electrophoresis 8 1987 93 99
7. H. Boucherie N. Bataille I.T. Fitch M. Perrot M.F. Tuite Differential synthesis of glyceraldehyde-3-phosphate dehydrogenase polypeptides in stressed yeast cells FEMS Microbiol. Lett. 125 1995 127 133
8. B.R. Braun M. van Het Hoog C. d’Enfert M. Martchenko J. Dungan A. Kuo D.O. Inglis M.A. Uhl H. Hogues M. Berriman M. Lorenz A. Levitin U. Oberholzer C. Bachewich D. Harcus A. Marcil D. Dignard T. Iouk R. Zito L. Frangeul F. Tekaia K. Rutherford E. Wang C.A. Munro S. Bates N.A. Gow L.L. Hoyer G. Kohler J. Morschhauser G. Newport S. Znaidi M. Raymond B. Turcotte G. Sherlock M. Costanzo J. Ihmels J. Berman D. Sanglard N. Agabian A.P. Mitchell A.D. Johnson M. Whiteway A. Nantel A human-curated annotation of the Candida albicans genome PLoS Genet. 1 2005 e1
9. K. Buttner J. Bernhardt C. Scharf R. Schmid U. Mader C. Eymann H. Antelmann A. Volker U. Volker M. Hecker A comprehensive two-dimensional map of cytosolic proteins of Bacillus subtilis Electrophoresis 22 2001 2908 2935
10. R. Calderone Candida and Candidiasis 2002 ASM Press Washington, DC
11. D. Chatterji A.K. Ojha Revisiting the stringent response, ppGpp and starvation signaling Curr. Opin. Microbiol. 4 2001 160 165
12. S.T. Coleman T.K. Fang S.A. Rovinsky F.J. Turano W.S. Moye-Rowley Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae J. Biol. Chem. 276 2001 244 250
13. M.C. Costanzo M.B. Arnaud M.S. Skrzypek G. Binkley C. Lane S.R. Miyasato G. Sherlock The Candida Genome Database: facilitating research on Candida albicans molecular biology FEMS Yeast Res. 6 2006 671 684
14. C. d’Enfert S. Goyard S. Rodriguez-Arnaveilhe L. Frangeul L. Jones F. Tekaia O. Bader A. Albrecht L. Castillo A. Dominguez J.F. Ernst C. Fradin C. Gaillardin S. Garcia-Sanchez P. de Groot B. Hube F.M. Klis S. Krishnamurthy D. Kunze M.C. Lopez A. Mavor N. Martin I. Moszer D. Onesime J. Perez Martin R. Sentandreu E. Valentin A.J. Brown CandidaDB: a genome database for Candida albicans pathogenomics Nucleic Acids Res. 33 2005 D353 D357
15. Y.X. Dong S. Sueda J. Nikawa H. Kondo Characterization of the products of the genes SNO1 and SNZ1 involved in pyridoxine synthesis in Saccharomyces cerevisiae Eur. J. Biochem. 271 2004 745 752
16. M.S. Donoviel E.T. Young Isolation and identification of genes activating UAS2-dependent ADH2 expression in Saccharomyces cerevisiae Genetics 143 1996 1137 1148
17. K. Enomoto Y. Arikawa H. Muratsubaki Physiological role of soluble fumarate reductase in redox balancing during anaerobiosis in Saccharomyces cerevisiae FEMS Microbiol. Lett. 215 2002 103 108
18. C. Eymann A. Dreisbach D. Albrecht J. Bernhardt D. Becher S. Gentner T. Tam le K. Buttner G. Buurman C. Scharf S. Venz U. Volker M. Hecker A comprehensive proteome map of growing Bacillus subtilis cells Proteomics 4 2004 2849 2876
19. S. Fillinger S. Boschi-Muller S. Azza E. Dervyn G. Branlant S. Aymerich Two glyceraldehyde-3-phosphate dehydrogenases with opposite physiological roles in a nonphotosynthetic bacterium J. Biol. Chem. 275 2000 14031 14037
20. M.T. Flikweert L. Van Der Zanden W.M. Janssen H.Y. Steensma J.P. Van Dijken J.T. Pronk Pyruvate decarboxylase: an indispensable enzyme for growth of Saccharomyces cerevisiae on glucose Yeast 12 1996 247 257
