IL-37 Inhibits Inflammasome Activation and Disease Severity in Murine Aspergillosis

PLoS Pathogens

Volumn 10, Issue 11, 2014, Pages

  Moretti, Silvia ^a   Bozza, Silvia ^a   Oikonomou, Vasilis ^a   Renga, Giorgia ^a   Casagrande, Andrea ^a,b   Iannitti, Rossana G ^a   Puccetti, Matteo ^a   Garlanda, Cecilia ^c   Kim, Soohyun ^d   Li, Suzhao ^d   van de Veerdonk, Frank L ^e   Dinarello, Charles A ^d,e   Romani, Luigina ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; CRYOPYRIN; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; DNA NUCLEOTIDYLEXOTRANSFERASE; GAMMA INTERFERON RECEPTOR 1; GLYCOPROTEIN GP 91; HYDROXYPROLINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INFLAMMASOME; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 4; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 14; MUCIN 1; MUCIN 5AC; MYELOPEROXIDASE; POLYCLONAL ANTIBODY; PROTEIN P47; PROTEIN P67; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 37; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR GATA 3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE; IL1B PROTEIN, MOUSE; IL37 PROTEIN, MOUSE; INTERLEUKIN 1; TIR8 PROTEIN, MOUSE;

ALLERGIC BRONCHOPULMONARY ASPERGILLOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASPERGILLUS FUMIGATUS; CELL COUNT; COLONY FORMING UNIT; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FAST PROTEIN LIQUID CHROMATOGRAPHY; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNOFLUORESCENCE TEST; INFLAMMATION; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; LUNG ASPERGILLOSIS; LUNG LAVAGE; MOUSE; MRNA EXPRESSION ASSAY; NEUTROPHIL CHEMOTAXIS; NICK END LABELING; NONHUMAN; PERIODIC ACID SCHIFF STAIN; PHAGOCYTOSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STEADY STATE; TH17 CELL; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY;

MURINAE;

ANIMALS; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1; INTERLEUKIN-1BETA; MICE; MICE, KNOCKOUT; PULMONARY ASPERGILLOSIS; RECEPTORS, INTERLEUKIN-1;

EID: 84912106429     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004462     Document Type: Article

References (47)

