Age-dependent susceptibility to pulmonary fibrosis is associated with NLRP3 inflammasome activation

American Journal of Respiratory Cell and Molecular Biology

Volumn 55, Issue 2, 2016, Pages 252-263

  Stout Delgado, Heather W ^a,b   Cho, Soo Jung ^a   Chu, Sarah G ^c   Mitzel, Dana N ^b   Villalba, Julian ^b,c   El Chemaly, Souheil ^b,c   Ryter, Stefan W ^a,c   Choi, Augustine M K ^a,c   Rosas, Ivan O ^b,c  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Aging; bleomycin; mitochondrial oxidative stress; NLRP3 inflammasome; pulmonary fibrosis

Indexed keywords

BLEOMYCIN; CHEMOKINE RECEPTOR CCR2; COLLAGEN TYPE 1; CRYOPYRIN; ENDOGLIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; REACTIVE OXYGEN METABOLITE; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; NLRP3 PROTEIN, MOUSE;

AGED; AGING; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; ENZYME ACTIVITY; GENE EXPRESSION; HISTOLOGY; LUNG ALVEOLUS MACROPHAGE; LUNG FIBROSIS; LUNG HOMOGENATE; LUNG INJURY; MACROPHAGE; MALE; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; COMPLICATION; DEFICIENCY; DRUG EFFECTS; DRUG INSTILLATION; LUNG; METABOLISM; MITOCHONDRION; PATHOLOGY; PULMONARY FIBROSIS;

AGING; ANIMALS; BLEOMYCIN; DISEASE SUSCEPTIBILITY; INFLAMMASOMES; INSTILLATION, DRUG; INTERLEUKIN-18; INTERLEUKIN-1BETA; LUNG; LUNG INJURY; MACROPHAGES; MALE; MICE, INBRED C57BL; MITOCHONDRIA; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PULMONARY FIBROSIS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84988945057     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2015-0222OC     Document Type: Article

References (49)

1. Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005;309:481-484.
2. Vermulst M, Wanagat J, Kujoth GC, Bielas JH, Rabinovitch PS, Prolla TA, Loeb LA. DNA deletions and clonal mutations drive premature aging in mitochondrial mutator mice. Nat Genet 2008;40:392-394.
3. Howcroft TK, Campisi J, Louis GB, Smith MT, Wise B, Wyss-Coray T, Augustine AD, McElhaney JE, Kohanski R, Sierra F. The role of inflammation in age-related disease. Aging (Albany, NY) 2013;5: 84-93.
4. Navaratnam V, Fleming KM, West J, Smith CJ, Jenkins RG, Fogarty A, Hubbard RB. The rising incidence of idiopathic pulmonary fibrosis in the U.K. Thorax 2011;66:462-467.
5. Bueno M, Lai YC, Romero Y, Brands J, St Croix CM, Kamga C, Corey C, Herazo-Maya JD, Sembrat J, Lee JS, et al. PINK1 deficiency impairs mitochondrial homeostasis and promotes lung fibrosis. J Clin Invest 2015;125:521-538.
6. Selman M, Pardo A. Revealing the pathogenic and aging-related mechanisms of the enigmatic idiopathic pulmonary fibrosis. An integral model. Am J Respir Crit Care Med 2014;189:1161-1172.
7. Gasse P, Mary C, Guenon I, Noulin N, Charron S, Schnyder-Candrian S, Schnyder B, Akira S, Quesniaux VF, Lagente V, et al. IL-1R1/MyD88 signaling and the inflammasome are essential in pulmonary inflammation and fibrosis in mice. J Clin Invest 2007;117:3786-3799.
8. Gasse P, Riteau N, Charron S, Girre S, Fick L, Pétrilli V, Tschopp J, Lagente V, Quesniaux VF, Ryffel B, et al. Uric acid is a danger signal activating NALP3 inflammasome in lung injury inflammation and fibrosis. Am J Respir Crit Care Med 2009;179:903-913.
9. Cassel SL, Eisenbarth SC, Iyer SS, Sadler JJ, Colegio OR, Tephly LA, Carter AB, Rothman PB, Flavell RA, Sutterwala FS. The Nalp3 inflammasome is essential for the development of silicosis. Proc Natl Acad Sci USA 2008;105:9035-9040.
10. Wu J, Yan Z, Schwartz DE, Yu J, Malik AB, Hu G. Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury. J Immunol 2013;190: 3590-3599.
11. Lasithiotaki I, Giannarakis I, Tsitoura E, Samara KD, Margaritopoulos GA, Choulaki C, Vasarmidi E, Tzanakis N, Voloudaki A, Sidiropoulos P, et al. NLRP3 inflammasome expression in idiopathic pulmonary fibrosis and rheumatoid lung. Eur Respir J 2016;47:910-918.
12. Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol 2013;13:397-411.
13. Xu JF, Washko GR, Nakahira K, Hatabu H, Patel AS, Fernandez IE, Nishino M, Okajima Y, Yamashiro T, Ross JC, et al.; COPDGene Investigators. Statins and pulmonary fibrosis: the potential role of NLRP3 inflammasome activation. Am J Respir Crit Care Med 2012; 185:547-556.
14. Liu RM. Oxidative stress, plasminogen activator inhibitor 1, and lung fibrosis. Antioxid Redox Signal 2008;10:303-319.
15. Araki T, Katsura H, Sawabe M, Kida K. A clinical study of idiopathic pulmonary fibrosis based on autopsy studies in elderly patients. Intern Med 2003;42:483-489.
16. Trujillo G, O?Connor EC, Kunkel SL, Hogaboam CM. A novel mechanism for CCR4 in the regulation of macrophage activation in bleomycininduced pulmonary fibrosis. Am J Pathol 2008;172:1209-1221.
17. Wilson MS, Madala SK, Ramalingam TR, Gochuico BR, Rosas IO, Cheever AW, Wynn TA. Bleomycin and IL-1b-mediated pulmonary fibrosis is IL-17A dependent. J Exp Med 2010;207: 535-552.
18. Bitterman PB, Adelberg S, Crystal RG. Mechanisms of pulmonary fibrosis. Spontaneous release of the alveolar macrophage-derived growth factor in the interstitial lung disorders. J Clin Invest 1983;72: 1801-1813.
19. Baran CP, Opalek JM, McMaken S, Newland CA, O?Brien JM Jr, Hunter MG, Bringardner BD, Monick MM, Brigstock DR, Stromberg PC, et al. Important roles for macrophage colonystimulating factor, CC chemokine ligand 2, and mononuclear phagocytes in the pathogenesis of pulmonary fibrosis. Am J Respir Crit Care Med 2007;176:78-89.
20. Gibbons MA, MacKinnon AC, Ramachandran P, Dhaliwal K, Duffin R, Phythian-Adams AT, van Rooijen N, Haslett C, Howie SE, Simpson AJ, et al. Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis. Am J Respir Crit Care Med 2011;184:569-581.
21. Prasse A, Pechkovsky DV, Toews GB, Jungraithmayr W, Kollert F, Goldmann T, Vollmer E, Müller-Quernheim J, Zissel G. A vicious circle of alveolar macrophages and fibroblasts perpetuates pulmonary fibrosis via CCL18. Am J Respir Crit Care Med 2006;173: 781-792.
22. Cui H, Kong Y, Zhang H. Oxidative stress, mitochondrial dysfunction, and aging. J Signal Transduct 2012;2012:646354.
23. Okuma T, Terasaki Y, Kaikita K, Kobayashi H, Kuziel WA, Kawasuji M, Takeya M. C-C chemokine receptor 2 (CCR2) deficiency improves bleomycin-induced pulmonary fibrosis by attenuation of both macrophage infiltration and production of macrophage-derived matrix metalloproteinases. J Pathol 2004;204:594-604.
