An Essential Role for the NLRP3 Inflammasome in Host Defense against the Human Fungal Pathogen Candida albicans

Cell Host and Microbe

Volumn 5, Issue 5, 2009, Pages 487-497

  Hise, Amy G ^a   Tomalka, Jeffrey ^a   Ganesan, Sandhya ^b   Patel, Krupen ^a   Hall, Brian A ^a   Brown, Gordon D ^c   Fitzgerald, Katherine A ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

MICROBIO; MOLIMMUNO

Indexed keywords

CRYOPYRIN; DECTIN 1; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; GENETIC TRANSCRIPTION; HOST RESISTANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CARRIER PROTEINS; CASPASE 1; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERLEUKIN-1BETA; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; MICE; MICE, INBRED C57BL;

BACTERIA (MICROORGANISMS); CANDIDA; CANDIDA ALBICANS; MURINAE;

EID: 65549154784     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2009.05.002     Document Type: Article

References (70)

1. Abu-Elteen K.H., and Abu-Alteen R.M. The prevalence of Candida albicans populations in the mouths of complete denture wearers. New Microbiol. 21 (1998) 41-48
2. Akita K., Ohtsuki T., Nukada Y., Tanimoto T., Namba M., Okura T., Takakura-Yamamoto R., Torigoe K., Gu Y., Su M.S., et al. Involvement of caspase-1 and caspase-3 in the production and processing of mature human interleukin 18 in monocytic THP.1 cells. J. Biol. Chem. 272 (1997) 26595-26603
3. Allen I.C., Scull M.A., Moore C.B., Holl E.K., McElvania-TeKippe E., Taxman D.J., Guthrie E.H., Pickles R.J., and Ting J.P. The NLRP3 inflammasome mediates in vivo innate immunity to influenza a virus through recognition of viral RNA. Immunity 30 (2009) 556-565
4. Amer A., Franchi L., Kanneganti T.D., Body-Malapel M., Ozoren N., Brady G., Meshinchi S., Jagirdar R., Gewirtz A., Akira S., and Nunez G. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281 (2006) 35217-35223
5. Bellocchio S., Montagnoli C., Bozza S., Gaziano R., Rossi G., Mambula S.S., Vecchi A., Mantovani A., Levitz S.M., and Romani L. The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J. Immunol. 172 (2004) 3059-3069
6. Brown G.D., Taylor P.R., Reid D.M., Willment J.A., Williams D.L., Martinez-Pomares L., Wong S.Y., and Gordon S. Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 196 (2002) 407-412
7. Brown G.D., Herre J., Williams D.L., Willment J.A., Marshall A.S., and Gordon S. Dectin-1 mediates the biological effects of beta-glucans. J. Exp. Med. 197 (2003) 1119-1124
8. Burckstummer T., Baumann C., Bluml S., Dixit E., Durnberger G., Jahn H., Planyavsky M., Bilban M., Colinge J., Bennett K.L., and Superti-Furga G. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10 (2009) 266-272
9. Cole G.T., Seshan K.R., Pope L.M., and Yancey R.J. Morphological aspects of gastrointestinal tract invasion by Candida albicans in the infant mouse. J. Med. Vet. Mycol. 26 (1988) 173-185
10. Daniluk T., Tokajuk G., Stokowska W., Fiedoruk K., Sciepuk M., Zaremba M.L., Rozkiewicz D., Cylwik-Rokicka D., Kedra B.A., Anielska I., et al. Occurrence rate of oral Candida albicans in denture wearer patients. Adv. Med. Sci. 51 Suppl 1 (2006) 77-80
11. Dinarello C.A. Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist. Int. Rev. Immunol. 16 (1998) 457-499
12. Dinarello C.A. The IL-1 family and inflammatory diseases. Clin. Exp. Rheumatol. 20 (2002) S1-S13
13. Dinarello C.A. Interleukin-1beta. Crit. Care Med. 33 (2005) S460-S462
14. Dongari-Bagtzoglou A., and Kashleva H. Candida albicans triggers interleukin-8 secretion by oral epithelial cells. Microb. Pathog. 34 (2003) 169-177
