NLRP3 Inflammasome Activation by Paracoccidioides brasiliensis

PLoS Neglected Tropical Diseases

Volumn 7, Issue 12, 2013, Pages

  Tavares, Aldo Henrique ^a   Magalhães, Kelly Grace ^a   Almeida, Raquel Das Neves ^a   Correa, Rafael ^a   Burgel, Pedro Henrique ^a   Bocca, Anamélia Lorenzetti ^a  

^a UNIVERSITY OF BRASILIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CATHEPSIN B; CRYOPYRIN; CYTOKINE; HOST FACTOR; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MYELOID DIFFERENTIATION FACTOR 88; NITRIC OXIDE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; POTASSIUM; PROTEIN KINASE SYK; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; COLONY FORMING UNIT; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HOST RESISTANCE; MACROPHAGE; MOUSE; NONHUMAN; PARACOCCIDIOIDES BRASILIENSIS;

ANIMALS; CARRIER PROTEINS; DENDRITIC CELLS; HOST-PARASITE INTERACTIONS; INFLAMMASOMES; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, INBRED C57BL; PARACOCCIDIOIDES;

EID: 84892749727     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002595     Document Type: Article

References (66)

1. Restrepo A, Gómez BL, Tobón A, (2012) Paracoccidioidomycosis: Latin America's Own Fungal Disorder. Current Fungal Infection Reports 6: 303-311.
2. San-Blas G, Burger E, (2011) Experimental medical mycological research in Latin America- a 2000-2009 overview. Rev Iberoam Micol 28: 1-25.
3. Prado M, Silva MB, Laurenti R, Travassos LR, Taborda CP, (2009) Mortality due to systemic mycoses as a primary cause of death or in association with AIDS in Brazil: a review from 1996 to 2006. Mem Inst Oswaldo Cruz 104: 513-21.
4. Brummer E, Castaneda E, Restrepo A, (1993) Paracoccidioidomycosis: an update. Clin Microbiol Rev 6: 89-117.
5. San-Blas G, (1993) Paracoccidioidomycosis and its etiologic agent Paracoccidioides brasiliensis. J Med Vet Mycol 31: 99-113.
6. San-Blas G, Niño-Vega G, Iturriaga T, (2002) Paracoccidioides brasiliensis and paracoccidioidomycosis: molecular approaches to morphogenesis, diagnosis, epidemiology, taxonomy and genetics. Med Mycol 40: 225-242.
7. Calich VLG, Costa TA, Felonato M, Arruda C, Bernardino S, et al. (2008) Innate immunity to Paracoccidioides brasiliensis infection. Mycopathologia 165: 223-236.
8. LeibundGut-Landmann S, Wuthrich M, Hohl TM, (2012) Immunity to fungi. Curr Opin Immunol 24: 449-458.
9. Brown GD, (2011) Innate antifungal immunity: the key role of phagocytes. Annu Rev Immunol 29: 1-21.
10. Diniz SN, Nomizo R, Cisalpino PS, Teixeira MM, Brown GD, et al. (2004) PTX3 function as an opsonin for the dectin-1-dependent internalization of zymosan by macrophages. J Leukoc Biol 75: 649-656.
11. 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.
12. Loures FV, Pina A, Felonato M, Araujo EF, Leite KR, et al. (2010) Toll-like receptor 4 signaling leads to severe fungal infection associated with enhanced proinflammatory immunity and impaired expansion of regulatory T cells. Infect Immun 78: 1078-1088.
13. Bonfim CV, Mamoni RL, Blotta MH, (2009) TLR-2, TLR-4 and dectin-1 expression in human monocytes and neutrophils stimulated by Paracoccidioides brasiliensis. Med Mycol 47: 722-733.
14. Tavares AH, Derengowski LS, Ferreira KS, Silva SS, Macedo C, et al. (2012) Murine dendritic cells transcriptional modulation upon Paracoccidioides brasiliensis infection. PLoS Negl Trop Dis 6: e1459.
15. Menino JF, Saraiva M, Gomes-Alves AG, Lobo-Silva D, Sturme M, et al. (2013) TLR9 Activation Dampens the Early Inflammatory Response to Paracoccidioides brasiliensis, Impacting Host Survival. PLoS Negl Trop Dis 7: e2317.
16. van de Veerdonk FL, Kullberg BJ, van der Meer JW, Gow NA, Netea MG, (2008) Host-microbe interactions: innate pattern recognition of fungal pathogens. Curr Opin Microbiol 11: 305-312.
17. Li P, Allen H, Banerjee S, Franklin S, Herzog L, et al. (1995) Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80: 401-11.
18. Martinon F, Mayor A, Tschopp J, (2009) The inflammasomes: guardians of the body. Annu Rev Immunol 27: 229-265.
