Identification and characterization of Cryptococcus neoformans protein fractions that induce protective immune responses

Proteomics

Volumn 13, Issue 23-24, 2013, Pages 3429-3441

  Chaturvedi, Ashok K ^a   Weintraub, Susan T ^b   Lopez Ribot, Jose L ^a   Wormley, Floyd L ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^b University of Texas Health Science Center   (United States)

Author keywords

Cryptococcosis; Cryptococcus neoformans; Cytoplasmic proteins; Microbiology; Surface proteins; Vaccination

Indexed keywords

CELL MEMBRANE PROTEIN; CRYPTOCOCCUS NEOFORMANS PROTEIN; CYTOPLASM PROTEIN; FUNGAL PROTEIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; CARBOHYDRATE METABOLISM; CELLULAR IMMUNITY; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; CYTOKINE RESPONSE; DRUG EFFICACY; ELECTROSPRAY MASS SPECTROMETRY; FEMALE; FUNGUS IMMUNITY; IMMUNIZATION; IMMUNOBLOTTING; IMMUNOREACTIVITY; IMMUNOSTIMULATION; INFECTION PREVENTION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; PROTEOMICS; PULMONARY CRYPTOCOCCOSIS; SIGNAL TRANSDUCTION; STRESS; SURVIVAL TIME; TH1 CELL;

CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; CYTOPLASMIC PROTEINS; MICROBIOLOGY; SURFACE PROTEINS; VACCINATION;

ANIMALS; CELL FRACTIONATION; CELL WALL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; CYTOKINES; CYTOPLASM; FEMALE; FUNGAL PROTEINS; FUNGAL VACCINES; LUNG DISEASES, FUNGAL; MICE; MICE, INBRED BALB C; PROTEOME; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY; TH1 CELLS; VACCINATION;

EID: 84890304132     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201300213     Document Type: Article

References (70)

