Derepressed hyphal growth and reduced virulence in a VH1 family-related protein phosphatase mutant of the human pathogen Candida albicans

Molecular Biology of the Cell

Volumn 8, Issue 12, 1997, Pages 2539-2551

  Csank, Csilla ^a,b   Makris, Constantin ^a   Meloche, Sylvain ^a   Schröppel, Klaus ^c   Röllinghoff, Martin ^c   Dignard, Daniel ^b   Thomas, David Y ^b,d   Whiteway, Malcolm ^b,d  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOPROTEIN PHOSPHATASE;

ARTICLE; BACTERIAL VIRULENCE; CANDIDA ALBICANS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; GENE DISRUPTION; GENE REPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); CANDIDA ALBICANS; EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 0030660201     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.12.2539     Document Type: Article

References (68)

1. Alessi, D.R., Smythe, C., and Keyse, S.M. (1993). The human CL100 gene encodes a Tyr/Thr-protein phosphatase which potently and specifically inactivates MAP kinase and suppresses its activation by oncogenic ras in Xenopus oocyte extracts. Oncogene 8, 2015-2020.
2. Anaiffie, E.J., Pinczowfski, H., and Louria, B. (1993). Candida infections in experimental animals. In: Candidiasis: Pathogenesis, Diagnosis and Treatment, ed. G.P. Bodey, New York: Raven Press, 43-58.
3. Bliska, J.B., Guan, K.L., Dixon, J.E., and Falkow, S. (1991). Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc. Natl. Acad. Sci. USA 88, 1187-1191.
4. Buffo, J., Herman, M.A., and Soll, D.R. (1984). A characterization of pH-regulated dimorphism in Candida albicans. Mycopathologia 85, 21-30.
5. Clark, K.L., Feldmann, P.J., Dignard, D., Larocque, R., Brown, A.J., Lee, M.G., Thomas, D.Y., and 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.
6. Couvé, A., and Hirsch, J.P. (1996). Loss of sustained Fus3p kinase activity and the G1 arrest response in cells expressing an inappropriate pheromone receptor. Mol. Cell. Biol. 16, 4478-4485.
7. Denu, J.M., Zhou, G., Wu, L., Zhao, R., Yuvaniyama, J., Saper, M.A., and Dixon, J.E. (1995). The purification and characterization of a human dual-specific protein tyrosine phosphatase. J. Biol. Chem. 270, 3796-3803.
8. Doi, K., Gartner, A., Ammerer, G., Errede, B., Shinkawa, H., Sugi-moto, K., and Matsumoto, K. (1994). MSG5, a novel protein phosphatase promotes adaptation to pheromone response in S. cerevisiae. EMBO J. 13, 61-70.
9. Dorfman, K., Carrasco, D., Gruda, M., Ryan, C., Lira, S.A., and Bravo, R. (1996). Disruption of the erp/mkp-1 gene does not affect mouse development: Normal MAP kinase activity in ERP/MKP-1-deficient fibroblasts. Oncogene 13, 925-931.
10. Fidel, P., Jr., and Sobel, J.D. (1994). The role of cell-mediated immunity in candidiasis. Trends Microbiol. 2, 202-206.
11. Fischer, E.H., Charbonneau, H., and Tonks, N.K. (1991). Protein tyrosine phosphatases: a diverse family of intracellular and trans-membrane enzymes. Science 253, 401-406.
12. Fonzi, W.A., and Irwin, M.Y. (1993). Isogenic strain construction and gene mapping in Candida albicans. Genetics 134, 717-728.
13. Fukuda, M., Gotoh, Y., Tachibana, T., Dell, K., Hattori, S., Yoneda, Y., and Nishida, E. (1995). Induction of neurite outgrowth by MAP kinase in PC12 cells. Oncogene 11, 239-244.
14. Gartner, A., Nasmyth, K., and Ammerer, G. (1992). Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of FUS3 and KSS1. Genes Dev. 6, 1280-1292.
15. Gil, C., Pomes, R., and Nombela, C. (1990). Isolation and characterization of Candida albicans morphological mutants derepressed for the formation of filamentous hypha-type structures. J. Bacteriol. 172, 2384-2391.
16. Gillum, A.M., Tsay, E.Y., H., 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.