21. C.L. Flores C. Rodriguez T. Petit C. Gancedo Carbohydrate and energy-yielding metabolism in non-conventional yeasts FEMS Microbiol. Rev. 24 2000 507 529
22. C. Fradin P. De Groot D. MacCallum M. Schaller F. Klis F.C. Odds B. Hube Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood Mol. Microbiol. 56 2005 397 415
23. A.M. Gillum E.Y. Tsay D.R. Kirsch 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 1984 179 182
24. E.J. Helmerhorst M. Stan M.P. Murphy F. Sherman F.G. Oppenheim The concomitant expression and availability of conventional and alternative, cyanide-insensitive, respiratory pathways in Candida albicans Mitochondrion 5 2005 200 211
25. P.K. Herman Stationary phase in yeast Curr. Opin. Microbiol. 5 2002 602 607
26. R. Hernandez C. Nombela R. Diez-Orejas C. Gil Two-dimensional reference map of Candida albicans hyphal forms Proteomics 4 2004 374 382
27. A.G. Hinnebusch K. Natarajan Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress Eukaryot. Cell 1 2002 22 32
28. H. Holzer H.W. Goedde Two ways from pyruvate to acetyl-coenzyme A in yeast Biochem. Z. 329 1957 175 191 (in German)
29. Y.M. Hong S.W. Park S.Y. Choi Expression of the CIP1 gene induced under cadmium stress in Candida sp Mol. Cells 8 1998 84 89
30. W.K. Huh S.O. Kang Molecular cloning and functional expression of alternative oxidase from Candida albicans J. Bacteriol. 181 1999 4098 4102
31. W.K. Huh S.O. Kang Characterization of the gene family encoding alternative oxidase from Candida albicans Biochem. J. 356 2001 595 604
32. T. Jones N.A. Federspiel H. Chibana J. Dungan S. Kalman B.B. Magee G. Newport Y.R. Thorstenson N. Agabian P.T. Magee R.W. Davis S. Scherer The diploid genome sequence of Candida albicans Proc. Natl. Acad. Sci. USA 101 2004 7329 7334
33. S.J. Kerscher Diversity and origin of alternative NADH:ubiquinone oxidoreductases Biochim. Biophys. Acta 1459 2000 274 283
34. H. Kusch S. Engelmann D. Albrecht J. Morschhauser M. Hecker Proteomic analysis of the oxidative stress response in Candida albicans Proteomics 7 2007 686 697
35. C. Lamarre J.D. LeMay N. Deslauriers Y. Bourbonnais 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 2001 43784 43791
36. B.D. Lemire K.S. Oyedotun The Saccharomyces cerevisiae mitochondrial succinate:ubiquinone oxidoreductase Biochim. Biophys. Acta 1553 2002 102 116
37. C.E. Leuker A. Sonneborn S. Delbruck J.F. Ernst Sequence and promoter regulation of the PCK1 gene encoding phosphoenolpyruvate carboxykinase of the fungal pathogen Candida albicans Gene 192 1997 235 240
38. M.C. Lorenz G.R. Fink The glyoxylate cycle is required for fungal virulence Nature 412 2001 83 86
39. M.C. Lorenz G.R. Fink Life and death in a macrophage: role of the glyoxylate cycle in virulence Eukaryot. Cell 1 2002 657 662
40. M.C. Lorenz J.A. Bender G.R. Fink Transcriptional response of Candida albicans upon internalization by macrophages Eukaryot. Cell 3 2004 1076 1087
41. U. Lutstorf R. Megnet Multiple forms of alcohol dehydrogenase in Saccharomyces cerevisiae . I. Physiological control of ADH-2 and properties of ADH-2 and ADH-4 Arch. Biochem. Biophys. 126 1968 933 944
42. L. McAlister M.J. Holland Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes J. Biol. Chem. 260 1985 15019 15027
