Impaired PRPP-synthesizing capacity compromises cell integrity signalling in Saccharomyces cerevisiae

Microbiology

Volumn 150, Issue 10, 2004, Pages 3327-3339

  Wang, Ke ^a   Vavassori, Stefano ^a   Schweizer, Lilian M ^a   Schweizer, Michael ^a  

^a HERIOT WATT UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CHITIN; GLUCAN SYNTHASE; MATING HORMONE ALPHA FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHORIBOSYL PYROPHOSPHATE; RIBOSEPHOSPHATE PYROPHOSPHOKINASE;

ARTICLE; CARBOHYDRATE SYNTHESIS; CATALYSIS; CELL METABOLISM; CELL WALL; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME SUBUNIT; FUNGAL CELL; FUNGAL STRAIN; FUNGUS GROWTH; GENE ACTIVITY; GENE DELETION; GENE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TWO HYBRID SYSTEM;

CELL WALL; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORIBOSYL PYROPHOSPHATE; RIBOSE-PHOSPHATE PYROPHOSPHOKINASE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TEMPERATURE; TRANSCRIPTION, GENETIC;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 6444227761     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.27373-0     Document Type: Article

References (72)

1. Angeles de la Torre-Ruiz, M., Torres, J., Arino, J. & Herrero, E. (2002). Sit4 is required for proper modulation of the biological functions mediated by Pkc1 and the cell integrity pathway in Saccharomyces cerevisiae. J Biol Chem 277, 33468-33476.
2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1995). Current Protocols in Molecular Biology. New York: Wiley.
3. Bader, G. D., Betel, D. & Hogue, C. W. (2003). BIND: the Biomolecular Interaction Network Database. Nucleic Acids Res 31, 248-250.
4. Becker, M. A. (2001). Phosphoribosylpyrophosphate synthetase and the regulation of phosphoribosylpyrophosphate production in human cells. Prog Nucleic Acid Res Mol Biol 69, 115-148.
5. Binley, K. M., Radcliffe, P. A., Trevethick, J., Duffy, K. A. & Sudbery, P. E. (1999). The yeast PRS3 gene is required for cell integrity, cell cycle arrest upon nutrient deprivation, ion homeostasis and the proper organization of the actin cytoskeleton. Yeast 15 1459-1469.
6. Boorsma, A., Nobel, H., Riet, B., Bargmann, B., Brul, S., Hellingwerf, K. J. & Klis, F. M. (2004). Characterization of the transcriptional response to cell wall stress in Saccharomyces cerevisiae. Yeast 21, 413-427.
7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
8. Buehrer, B. M. & Errede, B. (1997). Coordination of the mating and cell integrity mitogen-activated protein kinase pathways in Saccharomyces cerevisiae. Mol Cell Biol 17, 6517-6525.
9. Carter, A. T., Narbad, A., Pearson, B. M., Beck, K. F., Logghe, M., Contreras, R. & Schweizer, M. (1994). Phosphoribosylpyrophosphate synthetase (PRS): a new gene family in Saccharomyces cerevisiae. Yeast 10, 1031-1044.
10. Collister, M., Didmon, M. P., Maclsaac, F., Stark, M. J., MacDonald, N. Q. & Keyse, S. M. (2002). YIL113w encodes a functional dual-specificity protein phosphatase which specifically interacts with and inactivates the Slt2/Mpk1p MAP kinase in S. cerevisiae. FEBS Lett 527, 186-192.
11. de Groot, P. W. J., Ruiz, C., Vazguez, C. R. & other authors (2001). A genomic approach for the identification and classification of genes involved in cell wall formation and its regulation in Saccharomyces cerevisiae. Comp Funct Genomics 2, 124-142.
12. de Nobel, H., Ruiz, C., Martin, H., Morris, W., Brul, S., Molina, M. & Klis, F. M. (2000). Cell wall perturbation in yeast results in dual phosphorylation of the Slt2/Mpk1 MAP kinase and in an Slt2-mediated increase in FKS2-lacZ expression, glucanase resistance and thermotolerance. Microbiology 146, 2121-2132.
