IL-1 receptor antagonist ameliorates inflammasome-dependent inflammation in murine and human cystic fibrosis

Nature Communications

Volumn 7, Issue , 2016, Pages

  Iannitti, Rossana G ^a   Napolioni, Valerio ^a   Oikonomou, Vasilis ^a   De Luca, Antonella ^a   Galosi, Claudia ^a   Pariano, Marilena ^a   Massi Benedetti, Cristina ^a   Borghi, Monica ^a   Puccetti, Matteo ^a   Lucidi, Vincenzina ^b   Colombo, Carla ^c   Fiscarelli, Ersilia ^b   Lass Flörl, Cornelia ^d   Majo, Fabio ^b   Cariani, Lisa ^c   Russo, Maria ^c   Porcaro, Luigi ^c   Ricciotti, Gabriella ^b   Ellemunter, Helmut ^d   Ratclif, Luigi ^e   De Benedictis, Fernando Maria ^f   Talesa, Vincenzo Nicola ^a   Dinarello, Charles A ^g,h   Van De Veerdonk, Frank L ^g,h   Romani, Luigina ^a   more..

^a UNIVERSITY OF PERUGIA   (Italy)

^b BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^e Ospedale G Tatarella   (Italy)

^f Salesi Children's Hospital of Ancona   (Italy)

^g RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^h UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NLRC4 PROTEIN; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CARRIER PROTEIN; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; CFTR PROTEIN, HUMAN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYTOKINE; IL1RN PROTEIN, HUMAN; IL1RN PROTEIN, MOUSE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; IPAF PROTEIN, MOUSE; NLRC4 PROTEIN, HUMAN; NLRP3 PROTEIN, HUMAN; NLRP3 PROTEIN, MOUSE;

ABNORMALITY; COLONIZATION; DIGESTIVE SYSTEM DISORDER; EPIDEMIOLOGY; GENE EXPRESSION; HOMINID; MICROBIAL ACTIVITY; PATHOGEN; RECOMBINATION; RESPIRATORY DISEASE; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS FUMIGATUS; BACTERIAL LOAD; COMPARATIVE STUDY; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DRUG EFFICACY; FEMALE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; LONGITUDINAL STUDY; LUNG ASPERGILLOSIS; LUNG INFECTION; MAJOR CLINICAL STUDY; MICROBIAL COLONIZATION; MOUSE; NONHUMAN; PATHOGEN CLEARANCE; PNEUMONIA; PROSPECTIVE STUDY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; REGULATORY MECHANISM; ADOLESCENT; ADULT; ANIMAL; ASPERGILLOSIS; AUTOPHAGY; C57BL MOUSE; CELL LINE; CHILD; CYTOLOGY; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOLOGY; INFANT; INFLAMMATION; KNOCKOUT MOUSE; LUNG; MACROPHAGE; MALE; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PRESCHOOL CHILD; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TUNEL ASSAY; WESTERN BLOTTING; YOUNG ADULT;

MURINAE; MUS;

ADOLESCENT; ADULT; ANIMALS; APOPTOSIS REGULATORY PROTEINS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; AUTOPHAGY; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CARD SIGNALING ADAPTOR PROTEINS; CARRIER PROTEINS; CELL LINE; CHILD; CHILD, PRESCHOOL; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INFANT; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; LUNG; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; POLYMORPHISM, SINGLE NUCLEOTIDE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; YOUNG ADULT;

EID: 84961827538     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10791     Document Type: Article

References (71)

