Immune Modulation Mediated by Cryptococcal Laccase Promotes Pulmonary Growth and Brain Dissemination of Virulent Cryptococcus neoformans in Mice

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Qiu, Yafeng ^a,b   Davis, Michael J ^a,b   Dayrit, Jeremy K ^a,b   Hadd, Zachary ^b   Meister, Daniel L ^b   Osterholzer, John J ^a,b   Williamson, Peter R ^c,d   Olszewski, Michal A ^a,b  

^a Ann Arbor Veterans Administration Health System   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; LACCASE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DISSEMINATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; ENZYME ACTIVITY; EOSINOPHILIA; FEMALE; FUNGAL GENE; FUNGAL PHENOMENA AND FUNCTIONS; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE DELETION; IMMUNE RESPONSE; IMMUNOMODULATION; LAC1 GENE; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PULMONARY CRYPTOCOCCOSIS; PULMONARY GROWTH; TH1 CELL; TH17 CELL; TH2 CELL;

ADOPTIVE TRANSFER; ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; CYTOKINES; EOSINOPHILS; FLOW CYTOMETRY; GENE DELETION; IMMUNOMODULATION; LACCASE; LUNG; MICE; REAL-TIME POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY; VIRULENCE; VIRULENCE FACTORS;

EID: 84867723777     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047853     Document Type: Article

References (45)