13. Dodou, E. & Treisman, R. (1997). The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway. Mol Cell Biol 17, 1848-1859.
14. Elble, R. (1992). A simple and efficient procedure for transformation of yeasts. Biotechniques 13, 18-20.
15. Flandez, M., Cosano, I. C., Nombela, C., Martin, H. & Molina, M. (2004). Reciprocal regulation between Slt2 MAPK and isoforms of Msg5 dual-specificity protein phosphatase modulates the yeast cell integrity pathway. J Biol Chem 279, 11027-11034.
16. Garcia, R., Bermejo, C., Grau, C., Perez, R., Rodriguez-Pena, J. M., Francois, J., Nombela, C. & Arroyo, J. (2004 . The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J Biol Chem 279, 15183-15195.
17. Gietz, R. D. & Sugino, A. (1988). New yeast- Escherichia colishuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534.
18. Gietz, D., St Jean, A., Woods, R. A. & Schiestl, R. H. (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20, 1425.
19. Gray, J. V., Ogas, J. P., Kamada, Y., Stone, M., Levin, D. E. & Herskowitz, I. (1997). A role for the Pkc1 MAP kinase pathway of Saccharomyces cerevisiae in bud emergence and identification of a putative upstream regulator. EMBO J 16, 4924-4937.
20. Guarente, L. (1983). Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol 101, 181-191.
21. Gustin, M. C., Albertyn, J., Alexander, M. & Davenport, K. (1998). MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62, 1264-1300.
22. Hahn, J.-S. & Thiele, D. J. (2002). Regulation of the Saccharomyces cerevisiae Slt2 kinase pathway by the stress-inducible Sdp1 dual specificity phosphatase. J Biol Chem 277, 21278-21284.
23. Heinisch, J. J., Lorberg, A., Schmitz, H. P. & Jacoby, J. J. (1999). The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol Microbiol 32, 671-680.
24. Hernando, Y., Parr, A. & Schweizer, M. (1998). PRS5, the fifth member of the phosphoribosyl pyrophosphate synthetase gene family in Saccharomyces cerevisiae, is essential for cell viability in the absence of either PRS1 or PRS3. J Bacteriol 180, 6404-6407.
25. Hernando, Y., Carter, A. T., Parr, A., Hove-Jensen, B. & Schweizer, M. (1999). Genetic analysis and enzyme activity suggest the existence of more than one minimal functional unit capable of synthesizing phosphoribosyl pyrophosphate in Saccharomyces cerevisiae. J Biol Chem 274, 12480-12487.
26. Hohmann, S. (2002). Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66, 300-372.
27. Hove-Jensen, B. (1988). Mutation in the phosphoribosylpyrophosphate synthetase gene (prs) that results in simultaneous requirements for purine and pyrimidine nucleosides, nicotinamide nucleotide, histidine, and tryptophan in Escherichia coli. J Bacteriol 170, 1148-1152.
28. Huang, K. N. & Symington, L. S. (1995). Suppressors of a Saccharomyces cerevisiae pkc1 mutation identify alleles of the phosphatase gene PTC1 and of a novel gene encoding a putative basic leucine zipper protein. Genetics 141, 1275-1285.
29. 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.
30. Inoue, S. B., Takewaki, N., Takasuka, T. & other authors (1995). Characterization and gene cloning of 1,3 -beta- D-glucan synthase from Saccharomyces cerevisiae. Eur J Biochem 231 845-854.
31. Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M. & Sakaki, Y. (2001). A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci U S A 98, 4569-4574.
32. James, P., Halladay, J. & Craig, E. A. (1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436.