43. L. McAlister M.J. Holland Isolation and characterization of yeast strains carrying mutations in the glyceraldehyde-3-phosphate dehydrogenase genes J. Biol. Chem. 260 1985 15013 15018
44. H.B. McDonald A.H. Helfant E.M. Mahony S.K. Khosla L. Goetsch Mutational analysis reveals a role for the C terminus of the proteasome subunit Rpt4p in spindle pole body duplication in Saccharomyces cerevisiae Genetics 162 2002 705 720
45. S.M. Miller B. Magasanik Role of NAD-linked glutamate dehydrogenase in nitrogen metabolism in Saccharomyces cerevisiae J. Bacteriol. 172 1990 4927 4935
46. H. Muratsubaki K. Enomoto One of the fumarate reductase isoenzymes from Saccharomyces cerevisiae is encoded by the OSM1 gene Arch. Biochem. Biophys. 352 1998 175 181
47. J.P. Navarro-Avino R. Prasad V.J. Miralles R.M. Benito R. Serrano A proposal for nomenclature of aldehyde dehydrogenases in Saccharomyces cerevisiae and characterization of the stress-inducible ALD2 and ALD3 genes Yeast 15 1999 829 842
48. V. Neuhoff N. Arold D. Taube W. Ehrhardt Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250 Electrophoresis 9 1988 255 262
49. M. Niimi R.D. Cannon B.C. Monk Candida albicans pathogenicity: a proteomic perspective Electrophoresis 20 1999 2299 2308
50. F.C. Odds Candida and Candidosis 1988 Bailliere Tindall London
51. P.A. Padilla E.K. Fuge M.E. Crawford A. Errett M. Werner-Washburne The highly conserved, coregulated SNO and SNZ gene families in Saccharomyces cerevisiae respond to nutrient limitation J. Bacteriol. 180 1998 5718 5726
52. D. Pappagianis R. Marovitz Studies on ethanol production by Cryptococcus neoformans Sabouraudia 4 1966 250 255
53. A. Pitarch M. Sanchez C. Nombela C. Gil Analysis of the Candida albicans proteome. I. Strategies and applications J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 787 2003 101 128
54. A. Pitarch M. Sanchez C. Nombela C. Gil Analysis of the Candida albicans proteome. II. Protein information technology on the Net (update 2002) J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 787 2003 129 148
55. A. Pitarch C. Nombela C. Gil Candida albicans biology and pathogenicity: insights from proteomics Methods Biochem. Anal. 49 2006 285 330
56. A. Pitarch C. Nombela C. Gil Contributions of proteomics to diagnosis, treatment, and prevention of candidiasis Methods Biochem. Anal. 49 2006 331 361
57. O. Prigneau A. Porta J.A. Poudrier S. Colonna-Romano T. Noel B. Maresca Genes involved in beta-oxidation, energy metabolism and glyoxylate cycle are induced by Candida albicans during macrophage infection Yeast 20 2003 723 730
58. J.T. Pronk H. Yde Steensma J.P. Van Dijken Pyruvate metabolism in Saccharomyces cerevisiae Yeast 12 1996 1607 1633
59. M.A. Ramirez M.C. Lorenz Mutations in alternative carbon utilization pathways in Candida albicans attenuate virulence and confer pleiotropic phenotypes Eukaryot. Cell 6 2007 280 290
60. F. Ramos M. el Guezzar M. Grenson J.M. Wiame Mutations affecting the enzymes involved in the utilization of 4-aminobutyric acid as nitrogen source by the yeast Saccharomyces cerevisiae Eur. J. Biochem. 149 1985 401 404
61. B. Repetto A. Tzagoloff Structure and regulation of KGD1, the structural gene for yeast alpha-ketoglutarate dehydrogenase Mol. Cell. Biol. 9 1989 2695 2705
