The Yak1 kinase is involved in the initiation and maintenance of hyphal growth in Candida albicans

Molecular Biology of the Cell

Volumn 19, Issue 5, 2008, Pages 2251-2266

  Goyard, Sophie ^a   Knechtle, Philipp ^a,e   Chauvel, Murielle ^a   Mallet, Adeline ^a   Prévost, Marie Christine ^a   Proux, Caroline ^a   Coppée, Jean Yves ^a   Schwartz, Patrick ^b   Dromer, Françoise ^b   Park, Hyunsook ^c,d   Filler, Scott G ^c,d   Janbon, Guilhem ^b   D'Enfert, Christophe ^a  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c HARBOR UCLA MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e EVOLVA SA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BCR1; TRANSCRIPTION FACTOR TEC1; TRANSCRIPTION FACTOR TUP1; YAK1 KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BCR1 GENE; BIOFILM; CANDIDA ALBICANS; DOWN REGULATION; ENZYME ACTIVITY; EUKARYOTE; FUNGAL GENE; FUNGAL MORPHOLOGY; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE DISRUPTION; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENE REPRESSION; GENETIC TRANSCRIPTION; GENOME; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OROPHARYNX CANDIDIASIS; PRIORITY JOURNAL; TEC1 GENE; TUP1 GENE; UPREGULATION; YAK1 GENE; YEAST;

ANIMALIA; CANDIDA ALBICANS; EUKARYOTA;

EID: 48249156540     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-09-0960     Document Type: Article

References (89)