33. Jung, U. S. & Levin, D. E. (1999). Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol Microbiol 34, 1049-1057.
34. Kaida, D., Yashiroda, H., Toh-e, A. & Kikuchi, Y. (2002). Yeast Whi2 and Psr1-phosphatase form a complex and regulate STRE-mediated gene expression. Genes Cells 7, 543-552.
35. Kaiser, C., Michaelis, S. & Mitchell, A. (1994). Methods in Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
36. 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.
37. Ketela, T., Green, R. & Bussey, H. (1999). Saccharomyces cerevisiae Mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway. J Bacteriol 181, 3330-3340.
38. Khorana, H. G., Fernandes, J. F. & Kornberg, A. J. (1958). Pyrophosphorylation of ribose-5-phosphate in the enzymatic synthesis of 5-phosphorylribose-1-pyrophosphate. J Biol Chem 230, 941-948.
39. Kirchrath, L., Lorberg, A., Schmitz, H. P., Gengenbacher, U. & Heinisch, J. J. (2000). Comparative genetic and physiological studies of the MAP kinase Mpk1p from Kluyveromyces lactis and Saccharomyces cerevisiae. J Mol Biol 300, 743-758.
40. Klis, F. M., Mol, P., Hellingwerf, K. & Brul, S. (2002). Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol Rev 26, 239-256.
41. Krause, S. A. & Gray, J. V. (2002). The protein kinase C pathway is required for viability in quiescence in Saccharomyces cerevisiae. Curr Biol 12, 588-593.
42. Lagorce, A., Hauser, N. C., Labourdette, D., Rodriguez, C., Martin-Yken, H., Arroyo, J., Hoheisel, J. D. & Francois, J. (2003). Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J Biol Chem 278, 20345-20357.
43. Madden, S. L., Creasy, C. L., Srinivas, V., Fawcett, W. & Bergman, L. W. (1988). Structure and expression of the PHO80 gene of Saccharomyces cerevisiae. Nucleic Acids Res 16, 2625-2637.
44. Madden, S. L., Johnson, D. L. & Bergman, L. W. (1990). Molecular and expression analysis of the negative regulators involved in the transcriptional regulation of acid phosphatase production in Saccharomyces cerevisiae. Mol Cell Biol 10, 5950-5957.
45. Martin, H., Arroyo, J., Sanchez, M., Molina, M. & Nombela, C. (1993). Activity of the yeast MAP kinase homologue Slt2 is critically required for cell integrity at 37°C. Mol Gen Genet 241, 177-184.
46. Martin, H., Rodriguez-Pachon, J. M., Ruiz, C., Nombela, C. & Molina, M. (2000). Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J Biol Chem 275, 1511-1519.
47. Miller, J. H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
48. Orlean, P. (1997). Biogenesis of yeast wall surface components. In The Molecular and Cellular Biology of the Yeast Saccharomyces, pp. 299-362. Edited by J. R. Pringle, J. Broach & E. W. Jones. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
49. Philip, B. & Levin, D. E. (2001). Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol Cell Biol 21, 271-280.
50. Popolo, L. & Vai, M. (1999). The Gas1 glycoprotein, a putative wall polymer cross-linker. Biochim Biophys Acta 1426 385-400.
51. 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 ggp1delta mutant of Saccharomyces cerevisiae. J Bacteriol 179, 463-469.
52. Popolo, L., Gualtieri, T. & Ragni, E. (2001). The yeast cell-wall salvage pathway. Med Mycol 39, 111-121.
53. Queralt, E. & Igual, J. C. (2003). Cell cycle activation of the Swi6p transcription factor is linked to nucleocytoplasmic shuttling. Mol Cell Biol 23, 3126-3140.
54. Rajavel, M., Philip, B., Buehrer, B. M., Errede, B. & Levin, D. E. (1999). Mid2 is a putative sensor for cell integrity signaling in Saccharomyces cerevisiae. Mol Cell Biol 19 3969-3976.
