Cyclic AMP-Dependent Protein Kinase Controls Virulence of the Fungal Pathogen Cryptococcus neoformans

REFERENCES

• Aberg, J. A., L. M. Mundy, and W. G. Powderly. 1999. Pulmonary cryptococcosis in patients without HIV infection. Chest 115:734–740.
   PubMed Web of Science ®Google Scholar
• Alspaugh, J. A., L. M. Cavallo, J. R. Perfect, and J. Heitman. 2000. RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans Mol. Microbiol. 36:352–365.
   Google Scholar
• Alspaugh, J. A., R. C. Davidson, and J. Heitman. 2000. Morphogenesis of Cryptococcus neoformans. Dimorphism in human pathogenic and apathogenic yeasts. J. F. Ernst, and A. Schmidt. 5. Contributions in microbiology:217–238. Karger, Basel, Switzerland
   Google Scholar
• Alspaugh, J. A., J. R. Perfect, and J. Heitman. 1997. Cryptococcus neoformans mating and virulence are regulated by the G-protein α subunit GPA1 and cAMP. Genes Dev. 11:3206–3217.
   PubMedGoogle Scholar
• Borges-Walmsley, M. I., and A. R. Walmsley. 2000. cAMP signalling in pathogenic fungi: control of dimorphic switching and pathogenicity. Trends Microbiol. 8:133–141.
   PubMed Web of Science ®Google Scholar
• Bourbonnais, R., and M. G. Paice. 1990. Oxidation of non-phenolic substrates. An expanded role for laccase in lignin biodegradation. FEBS Lett. 267:99–102.
   PubMed Web of Science ®Google Scholar
• Casadevall, A., and J. R. Perfect. 1998. Cryptococcus neoformans. ASM Press, Washington, D.C.
   Google Scholar
• Casadevall, A., A. L. Rosas, and J. D. Nosanchuk. 2000. Melanin and virulence in Cryptococcus neoformans Curr. Opin. Microbiol. 3:354–358.
   PubMed Web of Science ®Google Scholar
• Chang, Y. C., R. Cherniak, T. R. Kozel, D. L. Granger, L. C. Morris, L. C. Weinhold, and K. J. Kwon-Chung. 1997. Structure and biological activities of acapsular Cryptococcus neoformans 602 complemented with the CAP64 gene. Infect. Immun. 65:1584–1592.
   PubMedGoogle Scholar
• Chang, Y. C., and K. J. Kwon-Chung. 1994. Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol. Cell. Biol. 14:4912–4919.
   PubMed Web of Science ®Google Scholar
• Chang, Y. C., and K. J. Kwon-Chung. 1999. Isolation, characterization, and localization of a capsule-associated gene, CAP10, of Cryptococcus neoformans. J. Bacteriol. 181:5636–5643.
   PubMedGoogle Scholar
• Chang, Y. C., L. A. Penoyer, and K. J. Kwon-Chung. 1996. The second capsule gene of Cryptococcus neoformans, CAP64, is essential for virulence. Infect. Immun. 64:1977–1983.
   PubMed Web of Science ®Google Scholar
• Chang, Y. C., B. L. Wickes, G. F. Miller, L. A. Penoyer, and K. J. Kwon-Chung. 2000. Cryptococcus neoformans STE12α regulates virulence but is not essential for mating. J. Exp. Med. 191:871–882.
   PubMedGoogle Scholar
• Chen, S., T. Sorrell, G. Nimmo, B. Speed, B. Currie, D. Ellis, D. Marriott, T. Pfeiffer, D. Parr, and K. Byth. 2000. Epidemiology and host- and variety-dependent characteristics of infection due to Cryptococcus neoformans in Australia and New Zealand. Clin. Infect. Dis. 31:499–508.
   PubMed Web of Science ®Google Scholar
• Cruickshank, J. G., R. Cavill, and M. Jelbert. 1973. Cryptococcus neoformans of unusual morphology. Appl. Microbiol. 25:309–312.
   PubMedGoogle Scholar
• Cruz, M. C., M. D. Poeta, P. Wang, R. Wenger, G. Zenke, V. F. J. Quesniaux, N. R. Movva, J. R. Perfect, M. E. Cardenas, and J. Heitman. 2000. Immunosuppressive and nonimmunosuppressive cyclosporin analogs are toxic to the opportunistic fungal pathogen Cryptococcus neoformans via cyclophilin-dependent inhibition of calcineurin. Antimicrob. Agents Chemother. 44:143–149.
