A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans

Microbiology

Volumn 144, Issue 2, 1998, Pages 411-424

  Navarro García, Federico ^a   Alonso Monge, Rebeca ^a   Rico, Hortensia ^b   Pla, Jesús ^a   Sentandreu, Rafael ^b   Nombela, César ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Antifungal; Confocal microscopy; MAP kinase; Pseudohyphal growth; Two hybrid system

Indexed keywords

AMPHOTERICIN B; ANTIFUNGAL AGENT; BETA 1,3 GLUCAN; CAFFEINE; CALCOFLUOR WHITE; CANAVANINE; CHITIN; CILOFUNGIN; ECHINOCANDIN B; FLUCONAZOLE; FLUCYTOSINE; GLYCOSYLATED PROTEIN; MICONAZOLE; MITOGEN ACTIVATED PROTEIN KINASE; NIKKOMYCIN Z; PROTEIN KINASE; STAUROSPORINE; TRICHODERMIN; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CELL STRUCTURE; CELL SURFACE; CELL WALL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG SENSITIVITY; FUNGAL GENETICS; FUNGUS MUTANT; GENE FUNCTION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SCANNING ELECTRON MICROSCOPY; TRANSCRIPTION REGULATION;

ARANEAE; CANDIDA ALBICANS; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0031888386     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-144-2-411     Document Type: Article

References (84)