1. Dinarello C, Arend W, Sims J, Smith D, Blumberg H, et al. (2010) IL-1 family nomenclature. Nat Immunol 11: 973.
2. Busfield SJ, Comrack CA, Yu G, Chickering TW, Smutko JS, et al. (2000) Identification and gene organization of three novel members of the IL-1 family on human chromosome 2. Genomics 66: 213–216.
3. Taylor SL, Renshaw BR, Garka KE, Smith DE, Sims JE, (2002) Genomic organization of the interleukin-1 locus. Genomics 79: 726–733.
4. Bufler P, Gamboni-Robertson F, Azam T, Kim SH, Dinarello CA, (2004) Interleukin-1 homologues IL-1F7b and IL-18 contain functional mRNA instability elements within the coding region responsive to lipopolysaccharide. Biochem J 381: 503–510.
5. Dinarello CA, Bufler P, (2013) Interleukin-37. Semin Immunol 25: 466–468.
6. Kumar S, Hanning CR, Brigham-Burke MR, Rieman DJ, Lehr R, et al. (2002) Interleukin-1F7B (IL-1H4/IL-1F7) is processed by caspase-1 and mature IL-1F7B binds to the IL-18 receptor but does not induce IFN-gamma production. Cytokine 18: 61–71.
7. Bufler P, Azam T, Gamboni-Robertson F, Reznikov LL, Kumar S, et al. (2002) A complex of the IL-1 homologue IL-1F7b and IL-18-binding protein reduces IL-18 activity. Proc Natl Acad Sci U S A 99: 13723–13728.
8. Sharma S, Kulk N, Nold MF, Graf R, Kim SH, et al. (2008) The IL-1 family member 7b translocates to the nucleus and down-regulates proinflammatory cytokines. J Immunol 180: 5477–5482.
9. Zuhdi Alimam M, Piazza FM, Selby DM, Letwin N, Huang L, et al. (2000) Muc-5/5ac mucin messenger RNA and protein expression is a marker of goblet cell metaplasia in murine airways. Am J Respir Cell Mol Biol 22: 253–260.
10. Bulau AM, Nold MF, Li S, Petry-Nold CA, Fink M, et al. (2014) The role of caspase 1 in the processing of IL 37 for nuclear translocation, release of the cytokine and the ability of IL 37 to inhibit innate immune responses. Proc Natl Acad Sci U S A 111: 2650–2655.
11. Nold MF, Nold-Petry CA, Zepp JA, Palmer BE, Bufler P, et al. (2010) IL-37 is a fundamental inhibitor of innate immunity. Nat Immunol 11: 1014–1022.
12. Boraschi D, Lucchesi D, Hainzl S, Leitner M, Maier E, et al. (2011) IL-37: a new anti-inflammatory cytokine of the IL-1 family. Eur Cytokine Netw 22: 127–147.
13. Imaeda H, Takahashi K, Fujimoto T, Kasumi E, Ban H, et al. (2013) Epithelial expression of interleukin-37b in inflammatory bowel disease. Clin Exp Immunol 172: 410–416.
14. McNamee EN, Masterson JC, Jedlicka P, McManus M, Grenz A, et al. (2011) Interleukin 37 expression protects mice from colitis. Proc Natl Acad Sci U S A 108: 16711–16716.
15. Bulau AM, Fink M, Maucksch C, Kappler R, Mayr D, et al. (2011) In vivo expression of interleukin-37 reduces local and systemic inflammation in concanavalin A-induced hepatitis. ScientificWorldJournal 11: 2480–2490.
16. Banchereau J, Pascual V, O'Garra A, (2012) From IL-2 to IL-37: the expanding spectrum of anti-inflammatory cytokines. Nat Immunol 13: 925–931.
17. Romani L, (2011) Immunity to fungal infections. Nat Rev Immunol 11: 275–288.
18. Sainz J, Perez E, Gomez-Lopera S, Jurado M, (2008) IL1 gene cluster polymorphisms and its haplotypes may predict the risk to develop invasive pulmonary aspergillosis and modulate C-reactive protein level. J Clin Immunol 28: 473–485.
19. Brieland JK, Jackson C, Menzel F, Loebenberg D, Cacciapuoti A, et al. (2001) Cytokine networking in lungs of immunocompetent mice in response to inhaled Aspergillus fumigatus. Infect Immun 69: 1554–1560.
20. Warris A, Netea MG, Verweij PE, Gaustad P, Kullberg BJ, et al. (2005) Cytokine responses and regulation of interferon-gamma release by human mononuclear cells to Aspergillus fumigatus and other filamentous fungi. Med Mycol 43: 613–621.
21. Bozza S, Zelante T, Moretti S, Bonifazi P, DeLuca A, et al. (2008) Lack of Toll IL-1R8 exacerbates Th17 cell responses in fungal infection. J Immunol 180: 4022–4031.
22. 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.
23. de Luca A, Bozza S, Zelante T, Zagarella S, D'Angelo C, et al. (2010) Non-hematopoietic cells contribute to protective tolerance to Aspergillus fumigatus via a TRIF pathway converging on IDO. Cell Mol Immunol 7: 459–470.
