Role of phospholipases in fungal fitness, pathogenicity, and drug development - lessons from Cryptococcus neoformans

Frontiers in Microbiology

Volumn 1, Issue NOV, 2010, Pages

  Djordjevic, Julianne Teresa ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cryptococcus neoformans; Drug development; Pathogenicity; Phosphatidylinositol specific phospholipase C; Phospholipase B; PI PLC Plc; Secretion; Signaling

Indexed keywords

EID: 84867710310     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2010.00125     Document Type: Article

References (110)

1. Aimanianda, V., Clavaud, C., Simenel, C., Fontaine, T., Delepierre, M., and Latge, J. P. (2009). Cell wall beta-(1,6)-glucan of Saccharomyces cerevisiae: structural characterization and in situ synthesis. J. Biol. Chem. 284, 13401-13412.
2. 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.
3. 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 Galpha protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryotic Cell 1, 75-84.
4. Alvarez, M., Burn, T., Luo, Y., Pirofski, L. A., and Casadevall, A. (2009). The outcome of Cryptococcus neoformans intracellular pathogenesis in human monocytes. BMC Microbiol. 9, 51.
5. Alvarez, M., and Casadevall, A. (2006). Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16, 2161-2165.
6. Alvarez, M., and Casadevall, A. (2007). Cell-to-cell spread and massive vacuole formation after Cryptococcus neoformans infection of murine macrophages. BMC Immunol. 8, 16.
7. Ansari, K., Martin, S., Farkasovsky, M., Ehbrecht, I. M., and Kuntzel, H. (1999). Phospholipase C binds to the receptor-like GPR1 protein and controls pseudohyphal differentiation in Saccharomyces cerevisiae. J. Biol. Chem. 274, 30052-30058.
8. Bagnat, M., Keranen, S., Shevchenko, A., and Simons, K. (2000). Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. U.S.A. 97, 3254-3259.
9. Bennett, D. E., McCreary, C. E., and Coleman, D. C. (1998). Genetic characterization of a phospholipase C gene from Candida albicans: presence of homologous sequences in Candida species other than Candida albicans. Microbiology 144 (Pt 1), 55-72.
10. Bubb, W. A., Wright, L. C., Cagney, M., Santangelo, R. T., Sorrell, T. C., and Kuchel, P. W. (1999). Heteronuclear NMR studies of metabolites produced by Cryptococcus neoformans in culture media: identification of possible virulence factors. Magn. Reson. Med. 42, 442-453.
11. Burrack, L. S., Harper, J. W., and Higgins, D. E. (2009). Perturbation of vacuolar maturation promotes listeriolysin O-independent vacuolar escape during Listeria monocytogenes infection of human cells. Cell. Microbiol. 11, 1382-1398.
12. Casadevall, A., Nosanchuk, J. D., Williamson, P., and Rodrigues, M. L. (2009). Vesicular transport across the fungal cell wall. Trends Microbiol. 17, 158-162.
13. Charlier, C., Nielsen, K., Daou, S., Brigitte, M., Chretien, F., and Dromer, F. (2009). Evidence of a role for monocytes in dissemination and brain invasion by Cryptococcus neoformans. Infect. Immun. 77, 120-127
14. Chau, T. T., Mai, N. H., Phu, N. H., Nghia, H. D., Chuong, L. V., Sinh, D. X., Duong, V. A., Diep, P. T., Campbell, J. I., Baker, S., Hien, T. T., Lalloo, D. G., Farrar, J. J., and Day, J. N. (2010). A prospective descriptive study of cryptococcal meningitis in HIV uninfected patients in Vietnam - high prevalence of Cryptococcus neoformans var grubii in the absence of underlying disease. BMC Infect. Dis. 10, 199.
15. Chayakulkeeree, M., Sorrell, T. C., Siafakas, A. R., Wilson, C. F., Pantarat, N., Gerik, K. J., Boadle, R., and Djordjevic, J. T. (2008). Role and mechanism of phosphatidylinositol-specific phospholipase C in survival and virulence of Cryptococcus neoformans. Mol. Microbiol. 69, 809-826.
16. Chen, S. C., Muller, M., Zhou, J. Z., Wright, L. C., and Sorrell, T. C. (1997a). Phospholipase activity in Cryptococcus neoformans: a new virulence factor? J. Infect. Dis. 175, 414-420.
