Cryptococcus neoformans modulates extracellular killing by neutrophils

Frontiers in Microbiology

Volumn 2, Issue SEP, 2011, Pages

  Qureshi, Asfia ^a   Grey, Angus ^b   Rose, Kristie L ^b   Schey, Kevin L ^b   Del Poeta, Maurizio ^a,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cryptococcus; Fungal infection; Immunodeficient mice; Neutrophils; Sphingolipid; Sphingomyelin

Indexed keywords

CANDIDA ALBICANS; FILOBASIDIELLA NEOFORMANS; MUS;

EID: 84875501666     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00193     Document Type: Article

References (63)

1. Alspaugh, J. A., Nichols, C. B., Xue, C., Shen,W. C.,andWang,P. (2011)."Gprotein signaling pathways: regulating morphogenesis and virulence of Cryptococcus," in Cryptococcus: From Human Pathogen to Model Yeast, eds J. Heitman, T. R. Kozel, K. J. Kwon-Chung, J. R. Perfect, and A. Casadevall (Washington, DC: ASM Press), 153-165.
2. Alvarez, M., and Casadevall, A. (2006). Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16, 2161-2165.
3. Bielawska, A., Szulc, Z., and Hannun, Y. A. (2000). Synthesis of key precursors of radiolabeled sphingolipids. Meth. Enzymol. 311, 518-535.
4. Bielawski, J., Pierce, J. S., Snider, J., Rembiesa, B., Szulc, Z. M., and Bielawska, A. (2009). Comprehensive quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods Mol. Biol. 579, 443-467.
5. Bielawski, J., Szulc, Z. M., Hannun,Y. A., and Bielawska,A. (2006). Simultane- ous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39, 82-91.
6. Bose, I., Reese, A. J., Ory, J. J., Janbon, G., and Doering, T. L. (2003). A yeast under cover: the capsule of Cryptococcus neoformans. Eukaryotic Cell 2, 655-663.
7. Bruns, S., Kniemeyer, O., Hasenberg, M., Aimanianda, V., Nietzsche, S., Thywissen, A., Jeron, A., Latge, J. P., Brakhage, A. A., and Gunzer, M. (2010). Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog. 6,e1000873. doi: 10.1371/journal.ppat.1000873
8. Diamond, R. D., Root, R. K., and Bennett, J. E. (1972). Factors influencing killing of Cryptococcus neoformans by human leukocytes in vitro. J. Infect. Dis. 125, 367-376.
9. Dickson, R. C., and Lester, R. L. (1999). Metabolism and selected functions of sphingolipids in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1438, 305-321.
10. Doering, T. L., Nosanchuk, J. D., Roberts, W. K., and Casadevall, A. (1999). Melanin as a potential cryptococcal defence against microbicidal proteins. Med. Mycol. 37, 175-181.
11. Eigenheer, R. A., Jin Lee, Y., Blumwald, E., Phinney, B. S., and Gelli, A. (2007). Extracellular glycosylphosphatidylinositol- anchored mannoproteins and proteases of Cryptococcus neoformans. FEMS Yeast Res. 7, 499-510.
12. Fan, W., Kraus, P. R., Boily, M. J., and Heitman, J. (2005). Cryptococ- cus neoformans gene expression during murine macrophage infection. Eukaryotic Cell 4, 1420-1433.
13. Feldmesser, M., Tucker, S., and Casadevall, A. (2001). Intracellular parasitism of macrophages by Cryptococcus neoformans. Trends Microbiol. 9, 273-278.
14. Fitzgerald, V., Blank, M. L., and Snyder, F. (1995). Molecular species of sphingomyelin in sphingomyelinase-sensitive and sphingomyelinase-resistant pools of HL-60 cells. Lipids 30, 805-809.
15. Fox, D. S., Djordjevic, J. T., and Sorrell, T. (2011). "Signaling cascades and enzymes as Cryptococcus virulence factors," in Cryptococcus: From Human Pathogen to Model Yeast,eds J. Heitman, T. R. Kozel, K. J. KwonChung, J. R. Perfect, and A. Casadevall (Washington, DC: ASM Press), 217-234.
16. Garcia, J., Shea, J., Alvarez-Vasquez, F., Qureshi, A., Luberto, C., Voit, E. O., and Del Poeta, M. (2008). Mathematical modeling of pathogenicity of Cryptococcus neoformans. Mol. Syst. Biol. 4, 183.