1. Arellano, M., Durán, A. & Pérez, P. (1996). Rho1 GTPase activates the (1-3)β-D-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO J 15, 4584-4591.
2. Bardwell, L., Cook, J. G., Inouye, C. J. & Thorner, J. (1994). Signal propagation and regulation in the mating pheromone response pathway of the yeast Saccharomyces cerevisiae. Dev Biol 166, 363-379.
3. Breeden, L. & Nasmyth, K. (1985). Regulation of the yeast HO gene. Cold Spring Harbor Symp Quant Biol 50, 643-650.
4. Brewster, J. L., de Valoir, T., Dwyer, N. D., Winter, E. & Gustin, M. C. (1993). An osmosensing signal transduction pathway in yeast. Science 259, 1760-1763.
5. Cabib, E. & Durán, A. (1975). Simple and sensitive procedure for screening yeast mutants that lyse at non-permissive temperatures. J Bacteriol 124, 1604-1606.
6. Chen, D. C., Yang, B. C. & Kuo, T. T. (1992). One-step transformation of yeast in stationary phase. Curr Genet 21, 83-84.
7. Clark, K. L., Feldmann, P. J., Dignard, D., Larocque, R., Brown, A. J. P., Lee, M. G., Thomas, D. Y. & Whiteway, M. (1995). Constitutive activation of the Saccharomyces cerevisiae mating response pathway by a MAP kinase kinase from Candida albicans. Mol Gen Genet 249, 609-621.
8. Costigan, C. & Snyder, M. (1994). SLK1, a yeast homolog of MAP kinase activators, has a RAS/cAMP-independent role in nutrient sensing. Mol Gen Genet 243, 286-296.
9. Costigan, C., Gehrung, S. & Snyder, M. (1992). A synthetic lethal screen identifies SLK1, a novel protein kinase homolog implicated in yeast cell morphogenesis and cell growth. Mol Cell Biol 12, 1162-1178.
10. Davenport, K. R., Sohaskey, M., Kamada, Y., Levin, D. E. & Gustin, M. C. (1995). A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270, 30157-30161.
11. Diez-Orejas, R., Molero, G., Navarro-García, F., Pla, J., Nombela, C. & Sánchez-Pérez, M. (1997). Reduced virulence of Candida albicans MKC1 mutants: a role for a mitogen-activated protein kinase in pathogenesis. Infect Immun 65, 833-837.
12. Drgonová, J., Drgon, T., Tanaka, K., Kollár, R., Chen, G. C., Ford, R. A., Chan, C. S., Takai, Y. & Cabib, E. (1996). Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272, 277-279.
13. Elorza, M. V., Rico, H., Gozalbo, D. & Sentandreu, R. (1983). Cell wall composition and protoplast regeneration in Candida albicans. Antonie Leeuwenhoek 49, 457-469.
14. Elorza, M. V., Mormeneo, S., García de la Cruz, F., Gimeno, C. & Sentandreu, R. (1989). Evidence for the formation of covalent bonds between macromolecules in the domain of the wall of Candida albicans mycelial cells. Biochem Biophys Res Commun 162, 1118-1125.
15. Errede, B. & Levin, D. E. (1993). A conserved kinase cascade for MAP kinase activation in yeast. Curr Opin Cell Biol 5, 254-260.
16. Errede, B., Cade, R. M., Yashar, B. M., Kamada, Y., Levin, D. E., Irie, K. & Matsumoto, K. (1995). Dynamics and organization of MAP kinase signal pathways. Mol Reprod Dev 42, 477-485.
17. Fields, S. & Song, O. (1989). A novel genetic system to detect protein-protein interactions. Nature 340, 245-246.
18. Fonzi, W. A. & Irwin, M. Y. (1993). Isogenic strain construction and gene mapping in Candida albicans. Genetics 134, 717-728.
19. Frost, D. J., Brandt, K. D., Cugier, D. & Goldman, R. (1995). A whole-cell Candida albicans assay for the detection of inhibitors towards fungal cell wall synthesis and assembly. J Antibiot 48, 306-310.
20. de la Fuente, J. M., Alvarez, A., Nombela, C. & Sánchez, M. (1992). Flow cytometric analysis of Saccharomyces cerevisiae autolytic mutants and protoplasts. Yeast 8, 39-45.
21. +-ATPase. Mol Cell Biol 15, 4103-4114.
22. Gillum, A. M., Tsay, E. Y. H. & 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.
23. Gimeno, C. J. & Fink, G. R. (1994). Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol Cell Biol 14, 2100-2112.
24. Gimeno, C. J., Ljungdahl, P. O., Styles, C. A. & Fink, G. R. (1992). Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68, 1077-1090.
25. Hall, J. P., Cherkasova, V., Elion, E. A., Gustin, M. C. & Winter, E. (1996). The osmoregulatory pathway represses mating pathway activity in Saccharomyces cerevisiae: isolation of a FUS3 mutant that is insensitive to the repression mechanism. Mol Cell Biol 16, 6715-6723.
26. Hanahan, D. (1988). Techniques for transformation of E. coli. In DNA Cloning, pp. 109-135. Edited by D. M. Glover. Oxford: IRL Press.
27. Herreros, E., García-Sáez, M. I., Nombela, C. & Sánchez, M. (1992). A reorganized Candida albicans DNA sequence promoting homologous non-integrative genetic transformation. Mol Microbiol 6, 3567-3574.
28. Herskowitz, I. (1995). MAP kinase pathways in yeast: for mating and more. Cell 80, 187-197.
29. Hill, J. E., Myers, A. M., Koerner, T. J. & Tzagoloff, A. (1986). Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast 2, 163-167.
30. Igual, J. C., Johnson, A. L. & Johnston, L. H. (1996). Coordinated regulation of gene expression by the cell cycle transcription factor SWI4 and the protein kinase C MAP kinase pathway for yeast cell integrity. EMBO J 15, 5001-5013.
