Drug target discovery through analysis of laccase regulatory networks of Cryptococccus neoformans

Current Enzyme Inhibition

Volumn 4, Issue 4, 2008, Pages 186-193

  Williamson, Peter R ^a,b   Shirong, Zhang ^a   Panepinto, John ^a   Gouwu, Hu ^a   Waterman, Scott R ^a   Yoon Dong, Park ^a   Soowan, Shin ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Biological markers; Clinical markers; Clinical outcome; Cryptococcus; Drug design; Fungus; Laccase; Regulation; Virulence

Indexed keywords

2 (2 DIFLUOROMETHYLBENZIMIDAZOL 1 YL) 4,6 DIMORPHOLINO 1,3,5 TRIAZINE; ANTIFUNGAL AGENT; COPPER; LACCASE; PHOSPHATIDYLINOSITOL; PHOSPHOLIPID; RAPAMYCIN; WORTMANNIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; AUTOPHAGY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DEVELOPING COUNTRY; DRUG MECHANISM; DRUG TARGETING; ENZYME ANALYSIS; FUNGAL VIRULENCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MENINGITIS; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DYNAMICS; NONHUMAN; NUTRIENT; POLYMERIZATION; PREDICTION; PREVALENCE; REVIEW; SIGNAL TRANSDUCTION; SURVIVAL;

FUNGI; MAMMALIA;

EID: 65649109002     PISSN: 15734080     EISSN: None     Source Type: Journal    
DOI: 10.2174/157340808786733640     Document Type: Review

References (73)

