A novel role for the NLRC4 inflammasome in mucosal defenses against the fungal pathogen Candida albicans

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  Tomalka, Jeffrey ^a   Ganesan, Sandhya ^b   Azodi, Elaheh ^a   Patel, Krupen ^a   Majmudar, Parth ^a   Hall, Brian A ^a   Fitzgerald, Katherine A ^b   Hise, Amy G ^a  

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

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INFLAMMASOME; NLRC4 INFLAMMASOME; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE; IPAF PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CANDIDA ALBICANS; CONTROLLED STUDY; DISEASE SEVERITY; GENE EXPRESSION; INFLAMMATORY CELL; INNATE IMMUNITY; MOUSE; MOUTH CAVITY; MUCOSAL IMMUNITY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; THRUSH; ANIMAL; C57BL MOUSE; CANDIDIASIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; MOUTH MUCOSA; REAL TIME POLYMERASE CHAIN REACTION;

CANDIDA; CANDIDA ALBICANS; MUS;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CALCIUM-BINDING PROTEINS; CANDIDA ALBICANS; CANDIDIASIS; CARRIER PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INFLAMMASOMES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOUTH MUCOSA; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84855296038     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002379     Document Type: Article

References (96)

1. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, et al. (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39: 309-317.
2. Jarvis KG, Donnenberg MS, Kaper JB, Jarvis WR, (1995) Predominant pathogens in hospital infections. Proc Natl Acad Sci USA 92: 1664-1668.
3. Fraser VJ, Jones M, Dunkel J, Storfer S, Medoff G, et al. (1992) Candidemia in a tertiary care hospital: epidemiology, risk factors, and predictors of mortality. Clin Infect Dis 15: 414-421.
4. Gantner BN, Simmons RM, Underhill DM, (2005) Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. Embo J 24: 1277-1286.
5. Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, et al. (2002) Dectin-1 is a major beta-glucan receptor on macrophages. J Exp Med 196: 407-412.
6. 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.
7. Gow NA, Netea MG, Munro CA, Ferwerda G, Bates S, et al. (2007) Immune recognition of Candida albicans beta-glucan by dectin-1. J Infect Dis 196: 1565-1571.
8. Mariathasan S, Monack DM, (2007) Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 7: 31-40.
9. Qu Y, Franchi L, Nunez G, Dubyak GR, (2007) Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J Immunol 179: 1913-1925.
10. Tschopp J, Martinon F, Burns K, (2003) NALPs: a novel protein family involved in inflammation. Nat Rev Mol Cell Biol 4: 95-104.
11. Dinarello CA, (1996) Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147.
12. Martinon F, Burns K, Tschopp J, (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10: 417-426.
13. Burckstummer T, Baumann C, Bluml S, Dixit E, Durnberger G, et al. (2009) An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10: 266-272.
14. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES, (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458: 509-513.
15. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, et al. (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458: 514-518.
16. Roberts TL, Idris A, Dunn JA, Kelly GM, Burnton CM, et al. (2009) HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323: 1057-1060.
17. Meylan E, Tschopp J, Karin M, (2006) Intracellular pattern recognition receptors in the host response. Nature 442: 39-44.
18. 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.
19. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, et al. (2010) NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464: 1357-1361.
20. 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.
21. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J, (2006) Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241.
22. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, et al. (2008) Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320: 674-677.
23. Zhou R, Yazdi AS, Menu P, Tschopp J, (2010) A role for mitochondria in NLRP3 inflammasome activation. Nature 469: 221-225.
24. 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.
25. Morishige T, Yoshioka Y, Inakura H, Tanabe A, Yao X, et al. (2010) The effect of surface modification of amorphous silica particles on NLRP3 inflammasome mediated IL-1beta production, ROS production and endosomal rupture. Biomaterials 31: 6833-6842.
26. Martinon F, (2010) Signaling by ROS drives inflammasome activation. Eur J Immunol 40: 616-619.
27. Schroder K, Zhou R, Tschopp J, (2010) The NLRP3 inflammasome: a sensor for metabolic danger? Science 327: 296-300.
28. Martinon F, Agostini L, Meylan E, Tschopp J, (2004) Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr Biol 14: 1929-1934.
29. 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.
30. Vinzing M, Eitel J, Lippmann J, Hocke AC, Zahlten J, et al. (2008) NAIP and Ipaf control Legionella pneumophila replication in human cells. J Immunol 180: 6808-6815.