17. Goldman, D., Lee, S. C., and Casadevall, A. (1994). Pathogenesis of pulmonary Cryptococcus neoformans infection in the rat. Infect. Immun. 62, 4755-4761.
18. Heidler, S. A., and Radding, J. A. (2000). Inositol phosphoryl transferases from human pathogenic fungi. Biochim. Biophys. Acta 1500, 147-152.
19. Henry, J., Guillotte, A., Luberto, C., and Del Poeta, M. (2011). Characterization of inositol phospho- sphingolipid-phospholipase C 1 (Isc1) in Cryptococcus neoformans reveals unique biochemical features. FEBS Lett. 585, 635-640.
20. Heung, L. J., Kaiser, A. E., Luberto, C., and Del Poeta, M. (2005). The role and mechanism of diacylglycerolprotein kinase C1 signaling in melanogenesis by Cryptococcus neoformans. J. Biol. Chem. 280, 28547-28555.
21. Hill, J. O., and Harmsen, A. G. (1991). Intrapulmonary growth and dissemination of an avirulent strain of Cryptococcus neoformans in mice depleted of CD4+ or CD8+ T cells. J. Exp. Med. 173, 755-758.
22. Huffnagle, G. B., Yates, J. L., and Lipscomb, M. F. (1991). Immunity to a pulmonary Cryptococcus neoformans infection requires both CD4+ and CD8+ T cells. J. Exp. Med. 173, 793-800.
23. Huffnagle, G. B., Yates, J. L., and Lipscomb, M. F. (1991). T cell-mediated immunity in the lung: a Cryptococcus neoformans pulmonary infection model using SCID and athymic nude mice. Infect. Immun. 59, 1423-1433.
24. Idnurm, A., Bahn, Y. S., Shen, W. C., Rutherford, J. C., and Muhlschlegel, F. A. (2011). Sensing extracellular signals in Cryptococcus neoformans," in Cryptococcus: From Human Pathogen to Model Yeast, eds J. Heitman, T. R. Kozel, K. J. KwonChung, J. R. Perfect and A. Casadevall (Washington, DC: ASM Press), 175-187.
25. Jesus, M. D., Nicola, A. M., Chow, S. K., Lee, I. R., Nong, S., Specht, C. A., Levitz, S. M., and Casadevall, A. (2010). Glucuronoxylomannan, galactoxylomannan, and mannoprotein occupy spatially separate and discrete regions in the capsule of Cryptococcus neoformans. Virulence 1, 500-508.
26. Jin, J., Hou, Q., Mullen, T. D., Zeidan, Y. H., Bielawski, J., Kraveka, J. M., Bielawska, A., Obeid, L. M., Hannun, Y. A., and Hsu, Y. T. (2008). Ceramide generated by sphingomyelin hydrolysis and the salvage pathway is involved in hypoxia/reoxygenation-induced Bax redistribution to mitochondria in NT-2 cells. J. Biol. Chem. 283, 26509-26517.
27. Jin, Z. X., Huang, C. R., Dong, L., Goda, S., Kawanami, T., Sawaki, T., Sakai, T., Tong, X. P., Masaki, Y., Fukushima, T., Tanaka, M., Mimori, T.,Tojo,H.,Bloom,E. T.,Okazaki,T., and Umehara, H. (2008). Impaired TCR signaling through dysfunction of lipid rafts in sphingomyelin synthase 1 (SMS1)-knockdown T cells. Int. Immunol. 20, 1427-1437.
28. Kawakami, K. (2002). Role of natural killer T cells in host defense against cryptococcal infection. Rev Iberoam Micol 19, 149-154.
29. King, J. W., and Dewitt, M. L. (2010). Cryptococcosis. eMedicine. Available at http://emedicine.medscape.com/ article/215354 [accessed December 14, 2010; Online].
30. Kono, M., Dreier, J. L., Ellis, J. M., Allende, M. L., Kalkofen, D. N., Sanders, K. M., Bielawski, J., Bielawska, A., Hannun, Y. A., and Proia, R. L. (2006). Neutral ceramidase encoded by the Asah2 gene is essential for the intestinal degradation of sphingolipids. J. Biol. Chem. 281, 7324-7331.
31. Kovacs, J. A., Kovacs, A. A., Polis, M., Wright, W. C., Gill, V. J., Tuazon, C. U.,Gelmann,E. P.,Lane,H. C.,Longfield, R., Overturf, G., Macher, A. M., Fauci, A. S., Parrillo, J., Bennett, J. E., and Masur, H. (1985). Cryptococcosis in the acquired immunodeficiency syndrome. Ann. Intern. Med. 103, 533-538.