1. Bicanic, T.; Wood, R.; Bekker, L.G.; Darder, M.; Meintjes, G.; Harrison, T.S. Antiretroviral roll-out, antifungal roll-back: Access to treatment for cryptococcal meningitis. Lancet Infect. Dis., 2005, 5, 530-1.
2. McCarthy, K.M.; Morgan, J.; Wannemuehler, K.A.; Mirza, S.A.; Gould, S.M.; Mhlongo, N.; Moeng, P.; Maloba, B.R.; Crewe-Brown, H.H.; Brandt, M.E.; Hajjeh, R.A. Population-based surveillance for cryptococcosis in an antiretroviral-naive South African province with a high HIV seroprevalence. AIDS, 2006, 20, 2199-206.
3. Spitzer, E.D.; Spitzer, S.G.; Freundlich, L.F.; Casadevall, A. Persistence of initial infection in recurrent Cryptococccus neoformans meningitis. Lancet, 1993, 341, 595-6.
4. Bicanic, T.; Meintjes, G.; Wood, R.; Hayes, M.; Rebe, K.; Bekker, L.; Harrison, T. Fungal burden, early fungicidal activity, and outcome in cryptococcal meningitis in antiretroviral-naive or antiretroviral-experienced patients treated with amphotericin B or fluconazole. Clin. Infect. Dis., 2007, 45, 76-80.
5. Jean, S.S.; Fang, C.T.; Shau, W.Y.; Chen, Y.C.; Chang, S.C.; Hsueh, P.R.; Hung, C.C.; Luh, K.T. Cryptococcaemia: Clinical features and prognostic factors. QJM, 2002, 95, 511-8.
6. Vilchez, R.A.; Irish, W.; Lacomis, J.; Costello, P.; Fung, J.; Kusne, S. The clinical epidemiology of pulmonary cryptococcosis in non-AIDS patients at a tertiary care medical center. Medicine (Baltimore), 2001, 80, 308-12.
7. Pagano, L.; Caira, M.; Fianchi, L. Pulmonary fungal infection with yeasts and pneumocystis in patients with hematological malignancy. Ann. Med., 2005, 37, 259-69.
8. Pagano, L.; Caira, M.; Falcucci, P.; Fianchi, L. Fungal CNS infections in patients with hematologic malignancy. Expert Rev. Anti Infect. Ther., 2005, 3, 775-85.
9. Jenny-Avital, E.; Abadi, M. Immune reconstitution cryptococcosis after initiation of successful highly active antiretroviral therapy. Clin. Infect. Dis., 2002, 35, e128-33.
10. Singh, N.; Lortholary, O.; Alexander, B.; Gupta, K.; John, G.; Pursell, K.; Munoz, P.; Klintmalm, G.; Stosor, V.; Del Busto, R.; Limaye, A.; Somani, J.; Lyon, M.; Houston, S.; House, A.; Pruett, T.; Orloff, S.; Humar, A.; Dowdy, L.; Garcia-Diaz, J.; Kalil, A.; Fisher, R.; Husain, S. An immune reconstitution syndrome-like illness associated with Cryptococccus neoformans infection in organ transplant recipients. Clin. Infect. Dis., 2005, 40, 1756-61.
11. Stephen, C.; Lester, S.; Black, W.; Fyfe, M.; Raverty, S. Multispecies outbreak of cryptococcosis on southern Vancouver Island, British Columbia. Can. Vet. J., 2002, 43, 792-4.
12. Staib, F. Cryptococccus neoformans and Guizotia abyssinica (syn. G. oleifera D.C.) (farbreadktion fur C. neoformans). Z. Hyg., 1962, 148, 466-475.
13. Chasakes, S.; Tyndall, R.L. Pigment production by Cryptococccus neoformans from para- and ortho-di-phenols: Effect of the nitrogen source. J. Clin. Microbiol., 1975, 1, 509-514.
14. Williamson, P.R. Biochemical and molecular characterization of the diphenol oxidase of Cryptococccus neoformans: Identification as a laccase. J. Bacteriol., 1994, 176, 656-64.
15. Liu, L.; Wakamatsu, K.; Ito, S.; Williamson, P.R. Catecholamine oxidative products, but not melanin, are produced by Cryptococccus neoformans during neuropathogenesis in mice. Infect. Immun., 1999, 67, 108-12.
16. Zhong, J.; Frases, S.; Wang, H.; Casadevall, A.; Stark, R.E. Following Fungal Melanin Biosynthesis with Solid-State NMR: Biopolymer Molecular Structures and Possible Connections to Cell-Wall Polysaccharides. Biochemistry, 2008, 47, 4701-10.
