Genetic deletion of IL-17A reduces cigarette smoke-induced inflammation and alveolar type II cell apoptosis

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 2, 2014, Pages

  Chang, Ying ^a,b   Al Alwan, Laila ^a   Audusseau, Severine ^a   Chouiali, Fazila ^a   Carlevaro Fita, Juna ^a   Iwakura, Yoichiro ^c,d   Baglole, Carolyn J ^a   Eidelman, David H ^a   Hamid, Qutayba ^a  

^a MCGILL UNIVERSITY   (Canada)

^b XI'AN JIAOTONG UNIVERSITY   (China)

^c Tokyo University of Science   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Chronic obstructive pulmonary disease; Interleukin 17

Indexed keywords

CIGARETTE SMOKE; INTERLEUKIN 17; INTERLEUKIN 6; MACROPHAGE ELASTASE; MACROPHAGE INFLAMMATORY PROTEIN 2; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CIGARETTE SMOKE INDUCED INFLAMMATION; CONTROLLED STUDY; FEMALE; GENE DELETION; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; LUNG ALVEOLUS CELL TYPE 2; LUNG ALVEOLUS EPITHELIUM; LUNG LAVAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CHRONIC OBSTRUCTIVE PULMONARY DISEASE; INTERLEUKIN-17;

ANIMALS; APOPTOSIS; BRONCHOALVEOLAR LAVAGE FLUID; CELLS, CULTURED; CHEMOKINE CXCL2; FEMALE; INTERLEUKIN-17; INTERLEUKIN-6; MATRIX METALLOPROTEINASE 12; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; PNEUMONIA; PULMONARY ALVEOLI; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY MUCOSA; SMOKING;

EID: 84892585498     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00111.2013     Document Type: Article

References (52)