1. Cohen, T. S., Prince, A. Cystic fibrosis: a mucosal immunodeficiency syndrome. Nat. Med. 18, 509-519 (2012).
2. Corvol, H. et al. Distinct cytokine production by lung and blood neutrophils from children with cystic fibrosis. Am. J. Physiol. Lung. Cell Mol. Physiol. 284, L997-L1003 (2003).
3. Iannitti, R. G. et al. 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 (2013).
4. Robinson, K. M., Alcorn, J. F. T-cell immunotherapy in cystic fibrosis: weighing the risk/reward. Am. J. Respir. Crit. Care Med. 187, 564-566 (2013).
5. dos Santos, G., Kutuzov, M. A., Ridge, K. M. The inflammasome in lung diseases. Am. J. Physiol. Lung. Cell Mol. Physiol. 303, L627-L633 (2012).
6. De Nardo, D., De Nardo, C. M., Latz, E. New insights into mechanisms controlling the NLRP3 inflammasome and its role in lung disease. Am. J. Pathol. 184, 42-54 (2014).
7. Reiniger, N. et al. Resistance to Pseudomonas aeruginosa chronic lung infection requires cystic fibrosis transmembrane conductance regulator-modulated interleukin-1 (IL-1) release and signaling through the IL-1 receptor. Infect. Immun. 75, 1598-1608 (2007).
8. Tang, A. et al. Inflammasome-mediated IL-1beta production in humans with cystic fibrosis. PLoS ONE 7, e37689 (2012).
9. Osika, E. et al. Distinct sputum cytokine profiles in cystic fibrosis and other chronic inflammatory airway disease. Eur. Respir. J. 14, 339-346 (1999).
10. Basu, R. et al. IL-1 signaling modulates activation of STAT transcription factors to antagonize retinoic acid signaling and control the TH17 cell-iTreg cell balance. Nat. Immunol. 16, 286-295 (2015).
11. Armstead, J., Morris, J., Denning, D. W. Multi-country estimate of different manifestations of aspergillosis in cystic fibrosis. PLoS ONE 9, e98502 (2014).
12. Jones, A. M., Horsley, A., Denning, D. W. What is the importance of classifying Aspergillus disease in cystic fibrosis patients? Expert Rev. Respir. Med. 8, 389-392 (2014).
13. deLuca, A. et al. IL-1 receptor blockade restores autophagy and reduces inflammation in chronic granulomatous disease in mice and in humans. Proc. Natl Acad. Sci. USA 111, 3526-3531 (2014).
14. Moretti, S. et al. IL-37 inhibits inflammasome activation and disease severity in murine aspergillosis. PLoS Pathog. 10, e1004462 (2014).
15. Caffrey, A. K. et al. IL-1alpha signaling is critical for leukocyte recruitment after pulmonary Aspergillus fumigatus challenge. PLoS Pathog. 11, e1004625 (2015).
16. Gresnigt, M. S., van de Veerdonk, F. L. The role of interleukin-1 family members in the host defence against Aspergillus fumigatus. Mycopathologia 178, 395-401 (2014).
17. Franchi, L. et al. Critical role for Ipaf in Pseudomonas aeruginosa-induced caspase-1 activation. Eur. J. Immunol. 37, 3030-3039 (2007).
18. Sutterwala, F. S. et al. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 204, 3235-3245 (2007).
19. Tolle, L. et al. Redundant and cooperative interactions between TLR5 and NLRC4 in protective lung mucosal immunity against Pseudomonas aeruginosa. J. Innate Immun. 7, 177-186 (2015).
20. Rimessi, A. et al. Mitochondrial Ca(2\+)-dependent NLRP3 activation exacerbates the Pseudomonas aeruginosa-driven inflammatory response in cystic fibrosis. Nat. Commun. 6, 6201 (2015).
21. Cohen, T. S., Prince, A. S. Activation of inflammasome signaling mediates pathology of acute P. aeruginosa pneumonia. J. Clin. Invest. 123, 1630-1637 (2013).
22. Faure, E. et al. Pseudomonas aeruginosa type-3 secretion system dampens host defense by exploiting the NLRC4-coupled inflammasome. Am. J. Respir. Crit. Care Med. 189, 799-811 (2014).
23. Said-Sadier, N., Padilla, E., Langsley, G., Ojcius, D. M. Aspergillus fumigatus stimulates the NLRP3 inflammasome through a pathway requiring ROS production and the Syk tyrosine kinase. PLoS ONE 5, e10008 (2010).
