Novel gene functions required for melanization of the human pathogen Cryptococcus neoformans

Molecular Microbiology

Volumn 57, Issue 5, 2005, Pages 1381-1396

  Walton, Felicia J ^a   Idnurm, Alexander ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATX1 PROTEIN; CARRIER PROTEIN; CHAPERONE; CHELATING AGENT; CHITIN SYNTHASE; CHS3 PROTEIN; COPPER; COPPER TRANSPORT PROTEIN CCC2; ENZYME; GENOMIC DNA; IRON; LACCASE; MELANIN; METAL ION; SNF5 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MBF1; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CRYPTOCOCCUS NEOFORMANS; CULTURE MEDIUM; FUNGAL VIRULENCE; FUNGUS CULTURE; FUNGUS MUTANT; GENE; GENE EXPRESSION; GENOTYPE; LAC1 GENE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SOUTHERN BLOTTING;

ALLELES; BASE SEQUENCE; CATION TRANSPORT PROTEINS; CHITIN SYNTHASE; COPPER; CRYPTOCOCCUS NEOFORMANS; FUNGAL PROTEINS; GENES, FUNGAL; HUMANS; IRON; IRON CHELATING AGENTS; LACCASE; MELANINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; PROMOTER REGIONS (GENETICS); RHIZOBIUM; TRANS-ACTIVATORS; VIRULENCE;

AGROBACTERIUM; FILOBASIDIELLA NEOFORMANS;

EID: 23844435604     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04779.x     Document Type: Article