19. Bauernfeind F, Hornung V, (2013) Of inflammasomes and pathogens-sensing of microbes by the inflammasome. EMBO Mol Med 5: 814-826.
20. van de Veerdonk FL, Netea MG, Dinarello CA, Joosten LA, (2011) Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol 32: 110-116.
21. Gross O, Poeck H, Bscheider M, Dostert C, Hannesschlager N, et al. (2009) Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459: 433-436.
22. Hise AG, Tomalka J, Ganesan S, Patel K, Hall BA, et al. (2009) An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5: 487-497.
23. Joly S, Ma N, Sadler JJ, Soll DR, Cassel SL, et al. (2009) Cutting edge: Candida albicans hyphae formation triggers activation of the Nlrp3 inflammasome. J Immunol 183: 3578-3581.
24. Li H, Wu S, Mao L, Lei G, Zhang L, et al. (2013) Human pathogenic fungus Trichophyton schoenleinii activates the NLRP3 inflammasome. Protein Cell 4: 529-538.
25. Lei G, Chen M, Li H, Niu JL, Wu S, et al. (2013) Biofilm from a clinical strain of Cryptococcus neoformans activates the NLRP3 inflammasome. Cell Res 23: 965-968.
26. Said-Sadier N, Padilla E, Langsley G, Ojcius DM, (2010) Aspergillus fumigatus stimulates the NLRP3 inflammasome through a pathway requiring ROS production and the Syk tyrosine kinase. PloS one 5: e10008.
27. Peraçoli M, (2003) Production of pro- and anti-inflammatory cytokines by monocytes from patients with paracoccidioidomycosis. Microbes and Infection 5: 413-418.
28. Kurokawa CS, Araujo JP Jr, Soares AM, Sugizaki MF, Peraçoli MT, (2007) Pro- and anti-inflammatory cytokines produced by human monocytes challenged in vitro with Paracoccidioides brasiliensis. Microbiol Immunol 51: 421-428.
29. Loures FV, Pina A, Felonato M, Feriotti C, de Araújo EF, et al. (2011) MyD88 signaling is required for efficient innate and adaptive immune responses to Paracoccidioides brasiliensis infection. Infect Immun 79: 2470-2480.
30. Pina A, de Araujo EF, Felonato M, Loures FV, Feriotti C, et al. (2013) Myeloid dendritic cells (DCs) of mice susceptible to paracoccidioidomycosis suppress T cell responses whereas myeloid and plasmacytoid DCs from resistant mice induce effector and regulatory T cells. Infect Immun 81: 1064-1077.
31. Lutz MB, Kukutsch N, Ogilvie AL, Rössner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. Immunol Methods 223: 77-92.
32. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
33. He Y, Franchi L, Nunez G, (2013) TLR agonists stimulate Nlrp3-dependent IL-1beta production independently of the purinergic P2X7 receptor in dendritic cells and in vivo. J Immunol 190: 334-339.
34. Gringhuis SI, Kaptein TM, Wevers BA, Theelen B, van der Vlist M, et al. (2012) Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1beta via a noncanonical caspase-8 inflammasome. Nat Immunol 13: 246-254.
35. Lamkanfi M, Mueller JL, Vitari AC, Misaghi S, Fedorova A, et al. (2009) Glyburide inhibits the Cryopyrin/Nalp3 inflammasome. J Cell Biol 187: 61-70.
36. Bauernfeind F, Bartok E, Rieger A, Franchi L, Nunez G, et al. (2011) Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J Immunol 187: 613-617.
37. Brummer E, Hanson LH, Restrepo A, Stevens DA, (1988) In vivo and in vitro activation of pulmonary macrophages by IFN-gamma for enhanced killing of Paracoccidioides brasiliensis or Blastomyces dermatitidis. J Immunol 140: 2786-2789.
38. Gonzalez A, de Gregori W, Velez D, Restrepo A, Cano LE, (2000) Nitric oxide participation in the fungicidal mechanism of gamma interferon-activated murine macrophages against Paracoccidioides brasiliensis conidia. Infect Immun 68: 2546-2552.
39. Nascimento FR, Calich VL, Rodríguez D, Russo M, (2002) Dual role for nitric oxide in paracoccidioidomycosis: essential for resistance, but overproduction associated with susceptibility. J Immunol 168: 4593-600.
40. Bauernfeind F, Rieger A, Schildberg FA, Knolle PA, Schmid-Burgk JL, et al. (2012) NLRP3 inflammasome activity is negatively controlled by miR-223. J Immunol 189: 4175-4181.
41. Guarda G, Zenger M, Yazdi AS, Schroder K, Ferrero I, et al. (2011) Differential expression of NLRP3 among hematopoietic cells. J Immunol 186: 2529-2534.
