IL-18 induces emphysema and airway and vascular remodeling via IFN-γ, IL-17A, and IL-13

American Journal of Respiratory and Critical Care Medicine

Volumn 185, Issue 11, 2012, Pages 1205-1217

  Kang, Min Jong ^a   Choi, Je Min ^b   Kim, Bo Hye ^a   Lee, Chang Min ^a   Cho, Won Kyung ^a   Choe, Gina ^a   Kim, Do Hyun ^b   Lee, Chun Geun ^a   Elias, Jack A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Hanyang University   (South Korea)

Author keywords

Airway fibrosis; Chronic obstructive pulmonary disease; IL 18; Mucus metaplasia; Vascular remodeling

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 18;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CYTOTOXICITY; EMPHYSEMA; EOSINOPHIL; HEART VENTRICLE HYPERTROPHY; LUNG FIBROSIS; MACROPHAGE; METAPLASIA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

AIRWAY RESISTANCE; ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; IMMUNOBLOTTING; IN SITU NICK-END LABELING; INTERLEUKIN-13; INTERLEUKIN-17; INTERLEUKIN-18; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY EMPHYSEMA; RANDOM ALLOCATION; RNA, MESSENGER; STATISTICS, NONPARAMETRIC;

EID: 84861777306     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201108-1545OC     Document Type: Article

References (68)