17. Plonka, P.M.; Grabacka, M. Melanin synthesis in microorganisms - biotechnological and medical aspects. Acta Biochim. Pol., 2006, 53, 429-43.
18. Hadesman, R.; Wiesner, R.; Go, V.; Tyce, G. Concentrations of 3,4-dighydroxyphenylalanine and catecholamines and metabolites in brain in an anhepatic model of hepatic encephalopathy. J. Neurochem., 1995, 65, 1166-75.
19. Nosanchuk, J.D.; Rosas, A.L.; Lee, S.C.; Casadevall, A. Melanisation of Cryptococccus neoformans in human brain tissue. Lancet, 2000, 355, 2049-50.
20. Nosanchuk, J.D.; Valadon, P.; Feldmesser, M.; Casadevall, A. Melanization of Cryptococccus neoformans in murine infection. Mol. Cell Biol., 1999, 19, 745-50.
21. Kwon-Chung, K.J.; Polacheck, I.; Popkin, T.J. Melanin-lacking mutants of Cryptococccus neoformans and their virulence for mice. J. Bacteriol., 1982, 150, 1414-21.
22. Kwon-Chung, K.J.; Rhodes, J.C. Encapsulation and melanin formation as indicators of virulence in Cryptococccus neoformans. Infect. Immun., 1986, 51, 218-23.
23. Rhodes, J.C.; Polacheck, I.; Kwon-Chung, K.J. Phenoloxidase activity and virulence in isogenic strains of Cryptococccus neoformans. Infect. Immun., 1982, 36, 1175-84.
24. Salas, S.D.; Bennett, J.E.; Kwon-Chung, K.J.; Perfect, J.R.; Williamson, P.R. Effect of the laccase gene CNLAC1, on virulence of Cryptococccus neoformans. J. Exp. Med., 1996, 184, 377-86.
25. Missall, T.; Moran, J.; Corbett, J.; Lodge, J. Distinct stress responses of two functional laccases in Cryptococccus neoformans are revealed in the absence of the thiol-specific antioxidant, Tsa1. Eukaryot. Cell, 2004, 4, 202-8.
26. Zhu, X.; Williamson, P. Role of laccase in the biology and virulence of Cryptococccus neoformans. FEMS Yeast Res., 2004, 5, 1-10.
27. Huffnagle, G.B.; Chen, G.H.; Curtis, J.L.; McDonald, R.A.; Strieter, R.M.; Toews, G.B. Down-regulation of the afferent phase of T cell-mediated pulmonary inflammation and immunity by a high melanin-producing strain of Cryptococccus neoformans. J. Immunol., 1995, 155, 3507-16.
28. Wang, Y.; Casadevall, A. Susceptibility of melanized and non-melanized Cryptococccus neoformans to nitrogen- and oxygen-derived oxidants. Infect. Immun., 1994, 62, 3004-7.
29. 2+, and relevance to Parkinson disease. J. Biol. Chem., 2005, 280, 15587-94.
30. Liu, L.; Tewari, R.P.; Williamson, P.R. Laccase protects Cryptococccus neoformans from antifungal activity of alveolar macrophages. Infect. Immun., 1999, 67, 6034-9.
31. van der Poll, T.; Opal, S.M. Host-pathogen interactions in sepsis. Lancet Infect. Dis., 2008, 8, 32-43.
32. Torres-Guererro, H.; Edman, J.C. Melanin-deficient mutants of Cryptococccus neoformans. J. Med. Vet. Mycol., 1994, 32, 303-13.
33. Erickson, T.; Liu, L.; Gueyikian, A.; Zhu, X.; Gibbons, J.; Williamson, P. Multiple virulence factors of Cryptococccus neoformans are dependent on VPH1. Mol. Microbiol., 2001, 42, 1121-31.
34. Nelson, R.T.; Hua, J.; Pryor, B.; Lodge, J.K. Identification of virulence mutants of the fungal pathogen Cryptococccus neoformans using signature-tagged mutagenesis. Genetics, 2001, 157, 935-47.
35. Alspaugh, J.A.; Pukilla-Worley, R.; Harashima, T.; Cavallo, L.; Funnel, D.; Cox, G.; Perfect, J.; Kronstad, J.; Heitman, J. Adenylylcyclase functions downstream of the G-alpha protein GPA1 and controls mating and pathogenicity. Eukaryot. Cell, 2002, 1, 75-84.
36. Odom, A.; Muir, S.; Lim, E.; Toffaletti, D.L.; Perfect, J.; Heitman, J. Calcineurin is required for virulence of Cryptococccus neoformans. EMBO J., 1997, 16, 2576-89.