15. Dongari-Bagtzoglou A., Kashleva H., and Villar C.C. Bioactive interleukin-1alpha is cytolytically released from Candida albicans-infected oral epithelial cells. Med. Mycol. 42 (2004) 531-541
16. Dostert C., Petrilli V., Van Bruggen R., Steele C., Mossman B.T., and Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320 (2008) 674-677
17. Eisenbarth S.C., Colegio O.R., O'Connor W., Sutterwala F.S., and Flavell R.A. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453 (2008) 1122-1126
18. Fantuzzi G., and Dinarello C.A. Interleukin-18 and interleukin-1 beta: Two cytokine substrates for ICE (caspase-1). J. Clin. Immunol. 19 (1999) 1-11
19. Fernandes-Alnemri T., Yu J.W., Datta P., Wu J., and Alnemri E.S. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458 (2009) 509-513
20. Figueiral M.H., Azul A., Pinto E., Fonseca P.A., Branco F.M., and Scully C. Denture-related stomatitis: Identification of aetiological and predisposing factors - A large cohort. J. Oral Rehabil. 34 (2007) 448-455
21. Franchi L., McDonald C., Kanneganti T.D., Am A., and Nunez G. Nucleotide-binding oligomerization domain-like receptors: Intracellular pattern recognition molecules for pathogen detection and host defense. J. Immunol. 177 (2006) 3507-3513
22. Franchi L., Warner N., Viani K., and Nunez G. Function of Nod-like receptors in microbial recognition and host defense. Immunol. Rev. 227 (2009) 106-128
23. Gantner B.N., Simmons R.M., Canavera S.J., Akira S., and Underhill D.M. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197 (2003) 1107-1117
24. Gantner B.N., Simmons R.M., and Underhill D.M. Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J. 24 (2005) 1277-1286
25. Ghayur T., Banerjee S., Hugunin M., Butler D., Herzog L., Carter A., Quintal L., Sekut L., Talanian R., Paskind M., et al. Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature 386 (1997) 619-623
26. Gross O., Poeck H., Bscheider M., Dostert C., Hannesschlager N., Endres S., Hartmann G., Tardivel A., Schweighoffer E., Tybulewicz V., et al. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature (2009) 10.1038/nature07965 in press. Published online April 1, 2009
27. Gu Y., Kuida K., Tsutsui H., Ku G., Hsiao K., Fleming M.A., Hayashi N., Higashino K., Okamura H., Nakanishi K., et al. Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science 275 (1997) 206-209
28. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., and Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 9 (2008) 857-865
29. Herre J., Marshall A.S., Caron E., Edwards A.D., Williams D.L., Schweighoffer E., Tybulewicz V., Reis e Sousa C., Gordon S., and Brown G.D. Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 104 (2004) 4038-4045
30. Hornung V., Bauernfeind F., Halle A., Samstad E.O., Kono H., Rock K.L., Fitzgerald K.A., and Latz E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9 (2008) 847-856
31. Hornung V., Ablasser A., Charrel-Dennis M., Bauernfeind F., Horvath G., Caffrey D.R., Latz E., and Fitzgerald K.A. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458 (2009) 514-518
32. Huysamen C., and Brown G.D. The fungal pattern recognition receptor, Dectin-1, and the associated cluster of C-type lectin-like receptors. FEMS Microbiol. Lett. 290 (2009) 121-128
33. Ichinohe T., Lee H.K., Ogura Y., Flavell R., and Iwasaki A. Inflammasome recognition of influenza virus is essential for adaptive immune responses. J. Exp. Med. 206 (2009) 79-87