1. Alonso-Monge, R., Roman, E., Nombela, C., and Pla, J. (2006). The MAP kinase signal transduction network in Candida albicans. Microbiology 152, 905-912.
2. Argimon, S. et al. (2007). Developmental regulation of an adhesin gene during cellular morphogenesis in the fungal pathogen Candida albicans. Eukaryotic Cell 6, 682-692.
3. Arnaud, M. B., Costanzo, M. C., Skrzypek, M. S., Shah, P., Binkley, G., Lane, C., Miyasato, S. R., and Sherlock, G. (2007). Sequence resources at the Candida Genome Database. Nucleic Acids Res. 35, D452-D456.
4. Becker, W., and Joost, H. G. (1999). Structural and functional characteristics of Dyrk, a novel subfamily of protein kinases with dual specificity. Prog. Nucleic Acid Res. Mol. Biol. 62, 1-17.
5. Berman, J. (2006). Morphogenesis and cell cycle progression in Candida albicans. Curr. Opin. Microbiol. 9, 595-601.
6. Birse, C. E., Irwin, M. Y., Fonzi, W. A., and Sypherd, P. S. (1993). Cloning and characterization of ECE1, a gene expressed in association with cell elongation of the dimorphic pathogen Candida albicans. Infect. Immun. 61, 3648-3655.
7. Bishop, A. C., Buzko, O., and Shokat, K. M. (2001). Magic bullets for protein kinases. Trends Cell Biol. 11, 167-172.
8. Bishop, A. C. et al. (2000). A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401.
9. Bockmuhl, D. P., Krishnamurthy, S., Gerads, M., Sonneborn, A., and Ernst, J. F. (2001). Distinct and redundant roles of the two protein kinase A isoforms Tpk1p and Tpk2p in morphogenesis and growth of Candida albicans. Mol. Microbiol. 42, 1243-1257.
10. 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.
11. 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.
12. Braun, B. R., and Johnson, A. D. (1997). Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277, 105-109.
13. Braun, B. R., Kadosh, D., and Johnson, A. D. (2001). NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 20, 4753-4761.
14. Braun, B. R. et al. (2005). A human-curated annotation of the Candida albicans genome. PLoS Genet. 1, 36-57.
15. Brown, D. H., Jr., Giusani, A. D., Chen, X., and Kumamoto, C. A. (1999). Filamentous growth of Candida albicans in response to physical environmental cues and its regulation by the unique CZF1 gene. Mol. Microbiol. 34, 651-662.
16. Cao, F., Lane, S., Raniga, P. P., Lu, Y., Zhou, Z., Ramon, K., Chen, J., and Liu, H. (2006). The Flo8 transcription factor is essential for hyphal development and virulence in Candida albicans. Mol. Biol. Cell 17, 295-307.
17. Chandra, J., Kuhn, D. M., Mukherjee, P. K., Hoyer, L. L., McCormick, T., and Ghannoum, M. A. (2001). Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183, 5385-5394.
18. Cornet, M., Bidard, F., Schwarz, P., Da Costa, G., Blanchin-Roland, S., Dromer, F., and Gaillardin, C. (2005). Deletions of endocytic components VPS28 and VPS32 affect growth at alkaline pH and virulence through both RIM101-dependent and RIM101-independent pathways in Candida albicans. Infect Immun. 73, 7977-7987.
19. Csank, C., and Haynes, K. (2000). Candida glabrata displays pseudohyphal growth. FEMS Microbiol. Lett. 189, 115-120.
20. Dephoure, N., Howson, R. W., Blethrow, J. D., Shokat, K. M., and O'Shea, E. K. (2005). Combining chemical genetics and proteomics to identify protein kinase substrates. Proc. Natl. Acad. Sci. USA 102, 17940-17945.
21. Doedt, T., Krishnamurthy, S., Bockmuhl, D. P., Tebarth, B., Stempel, C., Russell, C. L., Brown, A. J., and Ernst, J. F. (2004). APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 15, 3167-3180.
22. Donlan, R. M., and Costerton, J. W. (2002). Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167-193.
23. Douglas, L. J. (2003). Candida biofilms and their role in infection. Trends Microbiol. 11, 30-36.
24. Eckert, S. E., Sheth, C. C., and Mühlschlegel, F. A. (2007). Regulation of morphogenesis in Candida species. In: Candida: Comparative and Functional Genomics, ed. C. d'Enfert and B. Hube, Wymondham, United Kingdom: Caister Academic Press, 263-291.
25. Ernst, F. E. (2000). Transcription factors in Candida albicans-environmental control of morphogenesis. Microbiology 146, 1763-1774.
26. Fitzpatrick, D. A., Logue, M. E., Stajich, J. E., and Butler, G. (2006). A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol. Biol. 6, 99.
27. Garcia-Sanchez, S., Aubert, S., Iraqui, I., Janbon, G., Ghigo, J. M., and d'Enfert, C. (2004). Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot. Cell 3, 536-545.
28. Garcia-Sanchez, S., Mavor, A. L., Russell, C. L., Argimon, S., Dennison, P., Enjalbert, B., and Brown, A. J. (2005). Global roles of Ssn6 in Tup1- and Nrg1-dependent gene regulation in the fungal pathogen, Candida albicans. Mol. Biol. Cell 16, 2913-2925.
29. Garrett, S., and Broach, J. (1989). Loss of Ras activity in Saccharomyces cerevisiae is suppressed by disruptions of a new kinase gene, YAKI, whose product may act downstream of the cAMP-dependent protein kinase. Genes Dev. 3, 1336-1348.
30. Garrett, S., Menold, M. M., and Broach, J. R. (1991). The Saccharomyces cerevisiae YAK1 gene encodes a protein kinase that is induced by arrest early in the cell cycle. Mol. Cell. Biol. 11, 4045-4052.
31. 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.