17. Gimeno, C.J., Ljungdahl, P.O., Styles, C.A., and 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.
18. Gow, N.A., and Gooday, G.W. (1982). Growth kinetics and morphology of colonies of the filamentous form of Candida albicans. J. Gen. Microbiol. 128, 2187-2194.
19. Groom, L.A., Sneddon, A.A., Alessi, D.R., Dowd, S., and Keyse, S.M. (1996). Differential regulation of the MAP, SAP, and RK/p38 kinases by Pyst1, a novel cytosolic dual-specificity phosphatase. EMBO J. 15, 3621-3632.
20. Guan, K., Broyles, S.S., and Dixon, J.E. (1991). A Tyr/Ser protein phosphatase encoded by vaccinia virus. Nature 350, 359-362.
21. Guan, K., and Dixon, J.E. (1991). Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 292, 262-267.
22. Guan, K., Hakes, D.J., Wang, Y., Park, H.D., Cooper, T.G., and Dixon, J.E. (1992). A yeast protein phosphatase related to the vaccinia virus VH1 phosphatase is induced by nitrogen starvation. Proc. Natl. Acad. Sci. USA 89, 12175-12179.
23. Guan, K.L., and Butch, E. (1995). Isolation and characterization of a novel dual specific phosphatase, HVH2, which selectively dephosphorylates the mitogen-activated protein kinase. J. Biol. Chem. 270, 7197-7203.
24. Hakes, D.J., and Dixon, J.E. (1992). New vectors for High level expression of recombinant proteins in bacteria. Anal. Biochem. 202, 293-298.
25. Hakes, D.J., Martell, K.J., Zhao, W.-G., Massung, R.F., Esposito, J.J., and Dixon, J.E. (1993). A protein phosphatase related to the Vaccinia virus VH1 is encoded in the genomes of several orthopoxviruses and a baculovirus. Proc. Natl. Acad. Sci. USA 90, 4017-4021.
26. Haring, M.A., Siderius, M., Jonak, C., Hirt, H., Walton, K.M., and Musgrave, A. (1995). Tyrosine phosphatase signalling in a lower plant: cell-cycle and oxidative stress-regulated expression of the Chlamydomonas eugametos VH-PTP13 gene. Plant J. 7, 981-988.
27. Henikoff, S., Henikoff, J.G., Alford, W.J., and Pietrokovski, S. (1995). Automated construction and graphical presentation of protein blocks from unaligned sequences. Gene 263, GC17-GC26.
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., and Tzagoloff, A. (1986). Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast 2, 163-167.
30. Hubbard, M.J., Markie, D., and Poulter, R.T. (1986). Isolation and morphological characterization of a mycelial mutant of Candida albicans. J. Bacteriol. 165, 61-65.
31. Ishibashi, T., Bottaro, D.P., Chan, A., Miki, T., and Aaronson, S.A. (1992). Expression cloning of a human dual-specificity phosphatase. Proc. Natl. Acad. Sci. USA 89, 12170-12174.
32. Keyse, S.M. (1995). An emerging family of dual specificity MAP kinase phosphatases. Biochim. Biophys. Acta 1265, 152-160.
33. Keyse, S.M., and Ginsburg, M. (1993). Amino acid sequence similarity between CL100, a dual-specificity MAP kinase phosphatase and cdc25. Trends Biochem. Sci. 18, 377-378.
34. Kohler, J.R., and 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.
35. Kunkel, T.D., Roberts, J.D., and Zakour, R.A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382.
36. Kurtz, M.B., Cortelyou, M.W., and Kirsch, D.R. (1986). Integrative transformation of Candida albicans, using a cloned Candida ADE2 gene. Mol. Cell. Biol. 6, 142-149.
37. Kwak, S.P., and Dixon, J.E. (1995). Multiple dual specificity protein tyrosine phosphatases are expressed and regulated differentially in liver cell lines. J. Biol. Chem. 270, 1156-1160.
38. Leberer, E., Harcus, D., Broadbent, I.D., Clark, K.L., Dignard, D., Ziegelbauer, K., Schmidt, A., Gow, N.A., Brown, A.J., and Thomas, D.Y. (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. Leberer, E., Thomas, D.Y., and Whiteway, M. (1997a). Pheromone signalling and polarized morphogenesis in yeast. Curr. Opin. Genet. Dev. 7, 59-66.