31. Akhter A, Gavrilin MA, Frantz L, Washington S, Ditty C, et al. (2009) Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog 5: e1000361.
32. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, et al. (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213-218.
33. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, et al. (2010) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 107: 3076-3080.
34. Sutterwala FS, Mijares LA, Li L, Ogura Y, Kazmierczak BI, et al. (2007) Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J Exp Med 204: 3235-3245.
35. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozoren N, et al. (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7: 576-582.
36. Kumar H, Kumagai Y, Tsuchida T, Koenig PA, Satoh T, et al. (2009) Involvement of the NLRP3 inflammasome in innate and humoral adaptive immune responses to fungal beta-glucan. J Immunol 183: 8061-8067.
37. 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.
38. Basu S, Quilici C, Zhang HH, Grail D, Dunn AR, (2008) Mice lacking both G-CSF and IL-6 are more susceptible to Candida albicans infection: critical role of neutrophils in defense against Candida albicans. Growth Factors 26: 23-34.
39. Greenblatt MB, Aliprantis A, Hu B, Glimcher LH, (2010) Calcineurin regulates innate antifungal immunity in neutrophils. J Exp Med 207: 923-931.
40. Hope WW, Drusano GL, Moore CB, Sharp A, Louie A, et al. (2007) Effect of neutropenia and treatment delay on the response to antifungal agents in experimental disseminated candidiasis. Antimicrob Agents Chemother 51: 285-295.
41. Huang W, Na L, Fidel PL, Schwarzenberger P, (2004) Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 190: 624-631.
42. Conti HR, Shen F, Nayyar N, Stocum E, Sun JN, et al. (2009) Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med 206: 299-311.
43. van de Veerdonk FL, Marijnissen RJ, Kullberg BJ, Koenen HJ, Cheng SC, et al. (2009) The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5: 329-340.
44. Zelante T, De Luca A, Bonifazi P, Montagnoli C, Bozza S, et al. (2007) IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur J Immunol 37: 2695-2706.
45. LeibundGut-Landmann S, Gross O, Robinson MJ, Osorio F, Slack EC, et al. (2007) Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol 8: 630-638.
46. Feng Z, Jiang B, Chandra J, Ghannoum M, Nelson S, et al. (2005) Human beta-defensins: differential activity against candidal species and regulation by Candida albicans. J Dent Res 84: 445-450.
47. Bals R, (2000) Epithelial antimicrobial peptides in host defense against infection. Respiratory Research 1: 141-150.
48. Doss M, White MR, Tecle T, Hartshorn KL, (2010) Human defensins and LL-37 in mucosal immunity. J Leukoc Biol 87: 79-92.
49. Elssner A, Duncan M, Gavrilin M, Wewers MD, (2004) A novel P2X7 receptor activator, the human cathelicidin-derived peptide LL37, induces IL-1 beta processing and release. J Immunol 172: 4987-4994.
50. Yamamoto Y, Klein TW, Friedman H, Kimura S, Yamaguchi H, (1993) Granulocyte colony-stimulating factor potentiates anti-Candida albicans growth inhibitory activity of polymorphonuclear cells. FEMS Immunol Med Microbiol 7: 15-22.
51. Saunus JM, Wagner SA, Matias MA, Hu Y, Zaini ZM, et al. (2010) Early activation of the interleukin-23-17 axis in a murine model of oropharyngeal candidiasis. Mol Oral Microbiol 25: 343-356.
52. Drygin D, Koo S, Perera R, Barone S, Bennett CF, (2005) Induction of toll-like receptors and NALP/PAN/PYPAF family members by modified oligonucleotides in lung epithelial carcinoma cells. Oligonucleotides 15: 105-118.
53. McCall SH, Sahraei M, Young AB, Worley CS, Duncan JA, et al. (2008) Osteoblasts express NLRP3, a nucleotide-binding domain and leucine-rich repeat region containing receptor implicated in bacterially induced cell death. J Bone Miner Res 23: 30-40.
54. Dinarello CA, (1992) The biology of interleukin-1. Chem Immunol 51: 1-32.
55. Dinarello CA, (1997) Proinflammatory and anti-inflammatory cytokines as mediators in the pathogenesis of septic shock. Chest 112: 321S-329S.