1. Chuck, S. L., Sande, M. A., Infections with Cryptococcus neoformans in the acquired immunodeficiency syndrome. N. Engl. J. Med. 1989, 321, 794-799.
2. Dismukes, W. E., Cryptococcal meningitis in patients with AIDS. J. Infect. Dis. 1988, 157, 624-628.
3. Eng, R. H., Bishburg, E., Smith, S. M., Kapila, R., Cryptococcal infections in patients with acquired immune deficiency syndrome. Am. J. Med. 1986, 81, 19-23.
4. Gal, A. A., Koss, M. N., Hawkins, J., Evans, S., Einstein, H., The pathology of pulmonary cryptococcal infections in the acquired immunodeficiency syndrome. Arch. Pathol. Lab. Med. 1986, 110, 502-507.
5. Kovacs, J. A., Kovacs, A. A., Polis, M., Wright, W. C. et al., Cryptococcosis in the acquired immunodeficiency syndrome. Ann. Intern. Med. 1985, 103, 533-538.
6. Diamond, R. D., Bennett, J. E., Prognostic factors in cryptococcal meningitis. A study in 111 cases. Ann. Intern. Med. 1974, 80, 176-181.
7. Duperval, R., Hermans, P. E., Brewer, N. S., Roberts, G. D., Cryptococcosis, with emphasis on the significance of isolation of Cryptococcus neoformans from the respiratory tract. Chest 1977, 72, 13-19.
8. Goldstein, E., Rambo, O. N., Cryptococcal infection following steroid therapy. Ann. Intern. Med. 1962, 56, 114-120.
9. Collins, V. P., Gellhorn, A., Trimble, J. R., The coincidence of cryptococcosis and disease of the reticulo-endothelial and lymphatic systems. Cancer 1951, 4, 883-889.
10. Gendel, B. R., Ende, M., Norman, S. L., Cryptococcosis; a review with special reference to apparent association with Hodgkin's disease. Am. J. Med. 1950, 9, 343-355.
11. Keye, J. D., Jr., Magee, W. E., Fungal diseases in a general hospital; a study of 88 patients. Am. J. Clin. Pathol. 1956, 26, 1235-1253.
12. Lewis, J. L., Rabinovich, S., The wide spectrum of cryptococcal infections. Am. J. Med. 1972, 53, 315-322.
13. Husain, S., Wagener, M. M., Singh, N., Cryptococcus neoformans infection in organ transplant recipients: variables influencing clinical characteristics and outcome. Emerg. Infect. Dis. 2001, 7, 375-381.
14. Park, B. J., Wannemuehler, K. A., Marston, B. J., Govender, N. et al., Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 2009, 23, 525-530.
15. Vibhagool, A., Sungkanuparph, S., Mootsikapun, P., Chetchotisakd, P. et al., Discontinuation of secondary prophylaxis for cryptococcal meningitis in human immunodeficiency virus-infected patients treated with highly active antiretroviral therapy: a prospective, multicenter, randomized study. Clin. Infect. Dis. 2003, 36, 1329-1331.
16. Bozzette, S. A., Larsen, R. A., Chiu, J., Leal, M. A. et al., A placebo-controlled trial of maintenance therapy with fluconazole after treatment of cryptococcal meningitis in the acquired immunodeficiency syndrome. California Collaborative Treatment Group. N. Engl. J. Med. 1991, 324, 580-584.
17. Aberg, Judith A., Price, Richard W., Heeren, Dorie M., Bredt, B., A pilot study of the discontinuation of antifungal therapy for disseminated cryptococcal disease in patients with acquired immunodeficiency syndrome, following immunologic response to antiretroviral therapy. J. Infect. Dis. 2002, 185, 1179-1182.
18. Dromer, F., Mathoulin-Pelissier, S., Fontanet, A., Ronin, O. et al., Epidemiology of HIV-associated cryptococcosis in France (1985-2001): comparison of the pre- and post-HAART eras. AIDS 2004, 18, 555-562.
19. Singh, N., Perfect, J. R., Immune reconstitution syndrome associated with opportunistic mycoses. Lancet Infect. Dis. 2007, 7, 395-401.
20. Aguirre, K., Havell, E. A., Gibson, G. W., Johnson, L. L., Role of tumor necrosis factor and gamma interferon in acquired resistance to Cryptococcus neoformans in the central nervous system of mice. Infect Immun. 1995, 63, 1725-1731.
21. Collins, H. L., Bancroft, G. J., Cytokine enhancement of complement-dependent phagocytosis by macrophages: synergy of tumor necrosis factor-alpha and granulocyte-macrophage colony-stimulating factor for phagocytosis of Cryptococcus neoformans. Eur. J. Immunol. 1992, 22, 1447-1454.
22. Flesch, I. E., Schwamberger, G., Kaufmann, S. H., Fungicidal activity of IFN-gamma-activated macrophages. Extracellular killing of Cryptococcus neoformans. J. Immunol. 1989, 142, 3219-3224.
23. Huffnagle, G. B., Lipscomb, M. F., Cells and cytokines in pulmonary cryptococcosis. Res. Immunol. 1998, 149, 387-396.
24. Levitz, S. M., Activation of human peripheral blood mononuclear cells by interleukin-2 and granulocyte-macrophage colony-stimulating factor to inhibit Cryptococcus neoformans. Infect. Immun. 1991, 59, 3393-3397.
