Innate host defenses against Cryptococcus neoformans

다국어 초록 (Multilingual Abstract)

Cryptococcus neoformans, the predominant etiological agent of cryptococcosis, can cause life-threatening infections of the central nervous system in immunocompromised and immunocompetent individuals. Cryptococcal meningoencephalitis is the most common disseminated fungal infection in AIDS patients, and remains the third most common invasive fungal infection among organ transplant recipients. The administration of highly active antiretroviral therapy (HAART) has resulted in a decrease in the number of cases of AIDS-related cryptococcosis in developed countries, but in developing countries where HAART is not readily available, Cryptococcus is still a major concern. Therefore, there is an urgent need for the development of novel therapies and/or vaccines to combat cryptococcosis. Understanding the protective immune responses against Cryptococcus is critical for development of vaccines and immunotherapies to combat cryptococcosis.
Consequently, this review focuses on our current knowledge of protective immune responses to C. neoformans, with an emphasis on innate immune responses.

참고문헌 (Reference)

1 Szymczak, W. A., "X-linked immunodeficient mice exhibit enhanced susceptibility to Cryptococcus neoformans infection" 4 : e00265-13-, 2013

2 Walsh, T.J., "Treatment of fungal disease in the setting of neutropenia" 2013 : 423-427, 2013

3 van der Horst, C. M., "Treatment of cryptococcal meningitis associated with the acquired immunodeficiency syndrome" 337 : 15-21, 1997

4 Choi, K. H., "Treatment of asymptomatic pulmonary cryptococcosis in immunocompetent hosts with oral fluconazole" 43 : 380-385, 2011

5 Netea, M. G., "Trained immunity:a memory for innate host defense" 9 : 355-361, 2011

6 Tanaka, M., "Toll-like receptor 9-dependent activation of bone marrow-derived dendritic cells by URA5 DNA from Cryptococcus neoformans" 80 : 778-786, 2012

7 Huffnagle, G. B., "The role of CD4+ and CD8+ T-cells in the protective inflammatory response to a pulmonary cryptococcal infection" 55 : 35-42, 1994

8 Lupo, P., "The presence of capsule in Cryptococcus neoformans influences the gene expression profile in dendritic cells during interaction with the fungus" 76 : 1581-1589, 2008

9 Vecchiarelli, A., "The polysaccharide capsule of Cryptococcus neoformans interferes with human dendritic cell maturation and activation" 74 : 370-378, 2003

10 Oz, Y., "The effect of clinical characteristics on the performance of galactomannan and PCR for the diagnosis of invasive aspergillosis in febrile neutropenic patients" 59 : 86-92, 2015

11 Levitz, S.M., "The ecology of Cryptococcus neoformans and the epidemiology of cryptococcosis" 13 : 1163-1169, 1991

12 Kosmidis, C., "The clinical spectrum of pulmonary aspergillosis" 70 : 270-277, 2015

13 Zaragoza, O., "The capsule of the fungal pathogen Cryptococcus neoformans" 68 : 133-216, 2009

14 Subramaniam, K. S., "The absence of serum IgM enhances the susceptibility of mice to pulmonary challenge with Cryptococcus neoformans" 184 : 5755-5767, 2010

15 Li, S. S., "The NK receptor NKp30 mediates direct fungal recognition and killing and is diminished in NK cells from HIV-infected patients" 14 : 387-397, 2013

16 Grijpstra, J., "The Cryptococcus neoformans cap10 and cap59 mutant strains, affected in glucuronoxylomannan synthesis, differentially activate human dendritic cells" 57 : 142-150, 2009

17 Jain, A. V., "Th2 but not Th1 immune bias results in altered lung functions in a murine model of pulmonary Cryptococcus neoformans infection" 77 : 5389-5399, 2009

18 Huffnagle, G. B., "T-cell-mediated immunity in the lung - a Cryptococcus neoformans pulmonary infection model using SCID and athymic nude-mice" 59 : 1423-1433, 1991