34. Jarvis K.G., Donnenberg M.S., Kaper J.B., and Jarvis W.R. Predominant pathogens in hospital infections. Proc. Natl. Acad. Sci. USA 92 (1995) 1664-1668
35. Kanneganti T.D., Body-Malapel M., Am A., Park J.H., Whitfield J., Franchi L., Taraporewala Z.F., Miller D., Patton J.T., Inohara N., and Nunez G. Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 281 (2006) 36560-36568
36. Kanneganti T.D., Ozoren N., Body-Malapel M., Am A., Park J.H., Franchi L., Whitfield J., Barchet W., Colonna M., Vandenabeele P., et al. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440 (2006) 233-236
37. Kerrigan A.M., and Brown G.D. C-type lectins and phagocytosis. Immunobiology (2009) 10.1016/j.imbio.2008.11.003 in press. Published online March 3, 2009
38. Kuida K., Lippke J.A., Ku G., Harding M.W., Livingston D.J., Su M.S., and Flavell R.A. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267 (1995) 2000-2003
39. Lu Q., Jayatilake J.A., Samaranayake L.P., and Jin L. Hyphal invasion of Candida albicans inhibits the expression of human beta-defensins in experimental oral candidiasis. J. Invest. Dermatol. 126 (2006) 2049-2056
40. Mariathasan S., Weiss D.S., Newton K., McBride J., O'Rourke K., Roose-Girma M., Lee W.P., Weinrauch Y., Monack D.M., and Dixit V.M. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440 (2006) 228-232
41. Martinon F., Agostini L., Meylan E., and Tschopp J. Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr. Biol. 14 (2004) 1929-1934
42. Martinon F., Petrilli V., Mayor A., Tardivel A., and Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440 (2006) 237-241
43. Martinon F., and Tschopp J. Inflammatory caspases: Linking an intracellular innate immune system to autoinflammatory diseases. Cell 117 (2004) 561-574
44. Martinon F., and Tschopp J. NLRs join TLRs as innate sensors of pathogens. Trends Immunol. 26 (2005) 447-454
45. McCourtie J., and Douglas L.J. Relationship between cell surface composition, adherence, and virulence of Candida albicans. Infect. Immun. 45 (1984) 6-12
46. Mencacci A., Bacci A., Cenci E., Montagnoli C., Fiorucci S., Casagrande A., Flavell R.A., Bistoni F., and Romani L. Interleukin 18 restores defective Th1 immunity to Candida albicans in caspase 1-deficient mice. Infect. Immun. 68 (2000) 5126-5131
47. Meylan E., Tschopp J., and Karin M. Intracellular pattern recognition receptors in the host response. Nature 442 (2006) 39-44
48. Miao E.A., Alpuche-Aranda C.M., Dors M., Clark A.E., Bader M.W., Miller S.I., and Aderem A. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7 (2006) 569-575
49. Miao E.A., Ernst R.K., Dors M., Mao D.P., and Aderem A. Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc. Natl. Acad. Sci. USA 105 (2008) 2562-2567
50. Mostefaoui Y., Bart C., Frenette M., and Rouabhia M. Candida albicans and Streptococcus salivarius modulate IL-6, IL-8, and TNF-alpha expression and secretion by engineered human oral mucosa cells. Cell. Microbiol. 6 (2004) 1085-1096
51. Muruve D.A., Petrilli V., Zaiss A.K., White L.R., Clark S.A., Ross P.J., Parks R.J., and Tschopp J. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452 (2008) 103-107
52. Netea M.G., Stuyt R.J., Kim S.H., Van der Meer J.W., Kullberg B.J., and Dinarello C.A. The role of endogenous interleukin (IL)-18, IL-12, IL-1beta, and tumor necrosis factor-alpha in the production of interferon-gamma induced by Candida albicans in human whole-blood cultures. J. Infect. Dis. 185 (2002) 963-970
