Pathogenic NLRP3 inflammasome activity during Candida infection is negatively regulated by IL-22 via activation of NLRC4 and IL-1Ra

Cell Host and Microbe

Volumn 18, Issue 2, 2015, Pages 198-209

  Borghi, Monica ^a   De Luca, Antonella ^a   Puccetti, Matteo ^a   Jaeger, Martin ^c   Mencacci, Antonella ^a   Oikonomou, Vasilis ^a   Pariano, Marilena ^a   Garlanda, Cecilia ^b   Moretti, Silvia ^a   Bartoli, Andrea ^a   Sobel, Jack ^d   Van De Veerdonk, Frank L ^c   Dinarello, Charles A ^c,e   Netea, Mihai G ^c   Romani, Luigina ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CARRIER PROTEINS AND BINDING PROTEINS; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 22; NLRC4 PROTEIN; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CARRIER PROTEIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; IPAF PROTEIN, MOUSE; NLRP3 PROTEIN, HUMAN;

ARTICLE; BIOLOGICAL FUNCTIONS; DISEASE PREDISPOSITION; HUMAN; INFLAMMATION; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SUBSTITUTION THERAPY; VAGINA CANDIDIASIS; ANIMAL; ANTAGONISTS AND INHIBITORS; CANDIDA ALBICANS; CANDIDIASIS; DEFICIENCY; IMMUNOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CALCIUM-BINDING PROTEINS; CANDIDA ALBICANS; CANDIDIASIS; CARRIER PROTEINS; HUMANS; INFLAMMASOMES; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKINS; MICE;

EID: 84959346760     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.07.004     Document Type: Article

References (49)