31. Irie, K., Takase, M., Lee, K. S., Levin, D. E., Araki, H., Matsumoto, K. & Oshima, Y. (1993). MKK1 and MKK2, which encode Saccharomyces cerevisiae mitogen-activated protein kinase-kinase homologs, function in the pathway mediated by protein kinase C. Mol Cell Biol 13, 3076-3083.
32. Kamada, Y., Jung, U. S., Piotrowski, J. & Levin, D. E. (1995). The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 9, 1559-1571.
33. Kamada, Y., Qadota, H., Python, C. P., Anraku, Y., Ohya, Y. & Levin, D. E. (1996). Activation of yeast protein kinase C by Rho1 GTPase. J Biol Chem 271, 9193-9196.
34. Kapteyn, J. C., Montijn, R. C., Dijkgraaf, G. J., Van den Ende, H. & Klis, F. M. (1995). Covalent association of β-1,3-glucan with β-1,6-glucosylated mannoproteins in cell walls of Candida albicans. J Bacteriol 177, 3788-3792.
35. Köhler, J. & 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.
36. Kollár, R., Petráková, E., Ashwell, G., Robbins, P. W. & Cabib, E. (1995). Architecture of the yeast cell wall: the linkage between chitin and β(1-3)-glucan. J. Biol Chem 3, 1170-1178.
37. Krisak, L., Strich, R., Winters, R. S., Hall, J. P., Mallory, M. J., Kreitzer, D., Tuan, R. S. & Winter, E. (1994). SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev 8, 2151-2161.
38. Leberer, E., Harcus, D., Broadbent, I. D. & 7 other authors (1996). Signal transduction through homologs of the Ste20p and Ste7p protein kinases can trigger hyphal formation in the pathogenic fungus Candida albicans. Proc Natl Acad Sci USA 93, 13217-13222.
39. Lee, K. S. & Levin, D. E. (1992). Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homolog. Mol Cell Biol 12, 172-182.
40. Lee, K. L, Buckley, H. R. & Campbell, C. C. (1975). An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans. J Med Vet Mycol 13, 148-153.
41. Lee, K. S., Hines, L. K. & Levin, D. E. (1993a). A pair of functionally redundant yeast genes (PPZ1 and PPZ2) encoding type 1-related protein phosphatases function within the PKC1-mediated pathway. Mol Cell Biol 13, 5843-5853.
42. Lee, K. S., Irie, K., Gotoh, Y., Watanabe, Y., Araki, H., Nishida, E., Matsumoto, K. & Levin, D. E. (1993b). A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol Cell Biol 13, 3067-3075.
43. Levin, D. E. & Errede, B. (1995). The proliferation of MAP kinase signaling pathways in yeast. Curr Opin Cell Biol 7, 197-202.
44. Levin, D. E., Fields, F. O., Kunisawa, R., Bishop, J. M. & Thorner, J. (1990). A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell 62, 213-224.
45. Liu, H., Styles, C. A. & Fink, G. R. (1993). Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262, 1741-1744.
46. Liu, H., Köhler, J. & Fink, G. R. (1994). Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266, 1723-1726.
47. Madden, K., Sheu, Y. J., Baetz, K., Andrews, B. & Snyder, M. (1997). SBF cell cycle regulator as a target of the yeast PKC-MAP kinase pathway. Science 275, 1781-1784.
48. Malathi, K., Ganesan, K. & Datta, A. (1994). Identification of a putative transcription factor in Candida albicans that can complement the mating defect of Saccharomyces cerevisiae ste12 mutants. J Biol Chem 269, 22945-22951.
49. Marcilla, A., Mormeneo, S., Elorza, M. V., Manclus, J. J. & Sentandreu, R. (1993). Wall formation by Candida albicans yeast cells: synthesis, secretion and incorporation of two types of mannoproteins. J Gen Microbiol 139, 2985-2993.
50. Martín, H., Arroyo, J., Sánchez, M., Molina, M. & Nombela, C. (1993). Activity of the yeast MAP kinase homologue Slt2 is critically required for cell integrity at 37 degrees C. Mol Gen Genet 241, 177-184.
51. Martín, H., Castellanos, M. C., Cenamor, R., Sánchez, M., Molina, M. & Nombela, C. (1996). Molecular and functional characterization of a mutant allele of the mitogen-activated protein-kinase gene SLT2(MPK1) rescued from yeast autolytic mutants. Curr Genet 29, 516-522.
52. Mazzoni, C., Zarzov, P., Rambourg, A. & Mann, C. (1993). The SLT2 (MPK1) MAP kinase homolog is involved in polarized cell growth in Saccharomyces cerevisiae. J Cell Biol 123, 1821-1833.
53. Meissner, P. S., Sisk, W. P. & Berman, M. L. (1987). Bacteriophage lambda cloning system for the construction of directional cDNA libraries. Proc Natl Acad Sci USA 84, 4171-4175.
54. Mendoza, I., Rubio, F., Rodríguez-Navarro, A. & Pardo, J. M. (1994). The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J Biol Chem 269, 8792-8796.
55. Miret, J. J., Solari, A. J., Barderi, P. A. & Goldemberg, S. H. (1992). Polyamines and cell wall organization in Saccharomyces cerevisiae. Yeast 8, 1033-1041.
56. Nakamura, T., Ohmoto, T., Hirata, D., Tsuchiya, E. & Miyakawa, T. (1996). Genetic evidence for the functional redundancy of the calcineurin-and Mpk1-mediated pathways in the regulation of cellular events important for growth in Saccharomyces cerevisiae. Mol Gen Genet 251, 211-219.
57. National Committee for Clinical Laboratory Standards (1992). Reference method for broth dilution antifungal susceptibility testing of yeast. Proposed standard M27-P. National Committee for Clinical Laboratory Standards: Villanova, PA, USA.