17. Chen, S. C., Wright, L. C., Santangelo, R. T., Muller, M., Moran, V. R., Kuchel, P. W., and Sorrell, T. C. (1997b). Identification of extracellular phospholipase B, lysophospholipase, and acyltransferase produced by Cryptococcus neoformans. Infect. Immun. 65, 405-411.
18. Chen, S. C., Wright, L. C., Golding, J. C., and Sorrell, T. C. (2000). Purification and characterization of secretory phospholipase B, lysophospholipase and lysophospholipase/transacylase from a virulent strain of the pathogenic fungus Cryptococcus neoformans. Biochem. J. 347, 431-439.
19. Coe, J. G., Wilson, C. F., Sorrell, T. C., Latouche, N. G., and Wright, L. C. (2003). Cloning of CnLYSO1, a novel extracellular lysophospholipase of the pathogenic fungus Cryptococcus neoformans. Gene 316, 67-78.
20. Cox, G. M., McDade, H. C., Chen, S. C., Tucker, S. C., Gottfredsson, M., Wright, L. C., Sorrell, T. C., Leidich, S. D., Casadevall, A., Ghannoum, M. A., and Perfect, J. R. (2001). Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans. Mol. Microbiol. 39, 166-175.
21. de Almeida, M. L., and Heise, N. (1993). Proteins anchored via glycosylphosphatidylinositol and solubilizing phospholipases in Trypanosoma cruzi. Biol. Res. 26, 285-312.
22. Demczuk, A., Guha, N., Nguyen, P. H., Desai, P., Chang, J., Guzinska, K., Rollins, J., Ghosh, C. C., Goodwin, L., and Vancura, A. (2008). Saccharomyces cerevisiae phospholipase C regulates transcription of Msn2p-dependent stress-responsive genes. Eukaryotic Cell 7, 967-979.
23. Dessen, A. (2000). Structure and mechanism of human cytosolic phospholipase A(2). Biochim. Biophys. Acta 1488, 40-47.
24. Djordjevic, J. T., Del Poeta, M., Sorrell, T. C., Turner, K. M., and Wright, L. C. (2005). Secretion of cryptococcal phospholipase B1 (PLB1) is regulated by a glycosylphosphatidylinositol (GPI) anchor. Biochem. J. 389, 803-812.
25. Doering, T. L. (2009). How sweet it is! Cell wall biogenesis and polysaccharide capsule formation in Cryptococcus neoformans. Annu. Rev. Microbiol. 63, 223-247.
26. Farkas, V., Takeo, K., Macekova, D., Ohkusu, M., Yoshida, S., and Sipiczki, M. (2009). Secondary cell wall formation in Cryptococcus neoformans as a rescue mechanism against acidinduced autolysis. FEMS Yeast Res. 9, 311-320.
27. Feldmesser, M., Kress, Y., Novikoff, P., and Casadevall, A. (2000). Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect. Immun. 68, 4225-4237.
28. Flick, J. S., and Thorner, J. (1993). Genetic and biochemical characterization of a phosphatidylinositol-specific phospholipase C in Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 5861-5876.
29. Fox, D. S., Cox, G. M., and Heitman, J. (2003). Phospholipid-binding protein Cts1 controls septation and functions coordinately with calcineurin in Cryptococcus neoformans. Eukaryotic Cell 2, 1025-1035.
30. Fujii, T., Shimoi, H., and Iimura, Y. (1999). Structure of the glucan-binding sugar chain of Tip1p, a cell wall protein of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1427, 133-144.
31. Gagnon-Arsenault, I., Parise, L., Tremblay, J., and Bourbonnais, Y. (2008). Activation mechanism, functional role and shedding of glycosylphosphatidylinositol-anchored Yps1p at the Saccharomyces cerevisiae cell surface. Mol. Microbiol. 69, 982-993.
32. Ganendren, R., Carter, E., Sorrell, T., Widmer, F., and Wright, L. (2006). Phospholipase B activity enhances adhesion of Cryptococcus neoformans to a human lung epithelial cell line. Microbes Infect. 8, 1006-1015.
33. Ganendren, R., Widmer, F., Singhal, V., Wilson, C., Sorrell, T., and Wright, L. (2004). In vitro antifungal activities of inhibitors of phospholipases from the fungal pathogen Cryptococcus neoformans. Antimicrob. Agents Chemother. 48, 1561-1569.