1. Baglole CJ, Maggirwar SB, Gasiewicz TA, Thatcher TH, Phipps RP, Sime PJ. The aryl hydrocarbon receptor attenuates tobacco smoke-induced cyclooxygenase-2 and prostaglandin production in lung fibro-blasts through regulation of the NF-kappaB family member RelB. J Biol Chem 283: 28944-28957, 2008.
2. Baglole CJ, Sime PJ, Phipps RP. Cigarette smoke-induced expression of heme oxygenase-1 in human lung fibroblasts is regulated by intracellular glutathione. Am J Physiol Lung Cell Mol Physiol 295: L624-L636, 2008.
3. Barnes PJ. Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease. J Allergy Clin Immunol 131: 636-645, 2013.
4. Barnes PJ. The cytokine network in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 41: 631-638, 2009.
5. Barry M, Bleackley RC. Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol 2: 401-409, 2002.
6. Bartalesi B, Cavarra E, Fineschi S, Lucattelli M, Lunghi B, Martorana PA, Lungarella G. Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants. Eur Respir J 25: 15-22, 2005.
7. Bhowmik A, Seemungal TA, Sapsford RJ, Wedzicha JA. Relation of sputum inflammatory markers to symptoms and lung function changes in COPD exacerbations. Thorax 55: 114-120, 2000.
8. Bucchioni E, Kharitonov SA, Allegra L, Barnes PJ. High levels of interleukin-6 in the exhaled breath condensate of patients with COPD. Respir Med 97: 1299-1302, 2003.
9. Carp H, Janoff A. Possible mechanisms of emphysema in smokers. In vitro suppression of serum elastase-inhibitory capacity by fresh cigarette smoke and its prevention by antioxidants. Am Rev Respir Dis 118: 617-621, 1978.
10. Cazzola M, Matera MG. IL-17 in chronic obstructive pulmonary disease. Expert Rev Respir Med 6: 135-138, 2012.
11. Chang Y, Al-Alwan L, Risse PA, Halayko AJ, Martin JG, Baglole CJ, Eidelman DH, Hamid Q. Th17-associated cytokines promote human airway smooth muscle cell proliferation. FASEB J 26: 5152-5160, 2012.
12. Chang Y, Nadigel J, Boulais N, Bourbeau J, Maltais F, Eidelman DH, Hamid Q. CD8 positive T cells express IL-17 in patients with chronic obstructive pulmonary disease (Abstract). Respir Res 12: 43, 2011.
13. Cosio F, Bermejo-Alvarez MA, Fervienza P, Jimenez LJ, Castanon E, Diaz ML. Temporary trigeminal disorder as a result of pneumocephalus after subarachnoid block. Br J Anaesthesia 91: 430-432, 2003.
14. Demedts IK, Brusselle GG, Bracke KR, Vermaelen KY, Pauwels RA. Matrix metalloproteinases in asthma and COPD. Curr Opin Pharmacol 5: 257-263, 2005.
15. Demedts IK, Demoor T, Bracke KR, Joos GF, Brusselle GG. Role of apoptosis in the pathogenesis of COPD and pulmonary emphysema (Abstract). Respir Res 7: 53, 2006.
16. Devendra G, Spragg RG. Lung surfactant in subacute pulmonary disease (Abstract). Respir Res 3: 19, 2002.
17. Di Stefano A, Caramori G, Gnemmi I, Contoli M, Vicari C, Capelli A, Magno F, D'Anna SE, Zanini A, Brun P, Casolari P, Chung KF, Barnes PJ, Papi A, Adcock I, Balbi B. T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin Exp Immunol 157: 316-324, 2009.
18. Elkington PT, Friedland JS. Matrix metalloproteinases in destructive pulmonary pathology. Thorax 61: 259-266, 2006.
19. Fehrenbach H. Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2: 33-46, 2001.
20. Fossiez F, Djossou O, Chomarat P, Flores-Romo L, Ait-Yahia S, Maat C, Pin JJ, Garrone P, Garcia E, Saeland S, Blanchard D, Gaillard C, Das Mahapatra B, Rouvier E, Golstein P, Banchereau J, Lebecque S. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 183: 2593-2603, 1996.
21. Fujisawa T, Velichko S, Thai P, Hung LY, Huang F, Wu R. Regulation of airway MUC5AC expression by IL-1beta and IL-17A; the NF-kappaB paradigm. J Immunol 183: 6236-6243, 2009.
22. Hodge S, Hodge G, Holmes M, Reynolds PN. Increased airway epithelial and T-cell apoptosis in COPD remains despite smoking cessation. Eur Respir J 25: 447-454, 2005.
23. Hodge S, Hodge G, Scicchitano R, Reynolds PN, Holmes M. Alveolar macrophages from subjects with chronic obstructive pulmonary disease are deficient in their ability to phagocytose apoptotic airway epithelial cells. Immunol Cell Biol 81: 289-296, 2003.
24. Hot A, Miossec P. Effects of interleukin (IL)-17A and IL-17F in human rheumatoid arthritis synoviocytes. Ann Rheum Dis 70: 727-732, 2011.
25. Imai K, Mercer BA, Schulman LL, Sonett JR, D'Armiento JM. Correlation of lung surface area to apoptosis and proliferation in human emphysema. Eur Respir J 25: 250-258, 2005.
26. Jones CE, Chan K. Interleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-alpha, and granulocyte-colony-stimulating factor by human airway epithelial cells. Am J Respir Cell Mol Biol 26: 748-753, 2002.
27. Korn T, Mitsdoerffer M, Croxford AL, Awasthi A, Dardalhon VA, Galileos G, Vollmar P, Stritesky GL, Kaplan MH, Waisman A, Kuchroo VK, Oukka M. IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3 regulatory T cells. Proc Natl Acad Sci USA 105: 18460-18465, 2008.
28. Kramer JM, Gaffen SL. Interleukin-17: a new paradigm in inflammation, autoimmunity, and therapy. J Periodontol 78: 1083-1093, 2007.
