In Pulmonary Paracoccidioidomycosis IL-10 Deficiency Leads to Increased Immunity and Regressive Infection without Enhancing Tissue Pathology

PLoS Neglected Tropical Diseases

Volumn 7, Issue 10, 2013, Pages

  Costa, Tânia A ^a   Bazan, Silvia B ^a   Feriotti, Claudia ^a   Araújo, Eliseu F ^a   Bassi, Ênio J ^a   Loures, Flávio V ^a   Calich, Vera L G ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COLONY FORMING UNIT; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FUNGICIDAL ACTIVITY; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFLAMMATION; INFLAMMATORY INFILTRATE; INNATE IMMUNITY; LEUKOCYTE; MACROPHAGE; MALE; MORTALITY; MOUSE; NONHUMAN; PARACOCCIDIOIDES BRASILIENSIS; PHAGOCYTOSIS; PROTEIN DEFICIENCY; SOUTH AMERICAN BLASTOMYCOSIS; SURVIVAL RATE;

ANIMALS; ANTIBODIES, FUNGAL; COLONY COUNT, MICROBIAL; CYTOKINES; DISEASE MODELS, ANIMAL; HYPERSENSITIVITY, DELAYED; INTERLEUKIN-10; LUNG; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PARACOCCIDIOIDES; PARACOCCIDIOIDOMYCOSIS; PHAGOCYTOSIS; T-LYMPHOCYTES;

EID: 84887310119     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002512     Document Type: Article

References (75)