34. Gerik, K. J., Bhimireddy, S. R., Ryerse, J. S., Specht, C. A., and Lodge, J. K. (2008). PKC1 is essential for protection against both oxidative and nitrosative stresses, cell integrity, and normal manifestation of virulence factors in the pathogenic fungus Cryptococcus neoformans. Eukaryotic Cell 7, 1685-1698.
35. Ghannoum, M. A. (2000). Potential role of phospholipases in virulence and fungal pathogenesis. Clin. Microbiol. Rev. 13, 122-143, table of contents
36. Gilbert, N. M., Donlin, M. J., Gerik, K. J., Specht, C. A., Djordjevic, J. T., Wilson, C. F., Sorrell, T. C., and Lodge, J. K. (2010). KRE genes are required for beta-1,6-glucan synthesis, maintenance of capsule architecture and cell wall protein anchoring in Cryptococcus neoformans. Mol. Microbiol. 76, 517-534.
37. Heinz, D. W., Essen, L. O., and Williams, R. L. (1998). Structural and mechanistic comparison of prokaryotic and eukaryotic phosphoinositide-specific phospholipases C. J. Mol. Biol. 275, 635-650.
38. Heung, L. J., Kaiser, A. E., Luberto, C., and Del Poeta, M. (2005). The role and mechanism of diacylglycerol-protein kinase C1 signaling in melanogenesis by Cryptococcus neoformans. J. Biol. Chem. 280, 28547-28555.
39. Himmelreich, U., Allen, C., Dowd, S., Malik, R., Shehan, B. P., Mountford, C., and Sorrell, T. C. (2003). Identification of metabolites of importance in the pathogenesis of pulmonary cryptococcoma using nuclear magnetic resonance spectroscopy. Microbes Infect. 5, 285-290.
40. Holmstrom, T. E., Mattsson, C. L., Wang, Y., Iakovleva, I., Petrovic, N., and Nedergaard, J. (2010). Nontransactivational, dual pathways for LPA-induced Erk1/2 activation in primary cultures of brown pre-adipocytes. Exp. Cell Res. 316, 2664-2675.
41. Hoover, C. I., Jantapour, M. J., Newport, G., Agabian, N., and Fisher, S. J. (1998). Cloning and regulated expression of the Candida albicans phospholipase B (PLB1) gene. FEMS Microbiol. Lett. 167, 163-169.
42. 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., and Williamson, P. R. (2008). PI3K signaling of autophagy is required for starvation tolerance and virulenceof Cryptococcus neoformans. J. Clin. Invest. 118, 1186-1197.
43. Hu, G., Steen, B. R., Lian, T., Sham, A. P., Tam, N., Tangen, K. L., and Kronstad, J. W. (2007). Transcriptional regulation by protein kinase A in Cryptococcus neoformans. PLoS Pathog. 3:e42. doi: 10.1371/journal.ppat.0030042.
44. Ibrahim, A. S., Mirbod, F., Filler, S. G., Banno, Y., Cole, G. T., Kitajima, Y., Edwards, J. E. Jr., Nozawa, Y., and Ghannoum, M. A. (1995). Evidence implicating phospholipase as a virulence factor of Candida albicans. Infect. Immun. 63, 1993-1998.
45. Insenser, M., Nombela, C., Molero, G., and Gil, C. (2006). Proteomic analysis of detergent-resistant membranes from Candida albicans. Proteomics 6 (Suppl. 1), S74-S81.
46. Jones, P. M., Turner, K. M., Djordjevic, J. T., Sorrell, T. C., Wright, L. C., and George, A. M. (2007). Role of conserved active site residues in catalysis by phospholipase B1 from Cryptococcus neoformans. Biochemistry 46, 10024-10032.
47. Kapteyn, J. C., Montijn, R. C., Dijkgraaf, G. J., and Klis, F. M. (1994). Identification of beta-1,6-glucosylated cell wall proteins in yeast and hyphal forms of Candida albicans. Eur. J. Cell Biol. 65, 402-407.