   PubMed Web of Science ®Google Scholar
• Del Poeta, M., D. L. Toffaletti, T. H. Rude, C. C. Dykstra, J. Heitman, and J. R. Perfect. 1999. Topoisomerase I is essential in Cryptococcus neoformans: role in pathobiology and as an antifungal target. Genetics 152:167–178.
   PubMed Web of Science ®Google Scholar
• Dong, Z. M., and J. W. Murphy. 1996. Cryptococcal polysaccharides induce L-selectin shedding and tumor necrosis factor receptor loss from the surface of human neutrophils J. Clin. Investig. 97:689–698.
   Google Scholar
• Dong, Z. M., and J. W. Murphy. 1995. Effects of the two varieties of Cryptococcus neoformans cells and culture filtrate antigens on neutrophil locomotion. Infect. Immun. 63:2632–2644.
   PubMed Web of Science ®Google Scholar
• Donzeau, M., and W. Bandlow. 1999. The yeast trimeric guanine nucleotide-binding protein α subunit, Gpa2p, controls the meiosis-specific kinase Ime2p activity in response to nutrients. Mol. Cell. Biol. 19:6110–6119.
   PubMedGoogle Scholar
• Dromer, F., P. Aucouturier, J. P. Clauvel, G. Saimot, and P. Yeni. 1988. Cryptococcus neoformans antibody levels in patients with AIDS. Scand. J. Infect. Dis. 20:283–285.
   PubMed Web of Science ®Google Scholar
• Dromer, F., O. Ronin, and B. Dupont. 1992. Isolation of Cryptococcus neoformans var. gattii from an Asian patient in France: evidence for dormant infection in healthy subjects. J. Med. Vet. Mycol. 30:395–397.
   PubMedGoogle Scholar
• Dürrenberger, F., K. Wong, and J. W. Kronstad. 1998. Identification of a cAMP-dependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis. Proc. Natl. Acad. Sci. USA 95:5684–5689.
   PubMed Web of Science ®Google Scholar
• Feldmesser, M., Y. Kress, P. Novikoff, and A. Casadevall. 2000. Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect. Immun. 68:4225–4237.
   PubMed Web of Science ®Google Scholar
• Garcia-Hermoso, D., G. Janbon, and F. Dromer. 1999. Epidemiological evidence for dormant Cryptococcus neoformans infection. J. Clin. Microbiol. 37:3204–3209.
   PubMed Web of Science ®Google Scholar
• Gold, S., G. Duncan, K. Barrett, and J. Kronstad. 1994. cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev. 8:2805–2816.
   PubMed Web of Science ®Google Scholar
• Gold, S. E., S. M. Brogdon, M. E. Mayorga, and J. W. Kronstad. 1997. The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell 9:1585–1594.
   PubMed Web of Science ®Google Scholar
• Granger, D. L., J. R. Perfect, and D. T. Durack. 1985. Virulence of Cryptococcus neoformans: regulation of capsule synthesis by carbon dioxide. J. Clin. Investig. 76:508–516.
   PubMed Web of Science ®Google Scholar
• Henderson, D. K., J. E. Bennett, and M. A. Huber. 1982. Long-lasting specific immunologic unresponsiveness associated with cryptococcal meningitis. J. Clin. Investig. 69:1185–1190.
   PubMedGoogle Scholar
• Isshiki, T., N. Mochizuki, T. Maeda, and M. Yamamoto. 1992. Characterization of a fission yeast gene, gpa2, that encodes a Gα subunit involved in the monitoring of nutrition. Genes Dev. 6:2455–2462.
   PubMedGoogle Scholar
• Jacobson, E. S., and S. B. Tinnell. 1993. Antioxidant function of fungal melanin. J. Bacteriol. 175:7102–7104.
   PubMed Web of Science ®Google Scholar
• Kozel, T. R., and J. J. Cazin. 1971. Nonencapsulated variant of Cryptococcus neoformans. I. Virulence studies and characterization of soluble polysaccharide. Infect. Immun. 3:287–294.
   PubMed Web of Science ®Google Scholar
• Kraakman, L., K. Lemaire, P. Ma, A. W. R. H. Teunissen, M. C. V. Donaton, P. V. Dijck, J. Winderickx, J. H. De Winde, and J. M. Thevelein. 1999. A Saccharomyces cerevisiae G-protein coupled receptor, Gpr1, is specifically required for glucose activation of the cAMP pathway during the transition to growth on glucose. Mol. Microbiol. 32:1002–1012.