58. Navarro-García, F., Sánchez, M., Pla, J. & Nombela, C. (1995). Functional characterization of the MKC1 gene of Candida albicans, which encodes a mitogen-activated protein kinase homolog related to cell integrity. Mol Cell Biol 15, 2197-2206.
59. Nonaka, H., Tanaka, K., Hirano, H., Fujiwara, T., Hohno, H., Umikawa, M., Mino, A. & Yoshimi, T. (1995). A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. EMBO J 14, 5931-5938.
60. Odds, F. C. (1988). Candida and Candidosis, 2nd edn. London: Baillière Tindall.
61. Odds, F. C. (1994). Candida species and virulence. ASM News 60, 313-318.
62. Paravicini, G., Mendoza, A., Antonsson, B., Cooper, M., Losberger, C. & Payton, M. (1996). The Candida albicans PKC1 gene encodes a protein kinase C homolog necessary for cellular integrity but not dimorphism. Yeast 12, 741-756.
63. Popolo, L., Gilardelli, D., Bonfante, P. & Vai, M. (1997). Increase in chitin as an essential response to defects in assembly of cell wall polymers in the ggp1 delta mutant of Saccharomyces cerevisiae. J Bacteriol 179, 463-469.
64. Posas, F., Casamayor, A. & Ariño, J. (1993). The PPZ protein phosphatases are involved in the maintenance of osmotic stability of yeast cells. FEBS Lett 318, 282-286.
65. Posas, F., Camps, M. & Ariño, J. (1995). The PPZ protein phosphatases are important determinants of salt tolerance in yeast cells. J Biol Chem 270, 13036-13041.
66. Qadota, H., Python, C. P., Inoue, S. B., Arisawa, M., Anraku, Y., Zheng, Y., Watanabe, T., Levin, D. E. & Ohya, Y. (1996). Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science 272, 279-281.
67. Roberts, R. L. & Fink, G. R. (1994). Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev 8, 2974-2985.
68. Roemer, T., Paravicini, G., Payton, M. A. & Bussey, H. (1994). Characterization of the yeast (1-6)-β-glucan biosynthetic components, Kre6p and Skn1p, and genetic interactions between the PKC1 pathway and extracellular matrix assembly. J Cell Biol 127, 567-579.
69. Sanjuán, R., Zueco, J., Stock, R., Font de Mora, J. & Sentandreu, R. (1995). Identification of glucan-mannoprotein complexes in the cell wall of Candida albicans using a monoclonal antibody that reacts with a (1,6)-β-glucan epitope. Microbiology 141, 1545-1551.
70. Sengar, A. S., Markley, N. A., Marini, N. J. & Young, D. (1997). Mkh1, a MEK kinase required for cell wall integrity and proper response to osmotic and temperature stress in Schizosaccharomyces pombe. Mol Cell Biol 17, 3508-3519.
71. Shimizu, J., Yoda, K. & Yamasaki, M. (1994). The hypoosmolarity-sensitive phenotype of the Saccharomyces cerevisiae hpo2 mutant is due to a mutation in PKC1, which regulates expression of β-glucanase. Mol Gen Genet 242, 641-648.
72. Sikorski, R. S. & Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
73. Singh, P., Ganesan, K., Malathi, K., Ghosh, D. & Datta, A. (1994). ACPR, a STE12 homologue from Candida albicans, is a strong inducer of pseudohyphae in Saccharomyces cerevisiae haploids and diploids. Biochem Biophys Res Commun 205, 1079-1085.
74. Soler, M., Plovins, A., Martin, H., Molina, M. & Nombela, C. (1995). Characterization of domains in the yeast MAP kinase Slt2 (Mpk1) required for functional activity and in vivo interaction with protein kinases Mkk1 and Mkk2. Mol Microbiol 17, 833-842.
75. Sundstrom, P. M. & Kenny, G. E. (1984). Characterization of antigens specific to the surface of germ tubes of Candida albicans by immunofluorescence. Infect Immun 43, 850-855.
76. Tiedt, L. R., Jooste, W. R. & Hamilton-Attwell, V. L. (1987). Technique for preserving aerial fungus structure for scanning electron microscopy. Trans Br Mycol Soc 88, 420-422.
77. Toda, T., Uno, I., Ishikawa, T. & 7 other authors (1985). In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40, 27-36.
78. + gene encodes a novel mitogen-activated protein kinase homolog which regulates cell integrity and functions coordinately with the protein kinase C pathway. Mol Cell Biol 16, 6752-6764.
79. Torres, L., Martín, H., García-Sáez, M. I., Arroyo, J., Molina, M., Sánchez, M. & Nombela, C. (1991). A protein kinase gene complements the lytic phenotype of Saccharomyces cerevisiae lyt2 mutants. Mol Microbiol 5, 2845-2854.
80. Varela, J. C. S., Praekelt, U. M., Meacock, P. A., Planta, R. J. & Mager, W. H. (1995). The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol Cell Biol 15, 6232-6245.
81. Whiteway, M., Dignard, D. & Thomas, D. Y. (1992). Dominant negative selection of heterologous genes: isolation of Candida albicans genes that interfere with Saccharomyces cerevisiae mating factor-induced cell cycle arrest. Proc Natl Acad Sci USA 89, 9410-9414.
82. Williams, S. & Veldkamp, C. (1974). Preparation of fungi for scanning electron microscopy. Trans Br Mycol Soc 63, 409-412.
83. Zaitsevskaya-Carter, T. & Cooper, J. A. (1997). Spm1, a stress-activated MAP kinase that regulates morphogenesis in S. pombe. EMBO J 16, 1318-1331.
84. Zarzov, P., Mazzoni, C. & Mann, C. (1996). The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast. EMBO J 15, 83-91.