40. Leberer, E., Ziegelbauer, K., Schmidt, A., Harcus, D., Dignard, D., Ash, J., Johnson, L., and Thomas, D.Y. 0997b). Virulence and hyphal formation of Candida albicans require the Ste20p-like protein kinase CaCla4p. Curr. Biol. 7, 539-546.
41. 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 23, 148-153.
42. Liu, H., Kohler, J., and Fink, G.R. (1994). Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266, 1723-1726.
43. Liu, H., Styles, C.A., and Fink, G.R. (1993), Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262, 1741-1744.
44. Malathi, K., Ganesan, K., and 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.
45. Marshall, C.J. (1995). Specificity of tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
46. Martell, K.J., Seasholtz, A.F., Kwak, S.P., Clemens, K.K., and Dixon, J.E. (1995). hVH-5: a protein tyrosine phosphatase abundant in brain that inactivates mitogen-activated protein kinase. J. Neurochem. 65, 1823-1833.
47. 1/S transition. J. Cell Physiol. 163, 577-588.
48. mapk. Mol. Biol. Cell 3, 63-71.
49. Millar, J.B., Buck, V., and Wilkinson, M.G. (1995). Pyp1 and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev 9, 2117-2130.
50. Moore, S.A. (1984). Yeast cells recover from mating pheromone alpha factor-induced division arrest by desensitization in the absence of alpha-factor destruction. J. Biol. Chem. 259, 1004-1010.
51. Ninfa, E.G. (1994). Protein tyrosine phosphatases in disease processes. Trends Cell Biol. 4, 427-430.
52. Odds, F.C. (1988). Candida and Candidosis: A Review and Bibliography, 2nd ed., London: Bailliere Tindall.
53. Roberts, R.L., and 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.
54. Rogers, S., Wells, R., and Rechsteiner, M. (1986). Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234, 364-368.
55. Rohan, P.J., Davis, P., Moskaluk, CA., Kearns, M., Krutzsc, H., Siebenlist, U., and Kelly, K. (1993). PAC-1: a mitogen-induced nuclear protein tyrosine phosphatase. Science 259, 1763-1766.
56. Rose, M.D., Winston, F., and Hieter, P. (1990). Methods in Yeast Genetics: A Laboratory Course Manual, Plainview, NY: Cold Spring Harbor Laboratory Press.
57. Sambrooke, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Plainview, NY: Cold Spring Harbor Laboratory Press.
58. Sherwood, J., Gow, N.A., Gooday, G.W., Gregory, D.W., and Marshall, D. (1992). Contact sensing in Candida albicans: a possible aid to epithelial penetration. J. Med. Vet. Mycol. 30, 461-469.
59. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
60. Sobel, J.D., Muller, G., and Buckley, H.R. (1984). Critical role of germ tube formation in the pathogenesis of candidal vaginitis. Infect. Immun. 44, 576-580.
61. Soll, D.R. (1986). The regulation of cellular differentiation in the dimorphic yeast Candida albicans. Bioessays 5, 5-11.
62. Soll, D.R., Bedell, G.W., and Brummel, M. (1981). Zinc and regulation of growth and phenotype in the infectious yeast Candida albicans. Infect. Immun. 32, 1139-1147.
63. Walton, K.M., and Dixon, J.E. (1993). Protein tyrosine phosphatases. Annu. Rev. Biochem. 62, 101-120.
64. Whiteway, M., Csank, C., and Thomas, D.Y. (1993). Dominant negative selection of heterologous genes in yeast. Methods 5, 110-115.
65. Whiteway, M., Dignard, D., and 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.
66. Wu, J., Lau, L.F., and Sturgill, T.W. (1994). Rapid deactivation of MAP kinase in PC12 cells occurs independently of induction of phosphatase MKP-1. FEBS Lett. 353, 9-12.
67. Zhan, X.-L., Deschenes, R.J., and Guan, K.-L. (1997). Differential regulation of FUS3 MAP kinase by tyrosine-specific phosphatases PTP2/PTP3 and dual-specificity phosphatase MSG5 in Saccharomyces cerevisiae. Genes Dev. 11, 1690-1702.
68. Zolnierowicz, S., and Hemmings, B.A. (1996). Protein phosphatases on the piste. Trends Cell Biol. 6, 359-362.