24. Sutterwala FS, Ogura Y, Szczepanik M, Lara-TejeroM, Lichtenberger GS, Grant EP, Bertin J, Coyle AJ, Galán JE, Askenase PW, et al. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 2006;24: 317-327.
25. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, Muramatsu S, Steinman RM. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992;176:1693-1702.
26. Zhang X, Goncalves R, Mosser DM. The isolation and characterization of murine macrophages. Curr Protoc Immunol 2008;Chapter 14: Unit 14.1.
27. Stout-Delgado HW, Vaughan SE, Shirali AC, Jaramillo RJ, Harrod KS. Impaired NLRP3 inflammasome function in elderly mice during influenza infection is rescued by treatment with nigericin. J Immunol 2012;188:2815-2824.
28. Stout-Delgado HW, Du W, Shirali AC, Booth CJ, Goldstein DR. Aging promotes neutrophil-induced mortality by augmenting IL-17 production during viral infection. Cell Host Microbe 2009;6: 446-456.
29. Stout-Delgado HW, Yang X, Walker WE, Tesar BM, Goldstein DR. Aging impairs IFN regulatory factor 7 up-regulation in plasmacytoid dendritic cells during TLR9 activation. J Immunol 2008;181: 6747-6756.
30. Misharin AV, Morales-Nebreda L, Mutlu GM, Budinger GR, Perlman H. Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am J Respir Cell Mol Biol 2013;49: 503-510.
31. Egger C, Cannet C, Gérard C, Jarman E, Jarai G, Feige A, Suply T, Micard A, Dunbar A, Tigani B, et al. Administration of bleomycin via the oropharyngeal aspiration route leads to sustained lung fibrosis in mice and rats as quantified by UTE-MRI and histology. PLoS One 2013;8:e63432.
32. Redente EF, Jacobsen KM, Solomon JJ, Lara AR, Faubel S, Keith RC, Henson PM, Downey GP, Riches DW. Age and sex dimorphisms contribute to the severity of bleomycin-induced lung injury and fibrosis. Am J Physiol Lung Cell Mol Physiol 2011;301: L510-L518.
33. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
34. Rameshwar P, Chang VT, Gascón P. Implication of CD44 in adhesion-mediated overproduction of TGF-b and IL-1 in monocytes from patients with bone marrow fibrosis. Br J Haematol 1996;93:22-29.
35. Kolb M, Margetts PJ, Anthony DC, Pitossi F, Gauldie J. Transient expression of IL-1b induces acute lung injury and chronic repair leading to pulmonary fibrosis. J Clin Invest 2001;107: 1529-1536.
36. Gauldie J, Kolb M, Sime PJ. A new direction in the pathogenesis of idiopathic pulmonary fibrosis? Respir Res 2002;3:1.
37. Hoshino T, Okamoto M, Sakazaki Y, Kato S, Young HA, Aizawa H. Role of proinflammatory cytokines IL-18 and IL-1b in bleomycin-induced lung injury in humans and mice. Am J Respir Cell Mol Biol 2009;41: 661-670.
38. Segawa S, Goto D, Yoshiga Y, Sugihara M, Hayashi T, Chino Y, Matsumoto I, Ito S, Sumida T. Inhibition of transforming growth factor-b signalling attenuates interleukin (IL)-18 plus IL-2-induced interstitial lung disease in mice. Clin Exp Immunol 2010;160:394-402.
39. Kanneganti TD, Ozören N, Body-Malapel M, Amer A, Park JH, 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 2006;440:233-236.
40. Sutterwala FS, Ogura Y, Zamboni DS, Roy CR, Flavell RA. NALP3: a key player in caspase-1 activation. J Endotoxin Res 2006;12: 251-256.
41. Aimanianda V, Haensler J, Lacroix-Desmazes S, Kaveri SV, Bayry J. Novel cellular and molecular mechanisms of induction of immune responses by aluminum adjuvants. Trends Pharmacol Sci 2009;30: 287-295.
42. Elinav E, Strowig T, Henao-Mejia J, Flavell RA. Regulation of the antimicrobial response by NLR proteins. Immunity 2011;34: 665-679.
43. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011;12:222-230.
44. Lee HC, Wei YH. Mitochondria and aging. Adv Exp Med Biol 2012;942: 311-327.
45. Wallach-Dayan SB, Izbicki G, Cohen PY, Gerstl-Golan R, Fine A, Breuer R. Bleomycin initiates apoptosis of lung epithelial cells by ROS but not by Fas/FasL pathway. Am J Physiol Lung Cell Mol Physiol 2006;290:L790-L796.
46. Brar SS, Meyer JN, Bortner CD, Van Houten B, Martin WJ II. Mitochondrial DNA-depleted A549 cells are resistant to bleomycin. Am J Physiol Lung Cell Mol Physiol 2012;303:L413-L424.
47. Mitroulis I, Skendros P, Ritis K. Targeting IL-1b in disease; the expanding role of NLRP3 inflammasome. Eur J Intern Med 2010;21: 157-163.
48. Richter AG, Perkins GD, Chavda A, Sapey E, Harper L, Thickett DR. Neutrophil chemotaxis in granulomatosis with polyangiitis (Wegener?s) and idiopathic pulmonary fibrosis. Eur Respir J 2011;38: 1081-1088.
49. Okamura H, Tsutsi H, Komatsu T, Yutsudo M, Hakura A, Tanimoto T, Torigoe K, Okura T, Nukada Y, Hattori K, et al. Cloning of a new cytokine that induces IFN-g production by T cells. Nature 1995;378: 88-91.