24. Zielinski CE, Mele F, Aschenbrenner D, Jarrossay D, Ronchi F, et al. (2012) Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 484: 514–518.
25. Mehrad B, Strieter RM, Moore TA, Tsai WC, Lira SA, et al. (1999) CXC chemokine receptor-2 ligands are necessary components of neutrophil-mediated host defense in invasive pulmonary aspergillosis. J Immunol 163: 6086–6094.
26. Loeffler J, Ok M, Morton OC, Mezger M, Einsele H, (2010) Genetic polymorphisms in the cytokine and chemokine system: their possible importance in allogeneic stem cell transplantation. Curr Top Microbiol Immunol 341: 83–96.
27. Petrasek J, Bala S, Csak T, Lippai D, Kodys K, et al. (2012) IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice. J Clin Invest 122: 3476–3489.
28. Mao K, Chen S, Chen M, Ma Y, Wang Y, et al. (2013) Nitric oxide suppresses NLRP3 inflammasome activation and protects against LPS-induced septic shock. Cell Res 23: 201–212.
29. Jianjun Y, Zhang R, Lu G, Shen Y, Peng L, et al. (2013) T cell-derived inducible nitric oxide synthase switches off Th17 cell differentiation. J Exp Med 210: 1447–1462.
30. Bonifazi P, D'Angelo C, Zagarella S, Zelante T, Bozza S, et al. (2010) Intranasally delivered siRNA targeting PI3K/Akt/mTOR inflammatory pathways protects from aspergillosis. Mucosal Immunol 3: 193–205.
31. Dinarello CA, Bufler P, (2013) Interleukin-37. Semin Immunol 25: 466–468.
32. Bragonzi A, (2010) Murine models of acute and chronic lung infection with cystic fibrosis pathogens. Int J Med Microbiol 300: 584–593.
33. Cohen TS, Prince A, (2012) Cystic fibrosis: a mucosal immunodeficiency syndrome. Nat Med 18: 509–519.
34. Iannitti RG, Carvalho A, Cunha C, De Luca A, Giovannini G, et al. (2013) Th17/Treg imbalance in murine cystic fibrosis is linked to indoleamine 2,3-dioxygenase deficiency but corrected by kynurenines. Am J Respir Crit Care Med 187: 609–620.
35. 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.
36. 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.
37. Tomalka J, Ganesan S, Azodi E, Patel K, Majmudar P, et al. (2011) A novel role for the NLRC4 inflammasome in mucosal defenses against the fungal pathogen Candida albicans. PLoS Pathog 7: e1002379.
38. Cheng SC, van de Veerdonk FL, Lenardon M, Stoffels M, Plantinga T, et al. (2011) The dectin-1/inflammasome pathway is responsible for the induction of protective T-helper 17 responses that discriminate between yeasts and hyphae of Candida albicans. J Leukoc Biol 90: 357–366.
39. 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.
40. D'Angelo C, De Luca A, Zelante T, Bonifazi P, Moretti S, et al. (2009) Exogenous pentraxin 3 restores antifungal resistance and restrains inflammation in murine chronic granulomatous disease. J Immunol 183: 4609–4618.
41. Villena J, Suzuki R, Fujie H, Chiba E, Takahashi T, et al. (2012) Immunobiotic Lactobacillus jensenii modulates the Toll-like receptor 4-induced inflammatory response via negative regulation in porcine antigen-presenting cells. Clin Vaccine Immunol 19: 1038–1053.
42. 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.
43. Riva F, Bonavita E, Barbati E, Muzio M, Mantovani A, et al. (2012) TIR8/SIGIRR is an Interleukin-1 Receptor/Toll Like Receptor Family Member with Regulatory Functions in Inflammation and Immunity. Front Immunol 3: 322.
44. Ayres JS, Schneider DS, (2012) Tolerance of infections. Annu Rev Immunol 30: 271–294.
45. Zhou L, Dey CR, Wert SE, DuVall MD, Frizzell RA, et al. (1994) Correction of lethal intestinal defect in a mouse model of cystic fibrosis by human CFTR. Science 266: 1705–1708.
46. Sorci G, Giovannini G, Riuzzi F, Bonifazi P, Zelante T, et al. (2011) The danger signal S100B integrates pathogen- and danger-sensing pathways to restrain inflammation. PLoS Pathog 7: e1001315.
47. Bellocchio S, Moretti S, Perruccio K, Fallarino F, Bozza S, et al. (2004) TLRs govern neutrophil activity in aspergillosis. J Immunol 173: 7406–7415.