1. J.S. Ayres, N.J. Trinidad, and R.E. Vance Lethal inflammasome activation by a multidrug-resistant pathobiont upon antibiotic disruption of the microbiota Nat. Med. 18 2012 799 806
2. S. Bellocchio, C. Montagnoli, S. Bozza, R. Gaziano, G. Rossi, S.S. Mambula, A. Vecchi, A. Mantovani, S.M. Levitz, and L. Romani 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
3. S. Bozza, T. Zelante, S. Moretti, P. Bonifazi, A. DeLuca, C. D'Angelo, G. Giovannini, C. Garlanda, L. Boon, F. Bistoni, and et al. Lack of Toll IL-1R8 exacerbates Th17 cell responses in fungal infection J. Immunol. 180 2008 4022 4031
4. P. Broz, K. Newton, M. Lamkanfi, S. Mariathasan, V.M. Dixit, and D.M. Monack Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella J. Exp. Med. 207 2010 1745 1755
5. V.M. Bruno, A.C. Shetty, J. Yano, P.L. Fidel Jr., M.C. Noverr, and B.M. Peters Transcriptomic analysis of vulvovaginal candidiasis identifies a role for the NLRP3 inflammasome MBio 6 2015 6 10.1128/mBio.00182-15
6. A. De Luca, T. Zelante, C. D'Angelo, S. Zagarella, F. Fallarino, A. Spreca, R.G. Iannitti, P. Bonifazi, J.C. Renauld, F. Bistoni, and et al. IL-22 defines a novel immune pathway of antifungal resistance Mucosal Immunol. 3 2010 361 373
7. A. De Luca, A. Carvalho, C. Cunha, R.G. Iannitti, L. Pitzurra, G. Giovannini, A. Mencacci, L. Bartolommei, S. Moretti, C. Massi-Benedetti, and et al. IL-22 and IDO1 affect immunity and tolerance to murine and human vaginal candidiasis PLoS Pathog. 9 2013 e1003486
8. M.F. Denning, A.A. Dlugosz, D.W. Threadgill, T. Magnuson, and S.H. Yuspa Activation of the epidermal growth factor receptor signal transduction pathway stimulates tyrosine phosphorylation of protein kinase C delta J. Biol. Chem. 271 1996 5325 5331
9. C.A. Dinarello, and J.W. van der Meer Treating inflammation by blocking interleukin-1 in humans Semin. Immunol. 25 2013 469 484
10. C.A. Dinarello, A. Simon, and J.W. van der Meer Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases Nat. Rev. Drug Discov. 11 2012 633 652
11. P.L. Fidel Jr. Distinct protective host defenses against oral and vaginal candidiasis Med. Mycol. 40 2002 359 375
12. P.L. Fidel Jr. Immunity in vaginal candidiasis Curr. Opin. Infect. Dis. 18 2005 107 111
13. P.L. Fidel Jr. History and update on host defense against vaginal candidiasis Am. J. Reprod. Immunol. 57 2007 2 12
14. L. Franchi, N. Kamada, Y. Nakamura, A. Burberry, P. Kuffa, S. Suzuki, M.H. Shaw, Y.G. Kim, and G. Núñez NLRC4-driven production of IL-1β discriminates between pathogenic and commensal bacteria and promotes host intestinal defense Nat. Immunol. 13 2012 449 456
15. C. Garlanda, C.A. Dinarello, and A. Mantovani The interleukin-1 family: back to the future Immunity 39 2013 1003 1018
16. O. Gross, H. Poeck, M. Bscheider, C. Dostert, N. Hannesschläger, S. Endres, G. Hartmann, A. Tardivel, E. Schweighoffer, V. Tybulewicz, and et al. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence Nature 459 2009 433 436
17. G. Guarda, M. Braun, F. Staehli, A. Tardivel, C. Mattmann, I. Förster, M. Farlik, T. Decker, R.A. Du Pasquier, P. Romero, and J. Tschopp Type I interferon inhibits interleukin-1 production and inflammasome activation Immunity 34 2011 213 223
18. A.G. Hise, J. Tomalka, S. Ganesan, K. Patel, B.A. Hall, G.D. Brown, and K.A. Fitzgerald An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans Cell Host Microbe 5 2009 487 497
19. S. Huber, N. Gagliani, L.A. Zenewicz, F.J. Huber, L. Bosurgi, B. Hu, M. Hedl, W. Zhang, W. O'Connor Jr., A.J. Murphy, and et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine Nature 491 2012 259 263
20. M.S. Jabir, N.D. Ritchie, D. Li, H.K. Bayes, P. Tourlomousis, D. Puleston, A. Lupton, L. Hopkins, A.K. Simon, C. Bryant, and T.J. Evans Caspase-1 cleavage of the TLR adaptor TRIF inhibits autophagy and β-interferon production during Pseudomonas aeruginosa infection Cell Host Microbe 15 2014 214 227
21. S. Joly, and F.S. Sutterwala Fungal pathogen recognition by the NLRP3 inflammasome Virulence 1 2010 276 280
22. S. Joly, N. Ma, J.J. Sadler, D.R. Soll, S.L. Cassel, and F.S. Sutterwala Cutting edge: Candida albicans hyphae formation triggers activation of the Nlrp3 inflammasome J. Immunol. 183 2009 3578 3581
23. E.M. Kofoed, and R.E. Vance Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity Nature 477 2011 592 595
24. A.C. Koppel, A. Kiss, A. Hindes, C.J. Burns, B.L. Marmer, G. Goldberg, M. Blumenberg, and T. Efimova Delayed skin wound repair in proline-rich protein tyrosine kinase 2 knockout mice Am. J. Physiol. Cell Physiol. 306 2014 C899 C909
25. E. Latz, T.S. Xiao, and A. Stutz Activation and regulation of the inflammasomes Nat. Rev. Immunol. 13 2013 397 411
26. T. Leppänen, R. Korhonen, M. Laavola, R. Nieminen, R.K. Tuominen, and E. Moilanen Down-regulation of protein kinase Cδ inhibits inducible nitric oxide synthase expression through IRF1 PLoS ONE 8 2013 e52741