19 Chaturvedi, V., "Stress tolerance and pathogenic potential of a mannitol mutant of Cryptococcus neoformans" 142 (142): 937-943, 1996

20 Martinez, L.R., "Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy" 73 : 6350-6362, 2005

21 Leopold Wager, C. M., "STAT1 signaling within macrophages is required for anti-fungal activity against Cryptococcus neoformans" 83 : 4513-4527, 2015

22 Leopold Wager, C. M., "STAT1 Signaling is essential for protection against Cryptococcus neoformans infection in mice" 193 : 4060-4071, 2014

23 Dan, J. M., "Role of the mannose receptor in a murine model of Cryptococcus neoformans infection" 76 : 2362-2367, 2008

24 Osterholzer, J. J., "Role of dendritic cells and alveolar macrophages in regulating early host defense against pulmonary infection with Cryptococcus neoformans" 77 : 3749-3758, 2009

25 Wozniak, K. L., "Role of IL-17A on resolution of pulmonary C. neoformans infection" 6 : e17204-, 2011

26 Arora, S., "Role of IFN-gamma in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis" 174 : 6346-6356, 2005

27 Zhang, Y., "Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99" 175 : 2489-2500, 2009

28 Oykhman, P., "Requirement and redundancy of the Src family kinases Fyn and Lyn in perforin-dependent killing of Cryptococcus neoformans by NK cells" 81 : 3912-3922, 2013

29 Olszewski, M. A., "Regulatory effects of macrophage inflammatory protein 1alpha/CCL3 on the development of immunity to Cryptococcus neoformans depend on expression of early inflammatory cytokines" 69 : 6256-6263, 2001

30 McNeill, E., "Regulation of iNOS function and cellular redox state by macrophage Gch1 reveals specific requirements for tetrahydrobiopterin in NRF2 activation" 79 : 206-216, 2015

31 Donglei Sun, "Real-Time Imaging of Interactions of Neutrophils with Cryptococcus neoformans Demonstrates a Crucial Role of Complement C5a-C5aR Signaling" American Society for Microbiology 84 (84): 216-229, 2015

32 Garro, A. P., "Rat eosinophils stimulate the expansion of Cryptococcus neoformans-specific CD4+ and CD8+ T cells with a T-helper 1 profile" 132 : 174-187, 2011

33 Hardison, S. E., "Pulmonary infection with an interferon-gamma-producing Cryptococcus neoformans strain results in classical macrophage activation and protection" 176 : 774-785, 2010

34 Baddley, J. W., "Pulmonary cryptococcosis in patients without HIV infection: factors associated with disseminated disease" 27 : 937-943, 2008

35 Wu, B., "Pulmonary cryptococcosis in non-AIDS patients" 32 : E70-E77, 2009

36 Hardison, S. E., "Protective immunity against pulmonary cryptococcosis is associated with STAT1-mediated classical macrophage activation" 189 : 4060-4068, 2012

37 Murphy, J.W., "Protective cell-mediated immunity against Cryptococcus neoformans" 149 : 373-386, 1998

38 Syme, R. M., "Primary dendritic cells phagocytose Cryptococcus neoformans via mannose receptors and Fcgamma receptor II for presentation to T lymphocytes" 70 : 5972-5981, 2002

39 Andama, A. O., "Prevalence and outcomes of cryptococcal antigenemia in HIV-seropositive patients hospitalized for suspected tuberculosis in Uganda" 63 : 189-194, 2013

40 Saag, M. S., "Practice guidelines for the management of cryptococcal disease. Infectious Diseases Society of America" 30 : 710-718, 2000

41 Coenjaerts, F. E., "Potent inhibition of neutrophil migration by cryptococcal mannoprotein-4-induced desensitization" 167 : 3988-3995, 2001

42 Alvarez, M., "Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages" 16 : 2161-2165, 2006

43 Wiseman, J. C., "Perforin-dependent cryptococcal microbicidal activity in NK cells requires PI3K-dependent ERK1/2 signaling" 178 : 6456-6464, 2007