32. Kuroda, M., Hashida-Okado, T., Yasumoto, R., Gomi, K., Kato, I., and Takesako, K. (1999). An aureobasidin A resistance gene isolated from Aspergillus is a homolog of yeast AUR1, a gene responsible for inositol phosphorylceramide (IPC) synthase activity. Mol. Gen. Genet. 261, 290-296.
33. Li, S. S., and Mody, C. H. (2010). Cryptococcus. Proc. Am. Thorac. Soc. 7, 186-196.
34. Lim, T. S., and Murphy, J. W. (1980). Transfer of immunity to cryptococcosis by T-enriched splenic lymphocytes from Cryptococcus neoformans-sensitized mice. Infect. Immun. 30, 5-11.
35. Luberto, C., Martinez-Marino, B., Taraskiewicz, D., Bolanos, B., Chitano, P., Toffaletti, D. L., Cox, G. M., Perfect, J. R., Hannun, Y. A., Balish, E., and Del Poeta, M. (2003). Identification of App1 as a regulator of phagocytosis and virulence of Cryptococcus neoformans. J. Clin. Invest. 112, 1080-1094.
36. Luberto, C., Toffaletti, D. L., Wills, E. A., Tucker, S. C., Casadevall, A., Perfect, J. R., Hannun, Y. A., and Del Poeta, M. (2001). Roles for inositol-phosphoryl ceramide synthase 1 (IPC1) in pathogenesis of C. neoformans. Genes Dev. 15, 201-212.
37. 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.
38. Mambula, S. S., Simons, E. R., Hastey, R., Selsted, M. E., and Levitz, S. M. (2000). Human neutrophilmediated nonoxidative antifungal activity against Cryptococcus neoformans. Infect. Immun. 68, 6257-6264.
39. Merrill, A. H. Jr., Sullards, M. C., Allegood, J. C., Kelly, S., and Wang,E. (2005). Sphingolipidomics: high-throughput, structure-specific, and quantitative analysis of sphingolipids by liquid chromatography tandem mass spectrometry. Methods 36, 207-224.
40. Miller, M. F., and Mitchell, T. G. (1991). Killing of Cryptococcus neoformans strains by human neutrophils and monocytes. Infect. Immun. 59, 24-28.
41. Mullick, A., Elias, M., Harakidas, P., Marcil, A., Whiteway, M., Ge, B., Hudson, T. J., Caron, A. W., Bourget, L., Picard, S., Jovcevski, O., Massie,B.,and Thomas,D.Y. (2004). Gene expression in HL60 granulocytoids and human polymorphonuclear leukocytes exposed to Candida albicans. Infect. Immun. 72, 414-429.
42. Nielsen, K., and Kwon-Chung, K. J. (2011). "A role for mating in cryptococcal virulence," in Cryptococcus: From Human Pathogen to Model Yeast, eds J. Heitman, T. R. Kozel, K. J. Kwon-Chung, J. R. Perfect and A. Casadevall (Washington, DC: ASM Press), 167-174.
43. Nosanchuk, J. D., and Casadevall, A. (2003). The contribution of melanin to microbial pathogenesis. Cell. Microbiol. 5, 203-223.
44. Nosanchuk, J. D., and Casadevall, A. (2006). Impact of melanin on microbial virulence and clinical resistance to antimicrobial compounds. Antimicrob. Agents Chemother. 50, 3519-3528.
45. Pfaller, M. A., Lodge, J. K., and Ghannoum, M. A. (2011). "Drug resistance in Cryptococcus: epidemiology and molecular mechanisms," in Cryptococcus: From Human Pathogen to Model Yeast, eds J. Heitman, T. R. Kozel, K. J. Kwon-Chung, J. R. Perfect and A. Casadevall (Washington, DC: ASM Press), 203-216.
46. Qureshi, A., Subathra, M., Grey, A., Schey, K., Del Poeta, M., and Luberto, C. (2010). Role of sphingomyelin synthase in controlling the antimicrobial activity of neutrophils against Cryptococcus neoformans. PLoS ONE 5, e15587. doi: 10.1371/journal.pone.0015587
47. Rittershaus,P. C.,Kechichian,T. B.,Allegood, J. C., Merrill, A. H. Jr., Hennig, M., Luberto, C., and Del Poeta, M. (2006). Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J. Clin. Invest. 116, 1651-1659.