References (77)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Alspaugh, U.A., Perfect, U.R., and Heitman, J. (1997) Cryptococcus neoformans mating and virulence are regulated by the G-protein α subunit GPA1 and cAMP. Genes Dev 11: 3206-3217.
3. Askwith, C., Eide, D., Van Ho, A., Bernard, P.S., Li, L., Davis-Kaplan, S., et al. (1994) The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76: 000-000.
4. 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.
5. Barluzzi, R., Brozzetti, A., Mariucci, G., Tantucci, M., Neglia, R.G., Bistoni, F., and Blasi, E. (2000) Establishment of protective immunity against cerebral cryptococcosis by means of an avirulent, non melanogenic Cryptococcus neoformans strain. J Neuroimmunol 109: 75-86.
6. Bull, P.C., Thomas, G.R., Rommens, J.M., Forbes, J.R., and Cox, D.W. (1993) The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat Genet 5: 327-337.
7. Bundock, P., den Dulk-Ras, A., Beijersbergen, A., and Hooykaas, P.J.J. (1995) Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J 14: 3206-3214.
8. Bundock, P., van Attikum, H., den Dulk-Ras, A., and Hooykaas, P.J.J. (2002) Insertional mutagenesis in yeasts using T-DNA from Agrobacterium tumefaciens. Yeast 19: 529-536.
9. Casadevall, A., and Perfect, J. (1998) Cryptococcus neoformans. Washington, DC: American Society for Microbiology Press.
10. Covert, S.F., Kapoor, P., Lee, M.-H., Briley, A., and Nairn, C.J. (2001) Agrobacterium tumefaciens-mediated transformation of Fusarium circinatum. Mycol Res 105: 259-264.
11. Cruz, M.C., Cavallo, L.M., Görlach, J.M., Cox, G., Perfect, J.R., Cardenas, M.E., and Heitman, J. (1999) Rapamycin antifungal action is mediated via conserved complexes with FKBP12 and TOR kinase homologs in Cryptococcus neoformans. Mol Cell Biol 19: 4101-4112.
12. Cupples, G.G., Miller, J.H., and Huber, R.E. (1990) Determination of the roles of Glu-461 in beta-galactosidase (Escherichia coli) using site-specific mutagenesis. J Biol Chem 265: 5512-5518.
13. 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.
14. Davidson, R.C., Blankenship, J.R., Kraus, P.R., de Jesus Berrios, M., Hull, C.M., D'Souza, C., et al. (2002) A PCR-based strategy to generate integrative targeting alleles with large regions of homology. Microbiology 148: 2607-2615.
15. van Duin, D., Casadevall, A., and Nosanchuk, J.D. (2002) Melanization of Cryptococcus neoformans and Histoplasma capsulatum reduces their susceptibilities to amphotericin B and caspofungin. Antimicrob Agents Chemother 46: 3394-3400.
16. Erickson, T., Liu, L., Gueyikian, A., Zhu, X., Gibbons, J., and Williamson, P.R. (2001) Multiple virulence factors of Cryptococcus neoformans are dependent on VPH1. Mol Microbiol 42: 1121-1131.
17. Feng, B., Wang, X., Hauser, M., Kaufmann, S., Jentsch, S., Haase, G., et al. (2001) Molecular cloning and characterization of WdPKS1, a gene involved in dihydroxynaphthalene melanin biosynthesis and virulence in Wangiella (Exophiala) Dermatitidis. Infect Immun 69: 1781-1794.
18. Fox, D.S., Cruz, M.C., Sia, R.A., Ke, H., Cox, G.M., Cardenas, M.E., and Heitman, J. (2001) Calcineurin regulatory subunit is essential for virulence and mediates interactions with FKBP12-FK506 in Cryptococcus neoformans. Mol Microbiol 39: 835-849.
19. 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.
20. Hamza, I., Schaefer, M., Klomp, L.W.J., and Gitlin, J.D. (1999) Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis. Proc Natl Acad Sci USA 96: 13363-13368.
21. Hicks, U.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.
22. Hill, H.Z. (1992) The function of melanin or six blind people examine an elephant. Bioessays 14: 49-56.
23. Hirschhorn, J.N., Brown, S.A., Clark, C.D., and Winston, F. (1992) Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev 6: 2288-2298.
24. 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.
25. Howard, R.J., and Valent, B. (1996) Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu Rev Microbiol 50: 491-512.
26. Huffnagle, G.B., Chen, G.H., Curtis, J.L., McDonald, R.A., Strieter, R.M., and Toews, G.B. (1995) Down-regulation of the afferent phase of T cell-mediated pulmonary inflammation and immunity by a high melanin-producing strain of Cryptococcus neoformans. J Immunol 155: 3507-3516.
27. Idnurm, A., and Heitman, J. (2005) Light controls growth and development via a conserved pathway in the fungal kingdom. PloS Biol 3: E95.