1. Senior RM, Shapiro SD. Chronic obstructive pulmonary disease: epidemiology, pathophysiology, and pathogenesis. In: Fishman AP, Elias JA, Fishman JA, Grippi MA, Kaiser LR, Senior RM, editors. Fishman's pulmonary diseases and disorders. New York: McGraw-Hill; 1998; pp. 659-681.
2. Wang Z, Zheng T, Zhu Z, Homer RJ, Riese RJ, Chapman HA Jr, Shapiro SD, Elias JA. Interferon gamma induction of pulmonary emphysema in the adult murine lung. J Exp Med 2000;192:1587-1600.
3. Rabe KF, Hurd S, Anzueto A, Barnes PJ, Buist SA, Calverley P, Fukuchi Y, Jenkins C, Rodriguez-Roisin R, van Weel C, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 2007;176:532-555. (Pubitemid 47403272)
4. Calverley PM. COPD: what is the unmet need? Br J Pharmacol 2008; 155:487-493.
5. Larsson K. Aspects on pathophysiological mechanisms in COPD. J Intern Med 2007;262:311-340. (Pubitemid 47246974)
6. Hogg JC. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet 2004;364:709-721. (Pubitemid 39140629)
7. Hogg JC, Timens W. The pathology of chronic obstructive pulmonary disease. Annu Rev Pathol 2009;4:435-459.
8. Barbera JA, Blanco I. Pulmonary hypertension in patients with chronic obstructive pulmonary disease: advances in pathophysiology and management. Drugs 2009;69:1153-1171.
9. Magee F, Wright JL, Wiggs BR, Pare PD, Hogg JC. Pulmonary vascular structure and function in chronic obstructive pulmonary disease. Thorax 1988;43:183-189. (Pubitemid 18086542)
10. O'Shaughnessy TC, Ansari TW, Barnes NC, Jeffery PK. Inflammation in bronchial biopsies of subjects with chronic bronchitis: inverse relationship of CD8+ T lymphocytes with FEV1. Am J Respir Crit Care Med 1997;155:852-857. (Pubitemid 27133393)
11. Cosio MG, Guerassimov A. Chronic obstructive pulmonary disease. Inflammation of small airways and lung parenchyma. Am J Respir Crit Care Med 1999;160:S21-S25.
12. Saetta M, Baraldo S, Corbino L, Turato G, Braccioni F, Rea F, Cavallesco G, Tropeano G, Mapp CE, Maestrelli P, et al. CD8+ve cells in the lungs of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999;160:711-717. (Pubitemid 29380694)
13. Saetta M, Turato G, Maestrelli P, Mapp CE, Fabbri LM. Cellular and structural bases of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001;163:1304-1309. (Pubitemid 32506590)
14. Sutherland ER, Cherniack RM. Management of chronic obstructive pulmonary disease. N Engl J Med 2004;350:2689-2697.
15. Yao H, Rahman I. Current concepts on the role of inflammation in COPD and lung cancer. Curr Opin Pharmacol 2009;9:375-383.
16. Pauwels RA, Buist AS, Calverley PM, Jenkins CR, Hurd SS. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) Workshop summary. Am J Respir Crit Care Med 2001;163:1256-1276. (Pubitemid 32378468)
17. Saetta M, Mariani M, Panina-Bordignon P, Turato G, Buonsanti C, Baraldo S, Bellettato CM, Papi A, Corbetta L, Zuin R, et al. Increased expression of the chemokine receptor CXCR3 and its ligand CXCL10 in peripheral airways of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2002;165:1404-1409. (Pubitemid 34522945)
18. Grumelli S, Corry DB, Song LZ, Song L, Green L, Huh J, Hacken J, Espada R, Bag R, Lewis DE, et al. An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Med 2004;1:e8.
19. Barczyk A, Pierzchala W, Kon OM, Cosio B, Adcock IM, Barnes PJ. Cytokine production by bronchoalveolar lavage T lymphocytes in chronic obstructive pulmonary disease. J Allergy Clin Immunol 2006;117:1484-1492. (Pubitemid 43795735)
20. Zhu X, Gadgil AS, Givelber R, George MP, Stoner MW, Sciurba FC, Duncan SR. Peripheral T cell functions correlate with the severity of chronic obstructive pulmonary disease. J Immunol 2009;182:3270-3277.
21. Di Stefano A, Caramori G, Gnemmi I, Contoli M, Vicari C, Capelli A, Magno F, D'Anna SE, Zanini A, Brun P, et al. T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin Exp Immunol 2009;157:316-324.
22. Nakanishi K, Yoshimoto T, Tsutsui H, Okamura H. Interleukin-18 regulates both Th1 and Th2 responses. Annu Rev Immunol 2001;19:423-474. (Pubitemid 32368042)
23. Gracie JA, Robertson SE, McInnes IB. Interleukin-18. J Leukoc Biol 2003;73:213-224. (Pubitemid 36158296)
24. Dinarello CA. Interleukin-18 and the pathogenesis of inflammatory diseases. Semin Nephrol 2007;27:98-114.