1. Romani L, (2011) Immunity to fungal infections. Nat Rev Immunol 11: 275-288.
2. Romani L, (2004) Immunity to fungal infections. Nat Rev Immunol 4: 1-23.
3. Brown GD, (2011) Innate antifungal immunity: the key role of phagocytes. Annu Rev Immunol 29: 1-21.
4. Loures FV, Pina A, Felonato M, Calich VL, (2009) TLR2 is a negative regulator of Th17 cells and tissue pathology in a pulmonary model of fungal infection. J Immunol 183: 1279-1290.
5. Felonato M, Pina A, de Araujo EF, Loures FV, Bazan SB, et al. (2012) Anti-CD25 treatment depletes Treg cells and decreases disease severity in susceptible and resistant mice infected with Paracoccidioides brasiliensis. PLoS One 7: 1-20.
6. Brummer E, Castaneda E, Restrepo A, (1993) Paracoccidioidomycosis: an update. Clin Microbiol Rev 6: 89-117.
7. Calich VL, Kashino SS, (1998) Cytokines produced by susceptible and resistant mice in the course of Paracoccidioides brasiliensis infection. Braz J Med Biol Res 31: 615-623.
8. Calich VLG, Singer-Vermes LM, Burger E, (1985) Susceptibility and resistance of inbred mice to Paracoccidioides brasiliensis. Brit J Exp Path 66: 585-594.
9. Cano LE, Kashino SS, Arruda C, André D, Xidieh CF, et al. (1998) Protective role of interferon-gamma in experimental pulmonary paracoccidioidomycosis. Infect Immun 66: 800-806.
10. Mege JL, Meghari S, Honstettre A, Capo C, Raoult D, (2006) The two faces of interleukin 10 in human infectious diseases. Lancet Infect Dis 6: 557-569.
11. O'Garra A, Vieira P, (2007) T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol 7: 425-428.
12. Maynard CL, Weaver CT, (2008) Diversity in the contribution of interleukin-10 to T-cell-mediated immune regulation. Immunol Rev 226: 219-233.
13. Cyktor JC, Turner J, (2011) Interleukin-10 and immunity against prokaryotic and eukaryotic intracellular pathogens. Infect Immun 79: 2964-2973.
14. Hedrich CM, Bream JH, (2010) Cell type-specific regulation of IL-10 expression in inflammation and disease. Immunol Res 47: 185-206.
15. Sabat R, Grütz G, Warszawska K, Kirsch S, Witte E, et al. (2010) Biology of interleukin-10. Cytokine Growth Factor Rev 21: 331-344.
16. Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG, (2011) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 29: 71-109.
17. O'Garra A, Murphy KM, (2009) From IL-10 to IL-12: how pathogens and their products stimulate APCs to induce T(H)1 development. Nat Immunol 10: 929-932.
18. Couper KN, Blount DG, Riley EM, (2008) IL-10: the master regulator of immunity to infection. J Immunol 180: 5771-5777.
19. Fiorentino DF, Zlotnik A, Vieira P, Mosmann TR, Howard M, et al. (1991) IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol 146: 3444-3451.
20. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, et al. (1993) Interleukin-10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178: 1041-1048.
21. Jankovic D, Kullberg MC, Feng CG, Goldszmid RS, Collazo CM, et al. (2007) Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J Exp Med 204: 273-283.
22. Zielinski CE, Mele F, Aschenbrenner D, Jarrossay D, Ronchi F, et al. (2012) Pathogen-induced human TH17 cells produce IFN-γ or IL-10 and are regulated by IL-1β. Nature 484: 514-518.
23. Carvalho A, Cunha C, Pasqualotto AC, Pitzurra L, Denning DW, et al. (2010) Genetic variability of innate immunity impacts human susceptibility to fungal diseases. Int J Infect Dis 14: 460-468.
24. Moraes-Vasconcelos D, Grumach AS, Yamaguti A, Andrade ME, Fieschi C, et al. (2005) Paracoccidioides brasiliensis disseminated disease in a patient with inherited deficiency in the beta1 subunit of the interleukin (IL)-12/IL-23 receptor. Clin Infect Dis 41: 31-37.
25. Benard G, (2008) An overview of the immunopathology of human paracoccidioidomycosis. Mycopathologia 165: 209-221.
26. Romani L, (2008) Cell mediated immunity to fungi: a reassessment. Med Mycol 46: 515-529.
27. Brouard J, Knauer N, Boelle PY, Corvol H, Henrion-Caude A, et al. (2005) Influence of interleukin-10 on Aspergillus fumigatus infection in patients with cystic fibrosis. J Infect Dis 191: 1988-1991.
28. Romano CC, Mendes-Giannini MJ, Duarte AJ, Benard G, (2002) IL-12 and neutralization of endogenous IL-10 revert the in vitro antigen-specific cellular immunosuppression of paracoccidioidomycosis patients. Cytokine 18: 149-157.
29. Romano CC, Mendes-Giannini MJ, Duarte AJ, Benard G, (2005) The role of interleukin-10 in the differential expression of interleukin-12p70 and its beta2 receptor on patients with active or treated paracoccidioidomycosis and healthy infected subjects. Clin Immunol 114: 86-94.