   PubMedGoogle Scholar
• Kronstad, J., A. D. Maria, D. Funnell, R. D. Laidlaw, N. Lee, M. M. d. Sá, and M. Ramesh. 1998. Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways. Arch. Microbiol. 170:395–404.
   PubMed Web of Science ®Google Scholar
• Krüger, J., G. Loubradou, E. Regenfelder, A. Hartmann, and R. Kahmann. 1998. Crosstalk between cAMP and pheromone signalling pathways in Ustilago maydis. Mol. Gen. Genet. 260:193–198.
   PubMedGoogle Scholar
• Krüger, J., G. Loubradou, G. Wanner, E. Regenfelder, M. Feldbrugge, and R. Kahmann. 2000. Activation of the cAMP pathway in Ustilago maydis reduces fungal proliferation and teliospore formation in plant tumors. Mol. Plant-Microbe Interact. 13:1034–1040.
   PubMedGoogle Scholar
• Kübler, E., H. U. Mösch, S. Rupp, and M. P. Lisanti. 1997. Gpa2p, a G-protein alpha-subunit, regulates growth and pseudohyphal development in Saccharomyces cerevisiae via a cAMP-dependent mechanism. J. Biol. Chem. 272:20321–20323.
   PubMedGoogle Scholar
• Kwon-Chung, K. J.. 1975. A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 67:1197–1200.
   PubMed Web of Science ®Google Scholar
• Kwon-Chung, K. J.. 1976. A new species of Filobasidiella, the sexual state of Cryptococcus neoformans B and C serotypes. Mycologia 68:943–946.
   PubMed Web of Science ®Google Scholar
• Kwon-Chung, K. J., I. Polacheck, and T. J. Popkin. 1982. Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice. J. Bacteriol. 150:1414–1421.
   PubMed Web of Science ®Google Scholar
• Kwon-Chung, K. J., and J. C. Rhodes. 1986. Encapsulation and melanin formation as indicators of virulence in Cryptococcus neoformans. Infect. Immun. 51:218–223.
   PubMed Web of Science ®Google Scholar
• Landry, S., M. T. Pettit, E. Apolinario, and C. S. Hoffman. 2000. The fission yeast git5 gene encodes a Gβ subunit required for glucose-triggered adenylate cyclase activation. Genetics 154:1463–1471.
   PubMedGoogle Scholar
• Lengeler, K. B., R. C. Davidson, C. D'Souza, T. Harashima, W.-C. Shen, P. Wang, X. Pan, M. Waugh, and J. Heitman. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64:746–785.
   PubMed Web of Science ®Google Scholar
• Levitz, S. M., and D. J. DiBenedetto. 1988. Differential stimulation of murine resident peritoneal cells by selectively opsonized encapsulated and acapsular Cryptococcus neoformans. Infect. Immun. 56:2544–2551.
   PubMedGoogle Scholar
• Liu, L., K. Wakamatsu, S. Ito, and P. R. Williamson. 1999. Catecholamine oxidative products, but not melanin, are produced by Cryptococcus neoformans during neuropathogenesis in mice. Infect. Immun. 67:108–112.
   PubMed Web of Science ®Google Scholar
• Lorenz, M. C., and J. Heitman. 1997. Yeast pseudohyphal growth is regulated by GPA2, a G protein α homolog. EMBO J. 16:7008–7018.
   PubMedGoogle Scholar
• Lorenz, M. C., X. Pan, T. Harashima, M. E. Cardenas, Y. Xue, J. P. Hirsch, and J. Heitman. 2000. The G protein-coupled receptor GPR1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154:609–622.
   PubMedGoogle Scholar
• Loubradou, G., J. Begueret, and B. Turcq. 1999. MOD-D, a Gα subunit of the fungus Podospora anserina, is involved in both regulation of development and vegetative incompatibility. Genetics 152:519–528.
   PubMedGoogle Scholar
• Love, G. L., G. D. Boyd, and D. L. Greer. 1985. Large Cryptococcus neoformans isolated from brain abscess. J. Clin. Microbiol. 22:1068–1070.
   PubMedGoogle Scholar
• Ma, P., S. Wera, P. V. Dijck, and J. M. Thevelein. 1999. The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol. Biol. Cell. 10:91–104.