48. Kennedy, C. L., Lyras, D., Cheung, J. K., Hiscox, T. J., Emmins, J. J., and Rood, J. I. (2009). Cross-complementation of Clostridium perfringens PLC and Clostridium septicum alpha-toxin mutants reveals PLC is sufficient to mediate gas gangrene. Microbes Infect. 11, 413-418.
49. Kesson, A. M., Bellemore, M. C., O'Mara, T. J., Ellis, D. H., and Sorrell, T. C. (2009). Scedosporium prolificans osteomyelitis in an immunocompetent child treated with a novel agent, hexadecylphospocholine (miltefosine), in combination with terbinafine and voriconazole: a case report. Clin. Infect. Dis. 48, 1257-1261.
50. Kim, H. N., and Chung, H. S. (2008). Caveolin-1 inhibits membrane-type 1 matrix metalloproteinase activity. BMB Rep. 41, 858-862.
51. Kitagaki, H., Wu, H., Shimoi, H., and Ito, K. (2002). Two homologous genes, DCW1 (YKL046c) and DFG5, are essential for cell growth and encode glycosylphosphatidylinositol (GPI)-anchored membrane proteins required for cell wall biogenesis in Saccharomyces cerevisiae. Mol. Microbiol. 46, 1011-1022.
52. Knechtle, P., Goyard, S., Brachat, S., Ibrahim-Granet, O., and d'Enfert, C. (2005). Phosphatidylinositol-dependent phospholipases C Plc2 and Plc3 of Candida albicans are dispensable for morphogenesis and host-pathogen interaction. Res. Microbiol. 156, 822-829.
53. Kollar, R., Reinhold, B. B., Petrakova, E., Yeh, H. J., Ashwell, G., Drgonova, J., Kapteyn, J. C., Klis, F. M., and Cabib, E. (1997). Architecture of the yeast cell wall. Beta(1→6)-glucan interconnects mannoprotein, beta(1→3-glucan, and chitin. J. Biol. Chem. 272, 17762-17775.
54. Kozubowski, L., Lee, S. C., and Heitman, J. (2009). Signalling pathways in the pathogenesis of Cryptococcus. Cell. Microbiol. 11, 370-380.
55. 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.
56. Kristiansen, S., and Richter, E. A. (2002). GLUT4-containing vesicles are released from membranes by phospholipase D cleavage of a GPI anchor. Am. J. Physiol. Endocrinol. Metab. 283, E374-E382.
57. Kunze, D., Melzer, I., Bennett, D., Sanglard, D., MacCallum, D., Norskau, J., Coleman, D. C., Odds, F. C., Schafer, W., and Hube, B. (2005). Functional analysis of the phospholipase C gene CaPLC1 and two unusual phospholipase C genes, CaPLC2 and CaPLC3, of Candida albicans. Microbiology 151, 3381-3394.
58. Lee, K. S., Patton, J. L., Fido, M., Hines, L. K., Kohlwein, S. D., Paltauf, F., Henry, S. A., and Levin, D. E. (1994). The Saccharomyces cerevisiae PLB1 gene encodes a protein required for lysophospholipase and phospholipase B activity. J. Biol. Chem. 269, 19725-19730.
59. Leidich, S. D., Ibrahim, A. S., Fu, Y., Koul, A., Jessup, C., Vitullo, J., Fonzi, W., Mirbod, F., Nakashima, S., Nozawa, Y., and Ghannoum, M. A. (1998). Cloning and disruption of caPLB1, a phospholipase B gene involved in the pathogenicity of Candida albicans. J. Biol. Chem. 273, 26078-26086.
60. Levitz, S. M., Nong, S. H., Seetoo, K. F., Harrison, T. S., Speizer, R. A., and Simons, E. R. (1999). Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect. Immun. 67, 885-890.
61. Lu, C. F., Kurjan, J., and Lipke, P. N. (1994). A pathway for cell wall anchorage of Saccharomyces cerevisiae alpha-agglutinin. Mol. Cell. Biol. 14, 4825-4833.
62. Ma, H., Croudace, J. E., Lammas, D. A., and May, R. C. (2006). Expulsion of live pathogenic yeast by macrophages. Curr. Biol. 16, 2156-2160.
63. Ma, H., Croudace, J. E., Lammas, D. A., and May, R. C. (2007). Direct cell-tocell spread of a pathogenic yeast. BMC Immunol. 8, 15.