48. Schleimer, R. P., Freeland, H. S., Peters, S. P., Brown, K. E., and Derse, C. P. (1989). An assessment of the effects of glucocorticoids on degranulation, chemotaxis, binding to vascular endothelium and formation of leukotriene B4 by purified human neutrophils. J. Pharmacol. Exp. Ther. 250, 598-605.
49. Shao, X., Mednick, A., Alvarez, M., Van Rooijen, N., Casadevall, A., and Goldman, D. L. (2005). An innate immune system cell is a major determinant of species-related susceptibility differences to fungal pneumonia. J. Immunol. 175, 3244-3251.
50. Shea, J. M., Kechichian, T. B., Luberto, C., and Del Poeta, M. (2006). The cryptococcal enzyme inositol phosphosphingolipidphospholipase C confers resistance to the antifungal effects of macrophages and promotes fungal dissemination to the central nervous system. Infect. Immun. 74, 5977-5988.
51. Shimizu, Y., Dobashi, K., Iizuka, K., Horie, T., Suzuki, K., Tukagoshi, H., Nakazawa, T., Nakazato, Y., and Mori, M. (2001). Contribution of small GTPase Rho and its target protein rock in a murine model of lung fibrosis.Am. J. Respir. Crit. Care Med. 163, 210-217.
52. Smith, J. A. (1994). Neutrophils, host defense, and inflammation: a double-edged sword. J. Leukoc. Biol. 56, 672-686.
53. Spellberg, B. J., Collins, M., Avanesian, V., Gomez, M., Edwards, J. E. Jr., Cogle, C., Applebaum, D., Fu,Y., and Ibrahim, A. S. (2007). Optimization of a myeloid cell transfusion strategy for infected neutropenic hosts. J. Leukoc. Biol. 81, 632-641.
54. Spellberg, B. J., Collins, M., French, S. W., Edwards, J. E. Jr., Fu, Y., and Ibrahim, A. S. (2005). A phagocytic cell line markedly improves survival of infected neutropenic mice. J. Leukoc. Biol. 78, 338-344.
55. Stano, P., Williams, V., Villani, M., Cymbalyuk, E. S., Qureshi, A., Huang, Y., Morace, G., Luberto, C., Tomlinson, S., and Del Poeta, M. (2009). App1: an antiphagocytic protein that binds to complement receptors 3 and 2. J. Immunol. 182, 84-91.
56. Tommasino, N., Villani, M., Qureshi, A., Henry, J., Luberto, C., and Del Poeta, M. (2008). Atf2 transcription factor binds to the APP1 promoter in Cryptococcus neoformans: stimulatory effect of diacylglycerol. Eukaryotic Cell 7, 294-301.
57. Uezu, K., Kawakami, K., Miyagi, K., Kinjo, Y., Kinjo, T., Ishikawa, H., and Saito, A. (2004). Accumulation of gammadelta T cells in the lungs and their regulatory roles in Th1 response and host defense against pulmonary infection with Cryptococcus neoformans. J. Immunol. 172, 7629-7634.
58. Urban,C. F.,Lourido,S.,and Zychlinsky, A. (2006). How do microbes evade neutrophil killing? Cell. Microbiol. 8, 1687-1696.
59. Urban, C. F., Reichard, U., Brinkmann, V., and Zychlinsky, A. (2006). Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell. Microbiol. 8, 668-676.
60. Valsecchi, M., Mauri, L., Casellato, R., Prioni, S., Loberto, N., Prinetti, A., Chigorno, V., and Sonnino, S. (2007). Ceramide and sphingomyelin species of fibroblasts and neurons in culture. J. Lipid Res. 48, 417-424.
61. Venable, M. E., Lee, J. Y., Smyth, M. J., Bielawska, A., and Obeid, L. M. (1995). Role of ceramide incellular senescence. J. Biol. Chem. 270, 30701-30708.
62. Wang, B., Biron, C., She, J., Higgins, K., Sunshine,M. J.,Lacy,E.,Lonberg,N., and Terhorst, C. (1994). A block in both early T lymphocyte and natural killer cell development in transgenic mice with high-copy numbers of the human CD3E gene. Proc. Natl. Acad. Sci. U.S.A. 91, 9402-9406.
63. Wang, B., Simpson, S. J., Hollander, G. A., and Terhorst, C. (1997). Development and function of T lymphocytes and natural killer cells after bone marrow transplantation of severely immunodeficient mice. Immunol. Rev. 157, 53-60.