28. Idnurm, A., Reedy, J.L., Nussbaum, U.C., and Heitman, J. (2004) Cryptococcus neoformans virulence gene discovery through insertional mutagenesis. Eukaryot Cell 3: 420-429.
29. Ishida, S., Lee, J., Thiele, D.J., and Herskowitz, I. (2002) Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctrl in yeast and mammals. Proc Natl Acad Sci USA 99: 14298-14302.
30. Kwon-Chung, K.J., and Rhodes, J.C. (1986) Encapsulation and melanin formation as indicators of virulence in Cryptococcus neoformans. Infect Immun 51: 218-223.
31. Kwon-Chung, K.J., Polacheck, I., and Popkin, T.J. (1982) Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice. J Bacteriol 150: 1414-1421.
32. Kwon-Chung, K.J., Edman, J.C., and Wickes, B.L. (1992) Genetic association of mating types and virulence in Cryptococcus neoformans. Infect Immun 60: 602-605.
33. Langfelder, K., Streibel, M., Jahn, B., Haase, G., and Brakhage, A.A. (2003) Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet Biol 38: 143-158.
34. Lee, S.C., Dickson, D.W., and Casadevall, A. (1996) Pathology of cryptococcal meningoencephalitis: analysis of 27 patients with pathogenetic implications. Hum Pathol 27: 839-847.
35. Lee, J., Petris, M.J., and Thiele, D.J. (2002) Characterization of mouse embryonic cells deficient in the ctr1 high affinity copper transporter. Identification of a Ctr1-independent copper transport system. J Biol Chem 277: 40253-40259.
36. Lehmann-Horn, F., Mailander, V., Heine, R., and George, A.L. (1995) Myotonia levior is a chloride channel disorder. Hum Mol Genet 4: 1397-1402.
37. Li, R.K., and Rinaldi, M.G. (1999) In vitro antifungal activity of nikkomycin Z in combination with fluconazole or itraconazole. Antimicrob Agents Chemother 43: 1401-1405.
38. Missall, T.A., Moran, J.M., Corbett, J.A., and Lodge, J.K. (2005) Distinct stress responses of two functional laccases in Cryptococcus neoformans are revealed in the absence of the thiol-specific antioxidant Tsa1. Eukaryot Cell 4: 202-208.
39. Mitchell, T.G., and Perfect, J.R. (1995) Cryptococcosis in the era of AIDS-100 years after the discovery of Cryptococcus neoformans. Clin Microbiol Rev 8: 515-548.
40. Neigeborn, L., and Carlson, M. (1984) Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics 108: 845-858.
41. Nelson, R.T., Hua, J., Pryor, B., and Lodge, U.K. (2001) Identification of virulence mutants of the fungal pathogen Cryptococcus neoformans using signature-tagged mutagenesis. Genetics 157: 935-947.
42. 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.
43. Nosanchuk, J.D., and Casadevall, A. (2003) The contribution of melanin to microbial pathogenesis. Cell Microbiol 5: 203-223.
44. Nosanchuk, J.D., Gómez, B.L., Youngchim, S., Díez, S., Aisen, P., Zancopé-Oliveira, R.M., et al. (2002) Histoplasma capsulatum synthesizes melanin-like pigments in vitro and during mammalian infection. Infect Immun 70: 5124-5131.
45. O'Halloran, T.V., and Culotta, V.C. (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275: 25057-25060.
46. Pan, X., Li, Y., and Stein, L. (2005) Site preferences of insertional mutagenesis agents in Arabidopsis. Plant Physiol 137: 168-175.
47. Panepinto, J., Liu, L., Ramos, J., Zhu, X., Valyi-Nagy, T., Eksi, S., et al. (2005) The DEAD-box RNA helicase Vad1 regulates multiple virulence-associated genes in Cryptococcus neoformans. J Clin Invest 115: 632-641.
48. Parisot, D., Dufresne, M., Veneault, C., Lauge, R., and Langin, T. (2002) clap1, a gene encoding a copper-transporting ATPase involved in the process of infection by the phytopathogenic fungus Colletotrichum lindemuthianum. Mol Genet Genomics 268: 139-151.
49. Pitkin, J.W., Panaccione, D.G., and Walton, J.D. (1996) A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum. Microbiology 142: 1557-1565.
50. Polacheck, I., Hearing, V.J., and Kwon-Chung, K.J. (1982) Biochemical studies of phenoloxidase and utilization of catecholamines in Cryptococcus neoformans. J Bacteriol 150: 1212-1220.
51. Pufahl, R.A., Singer, C.P., Peariso, K.L., Lin, S.J., Schmidt, P.J., Fahrni, C.J., et al. (1997) Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science 278: 853-856.
52. Pukkila-Worley, R., Gerrald, Q.D., Kraus, P.P., Boily, M.-J., Davis, M.J., Giles, S.S., et al. (2005) Transcriptional network of multiple capsule and melanin genes governed by the Cryptococcus neoformans cyclic AMP cascade. Eukaryot Cell 4: 190-201.
