Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans

Molecular Biology of the Cell

Volumn 16, Issue 5, 2005, Pages 2285-2300

  Bahn, Yong Sun ^a   Kojima, Kaihei ^a   Cox, Gary M ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE HOG1; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE PBS2; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; EVOLUTION; FUNGAL VIRULENCE; GENE; HOG1 GENE; NONHUMAN; PATHOGENESIS; PBS2 GENE; PRIORITY JOURNAL; SEROTYPE;

CRYPTOCOCCUS NEOFORMANS; FUNGAL PROTEINS; GENES, FUNGAL; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; SEROTYPING; VIRULENCE;

CRYPTOCOCCUS NEOFORMANS VAR. GRUBII; FILOBASIDIELLA NEOFORMANS; FUNGI;

EID: 18244375808     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-11-0987     Document Type: Article

References (53)

1. Alepuz, P. M., Jovanovic, A., Reiser, V., and Ammerer, G. (2001). Stress-induced map kinase Hog1 is part of transcription activation complexes. Mol. Cell 7, 767-777.
2. Alonso-Monge, R., Navarro-Garcia, F., Roman, E., Negredo, A. I., Eisman, B., Nombela, C., and Pla, J. (2003). The Hog1 mitogon-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot. Cell 2, 351-361.
3. Alonso-Monge, R., Real, E., Wojda, I., Bebelman, J. P., Mager, W. H., and Siderius, M. (2001). Hyperosmotic stress response and regulation of cell wall integrity in Saccharomyces cerevisiae share common functional aspects. Mol. Microbiol. 41, 717-730.
4. Alspaugh, J. A., Perfect, J. R., and Heitman, J. (1997). Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev. 11, 3206-3217.
5. Alspaugh, J. A., Pukkila-Worley, R., Harashima, T., Cavallo, L. M., Funnell, D., Cox, G. M., Perfect, J. R., Kronstad, J. W., and Heitman, J. (2002). Adenylyl cyclase functions downstream of the Gα protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryot. Cell 1, 75-84.
6. Bahn, Y. S., Hicks, J. K., Giles, S. S., Cox, G. M., and Heitman, J. (2004). Adenylyl cyclase-associated protein Aca1 regulates virulence and differentiation of Cryptococcus neoformans via the cyclic AMP-protein kinase A cascade. Eukaryot. Cell 3, 1476-1491.
7. Buck, V., Quinn, J., Soto Pino, T., Martin, H., Saldanha, J., Makino, K., Morgan, B. A., and Millar, J. B. (2001). Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol. Biol. Cell 12, 407-419.
8. Casadevall, A., and Perfect, J. R. (1998). Cryptococcus neoformans. ASM Press, Washington, DC.
9. Chang, Y. C., Wickes, B. L., Miller, G. F., Penoyer, L. A., and Kwon-Chung, K. J. (2000). Cryptococcus neoformans STE12α regulates virulence but is not essential for mating. J. Exp. Med. 191, 871-882.
10. Cox, G. M., Mukherjee, J., Cole, G. T., Casadevall, A., and Perfect, J. R. (2000). Urease as a virulence factor in experimental cryptococcosis. Infect. Immun. 68, 443-448.
11. Cruz, M. C., Sia, R. A., Olson, M., Cox, G. M., and Heitman, J. (2000). Comparison of the roles of calcineurin in physiology and virulence in serotype D and serotype A strains of Cryptococcus neoformans. Infect. Immun. 68, 982-985.
12. D'Souza, C. A., Alspaugh, J. A., Yue, C., Harashima, T., Cox, G. M., Perfect, J. R., and Heitman, J. (2001). Cyclic AMP-dependent protein kinase controls virulence of the fungal pathogen Cryptococcus neoformans. Mol. Cell. Biol. 21, 3179-3191.
13. Davidson, R. C., Blankenship, J. R., Kraus, P. R., de Jesus Berrios, M., Hull, C. M., D'Souza, C., Wang, P., and Heitman, J. (2002). A PCR-based strategy to generate integrative targeting alleles with large regions of homology. Microbiology 148, 2607-2615.