55. Reinoso-Martin, C., Schüller, C., Schuetzer-Muehlbauer, M. & Kuchler, K. (2003). The yeast protein kinase C cell integrity pathway mediates tolerance to the antifungal drug caspofungin through activation of Slt2p mitogen-activated protein kinase signaling. Eukaryot Cell 2, 1200-1210.
56. Roder, K., Wolf, S. S., Larkin, K. J. & Schweizer, M. (1999). Interaction between the two ubiquitously expressed transcription factors NF-Y and Sp1. Gene 234, 61-69.
57. Rodriguez-Pachon, J. M., Martin, H., North, G., Rotger, R., Nombela, C. & Molina, M. (2002). A novel connection between the yeast Cdc42 GTPase and the Slt2-mediated cell integrity pathway identified through the effect of secreted Salmonella GTPase modulators. J Biol Chem 277, 27094-27102.
58. Roncero, C. (2002). The genetic complexity of chitin synthesis in fungi. Curr Genet 41, 367-378.
59. Roncero, C. & Duran, A. (1985). Effect of Calcofluor white and Congo red on fungal cell wall morphogenesis: in vivo activation of chitin polymerization. J Bacteriol 163, 1180-1185.
60. Roncero, C., Valdivieso, M. H., Ribas, J. C. & Duran, A. (1988). Effect of calcofluor white on chitin synthases from Saccharomyces cerevisiae. J Bacteriol 170, 1945-1949.
61. Ruiz-Herrera, J., Gonzalez-Prieto, J. M. & Ruiz-Medrano, R. (2002). Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Res 1, 247-256.
62. Schneiter, R., Carter, A. T., Hernando, Y., Zellnig, G., Schweizer, L. M. & Schweizer, M. (2000). The importance of the five phosphoribosyl-pyrophosphate synthetase (Prs) gene products of Saccharomyces cerevisiae in the maintenance of cell integrity and the subcellular localization of Prs1p. Microbiology 146, 3269-3278.
63. Schuetzer-Muehlbauer, M., Willinger, B., Krapf, G., Enzinger, S., Presterl, E. & Kuchler, K. (2003). The Candida albicans Cdr2p ATP-binding cassette (ABC) transporter confers resistance to caspofungin. Mol Microbiol 48, 225-235.
64. Torres, J., Di Como, C. J., Herrero, E. & De La Torre-Ruiz, M. A. (2002). Regulation of the cell integrity pathway by rapamycin-sensitive TOR function in budding yeast. J Biol Chem 277, 43495-43504.
65. Uetz, P., Giot, L., Cagney, G. & other authors (2000). A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403, 623-627.
66. Verna, J., Lodder, A., Lee, K., Vagts, A. & Ballester, R. (1997). A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94, 13804-13809.
67. Watanabe, Y., Irie, K. & Matsumoto, K. (1995). Yeast RLM1 encodes a serum response factor-like protein that may function downstream of the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol Cell Biol 15, 5740-5749.
68. Watanabe, Y., Takaesu, G., Hagiwara, M., Irie, K. & Matsumoto, K. (1997). Characterization of a serum response factor-like protein in Saccharomyces cerevisiae, Rlm1, which has transcriptional activity regulated by the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol Cell Biol 17, 2615-2623.
69. Woods, R. A. & Gietz, R. D. (2001). High-efficiency transformation of plasmid DNA into yeast. Methods Mol Biol 177 85-97.
70. 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.
71. Zhao, C., Jung, U. S., Garrett-Engele, P., Roe, T., Cyert, M. S. & Levin, D. E. (1998). Temperature-induced expression of yeast FKS2 is under the dual control of protein kinase C and calcineurin. Mol Cell Biol 18, 1013-1022.
72. Zu, T., Verna, J. & Ballester, R. (2001). Mutations in WSC genes for putative stress receptors result in sensitivity to multiple stress conditions and impairment of Rlm1-dependent gene expression in Saccharomyces cerevisiae. Mol Genet Genomics 266, 142-155.