53. Rees, E.M., and Thiele, D.J. (2004) From aging to virulence: forging connections through the study of copper homeostasis in eukaryotic microorganisms. Curr Opin Microbiol 7: 175-184.
54. Rhodes, J.C., Polacheck, I., and Kwon-Chung, K.J. (1982) Phenoloxidase activity and virulence in isogenic strains of Cryptococcus neoformans. Infect Immun 36: 1175-1184.
55. Roncero, C. (2002) The genetic complexity of chitin synthesis in fungi. Curr Genet 41: 367-378.
56. Rosas, A.L., Nosanchuk, J.D., Gomez, B.L., Edens, W.A., Henson, J.M., and Casadevall, A. (2000) Isolation and serological analyses of fungal melanins. J Immunol Methods 244: 69-80.
57. Ruiz-Herrera, J., Gonzalez-Prieto, J.M., and Ruiz-Medrano, R. (2002) Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Res 1: 247-256.
58. Rutherford, J.C., and Bird, A.J. (2004) Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot Cell 3: 1-13.
59. Salas, S.D., Bennett, J.E., Kwon-Chung, K.J., Perfect, J.R., and Williamson, P.R. (1996) Effect of the laccase gene CNLAC1, on virulence of Cryptococcus neoformans. J Exp Med 184: 377-386.
60. Smith, A.N., Skaug, J., Choate, K.A., Nayir, A., Bakkaloglu, A., Ozen, S., et al. (2000) Mutations in ATP6N1B, encoding a new kidney vacuolar proton pump 116-kD subunit, cause recessive distal renal tubular acidosis with preserved hearing. Nat Genet 26: 71-75.
61. Stearman, R., Yuan, D.S., Yamaguchi-Iwai, Y., Klausner, R.D., and Dancis, A. (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271: 1552-1557.
62. Steenbergen, J.N., Shuman, H.A., and Casadevall, A. (2001) Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci USA 98:15245-15250.
63. Sudarsanam, P., Iyer, V.R., Brown, P.O., and Winston, F. (2000) Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 97: 3364-3369.
64. Swanson, M.J., Qiu, H., Sumibcay, L., Krueger, A., Kim, S.J., Natarajan, K., et al. (2003) A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo. Mol Cell Biol 23: 2800-2820.
65. Takemaru, K.-i., Li, F.-Q., Ueda, H., and Hirose, S. (1997) Multiprotein bridging factor 1 (MBF1) is an evolutionary conserved transcriptional coactivator that connects a regulatory factor and TATA element-binding protein. Proc Natl Acad Sci USA 94: 7251-7256.
66. Torres-Guererro, H., and Edman, J.C. (1994) Melanin-deficient mutants of Cryptococcus neoformans. J Med Vet Mycol 32: 303-313.
67. Tsuji, G., Takeda, T., Furusawa, I., Horino, O., and Kubo, Y. (1997) Carpropamid, an anti-rice blast fungicide, inhibits scytalone dehydratase activity and appressorial penetration in Colletotrichum lagenarium. Pesticide Biochem Physiol 57: 211-219.
68. Uldschmid, A., Engel, M., Dombi, R., and Marbach, K. (2002) Identification and functional expression of tahA, a filamentous fungal gene involved in copper trafficking to the secretory pathway in Trametes versicolor. Microbiology 148: 4049-4058.
69. Uldschmid, A., Dombi, R., and Marbach, K. (2003) Identification and functional expression of ctaA, a P-type ATPase gene involved in copper trafficking in Trametes versicolor. Microbiology 149: 2039-2048.
70. Versteege, I., Sevenet, N., Lange, J., Rousseau-Merck, M.F., Ambros, P., Handgretinger, R., et al. (1998) Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394: 203-206.
71. Vulpe, C., Levinson, B., Whitney, S., Packman, S., and Gitschier, J. (1993) Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet 3: 7-13.
72. Williamson, P.R. (1994) Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J Bacteriol 176: 656-664.
73. Yamaguchi, Y., Heiny, M.E., Suzuki, M., and Gitlin, J.D. (1996) Biochemical characterization and intracellular localization of the Menkes disease protein. Proc Natl Acad Sci USA 93: 14030-14035.
74. Zhu, X., and Williamson, P.R. (2003) A CLC-type chloride channel gene is required for laccase activity and virulence in Cryptococcus neoformans. Mol Microbiol 50: 1271-1282.
75. Zhu, X., and Williamson, P.R. (2004) Role of laccase in the biology and virulence of Cryptococcus neoformans. FEMS Yeast Res 5: 1-10.
76. Zhu, X., Gibbons, J., Garcia-Rivera, J., Casadevall, A., and Williamson, P.R. (2001) Laccase of Cryptococcus neoformans is a cell wall-associated virulence factor. Infect Immun 69: 5589-5596.
77. Zhu, X., Gibbons, J., Zhang, S., and Williamson, P.R. (2003) Copper-mediated reversal of defective laccase in a Δvph1 avirulent mutant of Cryptococcus neoformans. Mol Microbiol 47: 1007-1014.