44 Panackal, A. A., "Paradoxical immune responses in non-HIV Cryptococcal meningitis" 11 : e1004884-, 2015

45 Mansour, M. K., "Optimal T cell responses to Cryptococcus neoformans mannoprotein are dependent on recognition of conjugated carbohydrates by mannose receptors" 168 : 2872-2879, 2002

46 Kelly, R. M., "Opsonic requirements for dendritic cell-mediated responses to Cryptococcus neoformans" 73 : 592-598, 2005

47 Humphreys, I. R., "OX40 ligation on activated T cells enhances the control of Cryptococcus neoformans and reduces pulmonary eosinophilia" 170 : 6125-6132, 2003

48 Ellerbroek, P. M., "O-acetylation of cryptococcal capsular glucuronoxylomannan is essential for interference with neutrophil migration" 173 : 7513-7520, 2004

49 Nicola, A. M., "Nonlytic exocytosis of Cryptococcus neoformans from macrophages occurs in vivo and is influenced by phagosomal pH" 2 : e00167-11-, 2011

50 Mednick, A. J., "Neutropenia alters lung cytokine production in mice and reduces their susceptibility to pulmonary cryptococcosis" 33 : 1744-1753, 2003

51 Ma, L. L., "NK cells use perforin rather than granulysin for anticryptococcal activity" 173 : 3357-3365, 2004

52 Rohatgi, S., "Molecular characterization of the early B cell response to pulmonary Cryptococcus neoformans infection" 189 : 5820-5830, 2012

53 Milam, J. E., "Modulation of the pulmonary type 2 T-cell response to Cryptococcus neoformans by intratracheal delivery of a tumor necrosis factor alpha-expressing adenoviral vector" 75 : 4951-4958, 2007

54 Hole, C. R., "Mechanisms of dendritic cell lysosomal killing of Cryptococcus" 2 : 739-, 2012

55 Pietrella, D., "Mannoproteins from Cryptococcus neoformans promote dendritic cell maturation and activation" 73 : 820-827, 2005

56 Ruckerl, D., "Macrophage proliferation, provenance, and plasticity in macroparasite infection" 262 : 113-133, 2014

57 Davis, M. J., "Macrophage M1/M2 polarization dynamically adapts to changes in cytokine microenvironments in Cryptococcus neoformans infection" 4 : e00264-13-, 2013

58 Pappas, P. G., "Invasive fungal infections among organ transplant recipients: results of the Transplant-Associated Infection Surveillance Network (TRANSNET)" 50 : 1101-1111, 2010

59 Loschi, M., "Invasive aspergillosis in neutropenic patients during hospital renovation: effectiveness of mechanical preventive measures in a prospective cohort of 438 patients" 179 : 337-345, 2015

60 Murdock, B. J., "Interleukin-17A enhances host defense against cryptococcal lung infection through effects mediated by leukocyte recruitment, activation, and gamma interferon production" 82 : 937-948, 2014

61 Hardison, S. E., "Interleukin-17 is not required for classical macrophage activation in a pulmonary mouse model of Cryptococcus neoformans infection" 78 : 5341-5351, 2010

62 Onishi, R.M., "Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease" 129 : 311-321, 2010

63 Wozniak, K. L., "Insights into the mechanisms of protective immunity against Cryptococcus neoformans infection using a mouse model of pulmonary cryptococcosis" 4 : e6854-, 2009

64 Wozniak, K. L., "In vivo role of dendritic cells in a murine model of pulmonary cryptococcosis" 74 : 3817-3824, 2006

65 Jones, G. J., "In contrast to anti-tumor activity, YT cell and primary NK cell cytotoxicity for Cryptococcus neoformans bypasses LFA-1" 21 : 423-432, 2009

66 Holmer, S. M., "Impact of surfactant protein D, interleukin-5, and eosinophilia on Cryptococcosis" 82 : 683-693, 2014

67 Subramaniam, K., "IgM(+) memory B cell expression predicts HIV-associated cryptococcosis status" 200 : 244-251, 2009

68 Huffnagle, G. B., "IL-5 is required for eosinophil recruitment, crystal deposition, and mononuclear cell recruitment during a pulmonary Cryptococcus neoformans infection in genetically susceptible mice (C57BL/6)" 160 : 2393-2400, 1998