25. Levitz, S. M., DiBenedetto, D. J., Differential stimulation of murine resident peritoneal cells by selectively opsonized encapsulated and acapsular Cryptococcus neoformans. Infect. Immun. 1988, 56, 2544-2551.
26. Mody, C. H., Tyler, C. L., Sitrin, R. G., Jackson, C., Toews, G. B., Interferon-gamma activates rat alveolar macrophages for anticryptococcal activity. Am. J. Respir. Cell. Mol. Biol. 1991, 5, 19-26.
27. McClelland, E. E., Nicola, A. M., Prados-Rosales, R., Casadevall, A., Ab binding alters gene expression in Cryptococcus neoformans and directly modulates fungal metabolism. J. Clin. Invest. 2010, 120, 1355-1361.
28. Brena, S., Cabezas-Olcoz, J., Moragues, M. D., Fernandez de Larrinoa, I. et al., Fungicidal monoclonal antibody C7 interferes with iron acquisition in Candida albicans. Antimicrob. Agents Chemother. 2011, 55, 3156-3163.
29. Casadevall, A., Pirofski, L. A., Antibody-mediated protection through cross-reactivity introduces a fungal heresy into immunological dogma. Infect. Immun. 2007, 75, 5074-5078.
30. Martinez, L. R., Casadevall, A., Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect. Immun. 2005, 73, 6350-6362.
31. Subramaniam, K. S., Datta, K., Quintero, E., Manix, C. et al., The absence of serum IgM enhances the susceptibility of mice to pulmonary challenge with Cryptococcus neoformans. J. Immunol. 2010, 184, 5755-5767.
32. Biondo, C., Messina, L., Bombaci, M., Mancuso, G. et al., Characterization of two novel cryptococcal mannoproteins recognized by immune sera. Infect. Immun. 2005, 73, 7348-7355.
33. Kakeya, H., Udono, H., Maesaki, S., Sasaki, E. et al., Heat shock protein 70 (hsp70) as a major target of the antibody response in patients with pulmonary cryptococcosis. Clin. Exp. Immunol. 1999, 115, 485-490.
34. Kakeya, H., Udono, H., Ikuno, N., Yamamoto, Y. et al., A 77-kilodalton protein of Cryptococcus neoformans, a member of the heat shock protein 70 family, is a major antigen detected in the sera of mice with pulmonary cryptococcosis. Infect. Immun. 1997, 65, 1653-1658.
35. Young, M., Macias, S., Thomas, D., Wormley, F. L., Jr., A proteomic-based approach for the identification of immunodominant Cryptococcus neoformans proteins. Proteomics 2009, 9, 2578-2588.
36. Wozniak, K. L., Hardison, S. E., Kolls, J. K., Wormley, F. L., Role of IL-17A on resolution of pulmonary C. neoformans infection. PLoS One 2011, 6, e17204.
37. Wormley, F. L., Jr., Perfect, J. R., Steele, C., Cox, G. M., Protection against cryptococcosis by using a murine gamma interferon-producing Cryptococcus neoformans strain. Infect. Immun. 2007, 75, 1453-1462.
38. Mitchell, T. G., Perfect, J. R., Cryptococcosis in the era of AIDS-100 years after the discovery of Cryptococcus neoformans. Clin. Microbiol. Rev. 1995, 8, 515-548.
39. Iseki, M., Anzo, M., Yamashita, N., Matsuo, N., Hyper-IgM immunodeficiency with disseminated cryptococcosis. Acta Paediatr. 1994, 83, 780-782.
40. Neto Rda, J., Guimaraes, M. C., Moya, M. J., Oliveira, F. R. et al., Hypogammaglobulinemia as risk factor for Cryptococcus neoformans infection: report of 2 cases. Rev. Soc. Bras. Med. Trop. 2000, 33, 603-608.
41. Antachopoulos, C., Walsh, T. J., Roilides, E., Fungal infections in primary immunodeficiencies. Eur. J. Pediatr. 2007, 166, 1099-1117.
42. Mukherjee, J., Feldmesser, M., Scharff, M. D., Casadevall, A., Monoclonal antibodies to Cryptococcus neoformans glucuronoxylomannan enhance fluconazole efficacy. Antimicrob. Agents Chemother. 1995, 39, 1398-1405.
43. Mukherjee, J., Zuckier, L. S., Scharff, M. D., Casadevall, A., Therapeutic efficacy of monoclonal antibodies to Cryptococcus neoformans glucuronoxylomannan alone and in combination with amphotericin B. Antimicrob. Agents Chemother. 1994, 38, 580-587.
44. Dromer, F., Charreire, J., Improved amphotericin B activity by a monoclonal anti-Cryptococcus neoformans antibody: study during murine cryptococcosis and mechanisms of action. J. Infect. Dis. 1991, 163, 1114-1120.
45. Feldmesser, M., Mukherjee, J., Casadevall, A., Combination of 5-flucytosine and capsule-binding monoclonal antibody in the treatment of murine Cryptococcus neoformans infections and in vitro. J. Antimicrob. Chemother. 1996, 37, 617-622.
46. Dromer, F., Charreire, J., Contrepois, A., Carbon, C., Yeni, P., Protection of mice against experimental cryptococcosis by anti-Cryptococcus neoformans monoclonal antibody. Infect. Immun. 1987, 55, 749-752.
47. Goldman, D. L., Lee, S. C., Casadevall, A., Tissue localization of Cryptococcus neoformans glucuronoxylomannan in the presence and absence of specific antibody. Infect. Immun. 1995, 63, 3448-3453.