24. Karki, R. et al. Concerted activation of the AIM2 and NLRP3 inflammasomes orchestrates host protection against Aspergillus Infection. Cell Host Microbe 17, 357-368 (2015).
25. Qu, Y. et al. Phosphorylation of NLRC4 is critical for inflammasome activation. Nature 490, 539-542 (2012).
26. Broz, P. et al. Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J. Exp. Med. 207, 1745-1755 (2010).
27. Pereira, M. S. et al. Activation of NLRC4 by flagellated bacteria triggers caspase-1-dependent and-independent responses to restrict Legionella pneumophila replication in macrophages and in vivo. J. Immunol. 187, 6447-6455 (2011).
28. Kofoed, E. M., Vance, R. E. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477, 592-595 (2011).
29. Antigny, F., Norez, C., Becq, F., Vandebrouck, C. CFTR and Ca signaling in cystic fibrosis. Front. Pharmacol. 2, 67 (2011).
30. Labbe, K., Saleh, M. Cell death in the host response to infection. Cell Death Differ. 15, 1339-1349 (2008).
31. Veliz Rodriguez, T. et al. Role of Toll interleukin-1 receptor (IL-1R) 8, a negative regulator of IL-1R/Toll-like receptor signaling, in resistance to acute Pseudomonas aeruginosa lung infection. Infect. Immun. 80, 100-109 (2012).
32. Bozza, S. et al. Lack of Toll IL-1R8 exacerbates Th17 cell responses in fungal infection. J. Immunol. 180, 4022-4031 (2008).
33. Man, S. M. et al. Inflammasome activation causes dual recruitment of NLRC4 and NLRP3 to the same macromolecular complex. Proc. Natl Acad. Sci. USA 111, 7403-7408 (2014).
34. Petrasek, J. et al. IL-1 receptor antagonist ameliorates inflammasomedependent alcoholic steatohepatitis in mice. J. Clin. Invest. 122, 3476-3489 (2012).
35. Levine, S. J., Wu, T., Shelhamer, J. H. 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, 5949-5957 (1997).
36. Borghi, M. et al. Pathogenic NLRP3 inflammasome Activity during Candida infection is negatively regulated by IL-22 via activation of NLRC4 and IL-1Ra. Cell Host Microbe 18, 198-209 (2015).
37. Han, S. et al. Lipopolysaccharide primes the NALP3 inflammasome by inhibiting its ubiquitination and degradation mediated by the SCFFBXL2 E3 ligase. J. Biol. Chem. 290, 18124-18133 (2015).
38. Kyrmizi, I. et al. Corticosteroids block autophagy protein recruitment in Aspergillus fumigatus phagosomes via targeting dectin-1/Syk kinase signaling. J. Immunol. 191, 1287-1299 (2013).
39. Martinez, J. et al. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat. Cell Biol. 17, 893-906 (2015).
40. Junkins, R. D., Shen, A., Rosen, K., McCormick, C., Lin, T. J. Autophagy enhances bacterial clearance during P. aeruginosa lung infection. PLoS ONE 8, e72263 (2013).
41. Junkins, R. D., McCormick, C., Lin, T. J. The emerging potential of autophagy-based therapies in the treatment of cystic fibrosis lung infections. Autophagy 10, 538-547 (2014).
42. Glick, D., Barth, S., Macleod, K. F. Autophagy: cellular and molecular mechanisms. J. Pathol. 221, 3-12 (2010).
43. Cross, A. R., Jones, O. T. The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase. Biochem. J. 237, 111-116 (1986).
44. Tomoda, H., Omura, S. Lactacystin, a proteasome inhibitor: discovery and its application in cell biology. Yakugaku Zasshi 120, 935-949 (2000).
45. Lilienbaum, A. Relationship between the proteasomal system and autophagy. Int. J. Biochem. Mol. Biol. 4, 1-26 (2013).
46. Galietta, L. J. et al. Modification of transepithelial ion transport in human cultured bronchial epithelial cells by interferon-gamma. Am. J. Physiol. Lung. Cell Mol. Physiol. 278, L1186-L1194 (2000).
47. Huang, Y. J., Lynch, S. V. The emerging relationship between the airway microbiota and chronic respiratory disease: clinical implications. Expert Rev. Respir. Med. 5, 809-821 (2011).
48. Miao, E. A. et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl Acad. Sci. USA 107, 3076-3080 (2010).