14. Davidson, R. C., Cruz, M. C., Sia, R. A., Allen, B., Alspaugh, J. A., and Heitman, J. (2000). Gene disruption by biolistic transformation in serotype D strains of Cryptococcus neoformans. Fungal Genet. Biol. 29, 38-48.
15. Degols, G., Shiozaki, K., and Russell, P. (1996). Activation and regulation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe. Mol. Cell. Biol. 16, 2870-2877.
16. Fraser, J. A., Subaran, R. L., Nichols, C. B., and Heitman, J. (2003). Recapitulation of the sexual cycle of the primary fungal pathogen Cryptococcus neoformans var. gattii: implications for an outbreak on Vancouver Island, Canada. Eukaryot. Cell 2, 1036-1045.
17. Garcia-Rodriguez, L. J., Duran, A., and Roncero, C. (2000). Calcofluor antifungal action depends on chitin and a functional high-osmolarity glycerol response (HOG) pathway: evidence for a physiological role of the Saccharomyces cerevisiae HOG pathway under noninducing conditions. J. Bacteriol. 182, 2428-2437.
18. Giaever, G. et al. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
19. Granger, D. L., Perfect, J. R., and Durack, D. T. (1985). Virulence of Cryptococcus neoformans. Regulation of capsule synthesis by carbon dioxide. J. Clin. Invest. 76, 508-516.
20. Hall, J. P., Cherkasova, V., Elion, E., Gustin, M. C., and 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.
21. Heitman, J., Allen, B., Alspaugh, J. A., and Kwon-Chung, K. J. (1999). On the origins of congenic MATα and MATa strains of the pathogenic yeast Cryptococcus neoformans. Fungal Genet. Biol. 28, 1-5.
22. Hicks, J. K., D'Souza, C. A., Cox, G. M., and Heitman, J. (2004). Cyclic AMP-dependent protein kinase catalytic subunits have divergent roles in virulence factor production in two varieties of the fungal pathogen Cryptococcus neoformans. Eukaryot. Cell 3, 14-26.
23. Hoang, L. M., Maguire, J. A., Doyle, P., Fyfe, M., and Roscoe, D. L. (2004). Cryptococcus neoformans infections at Vancouver Hospital and Health Sciences Centre (1997-2002): epidemiology, microbiology and histopathology. J. Med. Microbiol. 53, 935-940.
24. Hohmann, S. (2002). Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66, 300-372.
25. Hull, C. M., Davidson, R. C., and Heitman, J. (2002). Cell identity and sexual development in Cryptococcus neoformans are controlled by the mating-type-specific homeodomain protein Sxi1alpha. Genes Dev. 16, 3046-3060.
26. Hull, C. M., and Heitman, J. (2002). Genetics of Cryptococcus neoformans. Annu. Rev. Genet. 36, 557-615.
27. Jiang, B., Ram, A. F., Sheraton, J., Klis, F. M., and Bussey, H. (1995). Regulation of cell wall beta-glucan assembly: PTC1 negatively affects PBS2 action in a pathway that includes modulation of EXG1 transcription. Mol. Gen. Genet. 248, 260-269.
28. Kraus, P. R., Fox, D. S., Cox, G. M., and Heitman, J. (2003). The Cryptococcus neoformans MAP kinase Mpk1 regulates cell integrity in response to antifungal drugs and loss of calcineurin function. Mol. Microbiol. 48, 1377-1387.
29. Kwon-Chung, K. J., and Bennett, J. E. (1984). Epidemiologic differences between the two varieties of Cryptococcus neoformans. Am. J. Epidemiol. 120, 123-130.
30. Lengeler, K. B., Davidson, R. C., D'Souza, C., Harashima, T., Shen, W. C., Wang, P., Pan, X., Waugh, M., and Heitman, J. (2000). Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64, 746-785.
31. Loftus, B. J. et al. (2005). The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307, 1321-1324.
32. Maeda, T., Takekawa, M., and Saito, H. (1995). Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269, 554-558.
33. Maeda, T., Wurgler-Murphy, S. M., and Saito, H. (1994). A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369, 242-245.