56. Glaccum MB, Stocking KL, Charrier K, Smith JL, Willis CR, et al. (1997) Phenotypic and functional characterization of mice that lack the type I receptor for IL-1. J Immunol 159: 3364-3371.
57. Dinarello CA, (2000) Interleukin-18, a proinflammatory cytokine. Eur Cytokine Netw 11: 483-486.
58. Fantuzzi G, Dinarello CA, (1999) Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol 19: 1-11.
59. Omoto Y, Yamanaka K, Tokime K, Kitano S, Kakeda M, et al. (2010) Granzyme B is a novel interleukin-18 converting enzyme. J Dermatol Sci 59: 129-135.
60. Omoto Y, Tokime K, Yamanaka K, Habe K, Morioka T, et al. (2006) Human mast cell chymase cleaves pro-IL-18 and generates a novel and biologically active IL-18 fragment. J Immunol 177: 8315-8319.
61. Ghosh S, Howe N, Volk K, Tati S, Nickerson KW, et al. (2010) Candida albicans cell wall components and farnesol stimulate the expression of both inflammatory and regulatory cytokines in the murine RAW264.7 macrophage cell line. FEMS Immunol Med Microbiol 60: 63-73.
62. Kullberg BJ, Netea MG, Vonk AG, van der Meer JW, (1999) Modulation of neutrophil function in host defense against disseminated Candida albicans infection in mice. FEMS Immunol Med Microbiol 26: 299-307.
63. Rego D, Kumar A, Nilchi L, Wright K, Huang S, et al. (2011) IL-6 Production Is Positively Regulated by Two Distinct Src Homology Domain 2-Containing Tyrosine Phosphatase-1 (SHP-1)-Dependent CCAAT/Enhancer-Binding Protein {beta} and NF-{kappa}B Pathways and an SHP-1-Independent NF-{kappa}B Pathway in Lipopolysaccharide-Stimulated Bone Marrow-Derived Macrophages. J Immunol 186: 5443-5456.
64. Su L, Zhao Z, Bouchard P, Banville D, Fischer EH, et al. (1996) Positive effect of overexpressed protein-tyrosine phosphatase PTP1C on mitogen-activated signaling in 293 cells. J Biol Chem 271: 10385-10390.
65. Atkinson KJ, Rao RK, (2001) Role of protein tyrosine phosphorylation in acetaldehyde-induced disruption of epithelial tight junctions. Am J Physiol Gastrointest Liver Physiol 280: G1280-1288.
66. Valore EV, Park CH, Quayle AJ, Wiles KR, McCray PB Jr, et al. (1998) Human beta-defensin-1: an antimicrobial peptide of urogenital tissues. J Clin Invest 101: 1633-1642.
67. McCray PB Jr, Bentley L, (1997) Human airway epithelia express a beta-defensin. Am J Respir Cell Mol Biol 16: 343-349.
68. Goldman MJ, Anderson GM, Stolzenberg ED, Kari UP, Zasloff M, et al. (1997) Human beta-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 88: 553-560.
69. Smith JJ, Travis SM, Greenberg EP, Welsh MJ, (1996) Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell 85: 229-236.
70. Braida L, Boniotto M, Pontillo A, Tovo PA, Amoroso A, et al. (2004) A single-nucleotide polymorphism in the human beta-defensin 1 gene is associated with HIV-1 infection in Italian children. Aids 18: 1598-1600.
71. Milanese M, Segat L, Pontillo A, Arraes LC, de Lima Filho JL, et al. (2006) DEFB1 gene polymorphisms and increased risk of HIV-1 infection in Brazilian children. Aids 20: 1673-1675.
72. Segat L, Milanese M, Boniotto M, Crovella S, Bernardon M, et al. (2006) DEFB-1 genetic polymorphism screening in HIV-1 positive pregnant women and their children. J Matern Fetal Neonatal Med 19: 13-16.
73. Hu RC, Xu YJ, Zhang ZX, Ni W, Chen SX, (2004) Correlation of HDEFB1 polymorphism and susceptibility to chronic obstructive pulmonary disease in Chinese Han population. Chin Med J (Engl) 117: 1637-1641.
74. Kocsis AK, Lakatos PL, Somogyvari F, Fuszek P, Papp J, et al. (2008) Association of beta-defensin 1 single nucleotide polymorphisms with Crohn's disease. Scand J Gastroenterol 43: 299-307.