37. Zhang, S.; Hacham, M.; Panepinto, J.; Hu, G.; Shin, S.; Zhu, X.; Williamson, P. The Hsp70 member, Ssa1 acts as a DNA-binding transcriptional co-activator in Cryptococccus neoformans. Mol. Microbol., 2006, 62, 1090-101.
38. Waterman, S.; Hacham, M.; Hu, G.; Zhu, X.; Park, Y.; Shin, S.; Panepinto, J.; Valyi-Nagy, T.; Beam, C.; Husain, S.; Singh, N.; Williamson, P. Role of a CUF1-CTR4 copper regulatory axis in the virulence of Cryptococccus neoformans. J. Clin. Invest., 2007, 117, 794-802.
39. Rex, J.; Pfaller, M.; Barry, A.; Nelson, P.; Webb, C. Antifungal susceptibility testing of isolates from a randomized, multicenter trial of fluconazole vs. amphotericin B as treatment of non-neutropenic patients with candidemia. NIAID Mycoses Study Group and the Candidemia Study Group. Antimicrob. Agents Chemother., 1995, 39, 40-4.
40. Aller, A.I.; Martin-Mazuelos, E.; Lozano, F.; Gomez-Mateos, J.; Steele-Moore, L.; Holloway, W.J.; Gutierrez, M.J.; Recio, F.J.; Espinel-Ingroff, A. Correlation of fluconazole MICs with clinical outcome in cryptococcal infection. Antimicrob. Agents Chemother., 2000, 44, 1544-8.
41. Zerhouni, E. Translational and clinical science - time for a new vision. N. Engl. J. Med., 2005, 353, 1621-23.
42. Waterman, S.R.; Williamson, P.R. Pathogen diversity and adaptation to the host: Applications to clinical genomics. Future Microbiol., 2007, 2, 215-8.
43. Zhu, X.; Williamson, P. A CLC-type chloride channel gene is required for laccase activity and virulence in Cryptococccus neoformans. Mol. Microbiol., 2003, 50, 1271-81.
44. Bolanos, B.; Mitchell, T.G. Phagocytosis of Cryptococccus neoformans by rat alveolar macrophages. J. Med. Vet. Mycol., 1989, 27, 203-17.
45. Panepinto, J.; Liu, L.; Ramos, J.; Zhu, X.; Valyi-Nagy, T.; Eksi, S.; Fu, J.; Jaffe, H.; Wickes, B.; Williamson, P. The DEAD-box RNA helicase Vad1 regulates multiple virulence-associated genes in Cryptococccus neoformans. J. Clin. Invest., 2005, 115, 632-641.
46. Panepinto, J.C.; Komperda, K.W.; Hacham, M.; Shin, S.; Liu, X.; Williamson, P.R. Binding of serum mannan binding lectin to a cell integrity-defective Cryptococccus neoformans ccr4Delta mutant. Infect. Immun., 2007, 75, 4769-79.
47. Hu, G.; Hacham, M.; Waterman, S.R.; Panepinto, J.; Shin, S.; Liu, X.; Gibbons, J.; Valyi-Nagy, T.; Obara, K.; Jaffe, H.A.; Ohsumi, Y.; Williamson, P.R. PI3K signaling of autophagy is required for starvation tolerance and virulenceof Cryptococccus neoformans. J. Clin. Invest., 2008, 118, 1186-97.
48. Burda, P.; Padilla, S.; Sarkear, S.; Emr, S. Retromer function in endosome-to-Golgi retrograde transport is regulated by the yeast Vps35 PtdIns 3-kinase. J. Cell Sci., 2002, 115, 3889-900.
49. Kihara, A.; Noda, T.; Ishihara, N.; Ohsumi, Y. Two distinct vps34 phohatidylinositol 3-kinase complexes function in autophagy and carboxyeptidase Y sorting in Sacharomyces cerevisiae. J. Cell Biol., 2001, 152, 519-30.
50. Stack, J.; DeWald, D.; Takegawa, K.; Emr, S. Vesicle-mediated protein transport: Regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J. Cell Biol., 1995, 129, 321-34.
51. Klionsky, D. The molecular machinery of autophagy: Unanswered questions. J. Cell Sci., 2004, 118, 7-18.
52. Herman, P.; Emr, S. Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae. Mol. Cell Biol., 1990, 10, 6742-54.
53. Takegawa, K.; DeWald, D.; Emr, S. Schizosaccharormyces pombe Vps34p, a phosphatidylinositol-specific PI 3-kinase essential for normal cell growth and vacuole morphology. J. Cell Sci., 1995, 108, 3745-56.
54. Ma, L.; chen, Z.; Erdjument-Bromage, H.; Tempst, P.; Pandolfi, P. Phosphorylation and functional inactivation of TSC2 by Erk: Implications for tuberous sclerosis and cancer pathogenesis. Cell, 2005, 121, 179-193.