69 Grahnert, A., "IL-4 receptor-alpha-dependent control of Cryptococcus neoformans in the early phase of pulmonary infection" 9 : e87341-, 2014

70 Muller, U., "IL-13 induces disease-promoting type 2 cytokines, alternatively activated macrophages and allergic inflammation during pulmonary infection of mice with Cryptococcus neoformans" 179 : 5367-5377, 2007

71 Mambula, S. S., "Human neutrophil-mediated nonoxidative antifungal activity against Cryptococcus neoformans" 68 : 6257-6264, 2000

72 Allen, J.E., "Host protective roles of type 2 immunity: parasite killing and tissue repair, flip sides of the same coin" 26 : 329-340, 2014

73 Brena, S., "Fungicidal monoclonal antibody C7 interferes with iron acquisition in Candida albicans" 55 : 3156-3163, 2011

74 Charlier, C., "Evidence of a role for monocytes in dissemination and brain invasion by Cryptococcus neoformans" 77 : 120-127, 2009

75 Park, B. J., "Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS" 23 : 525-530, 2009

76 Pyrgos, V., "Epidemiology of cryptococcal meningitis in the US:1997-2009" 8 : e56269-, 2009

77 Garro, A. P., "Eosinophils elicit proliferation of naive and fungal-specific cells in vivo so enhancing a T helper type 1 cytokine profile in favour of a protective immune response against Cryptococcus neoformans infection" 134 : 198-213, 2011

78 Piehler, D., "Eosinophils contribute to IL-4 production and shape the T-helper cytokine profile and inflammatory response in pulmonary cryptococcosis" 179 : 733-744, 2011

79 Feldmesser, M., "Eosinophil-Cryptococcus neoformans interactions in vivo and in vitro" 65 : 1899-1907, 1997

80 Arora, S., "Effect of cytokine interplay on macrophage polarization during chronic pulmonary infection with Cryptococcus neoformans" 79 : 1915-1926, 2011

81 Qiu, Y., "Early induction of CCL7 downstream of TLR9 signaling promotes the development of robust immunity to cryptococcal infection" 188 : 3940-3948, 2012

82 Yamaguchi, H., "Disseminated cryptococcal infection with eosinophilia in a healthy person" 14 : 319-324, 2008

83 Yauch, L. E., "Direct inhibition of T-cell responses by the Cryptococcus capsular polysaccharide glucuronoxylomannan" 2 : e120-, 2006

84 Jarvis, J. N., "Determinants of mortality in a combined cohort of 501patients with HIV-associated Cryptococcal meningitis: implications for improving outcomes" 58 : 736-745, 2014

85 Wozniak, K. L., "Depletion of neutrophils in a protective model of pulmonary cryptococcosis results in increased IL-17A production by gammadelta T cells" 13 : 65-, 2012

86 Nakamura, K., "Deoxynucleic acids from Cryptococcus neoformans activate myeloid dendritic cells via a TLR9-dependent pathway" 180 : 4067-4074, 2008

87 Bauman, S. K., "Dendritic cells in the induction of protective and nonprotective anticryptococcal cell-mediated immune responses" 165 : 158-167, 2000

88 Nakamura, Y., "Dectin-2 deficiency promotes Th2 response and mucin production in the lungs after pulmonary infection with Cryptococcus neoformans" 83 : 671-681, 2015

89 Yamamoto, H., "Cryptococcus neoformans suppresses the activation of bone marrow-derived dendritic cells stimulated with its own DNA, but not with DNA from other fungi" 63 : 363-372, 2011