53. Roberts T.L., Idris A., Dunn J.A., Kelly G.M., Burnton C.M., Hodgson S., Hardy L.L., Garceau V., Sweet M.J., Ross I.L., et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323 (2009) 1057-1060
54. Rogers N.C., Slack E.C., Edwards A.D., Nolte M.A., Schulz O., Schweighoffer E., Williams D.L., Gordon S., Tybulewicz V.L., Brown G.D., and Reis e Sousa C. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22 (2005) 507-517
55. Saville S.P., Lazzell A.L., Monteagudo C., and Lopez-Ribot J.L. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2 (2003) 1053-1060
56. Saville S.P., Lazzell A.L., Chaturvedi A.K., Monteagudo C., and Lopez-Ribot J.L. Use of a genetically engineered strain to evaluate the pathogenic potential of yeast cell and filamentous forms during Candida albicans systemic infection in immunodeficient mice. Infect. Immun. 76 (2008) 97-102
57. Severa M., Coccia E.M., and Fitzgerald K.A. Toll-like receptor-dependent and -independent viperin gene expression and counter-regulation by PRDI-binding factor-1/BLIMP1. J. Biol. Chem. 281 (2006) 26188-26195
58. Solle M., Labasi J., Perregaux D.G., Stam E., Petrushova N., Koller B.H., Griffiths R.J., and Gabel C.A. Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 276 (2001) 125-132
59. Steele C., and Fidel Jr. P.L. Cytokine and chemokine production by human oral and vaginal epithelial cells in response to Candida albicans. Infect. Immun. 70 (2002) 577-583
60. Stuyt R.J., Netea M.G., Verschueren I., Fantuzzi G., Dinarello C.A., Van Der Meer J.W., and Kullberg B.J. Role of interleukin-18 in host defense against disseminated Candida albicans infection. Infect. Immun. 70 (2002) 3284-3286
61. Stuyt R.J., Netea M.G., van Krieken J.H., van der Meer J.W., and Kullberg B.J. Recombinant interleukin-18 protects against disseminated Candida albicans infection in mice. J. Infect. Dis. 189 (2004) 1524-1527
62. Sutterwala F.S., and Flavell R.A. NLRC4/IPAF: A CARD carrying member of the NLR family. Clin. Immunol. 130 (2009) 2-6
63. Sutterwala F.S., Ogura Y., and Flavell R.A. The inflammasome in pathogen recognition and inflammation. J. Leukoc. Biol. 82 (2007) 259-264
64. Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., Lu Y., Miyagishi M., Kodama T., Honda K., et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448 (2007) 501-505
65. Takeda K., and Akira S. Toll-like receptors in innate immunity. Int. Immunol. 17 (2005) 1-14
66. Thomas P.G., Dash P., Aldridge Jr. J.R., Ellebedy A.H., Reynolds C., Funk A.J., Martin W.J., Lamkanfi M., Webby R.J., Boyd K.L., et al. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30 (2009) 566-575
67. van de Veerdonk F.L., Joosten L.A., Devesa I., Mora-Montes H.M., Kanneganti T.D., Dinarello C.A., van der Meer J.W., Gow N.A., Kullberg B.J., and Netea M.G. Bypassing pathogen-induced inflammasome activation for the regulation of interleukin-1beta production by the fungal pathogen Candida albicans. J. Infect. Dis. 199 (2009) 1087-1096
68. Vonk A.G., Netea M.G., van Krieken J.H., Iwakura Y., van der Meer J.W., and Kullberg B.J. Endogenous interleukin (IL)-1 alpha and IL-1 beta are crucial for host defense against disseminated candidiasis. J. Infect. Dis. 193 (2006) 1419-1426
69. Wisplinghoff H., Bischoff T., Tallent S.M., Seifert H., Wenzel R.P., and Edmond M.B. Nosocomial bloodstream infections in US hospitals: Analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39 (2004) 309-317
70. Yoneyama M., and Fujita T. RIG-I family RNA helicases: Cytoplasmic sensor for antiviral innate immunity. Cytokine Growth Factor Rev. 18 (2007) 545-551