55. Fan, Q.W.; Cheng, C.K.; Nicolaides, T.P.; Hackett, C.S.; Knight, Z.A.; Shokat, K.M.; Weiss, W.A. A dual phosphoinositide-3-kinase alpha/mTOR inhibitor cooperates with blockade of epidermal growth factor receptor in PTEN-mutant glioma. Cancer Res., 2007, 67, 7960-5.
56. Pfaller, M.A.; Messer, S.A.; Boyken, L.; Rice, C.; Tendolkar, S.; Hollis, R.J.; Diekema, D.J. Evaluation of the NCCLS M44-P disk diffusion method for determining susceptibilities of 276 clinical isolates of Cryptococccus neoformans to fluconazole. J. Clin. Microbiol., 2004, 42, 380-3.
57. Maxwell, M.J.; Messer, S.A.; Hollis, R.J.; Diekema, D.J.; Pfaller, M.A. Evaluation of Etest method for determining voriconazole and amphotericin B MICs for 162 clinical isolates of Cryptococccus neoformans. J. Clin. Microbiol., 2003, 41, 97-9.
58. Bii, C.C.; Makimura, K.; Abe, S.; Taguchi, H.; Mugasia, O.M.; Revathi, G.; Wamae, N.C.; Kamiya, S. Antifungal drug susceptibility of Cryptococccus neoformans from clinical sources in Nairobi, Kenya. Mycoses, 2007, 50, 25-30.
59. Yaguchi, S.; Fukui, Y.; Koshimizu, I.; Yoshimi, H.; Matsuno, T.; Gouda, H.; Hirono, S.; Yamazaki, K.; Yamori, T. Antitumor activity of ZSTK474, a new phosphatidylinositol 3-kinase inhibitor. J. Natl. Cancer Inst., 2006, 98, 545-56.
60. Levine, B.; Yuan, J. Autophagy in cell death: An innocent convict? J. Clin. Invest., 2005, 115, 2679-88.
61. Abeliovich, H.; Dunn, W.; Kim, J.; Klionsky, D. Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J. Cell Biol., 2000, 151, 1025-33.
62. Fuchs, B.B.; Mylonakis, E. Using non-mammalian hosts to study fungal virulence and host defense. Curr. Opin. Microbiol., 2006, 9, 346-51.
63. Feldmesser, M.; Kress, Y.; Casadevall, A. Intracellular crystal formation as a mechanism of cytotoxicity in murine pulmonary Cryptococccus neoformans infection. Infect. Immun., 2001, 69, 2723-7.
64. Goldfine, H.; Wadsworth, S. Macrophage intracellular signaling induced by Listeria monocytogenes. Microbes Infect., 2002, 4, 1335-43.
65. Kusner, D. Mechanisms of mycobacterial persistence in tuberculosis. Clin. Immunol., 2005, 114, 239-47.
66. Woods, J. Knocking on the right door and making a comfortable home: Histoplasma capsulatum intracellular pathogenesis. Curr. Opin. Microbiol., 2003, 6, 327-31.
67. Veneault-Fourrey, C.; Barooah, M.; Egan, M.; Wakley, G.; Talbot, N. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science, 2006, 312, 580-3.
68. Besteiro, S.; Williams, R.A.; Morrison, L.S.; Coombs, G.H.; Mottram, J.C. Endosome sorting and autophagy are essential for differentiation and virulence of Leishmania major. J. Biol. Chem., 2006, 281, 11384-96.
69. Palmer, G.; Kelly, M.; Sturtevant, J. Autophagy in the pathogen Candida albicans. Microbiology, 2007, 153, 51-8.
70. Richie, D.L.; Fuller, K.K.; Fortwendel, J.; Miley, M.D.; McCarthy, J.W.; Feldmesser, M.; Rhodes, J.C.; Askew, D.S. Unexpected link between metal ion deficiency and autophagy in Aspergillus fumigatus. Eukaryot. Cell, 2007, 6, 2437-47.
71. Dromer, F.; Mathoulin, S.; Dupont, B.; Laporte, A. Epidemiology of cryptococcosis in France: A 9-year survey (1985-1993). French Cryptococcosis Study Group. Clin. Infect. Dis., 1996, 23, 82-90.
72. Birmingham, C.; Smith, A.; Bakowski, M.; Yoshimuori, T.; Brumell, J. Autophagy controls Salmonella infection in response to damage to the salmonella-containing vacuole. J. Biol. Chem., 2006, 281, 11374-11383.
73. Amer, A.; Swanson, M. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol., 2005, 7, 765-78.