64. Macekova, D., Farkas, V., Kishida, E., and Takeo, K. (2006). Ecto-glycanases and metabolic stability of the capsule in Cryptococcus neoformans. J. Basic Microbiol. 46, 470-479.
65. Mao, Y., Zhang, Z., Gast, C., and Wong, B. (2008). C-terminal signals regulate targeting of glycosylphosphatidylinositol-anchored proteins to the cell wall or plasma membrane in Candida albicans. Eukaryotic Cell 7, 1906-1915.
66. Martinez, L. R., Garcia-Rivera, J., and Casadevall, A. (2001). Cryptococcus neoformans var. neoformans (serotype D) strains are more susceptible to heat than C. neoformans var. grubii (serotype A) strains. J. Clin. Microbiol. 39, 3365-3367.
67. Merkel, O., Fido, M., Mayr, J. A., Pruger, H., Raab, F., Zandonella, G., Kohlwein, S. D., and Paltauf, F. (1999). Characterization and function in vivo of two novel phospholipases B/lysophospholipases from Saccharomyces cerevisiae. J. Biol. Chem. 274, 28121-28127.
68. Mirbod, F., Banno, Y., Ghannoum, M. A., Ibrahim, A. S., Nakashima, S., Kitajima, Y., Cole, G. T., and Nozawa, Y. (1995). Purification and characterization of lysophospholipase-transacylase (h-LPTA) from a highly virulent strain of Candida albicans. Biochim. Biophys. Acta 1257, 181-188.
69. Mukherjee, P. K., Seshan, K. R., Leidich, S. D., Chandra, J., Cole, G. T., and Ghannoum, M. A. (2001). Reintroduction of the PLB1 gene into Candida albicans restores virulence in vivo. Microbiology 147, 2585-2597.
70. Muller, G., Gross, E., Wied, S., and Bandlow, W. (1996). Glucose-induced sequential processing of a glycosylphosphatidylinositol-anchored ectoprotein in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 442-456.
71. Muniz, M., and Riezman, H. (2000). Intracellular transport of GPIanchored proteins. EMBO J. 19, 10-15.
72. Noverr, M. C., Cox, G. M., Perfect, J. R., and Huffnagle, G. B. (2003). Role of PLB1 in pulmonary inflammation and cryptococcal eicosanoid production. Infect. Immun. 71, 1538-1547.
73. Noverr, M. C., Toews, G. B., and Huffnagle, G. B. (2002). Production of prostaglandins and leukotrienes by pathogenic fungi. Infect. Immun. 70, 400-402.
74. Obando, D., Pantarat, N., Handke, R., Koda, Y., Widmer, F., Djordjevic, J. T., Ellis, D. H., Sorrell, T. C., and Jolliffe, K. A. (2009). Synthesis, antifungal, haemolytic and cytotoxic activities of a series of bis(alkylpyridinium) alkanes. Bioorg. Med. Chem. 17, 6329-6339.
75. Obando, D., Widmer, F., Wright, L. C., Sorrell, T. C., and Jolliffe, K. A. (2007). Synthesis, antifungal and antimicrobial activity of alkylphospholipids. Bioorg. Med. Chem. 15, 5158-5165.
76. Oishi, H., Tsuda, S., Watanabe, Y., and Tamai, Y. (1996). Purification and some properties of phospholipase B from Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 60, 1087-1092.
77. Panepinto, J., Komperda, K., Frases, S., Park, Y. D., Djordjevic, J. T., Casadevall, A., and Williamson, P. R. (2009). Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol. Microbiol. 71, 1165-1176.
78. Park, B. J., Wannemuehler, K. A., Marston, B. J., Govender, N., Pappas, P. G., and Chiller, T. M. (2009). Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23, 525-530.
79. Parkin, E. T., Watt, N. T., Turner, A. J., and Hooper, N. M. (2004). Dual mechanisms for shedding of the cellular prion protein. J. Biol. Chem. 279, 11170-11178.
80. Payne, W. E., and Fitzgerald-Hayes, M. (1993). A mutation in PLC1, a candidate phosphoinositide-specific phospholipase C gene from Saccharomyces cerevisiae, causes aberrant mitotic chromosome segregation. Mol. Cell. Biol. 13, 4351-4364.