29. Lacoste JY, Bousquet J, Chanez P, Van Vyve T, Simony-Lafontaine J, Lequeu N, Vic P, Enander I, Godard P, Michel FB. Eosinophilic and neutrophilic inflammation in asthma, chronic bronchitis, and chronic obstructive pulmonary disease. J Allergy Cli Immunol 92: 537-548, 1993.
30. Lee HT, Kim M, Kim JY, Brown KM, Ham A, D'Agati VD, Mori-Akiyama Y. Critical role of interleukin-17A in murine intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 304: G12-G25, 2013.
31. Liu AN, Mohammed AZ, Rice WR, Fiedeldey DT, Liebermann JS, Whitsett JA, Braciale TJ, Enelow RI. Perforin-independent CD8() T-cell-mediated cytotoxicity of alveolar epithelial cells is preferentially mediated by tumor necrosis factor-alpha: relative insensitivity to Fas ligand. Am J Respir Cell Mol Biol 20: 849-858, 1999.
32. Loverre A, Tataranni T, Castellano G, Divella C, Battaglia M, Ditonno P, Corcelli M, Mangino M, Gesualdo L, Schena FP, Grandaliano G. IL-17 expression by tubular epithelial cells in renal transplant recipients with acute antibody-mediated rejection. Am J Transplantation 11: 1248-1259, 2011.
33. McKinley L, Alcorn JF, Peterson A, Dupont RB, Kapadia S, Logar A, Henry A, Irvin CG, Piganelli JD, Ray A, Kolls JK. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol 181: 4089-4097, 2008.
34. Miyamoto M, Prause O, Sjostrand M, Laan M, Lotvall J, Linden A. Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways. J Immunol 170: 4665-4672, 2003.
35. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, Homma I, Sekikawa K, Asano M, Iwakura Y. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387, 2002.
36. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nature Immunol 6: 1133-1141, 2005.
37. Pauwels RA, Rabe KF. Burden and clinical features of chronic obstructive pulmonary disease (COPD). Lancet 364: 613-620, 2004.
38. Rahman I. Oxidative stress in pathogenesis of chronic obstructive pulmonary disease: cellular and molecular mechanisms. Cell Biochem Biophys 43: 167-188, 2005.
39. Ramage L, Jones AC, Whelan CJ. Induction of apoptosis with tobacco smoke and related products in A549 lung epithelial cells in vitro (Abstract). J Inflamm (Lond) 3: 3, 2006.
40. Rico de Souza A, Zago M, Pollock SJ, Sime PJ, Phipps RP, Baglole CJ. Genetic ablation of the aryl hydrocarbon receptor causes cigarette smoke-induced mitochondrial dysfunction and apoptosis. J Biol Chem 286: 43214-43228, 2011.
41. Ruddy MJ, Shen F, Smith JB, Sharma A, Gaffen SL. Interleukin-17 regulates expression of the CXC chemokine LIX/CXCL5 in osteoblasts: implications for inflammation and neutrophil recruitment. J Leukocyte Biol 76: 135-144, 2004.
42. Schnyder B, Schnyder-Candrian S, Pansky A, Schmitz ML, Heim M, Ryffel B, Moser R. IL-17 reduces TNF-induced Rantes and VCAM-1 expression. Cytokine 31: 191-202, 2005.
43. Segura-Valdez L, Pardo A, Gaxiola M, Uhal BD, Becerril C, Selman M. Upregulation of gelatinases A and B, collagenases 1 and 2, and increased parenchymal cell death in COPD. Chest 117: 684-694, 2000.
44. Shan M, Cheng HF, Song LZ, Roberts L, Green L, Hacken-Bitar J, Huh J, Bakaeen F, Coxson HO, Storness-Bliss C, Ramchandani M, Lee SH, Corry DB, Kheradmand F. Lung myeloid dendritic cells coordinately induce TH1 and TH17 responses in human emphysema. Sci Trans Med 1: 4-10, 2009.
45. Shan M, Yuan X, Song LZ, Roberts L, Zarinkamar N, Seryshev A, Zhang Y, Hilsenbeck S, Chang SH, Dong C, Corry DB, Kheradmand F. Cigarette smoke induction of osteopontin (SPP1) mediates T(H)17 inflammation in human and experimental emphysema. Sci Trans Med 4: 117-119, 2012.
46. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2,-3,-6,-7,-8, and-10 in a caspase-9-dependent manner. J Cell Biol 144: 281-292, 1999.
47. Tanaka S, Yoshimoto T, Naka T, Nakae S, Iwakura Y, Cua D, Kubo M. Natural occurring IL-17 producing T cells regulate the initial phase of neutrophil mediated airway responses. J Immunol 183: 7523-7530, 2009.
48. Thatcher TH, McHugh NA, Egan RW, Chapman RW, Hey JA, Turner CK, Redonnet MR, Seweryniak KE, Sime PJ, Phipps RP. Role of CXCR2 in cigarette smoke-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol 289: L322-L328, 2005.
49. Wuyts A, Haelens A, Proost P, Lenaerts JP, Conings R, Opdenakker G, Van Damme J. Identification of mouse granulocyte chemotactic protein-2 from fibroblasts and epithelial cells. Functional comparison with natural KC and macrophage inflammatory protein-2. J Immunol 157: 1736-1743, 1996.
50. Yao Z, Painter SL, Fanslow WC, Ulrich D, Macduff BM, Spriggs MK, Armitage RJ. Human IL-17: a novel cytokine derived from T cells. J Immunol 155: 5483-5486, 1995.
51. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, Shellito JE, Bagby GJ, Nelson S, Charrier K, Peschon JJ, Kolls JK. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 194: 519-527, 2001.
52. Zhu F, Wang Q, Guo C, Wang X, Cao X, Shi Y, Gao F, Ma C, Zhang L. IL-17 induces apoptosis of vascular endothelial cells: a potential mechanism for human acute coronary syndrome. Clin Immunol 141: 152-160, 2011.