32. Giusani, A. D., Vinces, M., and Kumamoto, C. A. (2002). Invasive filamentous growth of Candida albicans is promoted by Czf1p-dependent relief of Efg1p-mediated repression. Genetics 160, 1749-1753.
33. Gola, S., Martin, R., Walther, A., Dunkler, A., and Wendland, J. (2003). New modules for PCR-based gene targeting in Candida albicans: rapid and efficient gene targeting using 100 bp of flanking homology region. Yeast 20, 1339-1347.
34. Gow, N. A., Brown, A. J., and Odds, F. C. (2002). Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5, 366-371.
35. Griffioen, G., Branduardi, P., Ballarini, A., Anghileri, P., Norbeck, J., Baroni, M. D., and Ruis, H. (2001). Nucleocytoplasmic distribution of budding yeast protein kinase A regulatory subunit Bcy1 requires Zds1 and is regulated by Yak1-dependent phosphorylation of its targeting domain. Mol. Cell. Biol. 21, 511-523.
36. Habelhah, H., Shah, K., Huang, L., Burlingame, A. L., Shokat, K. M., and Ronai, Z. (2001). Identification of new JNK substrate using ATP pocket mutant JNK and a corresponding ATP analogue. J. Biol. Chem. 276, 18090-18095.
37. Harcus, D., Nantel, A., Marcil, A., Rigby, T., and Whiteway, M. (2004). Transcription profiling of cyclic AMP signaling in Candida albicans. Mol. Biol. Cell 15, 4490-4499.
38. Hartley, A. D., Ward, M. P., and Garrett, S. (1994). The Yak1 protein kinase of Saccharomyces cerevisiae moderates thermotolerance and inhibits growth by an Sch9 protein kinase-independent mechanism. Genetics 136, 465-474.
39. Hoyer, L. L., Payne, T. L., Bell, M., Myers, A. M., and Scherer, S. (1998). Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr. Genet. 33, 451-459.
40. Iraqui, I., Garcia-Sanchez, S., Dromer, F., Aubert, S., Ghigo, J. M., d'Enfert, C., and Janbon, G. (2005). The Yak1p kinase controls expression of adhesins and biofilm formation in Candida glabrata in a Sir4p-dependent pathway. Mol. Microbiol. 55, 1259-1271.
41. Jones, T. et al. (2004). The diploid genome sequence of Candida albicans. Proc. Natl. Acad. Sci. USA 101, 7329-7334.
42. Kadosh, D., and Johnson, A. D. (2001). Rfg1, a protein related to the Saccharomyces cerevisiae hypoxic regulator Rox1, controls filamentous growth and virulence in Candida albicans. Mol. Cell. Biol. 21, 2496-2505.
43. Kadosh, D., and Johnson, A. D. (2005). Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol. Biol. Cell 16, 2903-2912.
44. Kassis, S., Melhuish, T., Annan, R. S., Chen, S. L., Lee, J. C., Livi, G. P., and Creasy, C. L. (2000). Saccharomyces cerevisiae Yak1p protein kinase autophosphorylates on tyrosine residues and phosphorylates myelin basic protein on a C-terminal serine residue. Biochem. J. 348, 263-272.
45. Kim, S., Wolyniak, M. J., Staab, J. F., and Sundstrom, P. (2007). A 368-base-pair cis-acting HWP1 promoter region, HCR, of Candida albicans confers hyphaspecific gene regulation and binds architectural transcription factors Nhp6 and Gcf1p. Eukaryotic Cell 6, 693-709.
46. Lay, J., Henry, L. K., Clifford, J., Koltin, Y., Bulawa, C. E., and Becker, J. M. (1998). Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect. Immun. 66, 5301-5306.
47. Lee, K. L., Buckley, H. R., and Campbell, C. C. (1975). An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans. Sabouraudia 13, 148-153.
48. Lo, H. J., Köhler, J. R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., and Fink, G. R. (1997). Nonfilamentous C. albicans mutants are avirulent. Cell 90, 939-949.
49. Loeb, J. D., Sepulveda-Becerra, M., Hazan, I., and Liu, H. (1999). A G1 cyclin is necessary for maintenance of filamentous growth in Candida albicans. Mol. Cell. Biol. 19, 4019-4027.
50. Maidan, M. M., De Rop, L., Serneels, J., Exler, S., Rupp, S., Tournu, H., Thevelein, J. M., and Van Dijck, P. (2005). The G protein-coupled receptor Gpr1 and the Galpha protein Gpa2 act through the cAMP-protein kinase A pathway to induce morphogenesis in Candida albicans. Mol. Biol. Cell 16, 1971-1986.
51. Mao, X., Cao, F., Nie, X., Liu, H., and Chen, J. (2006). The Swi/Snf chromatin remodeling complex is essential for hyphal development in Candida albicans. FEBS Lett. 580, 2615-2622.
52. Martchenko, M., Alarco, A. M., Harcus, 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.
53. Martin, D. E., Soulard, A., and Hall, M. N. (2004). TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119, 969-979.
54. Moriya, H., Shimizu-Yoshida, Y., Omori, A., Iwashita, S., Katoh, M., and Sakai, A. (2001). Yak1p, a DYRK family kinase, translocates to the nucleus and phosphorylates yeast Pop2p in response to a glucose signal. Genes Dev. 15, 1217-1228.
55. Murad, A. M., d'Enfert, C., Gaillardin, C., Tournu, H., Tekaia, F., Talibi, D., Marechal, D., Marchais, V., Cottin, J., and Brown, A. J. (2001a). Transcript profiling in Candida albicans reveals new cellular functions for the transcriptional repressors CaTup1, CaMig1 and CaNrg1. Mol. Microbiol. 42, 981-993.
56. Murad, A. M., Lee, P. R., Broadbent, I. D., Barelle, C. J., and Brown, A. J. (2000). CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16, 325-327.
57. Murad, A. M. et al. (2001b). NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20, 4742-4752.
58. Nantel, A. et al. (2002). Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13, 3452-3465.