42. Netea MG, Nold-Petry CA, Nold MF, Joosten LA, Opitz B, et al. (2009) Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 113: 2324-2335.
43. Pelegrin P, Surprenant A, (2009) Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1beta release through pyrophosphates. EMBO J 28: 2114-2127.
44. Kankkunen P, Teirila L, Rintahaka J, Alenius H, Wolff H, et al. (2010) (1,3)-beta-glucans activate both dectin-1 and NLRP3 inflammasome in human macrophages. J Immunol 184: 6335-6342.
45. Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, et al. (2009) Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 183: 787-791.
46. Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM, (2003) Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 197: 1107-1117.
47. Goodridge HS, Shimada T, Wolf AJ, Hsu YM, Becker CA, et al. (2009) Differential use of CARD9 by dectin-1 in macrophages and dendritic cells. J Immunol 182: 1146-1154.
48. Kang TB, Yang SH, Toth B, Kovalenko A, Wallach D, (2013) Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 38: 27-40.
49. Dias MF, Filgueira AL, de Souza W, (2004) A morphological and cytochemical study of the interaction between Paracoccidiodes brasiliensis and neutrophils. Microsc Microanal 10: 215-223.
50. Dias MF, Mesquita J, Filgueira AL, De Souza W, (2008) Human neutrophils susceptibility to Paracoccidioides brasiliensis: an ultrastructural and cytochemical assay. Med Mycol 46: 241-249.
51. Tavares AH, Silva SS, Dantas A, Campos EG, Andrade RV, et al. (2007) Early transcriptional response of Paracoccidioides brasiliensis upon internalization by murine macrophages. Microbes Infect 9: 583-590.
52. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, et al. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9: 847-856.
53. Sharp FA, Ruane D, Claass B, Creagh E, Harris J, et al. (2009) Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc Natl Acad Sci USA 106: 870-875.
54. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, et al. (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 9: 857-865.
55. He X, Mekasha S, Mavrogiorgos N, Fitzgerald KA, Lien E, et al. (2010) Inflammation and fibrosis during Chlamydia pneumoniae infection is regulated by IL-1 and the NLRP3/ASC inflammasome. J Immunol 184: 5743-5754.
56. Cassel SL, Eisenbarth SC, Iyer SS, Sadler JJ, Colegio OR, et al. (2008) The Nalp3 inflammasome is essential for the development of silicosis. Proc Natl Acad Sci U S A 105: 9035-9040.
57. Romani L, (2011) Immunity to fungal infections. Nat Rev Immunol 11: 275-288.
58. Master SS, Rampini SK, Davis AS, Keller C, Ehlers S, et al. (2008) Mycobacterium tuberculosis prevents inflammasome activation. Cell Host Microbe 3: 224-232.
59. Lazarevic V, Martinon F, (2008) Linking inflammasome activation and phagosome maturation. Cell Host Microbe 3: 199-200.
60. Fremond CM, Togbe D, Doz E, Rose S, Vasseur V, et al. (2007) IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J Immunol 179: 1178-1189.
61. Newman SL, Bhugra B, Holly A, Morris RE, (2005) Enhanced killing of Candida albicans by human macrophages adherent to type 1 collagen matrices via induction of phagolysosomal fusion. Infect Immun 73: 770-777.
62. Strasser JE, Newman SL, Ciraolo GM, Morris RE, Howell ML, et al. (1999) Regulation of the macrophage vacuolar ATPase and phagosome-lysosome fusion by Histoplasma capsulatum. J Immunol 162: 6148-6154.
63. Gildea LA, Ciraolo GM, Morris RE, Newman SL, (2005) Human dendritic cell activity against Histoplasma capsulatum is mediated via phagolysosomal fusion. Infect Immun 73: 6803-6811.
64. Chen CC, Tsai SH, Lu CC, Hu ST, Wu TS, et al. (2012) Activation of an NLRP3 inflammasome restricts Mycobacterium kansasii infection. PloS one 7: e36292.
65. Havell EA, Moldawer LL, Helfgott D, Kilian PL, Sehgal PB, (1992) Type I IL-1 receptor blockade exacerbates murine listeriosis. J Immunol 148: 1486-1492.
66. Bellocchio S, Montagnoli C, Bozza S, Gaziano R, Rossi G, et al. (2004) The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 172: 3059-3069.