30. Kashino SS, Fazioli RA, Cafalli-Favati C, Meloni-Bruneri LH, Vaz CA, et al. (2000) Resistance to Paracoccidioides brasiliensis infection is linked to a preferential Th1 immune response, whereas susceptibility is associated with absence of IFN-gamma production. J Interferon Cytokine Res 20: 89-97.
31. Roilides E, Anastasiou-Katsiardani A, Dimitriadou-Georgiadou A, Kadiltsoglou I, Tsaparidou S, et al. (1998) Suppressive effects of interleukin-10 on human mononuclear phagocyte function against Candida albicans and Staphylococcus aureus. J Infect Dis 178: 1734-1742.
32. Moreira AP, Dias-Melicio LA, Soares AM, (2010) Interleukin-10 but not Transforming Growth Factor beta inhibits murine activated macrophages Paracoccidioides brasiliensis killing: effect on H2O2 and NO production. Cell Immunol 263: 196-203.
33. Romani L, Puccetti P, Mencacci A, Cenci E, Spaccapelo R, et al. (1994) Neutralization of IL-10 up-regulates nitric oxide production and protects susceptible mice from challenge with Candida albicans. J Immunol 152: 3514-3521.
34. Blackstock R, Buchanan KL, Adesina AM, Murphy JW, (1999) Differential regulation of immune responses by highly and weakly virulent Cryptococcus neoformans isolates. Infect Immun 67: 3601-3609.
35. Del Sero G, Mencacci A, Cenci E, d'Ostiani CF, Montagnoli C, et al. (1999) Antifungal type 1 responses are upregulated in IL-10-deficient mice. Microbes Infect 1: 1169-1180.
36. Clemons KV, Grunig G, Sobel RA, Mirels LF, Rennick DM, et al. (2000) Role of IL-10 in invasive aspergillosis: increased resistance of IL-10 gene knockout mice to lethal systemic aspergillosis. Clin Exp Immunol 122: 186-191.
37. Deepe GS Jr, Gibbons RS, (2003) Protective and memory immunity to Histoplasma capsulatum in the absence of IL-10. J Immunol 171: 5353-5362.
38. Kashino SS, Singer-Vermes LM, Calich VLG, Burger E, (1990) Alterations in the pathogenicity of one Paracoccidioides brasiliensis isolate do not correlative with its in vitro growth. Mycopathologia 111: 173-180.
39. Fava Netto C, (1969) Vegas VS, Sciannaméa IM, Guarnieri EDB, (1969) Antígeno polissacarídico do Paracoccidioides brasiliensis. Estudo do tempo de cultivo do P. brasiliensis necessário ao preparo do antígeno. Rev Inst Med Trop 11: 177-181.
40. Cano LE, Singer-Vermes LM, Vaz CA, Russo M, Calich VLG, (1995) Pulmonary paracoccidioidomycosis in resistant and susceptible mice: relationship among progression of infection, bronchoalveolar cell activation, cellular immune response, and specific isotype patterns. Infect Immun 63: 1777-1783.
41. Singer-Vermes LM, (1992) Ciavaglia MC, (1992) Kashino SS, (1992) Burger E, (1992) Calich VLG, (1992) The source of the growth-promoting factor(s) affects the plating efficiency of Paracoccidioides brasiliensis. J Med Vet Mycol 30: 261-264.
42. Ding AH, Nathan CF, Stuehr DJ, (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. J Immun 141: 2407-2412.
43. Fazioli RA, Singer-Vermes LM, Kashino SS, Burger E, De Franco MF, et al. (1994) Delayed-type hypersensitivity response in an isogenic murine model of paracoccidioidomycosis. Mycopathologia 126: 137-146.
44. Fava Netto C, (1955) Estudos quantitativos sobre fixação do complemento na blastomicose sul-americana com antígeno polissacarídico. Arq Cir Clin Exp 18: 197-254.
45. Lindell DM, Moore TA, Mcdonald RA, Toews GB, Huffnagke GB, (2006) Distinct compartmentalization of CD4+T-cell effector function versus proliferative capacity during pulmonary cryptococcosis. Am J Pathol 168: 847-855.
46. Camargo ZP, Taborda CP, Rodrigues EG, Travassos LR, (1991) The use of cell-free antigens of Paracoccidioides brasiliensis in serological tests. J Med Vet Mycol 29: 31-38.
47. Gomes GM, Cisalpino PS, Taborda CP, de Camargo ZP, (2000) PCR for diagnosis of paracoccidioidomycosis. J Clin Microbiol 38: 3478-3480.
48. Benard G, Romano CC, Cacere CR, Juvenale M, Mendes-Gianninni MJS, et al. (2001) Imbalance of IL-12, IFN-gamma and IL-10 secretion in the immunsupression associated with human paracoccidioidomycosis. Cytokine 13: 248-252.
49. Mamoni RL, Blotta MH, (2006) Flow-cytometric analysis of cytokine production in human paracoccidioidomycosis. Cytokine 35: 207-216.
50. Teder P, Vandivier RW, Jiang D, Liang J, Cohn L, et al. (2002) Resolution of lung inflammation by CD44. Science 296: 155-158.
51. Gazzinelli RT, Oswald IP, James SL, Sher A, (1992) IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages. J Immunol 148: 1792-1796.