   PubMedGoogle Scholar
• Mbonyi, K., L. V. Aelst, J. C. Argüelles, A. W. H. Jans, and J. M. Thevelein. 1990. Glucose-induced hyperaccumulation of cyclic AMP and defective glucose repression in yeast strains with reduced activity of cyclic AMP-dependent protein kinase. Mol. Cell Biol. 10:4518–4523.
   PubMedGoogle Scholar
• Mitchell, T. G., and J. R. Perfect. 1995. Cryptococcosis in the era of AIDS—100 years after the discovery of Cryptococcus neoformans. Clin. Microbiol. Rev. 8:515–548.
   PubMed Web of Science ®Google Scholar
• Neilson, J. B., R. A. Fromtling, and G. S. Bulmer. 1977. Cryptococcus neoformans: size range of infectious particles from aerosolized soil. Infect. Immun. 17:634–638.
   PubMed Web of Science ®Google Scholar
• Nikawa, J., S. Cameron, T. Toda, K. M. Ferguson, and M. Wigler. 1987. Rigorous feedback control of cAMP levels in Saccharomyces cerevisiae. Genes Dev. 1:931–937.
   PubMedGoogle Scholar
• Nocero, M., T. Isshiki, M. Yamamoto, and C. S. Hoffman. 1994. Glucose repression of fbp1 transcription in Schizosaccharomyces pombe is partially regulated by adenylate cyclase activation by a G protein α subunit encoded by gpa2 (git8). Genetics 138:39–45.
   PubMedGoogle Scholar
• Nosanchuk, J. D., A. L. Rosas, and A. Casadevall. 1998. The antibody response to fungal melanin in mice. J. Immunol. 160:6026–6031.
   PubMedGoogle Scholar
• Nosanchuk, J. D., A. L. Rosas, S. C. Lee, and A. Casadevall. 2000. Melanisation of Cryptococcus neoformans in human brain tissue. Lancet 355:2049–2050.
   PubMed Web of Science ®Google Scholar
• Nosanchuk, J. D., P. Valadon, M. Feldmesser, and A. Casadevall. 1999. Melanization of Cryptococcus neoformans in murine infection. Mol. Cell. Biol. 19:745–750.
   PubMed Web of Science ®Google Scholar
• Nunez, M., J. J. E. Peacock, and J. R. Chin. 2000. Pulmonary cryptococcosis in the immunocompetent host. Therapy with oral fluconazole: a report of four cases and a review of the literature. Chest 118:527–534.
   PubMed Web of Science ®Google Scholar
• Orth, A. B., M. Rzhetskaya, E. J. Pell, and M. Tien. 1995. A serine (threonine) protein kinase confers fungicide resistance in the phytopathogenic fungus Ustilago maydis. Appl. Environ. Microbiol. 61:2341–2345.
   PubMedGoogle Scholar
• Pan, X., and J. Heitman. 1999. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:4874–4887.
   PubMed Web of Science ®Google Scholar
• Patel, P., J. Ramanathan, M. Kayser, and J. J. Baran. 2000. Primary cutaneous cryptococcosis of the nose in an immunocompetent woman. J. Am. Acad. Dermatol. 43:344–345.
   PubMed Web of Science ®Google Scholar
• Perfect, J. R., D. L. Toffaletti, and T. H. Rude. 1993. The gene encoding phosphoribosylaminoimidazole carboxylase (ADE2) is essential for growth of Cryptococcus neoformans in cerebrospinal fluid. Infect. Immun. 61:4446–4451.
   PubMed Web of Science ®Google Scholar
• Regenfelder, E., T. Spellig, A. Hartmann, S. Lauenstein, M. Bölker, and R. Kahmann. 1997. G proteins in Ustilago maydis: transmission of multiple signals?. EMBO J. 16:1934–1942.
   PubMedGoogle Scholar
• Robertson, L. S., and G. R. Fink. 1998. The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc. Natl. Acad. Sci. USA 95:13783–13787.
   PubMed Web of Science ®Google Scholar
• Rosas, A. L., J. D. Nosanchuk, M. Feldmesser, G. M. Cox, H. C. McDade, and A. Casadevall. 2000. Synthesis of polymerized melanin by Cryptococcus neoformans in infected rodents. Infect. Immun. 68:2845–2853.
   PubMed Web of Science ®Google Scholar
• Rupp, S., E. Summers, H. Lo, H. Madhani, and G. Fink. 1999. MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J. 18:1257–1269.
   PubMed Web of Science ®Google Scholar
• Salas, S. D., J. E. Bennett, K. J. Kwon-Chung, J. R. Perfect, and P. R. Williamson. 1996. Effect of the laccase gene, CNLAC1, on virulence of Cryptococcus neoformans. J. Exp. Med. 184:377–386.