81. Pickard, R. T., Chiou, X. G., Strifler, B. A., DeFelippis, M. R., Hyslop, P. A., Tebbe, A. L., Yee, Y. K., Reynolds, L. J., Dennis, E. A., Kramer, R. M., and Sharp, J. D. (1996). Identification of essential residues for the catalytic function of 85-kDa cytosolic phospholipase A2. Probing the role of histidine, aspartic acid, cysteine, and arginine. J. Biol. Chem. 271, 19225-19231.
82. Poussin, M. A., and Goldfine, H. (2005). Involvement of Listeria monocytogenes phosphatidylinositol-specific phospholipase C and host protein kinase C in permeabilization of the macrophage phagosome. Infect. Immun. 73, 4410-4413.
83. Poussin, M. A., Leitges, M., and Goldfine, H. (2009). The ability of Listeria monocytogenes PI-PLC to facilitate escape from the macrophage phagosome is dependent on host PKCbeta. Microb. Pathog. 46, 1-5.
84. Price, M. F., Wilkinson, I. D., and Gentry, L. O. (1982). Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia 20, 7-14.
85. Rahman, M. S., Ammerman, N. C., Sears, K. T., Ceraul, S. M., and Azad, A. F. (2010). Functional characterization of a phospholipase A(2) homolog from Rickettsia typhi. J. Bacteriol. 192, 3294-3303.
86. Rodrigues, M. L., Nakayasu, E. S., Oliveira, D. L., Nimrichter, L., Nosanchuk, J. D., Almeida, I. C., and Casadevall, A. (2008). Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryotic Cell 7, 58-67.
87. Rodrigues, M. L., Nimrichter, L., Oliveira, D. L., Frases, S., Miranda, K., Zaragoza, O., Alvarez, M., Nakouzi, A., Feldmesser, M., and Casadevall, A. (2007). Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryotic Cell 6, 48-59.
88. Saito, K., Sugatani, J., and Okumura, T. (1991). Phospholipase B from Penicillium notatum. Meth. Enzymol. 197, 446-456.
89. Santangelo, R., Zoellner, H., Sorrell, T., Wilson, C., Donald, C., Djordjevic, J., Shounan, Y., and Wright, L. (2004). Role of extracellular phospholipases and mononuclear phagocytes in dissemination of cryptococcosis in a murine model. Infect. Immun. 72, 2229-2239.
90. Santangelo, R. T., Chen, S. C., Sorrell, T. C., and Wright, L. C. (2005). Detection of antibodies to phospholipase B in patients infected with Cryptococcus neoformans by enzyme-linked immunosorbent assay (ELISA). Med. Mycol. 43, 335-341.
91. Santangelo, R. T., Nouri-Sorkhabi, M. H., Sorrell, T. C., Cagney, M., Chen, S. C., Kuchel, P. W., and Wright, L. C. (1999). Biochemical and functional characterisation of secreted phospholipase activities from Cryptococcus neoformans in their naturally occurring state. J. Med. Microbiol. 48, 731-740.
92. Shen, D. K., Noodeh, A. D., Kazemi, A., Grillot, R., Robson, G., and Brugere, J. F. (2004). Characterisation and expression of phospholipases B from the opportunistic fungus Aspergillus fumigatus. FEMS Microbiol. Lett. 239, 87-93.
93. Siafakas, A. R., Sorrell, T. C., Wright, L. C., Wilson, C., Larsen, M., Boadle, R., Williamson, P. R., and Djordjevic, J. T. (2007). Cell wall-linked cryptococcal phospholipase B1 is a source of secreted enzyme and a determinant of cell wall integrity. J. Biol. Chem. 282, 37508-37514.
94. Siafakas, A. R., Wright, L. C., Sorrell, T. C., and Djordjevic, J. T. (2006). Lipid rafts in Cryptococcus neoformans concentrate the virulence determinants phospholipase B1 and Cu/Zn superoxide dismutase. Eukaryotic Cell 5, 488-498.
95. Silverman, D. J., Santucci, L. A., Meyers, N., and Sekeyova, Z. (1992). Penetration of host cells by Rickettsia rickettsii appears to be mediated by a phospholipase of rickettsial origin. Infect. Immun. 60, 2733-2740.
96. Sorrell, T. C., Wright, L. C., Malik, R., and Himmelreich, U. (2006). Application of proton nuclear magnetic resonance spectroscopy to the study of Cryptococcus and cryptococcosis. FEMS Yeast Res. 6, 558-566.