34. Marra, R. E., Huang, J. C., Fung, E., Nielsen, K., Heitman, J., Vilgalys, R., and Mitchell, T. G. (2004). A genetic linkage map of Cryptococcus neoformans variety neoformans serotype D (Filobasidiella neoformans). Genetics 167, 619-631.
35. Mattison, C. P., Spencer, S. S., Kresge, K. A., Lee, J., and Ota, I. M. (1999). Differential regulation of the cell wall integrity mitogen-activated protein kinase pathway in budding yeast by the protein tyrosine phosphatases Ptp2 and Ptp3. Mol. Cell. Biol. 19, 7651-7660.
36. Moore, T. D., and Edman, J. C. (1993). The alpha-mating type locus of Cryptococcus neofoemans contains a peptide pheromone gene. Mol. Cell. Biol. 13, 1962-1970.
37. Nelson, R. T., Pryor, B. A., and Lodge, J. K. (2003). Sequence length required for homologous recombination in Cryptococcus neoformans. Fungal Genet. Biol. 38, 1-9.
38. Nielsen, K., Cox, G. M., Wang, P., Toffaletti, D. L, Perfect, J. R., and Heitman, J. (2003). Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and α isolates. Infect. Immun. 71, 4831-4841.
39. O'Rourke, S. M., and Herskowitz, I. (1998). The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev. 12, 2874-2886.
40. O'Rourke, S. M., Herskowitz, I., and O'Shea, E. K. (2002). Yeast go the whole HOG for the hyperosmotic response. Trends Genet. 18, 405-412.
41. Perfect, J. R., Ketabchi, N., Cox, G. M., Ingram, C. W., and Beiser, C. L. (1993). Karyotyping of Cryptococcus neoformans as an epidemiological tool. J. Clin. Microbiol. 31, 3305-3309.
42. Posas, F., and Saito, H. (1997). Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276, 1702-1705.
43. Posas, F., and Saito, H. (1998). Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J. 17, 1385-1394.
44. Posas, F., Witten, E. A., and Saito, H. (1998). Requirement of STE50 for osmostress-induced activation of the STE11 mitogen-activated protein kinase kinase kinase in the high-osmolarity glycerol response pathway. Mol. Cell. Biol. 18, 5788-5796.
45. Posas, F., Wurgler-Murphy, S. M., Maeda, T., Witten, E. A., Thai, T. C., and Saito, H. (1996). Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell 86, 865-875.
46. Reiser, V., Ruis, H., and Ammerer, G. (1999). Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae. Mol. Biol. Cell 10, 1147-1161.
47. Speed, B., and Dunt, D. (1995). Clinical and host differences between infections with the two varieties of Cryptococcus neoformans. Clin. Infect. Dis. 21, 28-34; discussion 35-36.
48. Van Wuytswinkel, O., Reiser, V., Siderius, M., Kelders, M. C., Ammerer, G., Ruis, H., and Mager, W. H. (2000). Response of Saccharomyces cerevisiae to severe osmotic stress: evidence for a novel activation mechanism of the HOG MAP kinase pathway. Mol. Microbiol, 37, 382-397.
49. Wang, P., Cutler, J., King, J., and Palmer, D. (2004). Mutation of the regulator of G protein signaling Crg1 increases virulence in Cryptococcus neoformans. Eukaryot. Cell 3, 1028-1035.
50. Wang, P., Nichols, C. B., Lengeler, K. B., Cardenas, M. E., Cox, G. M., Perfect, J. R., and Heitman, J. (2002). Mating-type-specific and nonspecific PAK kinases play shared and divergent roles in Cryptococcus neoformans. Eukaryot. Cell 1, 257-272.
51. Xu, J., Vilgalys, R., and Mitchell, T. G. (2000). Multiple gene genealogies reveal recent dispersion and hybridization in the human pathogenic fungus Cryptococcus neoformans. Mol. Ecol. 9, 1471-1481.
52. Yue, C., Cavallo, L. M., Alspaugh, J. A., Wang, P., Cox, G. M., Perfect, J. R., and Heitman, J. (1999). The STE12α homolog is required for haploid filamentation but largely dispensable for mating and virulence in Cryptococcus neoformans. Genetics 153, 1601-1615.
53. 2. Infect. Immun. 71, 6155-6164.