48. Mukherjee, J., Scharff, M. D., Casadevall, A., Protective murine monoclonal antibodies to Cryptococcus neoformans. Infect. Immun. 1992, 60, 4534-4541.
49. Mukherjee, S., Lee, S., Mukherjee, J., Scharff, M. D., Casadevall, A., Monoclonal antibodies to Cryptococcus neoformans capsular polysaccharide modify the course of intravenous infection in mice. Infect. Immun. 1994, 62, 1079-1088.
50. Martinez, L. R., Christaki, E., Casadevall, A., Specific antibody to Cryptococcus neoformans glucurunoxylomannan antagonizes antifungal drug action against cryptococcal biofilms in vitro. J. Infect. Dis. 2006, 194, 261-266.
51. Martinez, L. R., Casadevall, A., Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect. Immun. 2005, 73, 6350-6362.
52. Casadevall, A., Pirofski, L. A., Antibody-mediated protection through cross-reactivity introduces a fungal heresy into immunological dogma. Infect. Immun. 2007, 75, 5074-5078.
53. Zhang, Y., Wang, F., Tompkins, K. C., McNamara, A. et al., Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99. Am. J. Pathol. 2009, 175, 2489-2500.
54. Muller, U., Stenzel, W., Kohler, G., Werner, C. et al., IL-13 induces disease-promoting type 2 cytokines, alternatively activated macrophages and allergic inflammation during pulmonary infection of mice with Cryptococcus neoformans. J. Immunol. 2007, 179, 5367-5377.
55. Hardison, S. E., Wozniak, K. L., Kolls, J. K., Wormley, F. L., Jr., Interleukin-17 is not required for classical macrophage activation in a pulmonary mouse model of Cryptococcus neoformans infection. Infect. Immun. 2010, 78, 5341-5351.
56. Wozniak, K. L., Ravi, S., Macias, S., Young, M. L. et al., Insights into the mechanisms of protective immunity against Cryptococcus neoformans infection using a mouse model of pulmonary cryptococcosis. PLoS One 2009, 4, e6854.
57. Chaffin, W. L., Lopez-Ribot, J. L., Casanova, M., Gozalbo, D., Martinez, J. P., Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol. Mol. Biol. Rev. 1998, 62, 130-180.
58. Martinez-Lopez, R., Nombela, C., Diez-Orejas, R., Monteoliva, L., Gil, C., Immunoproteomic analysis of the protective response obtained from vaccination with Candida albicans ecm33 cell wall mutant in mice. Proteomics 2008, 8, 2651-2664.
59. De Groot, P. W., Ram, A. F., Klis, F. M., Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet. Biol. 2005, 42, 657-675.
60. Robbins, N., Uppuluri, P., Nett, J., Rajendran, R. et al., Hsp90 governs dispersion and drug resistance of fungal biofilms. PLoS Pathog. 2011, 7, e1002257.
61. Cowen, L. E., Hsp90 orchestrates stress response signaling governing fungal drug resistance. PLoS Pathog. 2009, 5, e1000471.
62. Singh, S. D., Robbins, N., Zaas, A. K., Schell, W. A. et al., Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog. 2009, 5, e1000532.
63. Cowen, L. E., Lindquist, S., Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 2005, 309, 2185-2189.
64. Deepe, G. S., Jr., Gibbons, R. S., Cellular and molecular regulation of vaccination with heat shock protein 60 from Histoplasma capsulatum. Infect. Immun. 2002, 70, 3759-3767.
65. Gomez, F. J., Allendoerfer, R., Deepe, G. S., Jr., Vaccination with recombinant heat shock protein 60 from Histoplasma capsulatum protects mice against pulmonary histoplasmosis. Infect. Immun. 1995, 63, 2587-2595.
66. de Bastos Ascenco Soares, R., Gomez, F. J., de Almeida Soares, C. M., Deepe, G. S., Jr., Vaccination with heat shock protein 60 induces a protective immune response against experimental Paracoccidioides brasiliensis pulmonary infection. Infect. Immun. 2008, 76, 4214-4221.
67. Li, W., Hu, X., Zhang, X., Ge, Y. et al., Immunisation with the glycolytic enzyme enolase confers effective protection against Candida albicans infection in mice. Vaccine 2011, 29, 5526-5533.
68. Raska, M., Belakova, J., Horynova, M., Krupka, M. et al., Systemic and mucosal immunization with Candida albicans hsp90 elicits hsp90-specific humoral response in vaginal mucosa which is further enhanced during experimental vaginal candidiasis. Med. Mycol. 2008, 46, 411-420.
69. Li, K., Yu, J. J., Hung, C. Y., Lehmann, P. F., Cole, G. T., Recombinant urease and urease DNA of Coccidioides immitis elicit an immunoprotective response against coccidioidomycosis in mice. Infect. Immun. 2001, 69, 2878-2887.
70. Wozniak, K. L., Young, M. L., Wormley, F. L., Jr., Protective immunity against experimental pulmonary cryptococcosis in T cell-depleted mice. Clin. Vaccine Immunol. 2011, 18, 717-723.