97. Stulnig, T. M., Berger, M., Sigmund, T., Stockinger, H., Horejsi, V., and Waldhausl, W. (1997). Signal transduction via glycosyl phosphatidylinositolanchored proteins in T cells is inhibited by lowering cellular cholesterol. J. Biol. Chem. 272, 19242-19247.
98. Sugiyama, Y., Nakashima, S., Mirbod, F., Kanoh, H., Kitajima, Y., Ghannoum, M. A., and Nozawa, Y. (1999). Molecular cloning of a second phospholipase B gene, caPLB2 from Candida albicans. Med. Mycol. 37, 61-67.
99. Sutterlin, C., Doering, T. L., Schimmoller, F., Schroder, S., and Riezman, H. (1997). Specific requirements for the ER to Golgi transport of GPIanchored proteins in yeast. J. Cell. Sci. 110 (Pt 21), 2703-2714.
100. Takahashi, M., Banno, Y., Shikano, Y., Mori, S., and Nozawa, Y. (1991). Purification and characterization of lysophospholipase-transacylase of pathogenic fungus Candida albicans. Biochim. Biophys. Acta 1082, 161-169.
101. Theiss, S., Ishdorj, G., Brenot, A., Kretschmar, M., Lan, C. Y., Nichterlein, T., Hacker, J., Nigam, S., Agabian, N., and Kohler, G. A. (2006). Inactivation of the phospholipase B gene PLB5 in wild-type Candida albicans reduces cell-associated phospholipase A2 activity and attenuates virulence. Int. J. Med. Microbiol. 296, 405-420.
102. Trofa, D., Gacser, A., and Nosanchuk, J. D. (2008). Candida parapsilosis, an emerging fungal pathogen. Clin. Microbiol. Rev. 21, 606-625.
103. Turner, K. M., Wright, L. C., Sorrell, T. C., and Djordjevic, J. T. (2006). N-linked glycosylation sites affect secretion of cryptococcal phospholipase B1, irrespective of glycosylphosphatidylinositol anchoring. Biochim. Biophys. Acta 1760, 1569-1579.
104. Wei, Z., Zenewicz, L. A., and Goldfine, H. (2005). Listeria monocytogenes phosphatidylinositol-specific phospholipase C has evolved for virulence by greatly reduced activity on GPI anchors. Proc. Natl. Acad. Sci. U.S.A. 102, 12927-12931.
105. Widmer, F., Wright, L. C., Obando, D., Handke, R., Ganendren, R., Ellis, D. H., and Sorrell, T. C. (2006). Hexadecylphosphocholine (miltefosine) has broad-spectrum fungicidal activity and is efficacious in a mouse model of cryptococcosis. Antimicrob. Agents Chemother. 50, 414-421.
106. Witt, W., Schweingruber, M. E., and Mertsching, A. (1984). Phospholipase B from the plasma membrane of Saccharomyces cerevisiae. Separation of two forms with different carbohydrate content. Biochim. Biophys. Acta 795, 108-116.
107. Wright, L. C., Payne, J., Santangelo, R. T., Simpanya, M. F., Chen, S. C., Widmer, F., and Sorrell, T. C. (2004). Cryptococcal phospholipases: a novel lysophospholipase discovered in the pathogenic fungus Cryptococcus gattii. Biochem. J. 384, 377-384.
108. Wright, L. C., Santangelo, R. M., Ganendren, R., Payne, J., Djordjevic, J. T., and Sorrell, T. C. (2007). Cryptococcal lipid metabolism: phospholipase B1 is implicated in transcellular metabolism of macrophage-derived lipids. Eukaryotic Cell 6, 37-47.
109. Yoko-o, T., Matsui, Y., Yagisawa, H., Nojima, H., Uno, I., and Toh-e, A. (1993). The putative phosphoinositide-specific phospholipase C gene, PLC1, of the yeast Saccharomyces cerevisiae is important for cell growth. Proc. Natl. Acad. Sci. U.S.A. 90, 1804-1808.
110. Yoneda, A., and Doering, T. L. (2006). A eukaryotic capsular polysaccharide is synthesized intracellularly and secreted via exocytosis. Mol. Biol. Cell 17, 5131-5140.