   PubMed Web of Science ®Google Scholar
• Sia, R. A., K. B. Lengeler, and J. Heitman. 2000. Diploid strains of the pathogenic basidiomycete Cryptococcus neoformans are thermally dimorphic. Fungal Genet. Biol. 29:153–163.
   PubMedGoogle Scholar
• Sudarshan, S., R. C. Davidson, J. Heitman, and J. A. Alspaugh. 1999. Molecular analysis of the Cryptococcus neoformans ADE2 gene, a selectable marker for transformation and gene disruption. Fungal Genet. Biol. 27:36–48.
   PubMedGoogle Scholar
• Sukroongreung, S., K. Kitiniyom, C. Nilakul, and S. Tantimavanich. 1998. Pathogenicity of basidiospores of Filobasidiella neoformans var. neoformans. Med. Mycol. 36:419–424.
   PubMed Web of Science ®Google Scholar
• Thevelein, J. M., L. Cauwenberg, S. Colombo, J. H. De Winde, M. Donaton, F. Dumortier, L. Kraakman, K. Lemaire, P. Ma, D. Nauwelaers, F. Rolland, A. Teunissen, P. V. Dijck, M. Versele, S. Wera, and J. Winderickx. 2000. Nutrient-induced signal transduction through the protein kinase A pathway and its role in the control of metabolism, stress resistance, and growth in yeast Enzyme Microb. Technol. 26:819–825.
   Google Scholar
• Thevelein, J. M., and J. H. De Winde. 1999. Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 33:904–18.
   PubMed Web of Science ®Google Scholar
• Vartivarian, S. E., E. J. Anaissie, R. E. Cowart, H. A. Sprigg, M. J. Tingler, and E. S. Jacobson. 1993. Regulation of cryptococcal capsular polysaccharide by iron. J. Infect. Dis. 167:186–190.
   PubMed Web of Science ®Google Scholar
• Vecchiarelli, A., C. Retini, C. Monari, C. Tascini, F. Bistoni, and T. R. Kozel. 1996. Purified capsular polysaccharide of Cryptococcus neoformans induces interleukin-10 secretion by human monocytes. Infect. Immun. 64:2846–2849.
   PubMedGoogle Scholar
• Vecchiarelli, A., C. Retini, D. Pietrella, C. Monari, C. Tascini, T. Beccari, and T. R. Kozel. 1995. Downregulation by cryptococcal polysaccharide of tumor necrosis factor alpha and interleukin-1β secretion from human monocytes. Infect. Immun. 63:2919–2923.
   PubMed Web of Science ®Google Scholar
• Wang, Y., and A. Casadevall. 1994. Susceptibility of melanized and nonmelanized Cryptococcus neoformans to nitrogen- and oxygen-derived oxidants. Infect. Immun. 62:3004–3007.
   PubMed Web of Science ®Google Scholar
• Welton, R. M., and C. S. Hoffman. 2000. Glucose monitoring in fission yeast via the gpa2 Gα, the git5 Gβ and the git3 putative glucose receptor. Genetics 156:513–521.
   PubMed Web of Science ®Google Scholar
• Wickes, B. L., U. Edman, and J. C. Edman. 1997. The Cryptococcus neoformans STE12α gene: a putative Saccharomyces cerevisiae STE12 homologue that is mating type specific. Mol. Microbiol. 26:951–960.
   PubMed Web of Science ®Google Scholar
• Xue, Y., M. Batlle, and J. P. Hirsch. 1998. GPR1 encodes a putative G protein-coupled receptor that associates with the Gpa2p Gα subunit and functions in a Ras-independent pathway. EMBO J. 17:1996–2007.
   PubMed Web of Science ®Google Scholar
• Yasuoka, A., S. Kohno, H. Yamada, M. Kaku, and H. Koga. 1994. Influence of molecular sizes of Cryptococcus neoformans capsular polysaccharide on phagocytosis. Microbiol. Immunol. 38:851–856.
   PubMedGoogle Scholar
• Yue, C., L. M. Cavallo, J. A. Alspaugh, P. Wang, G. M. Cox, J. R. Perfect, and J. Heitman. 1999. The STE12α homolog is required for haploid filamentation but largely dispensable for mating and virulence in Cryptococcus neoformans. Genetics 153:1601–1615.
   PubMed Web of Science ®Google Scholar