59. Nobile, C. J., Andes, D. R., Nett, J. E., Smith, F. J., Yue, F., Phan, Q. T., Edwards, J. E., Filler, S. G., and Mitchell, A. P. (2006a). Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathogens 2, e63.
60. Nobile, C. J., and Mitchell, A. P. (2005). Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr. Biol. 15, 1150-1155.
61. Nobile, C. J., and Mitchell, A. P. (2006). Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol. 8, 1382-1391.
62. Nobile, C. J., Nett, J. E., Andes, D. R., and Mitchell, A. P. (2006b). Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot. Cell 5, 1604-1610.
63. Noble, S. M., and Johnson, A. D. (2007). Genetics of Candida albicans, a diploid human fungal pathogen. Annu. Rev. Genet. 41, 193-211.
64. Park, H., Myers, C. L., Sheppard, D. C., Phan, Q. T., Sanchez, A. A., E Edwards, J., and Filler, S. G. (2005). Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell Microbiol. 7, 499-510.
65. Peltroche-Llacsahuanga, H., Goyard, S., d'Enfert, C., Prill, S. K., and Ernst, J. F. (2006). Protein O-mannosyltransferase isoforms regulate biofilm formation in Candida albicans. Antimicrob. Agents Chemother. 50, 3488-3491.
66. Pfaller, M. A., and Diekema, D. J. (2007). Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20, 133-163.
67. Pratt, Z. L., Drehman, B. J., Miller, M. E., and Johnston, S. D. (2007). Mutual interdependence of MSI1 (CAC3) and YAK1 in Saccharomyces cerevisiae. J. Mol. Biol. 368, 30-43.
68. Ptacek, J. et al. (2005). Global analysis of protein phosphorylation in yeast. Nature 438, 679-684.
69. Ramage, G., VandeWalle, K., Lopez-Ribot, J. L., and Wickes, B. L. (2002). The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol. Lett. 214, 95-100.
70. Richard, M. L., Nobile, C. J., Bruno, V. M., and Mitchell, A. P. (2005). Candida albicans biofilm-defective mutants. Eukaryot. Cell 4, 1493-1502.
71. Saville, S. P., Lazzell, A. L., Monteagudo, C., and Lopez-Ribot, J. L. (2003). Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2, 1053-1060.
72. Schweizer, A., Rupp, S., Taylor, B. N., Röllinghof, M., and Schröppel, K. (2000). The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans. Mol. Microbiol. 38, 435-445.
73. Selmecki, A., Bergmann, S., and Berman, J. (2005). Comparative genome hybridization reveals widespread aneuploidy in Candida albicans laboratory strains. Mol. Microbiol. 55, 1553-1565.
74. Shah, K., Liu, Y., Deirmengian, C., and Shokat, K. M. (1997). Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates. Proc. Natl. Acad. Sci. USA 94, 3565-3570.
75. Sharkey, L. L., McNemar, M. D., Saporito-Irwin, S. M., Sypherd, P. S., and Fonzi, W. A. (1999). HWP1 functions in the morphological development of Candida albicans downstream of EFG1, TUP1, and RBF1. J. Bacteriol. 181, 5273-5279.
76. Staab, J. F., and Sundstrom, P. (1998). Genetic organization and sequence analysis of the hypha-specific cell wall protein gene HWP1 of Candida albicans. Yeast 14, 681-686.
77. 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.
78. Tebarth, B., Doedt, T., Krishnamurthy, S., Weide, M., Monterola, F., Dominguez, A., and Ernst, J. F. (2003). Adaptation of the Efg1p morphogenetic pathway in Candida albicans by negative autoregulation and PKA-dependent repression of the EFG1 gene. J. Mol. Biol. 329, 949-962.
79. Uetz, P. et al. (2000). A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403, 623-627.
80. van het Hoog, M. et al. (2007). Assembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes. Genome Biol. 8, R52.
81. Walther, A., and Wendland, J. (2003). An improved transformation protocol for the human fungal pathogen Candida albicans. Curr. Genet 42, 339-343.
82. Ward, M. P., and Garrett, S. (1994). Suppression of a yeast cyclic AMP-dependent protein kinase defect by overexpression of SOK1, a yeast gene exhibiting sequence similarity to a developmentally regulated mouse gene. Mol. Cell. Biol. 14, 5619-5627.
83. Whiteway, M., and Bachewich, C. (2007). Morphogenesis in Candida albicans. Annu. Rev. Microbiol. 61, 529-553.
84. Wilson, R. B., Davis, D., and Mitchell, A. P. (1999). Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181, 1868-1874.
85. Zakikhany, K., Naglik, J. R., Schmidt-Westhausen, A., Holland, G., Schaller, M., and Hube, B. (2007). In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell Microbiol. 9, 2938-2954.
86. Zappacosta, F., Huddleston, M. J., Karcher, R. L., Gelfand, V. I., Carr, S. A., and Annan, R. S. (2002). Improved sensitivity for phosphopeptide mapping using capillary column HPLC and microionspray mass spectrometry: comparative phosphorylation site mapping from gel-derived proteins. Anal. Chem. 74, 3221-3231.
87. Zhang, Z., Smith, M. M., and Mymryk, J. S. (2001). Interaction of the E1A oncoprotein with Yak1p, a novel regulator of yeast pseudohyphal differentiation, and related mammalian kinases. Mol. Biol. Cell 12, 699-710.
88. Zhao, X., Daniels, K. J., Oh, S. H., Green, C. B., Yeater, K. M., Soll, D. R., and Hoyer, L. L. (2006). Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152, 2287-2299.
89. Zheng, X., Wang, Y., and Wang, Y. (2004). Hgc1, a novel hypha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J. 23, 1845-1856.