25. Sakai A, Sugawara Y, Kuroishi T, Sasano T, Sugawara S. Identification of IL-18 and Th17 cells in salivary glands of patients with Sjogren's syndrome, and amplification of IL-17-mediated secretion of inflammatory cytokines from salivary gland cells by IL-18. J Immunol 2008;181:2898-2906.
26. Boraschi D, Dinarello CA. IL-18 in autoimmunity [review]. Eur Cytokine Netw 2006;17:224-252.
27. Kang MJ, Homer RJ, Gallo A, Lee CG, Crothers KA, Cho SJ, Rochester C, Cain H, Chupp G, Yoon HJ, et al. IL-18 is induced and IL-18 receptor alpha plays a critical role in the pathogenesis of cigarette smoke-induced pulmonary emphysema and inflammation. J Immunol 2007;178:1948-1959. (Pubitemid 46154668)
28. Imaoka H, Hoshino T, Takei S, Kinoshita T, Okamoto M, Kawayama T, Kato S, Iwasaki H, Watanabe K, Aizawa H. Interleukin-18 production and pulmonary function in COPD. Eur Respir J 2008;31:287-297.
29. Rovina N, Dima E, Gerassimou C, Kollintza A, Gratziou C, Roussos C. Interleukin-18 in induced sputum: association with lung function in chronic obstructive pulmonary disease. Respir Med 2009;103:1056-1062.
30. Kang MJ, Choi JM, Lee CG, Elias JA. Interleukin-18 induces pulmonary inflammation and remodeling via an interleukin-17-dependent pathway. Presented at the American Thoracic Society International Conference. May 14-18, 2010, New Orleans, LA. Abstract 3994.
31. Ray P, Tang W, Wang P, Homer R, Kuhn C III, Flavell RA, Elias JA. Regulated overexpression of interleukin 11 in the lung: use to dissociate development-dependent and -independent phenotypes. J Clin Invest 1997;100:2501-2511. (Pubitemid 27514889)
32. Lee CG, Link H, Baluk P, Homer RJ, Chapoval S, Bhandari V, Kang MJ, Cohn L, Kim YK, McDonald DM, et al. Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat Med 2004;10:1095-1103. (Pubitemid 39424871)
33. Lee CG, Hartl D, Lee GR, Koller B, Matsuura H, Da Silva CA, Sohn MH, Cohn L, Homer RJ, Kozhich AA, et al. Role of breast regression protein 39 (BRP-39)/chitinase 3-like-1 in Th2 and IL-13-induced tissue responses and apoptosis. J Exp Med 2009;206:1149-1166.
34. Londhe VA, Maisonet TM, Lopez B, Jeng JM, Li C, Minoo P. A subset of epithelial cells with CCSP promoter activity participates in alveolar development. Am J Respir Cell Mol Biol 2011;44:804-812.
35. Hackett BP, Shimizu N, Gitlin JD. Clara cell secretory protein gene expression in bronchiolar epithelium. Am J Physiol 1992;262:L399-L404.
36. Cunningham RE. Tissue disaggregation. Methods Mol Biol 1994;34:225-228.
37. Zhang J, Dong Z, Zhou R, Luo D, Wei H, Tian Z. Isolation of lymphocytes and their innate immune characterizations from liver, intestine, lung and uterus. Cell Mol Immunol 2005;2:271-280.
38. Jaatinen T, Laine J. Isolation of mononuclear cells from human cord blood by Ficoll-Paque density gradient. Curr Protoc Stem Cell Biol 2007;Chapter 2:Unit 2A.1.
39. Kang MJ, Lee CG, Lee JY, Dela Cruz CS, Chen ZJ, Enelow R, Elias JA. Cigarette smoke selectively enhances viral PAMP- and virus-induced pulmonary innate immune and remodeling responses in mice. J Clin Invest 2008;118:2771-2784.
40. Lee CG, Homer RJ, Cohn L, Link H, Jung S, Craft JE, Graham BS, Johnson TR, Elias JA. Transgenic overexpression of interleukin (IL)- 10 in the lung causes mucus metaplasia, tissue inflammation, and airway remodeling via IL-13-dependent and -independent pathways. J Biol Chem 2002;277:35466-35474.
41. Daley E, Emson C, Guignabert C, de Waal Malefyt R, Louten J, Kurup VP, Hogaboam C, Taraseviciene-Stewart L, Voelkel NF, Rabinovitch M, et al. Pulmonary arterial remodeling induced by a Th2 immune response. J Exp Med 2008;205:361-372. (Pubitemid 351281602)
42. Azoulay E, Eddahibi S, Marcos E, Levame M, Harf A, Schlemmer B, Adnot S, Delclaux C. Granulocyte colony-stimulating factor enhances alpha- naphthylthiourea-induced pulmonary hypertension. J Appl Physiol 2003;94:2027-2033. (Pubitemid 36457456)
43. Borchers MT, Wesselkamper SC, Curull V, Ramirez-Sarmiento A, Sanchez-Font A, Garcia-Aymerich J, Coronell C, Lloreta J, Agusti AG, Gea J, et al. Sustained CTL activation by murine pulmonary epithelial cells promotes the development of COPD-like disease. J Clin Invest 2009;119:636-649.
44. Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 2004;350:2645-2653. (Pubitemid 38787999)
45. Peinado VI, Pizarro S, Barbera JA. Pulmonary vascular involvement in COPD. Chest 2008;134:808-814.