1. Chuck SL, Sande MA, (1989) Infections with Cryptococcus neoformans in the acquired immunodeficiency syndrome. N Engl J Med 321: 794-799.
2. Pappas PG, Perfect JR, Cloud GA, Larsen RA, Pankey GA, et al. (2001) Cryptococcosis in human immunodeficiency virus-negative patients in the era of effective azole therapy. Clin Infect Dis 33: 690-699.
3. Jarvis JN, Harrison TS, (2007) HIV-associated cryptococcal meningitis. AIDS 21: 2119-2129.
4. Buchanan KL, Doyle HA, (2000) Requirement for CD4 (+) T lymphocytes in host resistance against Cryptococcus neoformans in the central nervous system of immunized mice. Infect Immun 68: 456-462.
5. Huffnagle GB, Lipscomb MF, Lovchik JA, Hoag KA, Street NE, (1994) The role of CD4+ and CD8+ T cells in the protective inflammatory response to a pulmonary cryptococcal infection. J Leukoc Biol 55: 35-42.
6. Huffnagle GB, Yates JL, Lipscomb MF, (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.
7. Huffnagle GB, Yates JL, Lipscomb MF, (1991) Immunity to a pulmonary Cryptococcus neoformans infection requires both CD4+ and CD8+ T cells. J Exp Med 173: 793-800.
8. Kawakami K, Tohyama M, Teruya K, Kudeken N, Xie Q, et al. (1996) Contribution of interferon-gamma in protecting mice during pulmonary and disseminated infection with Cryptococcus neoformans. FEMS Immunol Med Microbiol 13: 123-130.
9. Mody CH, Chen GH, Jackson C, Curtis JL, Toews GB, (1993) Depletion of murine CD8+ T cells in vivo decreases pulmonary clearance of a moderately virulent strain of Cryptococcus neoformans. J Lab Clin Med 121: 765-773.
10. Wormley FL Jr, Perfect JR, Steele C, Cox GM, (2007) Protection against cryptococcosis by using a murine gamma interferon-producing Cryptococcus neoformans strain. Infect Immun 75: 1453-1462.
11. Chen GH, McNamara DA, Hernandez Y, Huffnagle GB, Toews GB, et al. (2008) Inheritance of immune polarization patterns is linked to resistance versus susceptibility to Cryptococcus neoformans in a mouse model. Infect Immun 76: 2379-2391.
12. Jain AV, Zhang Y, Fields WB, McNamara DA, Choe MY, et al. (2009) Th2 but not Th1 immune bias results in altered lung functions in a murine model of pulmonary Cryptococcus neoformans infection. Infect Immun 77: 5389-5399.
13. Traynor TR, Kuziel WA, Toews GB, Huffnagle GB, (2000) CCR2 expression determines T1 versus T2 polarization during pulmonary Cryptococcus neoformans infection. J Immunol 164: 2021-2027.
14. Kleinschek MA, Muller U, Brodie SJ, Stenzel W, Kohler G, et al. (2006) IL-23 enhances the inflammatory cell response in Cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12. J Immunol 176: 1098-1106.
15. Muller U, Stenzel W, Kohler G, Werner C, Polte T, et al. (2007) IL-13 induces disease-promoting type 2 cytokines, alternatively activated macrophages and allergic inflammation during pulmonary infection of mice with Cryptococcus neoformans. J Immunol 179: 5367-5377.
16. Zhang Y, Wang F, Tompkins KC, McNamara A, Jain AV, et al. (2009) Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99. Am J Pathol 175: 2489-2500.
17. Wozniak KL, Hardison SE, Kolls JK, Wormley FL, (2011) Role of IL-17A on resolution of pulmonary C. neoformans infection. PLoS One 6: e17204.
18. Blackstock R, Murphy JW, (2004) Role of interleukin-4 in resistance to Cryptococcus neoformans infection. Am J Respir Cell Mol Biol 30: 109-117.
19. Kawakami K, Hossain Qureshi M, Zhang T, Koguchi Y, Xie Q, et al. (1999) Interleukin-4 weakens host resistance to pulmonary and disseminated cryptococcal infection caused by combined treatment with interferon-gamma-inducing cytokines. Cell Immunol 197: 55-61.
20. Olszewski MA, Zhang Y, Huffnagle GB, (2010) Mechanisms of cryptococcal virulence and persistence. Future Microbiol 5: 1269-1288.
21. Alanio A, Desnos-Ollivier M, Dromer F (2011) Dynamics of Cryptococcus neoformans-macrophage interactions reveal that fungal background influences outcome during cryptococcal meningoencephalitis in humans. MBio 2.
22. Blackstock R, Buchanan KL, Cherniak R, Mitchell TG, Wong B, et al. (1999) Pathogenesis of Cryptococcus neoformans is associated with quantitative differences in multiple virulence factors. Mycopathologia 147: 1-11.
23. Kronstad JW, Attarian R, Cadieux B, Choi J, D'Souza CA, et al. (2011) Expanding fungal pathogenesis: Cryptococcus breaks out of the opportunistic box. Nat Rev Microbiol 9: 193-203.
24. Panepinto JC, Williamson PR, (2006) Intersection of fungal fitness and virulence in Cryptococcus neoformans. FEMS Yeast Res 6: 489-498.
25. Pukkila-Worley R, Gerrald QD, Kraus PR, Boily MJ, Davis MJ, et al. (2005) Transcriptional network of multiple capsule and melanin genes governed by the Cryptococcus neoformans cyclic AMP cascade. Eukaryot Cell 4: 190-201.
26. Salas SD, Bennett JE, Kwon-Chung KJ, Perfect JR, Williamson PR, (1996) Effect of the laccase gene CNLAC1, on virulence of Cryptococcus neoformans. J Exp Med 184: 377-386.
27. Liu L, Tewari RP, Williamson PR, (1999) Laccase protects Cryptococcus neoformans from antifungal activity of alveolar macrophages. Infect Immun 67: 6034-6039.
28. Eisenman HC, Mues M, Weber SE, Frases S, Chaskes S, et al. (2007) Cryptococcus neoformans laccase catalyses melanin synthesis from both D- and L-DOPA. Microbiology 153: 3954-3962.
29. Erb-Downward JR, Noggle RM, Williamson PR, Huffnagle GB, (2008) The role of laccase in prostaglandin production by Cryptococcus neoformans. Mol Microbiol 68: 1428-1437.
30. Noverr MC, Williamson PR, Fajardo RS, Huffnagle GB, (2004) CnLAC1 is required for extrapulmonary dissemination of Cryptococcus neoformans but not pulmonary persistence. Infect Immun 72: 1693-1699.
31. Valdez PA, Vithayathil PJ, Janelsins BM, Shaffer AL, Williamson PR, et al. (2012) Prostaglandin e2 suppresses antifungal immunity by inhibiting interferon regulatory factor 4 function and interleukin-17 expression in T cells. Immunity 36: 668-679.
32. Shreiner AB, Murdock BJ, Sadighi Akha AA, Falkowski NR, Christensen PJ, et al. (2012) Repeated exposure to Aspergillus fumigatus conidia results in CD4+ T cell-dependent and-independent pulmonary arterial remodeling in a mixed Th1/Th2/Th17 microenvironment that requires interleukin-4 (IL-4) and IL-10. Infect Immun 80: 388-397.
33. Classen A, Lloberas J, Celada A, (2009) Macrophage activation: classical versus alternative. Methods Mol Biol 531: 29-43.
34. Gordon S, Martinez FO, (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32: 593-604.
35. Arora S, Hernandez Y, Erb-Downward JR, McDonald RA, Toews GB, et al. (2005) Role of IFN-gamma in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis. J Immunol 174: 6346-6356.
36. Arora S, Olszewski MA, Tsang TM, McDonald RA, Toews GB, et al. (2011) Effect of cytokine interplay on macrophage polarization during chronic pulmonary infection with Cryptococcus neoformans. Infect Immun 79: 1915-1926.
37. Hardison SE, Ravi S, Wozniak KL, Young ML, Olszewski MA, et al. (2010) Pulmonary infection with an interferon-gamma-producing Cryptococcus neoformans strain results in classical macrophage activation and protection. Am J Pathol 176: 774-785.
38. Erb-Downward JR, Huffnagle GB, (2007) Cryptococcus neoformans produces authentic prostaglandin E2 without a cyclooxygenase. Eukaryot Cell 6: 346-350.
39. Noverr MC, Cox GM, Perfect JR, Huffnagle GB, (2003) Role of PLB1 in pulmonary inflammation and cryptococcal eicosanoid production. Infect Immun 71: 1538-1547.
40. Osterholzer JJ, Surana R, Milam JE, Montano GT, Chen GH, et al. (2009) Cryptococcal urease promotes the accumulation of immature dendritic cells and a non-protective T2 immune response within the lung. Am J Pathol 174: 932-943.
41. Hofford JM, Milakofsky L, Pell S, Vogel W, (1996) A profile of amino acid and catecholamine levels during endotoxin-induced acute lung injury in sheep: searching for potential markers of the acute respiratory distress syndrome. J Lab Clin Med 128: 545-551.
42. Huffnagle GB, Chen GH, Curtis JL, McDonald RA, Strieter RM, et al. (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.
43. Huffnagle GB, Toews GB, Burdick MD, Boyd MB, McAllister KS, et al. (1996) Afferent phase production of TNF-alpha is required for the development of protective T cell immunity to Cryptococcus neoformans. J Immunol 157: 4529-4536.
44. Olszewski MA, Huffnagle GB, McDonald RA, Lindell DM, Moore BB, et al. (2000) The role of macrophage inflammatory protein-1 alpha/CCL3 in regulation of T cell-mediated immunity to Cryptococcus neoformans infection. J Immunol 165: 6429-6436.
45. Olszewski MA, Huffnagle GB, Traynor TR, McDonald RA, Cook DN, et al. (2001) Regulatory effects of macrophage inflammatory protein 1alpha/CCL3 on the development of immunity to Cryptococcus neoformans depend on expression of early inflammatory cytokines. Infect Immun 69: 6256-6263.