49. Zhao, Y. et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477, 596-600 (2011).
50. Simonin-Le Jeune, K. et al. Impaired functions of macrophage from cystic fibrosis patients: CD11b, TLR-5 decrease and sCD14, inflammatory cytokines increase. PLoS ONE 8, e75667 (2013).
51. Haerynck, F. et al. Genetic variations in toll-like receptor pathway and lung function decline in Cystic fibrosis patients. Hum. Immunol. 74, 1649-1655 (2013).
52. Adamo, R., Sokol, S., Soong, G., Gomez, M. I., Prince, A. Pseudomonas aeruginosa flagella activate airway epithelial cells through asialoGM1 and toll-like receptor 2 as well as toll-like receptor 5. Am. J. Respir. Cell Mol. Biol. 30, 627-634 (2004).
53. Murugappan, S. et al. Molecular mechanism and functional implications of thrombin-mediated tyrosine phosphorylation of PKCdelta in platelets. Blood 106, 550-557 (2005).
54. Wen, H., Miao, E. A., Ting, J. P. Mechanisms of NOD-like receptorassociated inflammasome activation. Immunity 39, 432-441 (2013).
55. Bonfield, T. L., Hodges, C. A., Cotton, C. U., Drumm, M. L. Absence of the cystic fibrosis transmembrane regulator (Cftr) from myeloid-derived cells slows resolution of inflammation and infection. J. Leukoc. Biol. 92, 1111-1122 (2012).
56. Johansson, A. et al. The NLRC4 inflammasome is an important regulator of interleukin-18 levels in patients with acute coronary syndromes: a genome-wide association study in the PLATO trial. Circ.Cardiovasc.Genet. 8, 498-506 (2015).
57. Saldanha, I. J., Akinyede, O., McKoy, N. A., Robinson, K. A. Immunosuppressive drug therapy for preventing rejection following lung transplantation in cystic fibrosis. Cochrane Database Syst Rev 12, CD009421 (2013).
58. Dinarello, C. A., Simon, A., van der Meer, J. W. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat. Rev. Drug Discov. 11, 633-652 (2012).
59. Fritzsching, B. et al. Hypoxic epithelial necrosis triggers neutrophilic inflammation via IL-1 receptor signaling in cystic fibrosis lung disease. Am. J. Respir. Crit. Care Med. 191, 902-913 (2015).
60. Vamvakopoulos, J., Green, C., Metcalfe, S. Genetic control of IL-1beta bioactivity through differential regulation of the IL-1 receptor antagonist. Eur. J. Immunol. 32, 2988-2996 (2002).
61. Zhou, L. et al. Correction of lethal intestinal defect in a mouse model of cystic fibrosis by human CFTR. Science 266, 1705-1708 (1994).
62. Chamberlain, C. S. et al. Interleukin expression after injury and the effects of interleukin-1 receptor antagonist. PLoS ONE 8, e71631 (2013).
63. Bozza, S. et al. Immune sensing of Aspergillus fumigatus proteins, glycolipids, and polysaccharides and the impact on Th immunity and vaccination. J. Immunol. 183, 2407-2414 (2009).
64. Collins, T. J. ImageJ for microscopy. BioTechniques 43, 25-30 (2007).
65. De Luca, A. et al. CD4(\+) T cell vaccination overcomes defective crosspresentation of fungal antigens in a mouse model of chronic granulomatous disease. J. Clin. Invest. 122, 1816-1831 (2012).
66. Jaiswal, D., Trivedi, S., Singh, R., Dada, R., Singh, K. Association of the IL1RN gene VNTR polymorphism with human male infertility. PLoS ONE 7, e51899 (2012).
67. Barrett, J. C., Fry, B., Maller, J., Daly, M. J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265 (2005).
68. Dudbridge, F. Pedigree disequilibrium tests for multilocus haplotypes. Genet. Epidemiol. 25, 115-121 (2003).
69. Lou, X. Y. et al. A generalized combinatorial approach for detecting gene-by-gene and gene-by-environment interactions with application to nicotine dependence. Am. J. Hum. Genet. 80, 1125-1137 (2007).
70. Hahn, L. W., Ritchie, M. D., Moore, J. H. Multifactor dimensionality reduction software for detecting gene-gene and gene-environment interactions. Bioinformatics 19, 376-382 (2003).
71. Perneger, T. V. What's wrong with Bonferroni adjustments. BMJ 316, 1236-1238 (1998).