62. A. Rodaki T. Young A.J. Brown Effects of depleting the essential central metabolic enzyme fructose-1,6-bisphosphate aldolase on the growth and viability of Candida albicans : implications for antifungal drug target discovery Eukaryot. Cell 5 2006 1371 1377
63. F. Ruy A.E. Vercesi A.J. Kowaltowski Inhibition of specific electron transport pathways leads to oxidative stress and decreased Candida albicans proliferation J. Bioenerg. Biomembr. 38 2006 129 135
64. F. Saint-Prix L. Bonquist S. Dequin Functional analysis of the ALD gene family of Saccharomyces cerevisiae during anaerobic growth on glucose: the NADP+-dependent Ald6p and Ald5p isoforms play a major role in acetate formation Microbiology 150 2004 2209 2220
65. K. Sohn M. Roehm C. Urban N. Saunders D. Rothenstein F. Lottspeich K. Schroppel H. Brunner S. Rupp Identification and characterization of Cor33p, a novel protein implicated in tolerance towards oxidative stress in Candida albicans Eukaryot. Cell 4 2005 2160 2169
66. A.L. Subhi P. Diegelman C.W. Porter B. Tang Z.J. Lu G.D. Markham W.D. Kruger Methylthioadenosine phosphorylase regulates ornithine decarboxylase by production of downstream metabolites J. Biol. Chem. 278 2003 49868 49873
67. G. Tripathi C. Wiltshire S. Macaskill H. Tournu S. Budge A.J. Brown Gcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans EMBO J. 21 2002 5448 5456
68. P. Uppuluri B. Sarmah W.L. Chaffin Candida albicans SNO1 and SNZ1 expressed in stationary-phase planktonic yeast cells and base of biofilm Microbiology 152 2006 2031 2038
69. H. Valadi A. Valadi R. Ansell L. Gustafsson L. Adler J. Norbeck A. Blomberg NADH-reductive stress in Saccharomyces cerevisiae induces the expression of the minor isoform of glyceraldehyde-3-phosphate dehydrogenase (TDH1) Curr. Genet. 45 2004 90 95
70. M.A. Van den Berg H.Y. Steensma ACS2, a Saccharomyces cerevisiae gene encoding acetyl-coenzyme A synthetase, essential for growth on glucose Eur. J. Biochem. 231 1995 704 713
71. B. Voigt T. Schweder D. Becher A. Ehrenreich G. Gottschalk J. Feesche K.H. Maurer M. Hecker A proteomic view of cell physiology of Bacillus licheniformis Proteomics 4 2004 1465 1490
72. E.O. Voit Biochemical and genomic regulation of the trehalose cycle in yeast: review of observations and canonical model analysis J. Theor. Biol. 223 2003 55 78
73. M. Werner-Washburne E. Braun G.C. Johnston R.A. Singer Stationary phase in the yeast Saccharomyces cerevisiae Microbiol. Rev. 57 1993 383 401
74. M. Werner-Washburne E.L. Braun M.E. Crawford V.M. Peck Stationary phase in Saccharomyces cerevisiae Mol. Microbiol. 19 1996 1159 1166
75. D.E. Wilson T.W. Williams Jr. J.E. Bennett Further experience with the alcohol test for cryptococcal meningitis Am. J. Med. Sci. 252 1966 532 536
76. M. Wu A. Tzagoloff Mitochondrial and cytoplasmic fumarases in Saccharomyces cerevisiae are encoded by a single nuclear gene FUM1 J. Biol. Chem. 262 1987 12275 12282
77. Z. Yin D. Stead L. Selway J. Walker I. Riba-Garcia T. McLnerney S. Gaskell S.G. Oliver P. Cash A.J. Brown Proteomic response to amino acid starvation in Candida albicans and Saccharomyces cerevisiae Proteomics 4 2004 2425 2436
78. M.L. Zeuthen N. Dabrowa C.M. Aniebo D.H. Howard Ethanol tolerance and the induction of stress proteins by ethanol in Candida albicans J. Gen. Microbiol. 134 1988 1375 1384