46. Wright JL, Levy RD, Churg A. Pulmonary hypertension in chronic obstructive pulmonary disease: current theories of pathogenesis and their implications for treatment. Thorax 2005;60:605-609. (Pubitemid 40966216)
47. Barbera JA, Riverola A, Roca J, Ramirez J, Wagner PD, Ros D, Wiggs BR, Rodriguez-Roisin R. Pulmonary vascular abnormalities and ventilation-perfusion relationships in mild chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1994;149:423-429. (Pubitemid 24068990)
48. Hale KA, Ewing SL, Gosnell BA, Niewoehner DE. Lung disease in long-term cigarette smokers with and without chronic air-flow obstruction. Am Rev Respir Dis 1984;130:716-721. (Pubitemid 15209548)
49. Lee CG, Homer RJ, Zhu Z, Lanone S, Wang X, Koteliansky V, Shipley JM, Gotwals P, Noble P, Chen Q, et al. Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor beta(1). J Exp Med 2001;194:809-821. (Pubitemid 32983016)
50. Brusselle GG, Joos GF, Bracke KR. New insights into the immunology of chronic obstructive pulmonary disease. Lancet 2011;378:1015-1026.
51. Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med 2009;360:2445-2454.
52. Zheng T, Kang MJ, Crothers K, Zhu Z, Liu W, Lee CG, Rabach LA, Chapman HA, Homer RJ, Aldous D, et al. Role of cathepsin S-dependent epithelial cell apoptosis in IFN-gamma-induced alveolar remodeling and pulmonary emphysema. J Immunol 2005;174:8106-8115. (Pubitemid 40806322)
53. Kang MJ, Lee CG, Cho SJ, Homer RJ, Elias JA. IFN-gamma-dependent DNA injury and/or apoptosis are critical in cigarette smoke-induced murine emphysema. Proc Am Thorac Soc 2006;3:517-518. (Pubitemid 44285542)
54. Villalta SA, Deng B, Rinaldi C, Wehling-Henricks M, Tidball JG. IFN-gamma promotes muscle damage in the mdx mouse model of Duchenne muscular dystrophy by suppressing M2 macrophage activation and inhibiting muscle cell proliferation. J Immunol 2011;187:5419-5428.
55. Lawrence T, Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 2011;11:750-761.
56. Snider GL, Lucey EC, Stone PJ. Pitfalls in antiprotease therapy of emphysema. Am J Respir Crit Care Med 1994;150:S131-S137. (Pubitemid 24364337)
57. Amy RW, Bowes D, Burri PH, Haines J, Thurlbeck WM. Postnatal growth of the mouse lung. J Anat 1977;124:131-151. (Pubitemid 8187543)
58. Burri PH. Structural aspects of postnatal lung development: alveolar formation and growth. Biol Neonate 2006;89:313-322. (Pubitemid 43886947)
59. Tang W, Geba GP, Zheng T, Ray P, Homer RJ, Kuhn C III, Flavell RA, Elias JA. Targeted expression of IL-11 in the murine airway causes lymphocytic inflammation, bronchial remodeling, and airways obstruction. J Clin Invest 1996;98:2845-2853. (Pubitemid 26427414)
60. Zhou L, Dey CR, Wert SE, Whitsett JA. Arrested lung morphogenesis in transgenic mice bearing an SP-C-TGF-beta 1 chimeric gene. Dev Biol 1996;175:227-238.
61. Hoshino T, Kato S, Oka N, Imaoka H, Kinoshita T, Takei S, Kitasato Y, Kawayama T, Imaizumi T, Yamada K, et al. Pulmonary inflammation and emphysema: role of the cytokines IL-18 and IL-13. Am J Respir Crit Care Med 2007;176:49-62. (Pubitemid 47048054)
62. Vicencio AG, Lee CG, Cho SJ, Eickelberg O, Chuu Y, Haddad GG, Elias JA. Conditional overexpression of bioactive transforming growth factor-beta1 in neonatal mouse lung: a new model for bronchopulmonary dysplasia? Am J Respir Cell Mol Biol 2004;31:650-656. (Pubitemid 39587495)
63. Celli BR. Roger S. Mitchell lecture. Chronic obstructive pulmonary disease phenotypes and their clinical relevance. Proc Am Thorac Soc 2006;3:461-465. (Pubitemid 44285511)
64. Han MK, Agusti A, Calverley PM, Celli BR, Criner G, Curtis JL, Fabbri LM, Goldin JG, Jones PW, Macnee W, et al. Chronic obstructive pulmonary disease phenotypes: the future of COPD. Am J Respir Crit Care Med 2010;182:598-604.
65. SubPopulations and InteRmediate Outcome Measures In COPD Study (SPIROMICS) [Internet; accessed 2011 Jul 23]. Available from: http://www.fnih.org/work/programs-development/spiromics.
66. Lee JH, Lee YK, Kim EK, Kim TH, Huh JW, Kim WJ, Lee SM, Lee S, Lim SY, Shin TR, et al. Responses to inhaled long-acting beta-agonist and corticosteroid according to COPD subtype. Respir Med 2010;104:542-549.
67. Rennard SI. COPD heterogeneity: what this will mean in practice. Respir Care 2011;56:1181-1187.
68. Walsh GM. Tralokinumab, an anti-IL-13 mAb for the potential treatment of asthma and COPD. Curr Opin Investig Drugs 2010;11:1305-1312.