52. Kelly JP, Bancroft GJ, (1996) Administration of interleukin-10 abolishes innate resistance to Listeria monocytogenes. Eur J Immunol 26: 356-364.
53. Hu X, Paik PK, Chen J, Yarilina A, Kockeritz L, et al. (2006) IFN-gamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1proteins. Immunity 24: 563-574.
54. Schroder K, Hertzog PJ, Ravasi T, Hume DA, (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75: 163-189.
55. Feriotti C, Loures FV, Frank de Araújo E, da Costa TA, Calich VL, (2013) Mannosyl-recognizing receptors induce an M1-like phenotype in macrophages of susceptible mice but an M2-like phenotype in mice resistant to a fungal infection. PLoS One 8: e54845, 1-17.
56. Huffnagle GB, Strieter RM, Staniford J, Mcdonald RA, Burdick MD, et al. (1995) The role of monocyte chemotactic protein-1 (MCP-1) in the recruitment of monocytes and CD4+ T cells during a pulmonary Cryptococcus neoformans infection. J Immunol 155: 4790-4797.
57. Kawakami K, Kinjo Y, Uezu K, Satomi Y, Miyagi K, et al. (2001) Monocyte chemoattractant protein-1-dependent increase of Vα14 NKT cells lungs and their roles in Th1 response and host defense in Cryptococcal infection. J Immunol 167: 6525-6532.
58. North RJ, (1998) Mice incapable of making IL-4 or IL-10 display normal resistance to infection with Mycobacterium tuberculosis. Clin Exp Immunol 113: 55-58.
59. Yang X, Gartner J, Zhu L, Wang S, Brunham RC, (1999) IL-10 gene knockout mice show enhanced Th1-like protective immunity and absent granuloma formation following Chlamydia trachomatis lung infection. J Immunol 162: 1010-1017.
60. Noben-Trauth N, Lira R, Nagase H, Paul WE, Sacks DL, (2003) The relative contribution of IL-4 receptor signaling and IL-10 to susceptibility to Leishmania major. J Immunol 170: 5152-5158.
61. Murphy ML, Wille U, Villegas EN, Hunter CA, Farrell JP, (2001) IL-10 mediates susceptibility to Leishmania donovani infection. Eur J Immunol 31: 2848-2856.
62. Li C, Corraliza I, Langhorne J, (1999) A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect Immun 67: 4435-4442.
63. Hunter CA, Ellis-Neyes LA, Slifer T, Kanaly S, Grünig G, et al. (1997) IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. J Immunol 158: 3311-3316.
64. Gazzinelli RT, Wysocka M, Hieny S, Scharton-Kersten T, Cheever A, et al. (1996) In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J Immunol 157: 798-805.
65. Mege JL, Meghari S, Honstettre A, Capo C, Raoult D, (2006) The two faces of interleukin 10 in human infectious diseases. Lancet Infect Dis 6: 557-569.
66. Romani L, Mocci S, Bietta C, Lanfaloni L, Puccetti P, et al. (1991) Th1 and Th2 cytokine secretion patterns in murine candidiasis: association of Th1 responses with acquired resistance. Infect Immun 59: 4647-4654.
67. Taborda CP, Juliano MA, Puccia R, Franco M, Travassos LR, (1998) Mapping of the T-cell epitope in the major 43-kilodalton glycoprotein of Paracoccidioides brasiliensis which induces a Th-1 response protective against fungal infection in BALB/c mice. Infect Immun 66: 786-793.
68. Casadevall A, Feldmesser M, Pirofski LA, (2002) Induced humoral immunity and vaccination against major human fungal pathogens. Curr Opin Microbiol 5: 386-391.
69. Vazquez-Torres A, Jones-Carson J, Wagner RD, Warner T, Balish E, (1999) Early resistance of interleukin-10 knockout mice to acute systemic candidiasis. Infect Immun 67: 670-674.
70. Murray PJ, Young RA, (1999) Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect Immun 67: 3087-3095.
71. Dai WJ, Köhler G, Brombacher F, (1997) Both innate and acquired immunity to Listeria monocytogenes infection are increased in IL-10-deficient mice. J Immunol 158: 2259-2267.
72. Guimarães AJ, Frases S, Gomez FJ, Zancopé-Oliveira RM, Nosanchuk JD, (2009) Monoclonal antibodies to heat shock protein 60 alter the pathogenesis of Histoplasma capsulatum. Infect Immun 77: 1357-1367.
73. Nosanchuk JD, Steenbergen JN, Shi L, Deepe GS Jr, Casadevall A, (2003) Antibodies to a cell surface histone-like protein protect against Histoplasma capsulatum. J Clin Invest 12: 1164-1175.
74. Netea MG, Sutmuller R, Hermann C, Van der Graaf CA, Van der Meer JW, et al. (2004) Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J Immunol 172: 3712-3718.
75. Montagnoli C, Bacci A, Bozza S, Gaziano R, Mosci P, et al. (2002) B7/CD28-dependent CD4+CD25+ regulatory T cells are essential components of the memory-protective immunity to Candida albicans. J Immunol 169: 6298-3608.