90 Chen, J., "Cryptococcus neoformans strains and infection in apparently immunocompetent patients" 14 : 755-762, 2008

91 Qureshi, A., "Cryptococcus neoformans modulates extracellular killing by neutrophils" 2 : 193-, 2011

92 Husain, S., "Cryptococcus neoformans infection in organ transplant recipients: variables influencing clinical characteristics and outcome" 7 : 375-381, 2001

93 Mansour, M. K., "Cryptococcus neoformans glycoantigens are captured by multiple lectin receptors and presented by dendritic cells" 176 : 3053-3061, 2006

94 Wozniak, K.L., "Cryptococcus neoformans enters the endolysosomal pathway of dendritic cells and is killed by lysosomal components" 76 : 4764-4771, 2008

95 Marr, K. J., "Cryptococcus neoformans directly stimulates perforin production and rearms NK cells for enhanced anticryptococcal microbicidal activity" 77 : 2436-2446, 2009

96 Mitchell, T.G., "Cryptococcosis in the Era of AIDS - 100 years after the discovery of Cryptococcus neoformans" 8 : 515-548, 1995

97 Osterholzer, J. J., "Cryptococcal urease promotes the accumulation of immature dendritic cells and a non-protective T2 immune response within the lung" 174 : 932-943, 2009

98 Sorrell, T. C., "Cryptococcal transmigration across a model brain blood-barrier:evidence of the Trojan horse mechanism and differences between Cryptococcus neoformans var. grubii strain H99 and Cryptococcus gattii strain R265" 18 : 57-67, 2015

99 Powderly, W.G., "Cryptococcal meningitis and AIDS" 17 : 837-842, 1993

100 Dan, J. M., "Cooperative stimulation of dendritic cells by Cryptococcus neoformans mannoproteins and CpG oligodeoxynucleotides" 3 : e2046-, 2008

101 Aratani, Y., "Contribution of the myeloperoxidase-dependent oxidative system to host defence against Cryptococcus neoformans" 55 : 1291-1299, 2006

102 Leopold Wager, C.M., "Classical versus alternative macrophage activation: the Ying and the Yang in host defense against pulmonary fungal infections" 7 : 1023-1035, 2014

103 Wiesner, D. L., "Chitin recognition via chitotriosidase promotes pathologic type-2 helper T cell responses to cryptococcal infection" 11 : e1004701-, 2015

104 Rocha, J. D., "Capsular polysaccharides from Cryptococcus neoformans modulate production of neutrophil extracellular traps (NETs) by human neutrophils" 5 : 8008-, 2015

105 Quintin, J., "Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes" 12 : 223-232, 2012

106 Osterholzer, J. J., "CCR2 mediates conventional dendritic cell recruitment and the formation of bronchovascular mononuclear cell infiltrates in the lungs of mice infected with Cryptococcus neoformans" 181 : 610-620, 2008

107 Gedik, H., "Bloodstream infections in patients with hematological malignancies: which is more fatal -cancer or resistant pathogens?" 10 : 743-752, 2014

108 Kleinnijenhuis, J., "Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes" 109 : 17537-17542, 2012

109 Casadevall, A., "Antibody-mediated protection through cross-reactivity introduces a fungal heresy into immunological dogma" 75 : 5074-5078, 2007

110 Casadevall, A., "Antibody immunity and invasive fungal infections" 63 : 4211-4218, 1995

111 Kleinschek, M. A., "Administration of IL-23 engages innate and adaptive immune mechanisms during fungal infection" 22 : 81-90, 2010

112 Sun, J. C., "Adaptive immune features of natural killer cells" 457 : 557-561, 2009

113 Osterholzer, J. J., "Accumulation of CD11b+lung dendritic cells in response to fungal infection results from the CCR2-mediated recruitment and differentiation of Ly-6Chigh monocytes" 183 : 8044-8053, 2009

114 McClelland, E. E., "Ab binding alters gene expression in Cryptococcus neoformans and directly modulates fungal metabolism" 120 : 1355-1361, 2010

115 Kramer, P. A., "A review of the mitochondrial and glycolytic metabolism in human platelets and leukocytes: implications for their use as bioenergetic biomarkers" 2 : 206-210, 2014