27. S.J. Levine, T. Wu, and J.H. Shelhamer Extracellular release of the type I intracellular IL-1 receptor antagonist from human airway epithelial cells: differential effects of IL-4, IL-13, IFN-gamma, and corticosteroids J. Immunol. 158 1997 5949 5957
28. G.J. Litherland, M.S. Elias, W. Hui, C.D. Macdonald, J.B. Catterall, M.J. Barter, M.J. Farren, M. Jefferson, and A.D. Rowan Protein kinase C isoforms zeta and iota mediate collagenase expression and cartilage destruction via STAT3- and ERK-dependent c-fos induction J. Biol. Chem. 285 2010 22414 22425
29. S.M. Man, L.J. Hopkins, E. Nugent, S. Cox, I.M. Glück, P. Tourlomousis, J.A. Wright, P. Cicuta, T.P. Monie, and C.E. Bryant Inflammasome activation causes dual recruitment of NLRC4 and NLRP3 to the same macromolecular complex Proc. Natl. Acad. Sci. USA 111 2014 7403 7408
30. A. Mencacci, A. Bacci, E. Cenci, C. Montagnoli, S. Fiorucci, A. Casagrande, R.A. Flavell, F. Bistoni, and L. Romani Interleukin 18 restores defective Th1 immunity to Candida albicans in caspase 1-deficient mice Infect. Immun. 68 2000 5126 5131
31. E.A. Miao, D.P. Mao, N. Yudkovsky, R. Bonneau, C.G. Lorang, S.E. Warren, I.A. Leaf, and A. Aderem Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome Proc. Natl. Acad. Sci. USA 107 2010 3076 3080
32. S. Nordlander, J. Pott, and K.J. Maloy NLRC4 expression in intestinal epithelial cells mediates protection against an enteric pathogen Mucosal Immunol. 7 2014 775 785
33. B.M. Peters, G.E. Palmer, A.K. Nash, E.A. Lilly, P.L. Fidel Jr., and M.C. Noverr Fungal morphogenetic pathways are required for the hallmark inflammatory response during Candida albicans vaginitis Infect. Immun. 82 2014 532 543
34. B.M. Peters, J. Yano, M.C. Noverr, and P.L. Fidel Jr. Candida vaginitis: when opportunism knocks, the host responds PLoS Pathog. 10 2014 e1003965
35. J. Petrasek, S. Bala, T. Csak, D. Lippai, K. Kodys, V. Menashy, M. Barrieau, S.Y. Min, E.A. Kurt-Jones, and G. Szabo IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice J. Clin. Invest. 122 2012 3476 3489
36. M.P. Piccinni, A. Vultaggio, C. Scaletti, C. Livi, M.J. Gomez, M.G. Giudizi, R. Biagiotti, A. Cassone, S. Romagnani, and E. Maggi Type 1 T helper cells specific for Candida albicans antigens in peripheral blood and vaginal mucosa of women with recurrent vaginal candidiasis J. Infect. Dis. 186 2002 87 93
37. Y. Qu, S. Misaghi, A. Izrael-Tomasevic, K. Newton, L.L. Gilmour, M. Lamkanfi, S. Louie, N. Kayagaki, J. Liu, L. Kömüves, and et al. Phosphorylation of NLRC4 is critical for inflammasome activation Nature 490 2012 539 542
38. M.E. Reyland Protein kinase C isoforms: Multi-functional regulators of cell life and death Front. Biosci. (Landmark Ed.) 14 2009 2386 2399
39. S.P. Soltoff Rottlerin: an inappropriate and ineffective inhibitor of PKCdelta Trends Pharmacol. Sci. 28 2007 453 458
40. D.J. Taxman, M.T. Huang, and J.P. Ting Inflammasome inhibition as a pathogenic stealth mechanism Cell Host Microbe 8 2010 7 11
41. J. Tomalka, S. Ganesan, E. Azodi, K. Patel, P. Majmudar, B.A. Hall, K.A. Fitzgerald, and A.G. Hise A novel role for the NLRC4 inflammasome in mucosal defenses against the fungal pathogen Candida albicans PLoS Pathog. 7 2011 e1002379
42. A.G. Vonk, M.G. Netea, J.H. van Krieken, Y. Iwakura, J.W. van der Meer, and B.J. Kullberg Endogenous interleukin (IL)-1 alpha and IL-1 beta are crucial for host defense against disseminated candidiasis J. Infect. Dis. 193 2006 1419 1426
43. M. Wellington, K. Koselny, and D.J. Krysan Candida albicans morphogenesis is not required for macrophage interleukin 1β production MBio 4 2012 e00433-12
44. M. Wellington, K. Koselny, F.S. Sutterwala, and D.J. Krysan Candida albicans triggers NLRP3-mediated pyroptosis in macrophages Eukaryot. Cell 13 2014 329 340
45. J. Yano, M.C. Noverr, and P.L. Fidel Jr. Cytokines in the host response to Candida vaginitis: identifying a role for non-classical immune mediators, S100 alarmins Cytokine 58 2012 118 128
46. T. Zelante, R. Iannitti, A. De Luca, and L. Romani IL-22 in antifungal immunity Eur. J. Immunol. 41 2011 270 275
47. T. Zelante, R.G. Iannitti, A. De Luca, J. Arroyo, N. Blanco, G. Servillo, D. Sanglard, U. Reichard, G.E. Palmer, J.P. Latgè, and et al. Sensing of mammalian IL-17A regulates fungal adaptation and virulence Nat. Commun. 3 2012 683
48. T. Zelante, R.G. Iannitti, C. Cunha, A. De Luca, G. Giovannini, G. Pieraccini, R. Zecchi, C. D'Angelo, C. Massi-Benedetti, F. Fallarino, and et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22 Immunity 39 2013 372 385
49. Y. Zhao, J. Yang, J. Shi, Y.N. Gong, Q. Lu, H. Xu, L. Liu, and F. Shao The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus Nature 477 2011 596 600