75. Bals R, Goldman MJ, Wilson JM, (1998) Mouse beta-defensin 1 is a salt-sensitive antimicrobial peptide present in epithelia of the lung and urogenital tract. Infect Immun 66: 1225-1232.
76. Schroder JM, Harder J, (1999) Human beta-defensin-2. Int J Biochem Cell Biol 31: 645-651.
77. Joly S, Maze C, McCray PB Jr, Guthmiller JM, (2004) Human beta-defensins 2 and 3 demonstrate strain-selective activity against oral microorganisms. J Clin Microbiol 42: 1024-1029.
78. Singh PK, Jia HP, Wiles K, Hesselberth J, Liu L, et al. (1998) Production of beta-defensins by human airway epithelia. Proc Natl Acad Sci USA 95: 14961-14966.
79. Quinones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, et al. (2003) Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. Aids 17: F39-48.
80. Weinberg A, Quinones-Mateu ME, Lederman MM, (2006) Role of human beta-defensins in HIV infection. Adv Dent Res 19: 42-48.
81. Morrison GM, Davidson DJ, Dorin JR, (1999) A novel mouse beta defensin, Defb2, which is upregulated in the airways by lipopolysaccharide. FEBS Lett 442: 112-116.
82. Rohrl J, Yang D, Oppenheim JJ, Hehlgans T, (2008) Identification and Biological Characterization of Mouse beta-defensin 14, the orthologue of human beta-defensin 3. J Biol Chem 283: 5414-5419.
83. den Hertog AL, van Marle J, van Veen HA, Van't Hof W, Bolscher JG, et al. (2005) Candidacidal effects of two antimicrobial peptides: histatin 5 causes small membrane defects, but LL-37 causes massive disruption of the cell membrane. Biochem J 388: 689-695.
84. den Hertog AL, van Marle J, Veerman EC, Valentijn-Benz M, Nazmi K, et al. (2006) The human cathelicidin peptide LL-37 and truncated variants induce segregation of lipids and proteins in the plasma membrane of Candida albicans. Biol Chem 387: 1495-1502.
85. Turner J, Cho Y, Dinh NN, Waring AJ, Lehrer RI, (1998) Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob Agents Chemother 42: 2206-2214.
86. Andersson E, Rydengard V, Sonesson A, Morgelin M, Bjorck L, et al. (2004) Antimicrobial activities of heparin-binding peptides. Eur J Biochem 271: 1219-1226.
87. Lopez-Garcia B, Lee PH, Yamasaki K, Gallo RL, (2005) Anti-fungal activity of cathelicidins and their potential role in Candida albicans skin infection. J Invest Dermatol 125: 108-115.
88. Kanda N, Ishikawa T, Kamata M, Tada Y, Watanabe S, (2010) Increased serum leucine, leucine-37 levels in psoriasis: positive and negative feedback loops of leucine, leucine-37 and pro- or anti-inflammatory cytokines. Hum Immunol 71: 1161-1171.
89. Nagaoka I, Tamura H, Hirata M, (2006) An antimicrobial cathelicidin peptide, human CAP18/LL-37, suppresses neutrophil apoptosis via the activation of formyl-peptide receptor-like 1 and P2X7. J Immunol 176: 3044-3052.
90. Tomasinsig L, Pizzirani C, Skerlavaj B, Pellegatti P, Gulinelli S, et al. (2008) The human cathelicidin LL-37 modulates the activities of the P2X7 receptor in a structure-dependent manner. J Biol Chem 283: 30471-30481.
91. Broz P, Newton K, Lamkanfi M, Mariathasan S, Dixit VM, et al. (2010) Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J Exp Med 207: 1745-1755.
92. Schroeder GN, Jann NJ, Hilbi H, (2007) Intracellular type III secretion by cytoplasmic Shigella flexneri promotes caspase-1-dependent macrophage cell death. Microbiology 153: 2862-2876.
93. Suzuki T, Franchi L, Toma C, Ashida H, Ogawa M, et al. (2007) Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog 3: e111.
94. Amer A, Franchi L, Kanneganti TD, Body-Malapel M, Ozoren N, et al. (2006) Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J Biol Chem 281: 35217-35223.
95. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, et al. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7: 569-575.
96. Franchi L, Stoolman J, Kanneganti TD, Verma A, Ramphal R, et al. (2007) Critical role for Ipaf in Pseudomonas aeruginosa-induced caspase-1 activation. Eur J Immunol 37: 3030-3039.