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Role of Th17 Cell and Autoimmunity in Chronic Obstructive Pulmonary Disease

  • Hong, Seok Chan (Graduate School of Medical Science and Engineering, Biomedical Research Center, KAIST Institute for the BioCentury, Korea Advanced Institute of Science and Technology) ;
  • Lee, Seung-Hyo (Graduate School of Medical Science and Engineering, Biomedical Research Center, KAIST Institute for the BioCentury, Korea Advanced Institute of Science and Technology)
  • Received : 2010.08.05
  • Accepted : 2010.08.13
  • Published : 2010.08.31

Abstract

The molecular mechanisms involved in the pathogenesis of chronic obstructive pulmonary disease (COPD) are poorly defined. Accumulating evidences indicate that chronic inflammatory responses and adaptive immunity play important roles in the development and progression of the disease. Recently, it has been shown that IL-17 producing CD4 T cells, named Th17 cells, which have been implicated in the pathogenesis of several inflammatory and autoimmune diseases, are involved in airway inflammation and COPD. In addition, we and others suggest that autoimmunity may play a critical role in the pathogenesis of COPD. Here, we will review the current understanding of roles of Th17 cells and autoimmune responses in COPD.

Keywords

References

  1. Hogg JC, Timens W: The pathology of chronic obstructive pulmonary disease. Annu Rev Pathol 4;435-459, 2009 https://doi.org/10.1146/annurev.pathol.4.110807.092145
  2. Mathers CD, Loncar D: Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3;e442, 2006 https://doi.org/10.1371/journal.pmed.0030442
  3. Fletcher C, Peto R: The natural history of chronic airflow obstruction. Br Med J 1;1645-1648, 1977 https://doi.org/10.1136/bmj.1.6077.1645
  4. Ind PW: COPD disease progression and airway inflammation: uncoupled by smoking cessation. Eur Respir J 26;764-766, 2005 https://doi.org/10.1183/09031936.05.00102805
  5. Simmons MS, Connett JE, Nides MA, Lindgren PG, Kleerup EC, Murray RP, Bjornson WM, Tashkin DP: Smoking reduction and the rate of decline in FEV(1): results from the Lung Health Study. Eur Respir J 25;1011-1017, 2005 https://doi.org/10.1183/09031936.05.00086804
  6. Chung KF, Adcock IM: Multifaceted mechanisms in COPD: inflammation, immunity, and tissue repair and destruction. Eur Respir J 31;1334-1356, 2008 https://doi.org/10.1183/09031936.00018908
  7. Sharafkhaneh A, Hanania NA, Kim V: Pathogenesis of emphysema: from the bench to the bedside. Proc Am Thorac Soc 5; 475-477, 2008 https://doi.org/10.1513/pats.200708-126ET
  8. Taraseviciene-Stewart L, Voelkel NF: Molecular pathogenesis of emphysema. J Clin Invest 118;394-402, 2008 https://doi.org/10.1172/JCI31811
  9. Tuder RM, Yoshida T, Arap W, Pasqualini R, Petrache I: State of the art. Cellular and molecular mechanisms of alveolar destruction in emphysema: an evolutionary perspective. Proc Am Thorac Soc 3;503-510, 2006 https://doi.org/10.1513/pats.200603-054MS
  10. Motz GT, Eppert BL, Sun G, Wesselkamper SC, Linke MJ, Deka R, Borchers MT: Persistence of lung CD8 T cell oligoclonal expansions upon smoking cessation in a mouse model of cigarette smoke-induced emphysema. J Immunol 181;8036-8043, 2008 https://doi.org/10.4049/jimmunol.181.11.8036
  11. Motz GT, Eppert BL, Wesselkamper SC, Flury JL, Borchers MT: Chronic cigarette smoke exposure generates pathogenic T cells capable of driving COPD-like disease in Rag2-/- mice. Am J Respir Crit Care Med 181;1223-1233, 2010 https://doi.org/10.1164/rccm.200910-1485OC
  12. Sullivan AK, Simonian PL, Falta MT, Mitchell JD, Cosgrove GP, Brown KK, Kotzin BL, Voelkel NF, Fontenot AP: Oligoclonal CD4+ T cells in the lungs of patients with severe emphysema. Am J Respir Crit Care Med 172;590-596, 2005 https://doi.org/10.1164/rccm.200410-1332OC
  13. Lee SH, Goswami S, Grudo A, Song LZ, Bandi V, Goodnight- White S, Green L, Hacken-Bitar J, Huh J, Bakaeen F, Coxson HO, Cogswell S, Storness-Bliss C, Corry DB, Kheradmand F: Antielastin autoimmunity in tobacco smoking-induced emphysema. Nat Med 13;567-569, 2007 https://doi.org/10.1038/nm1583
  14. Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, Pare PD: The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 350;2645-2653, 2004 https://doi.org/10.1056/NEJMoa032158
  15. Baraldo S, Turato G, Badin C, Bazzan E, Beghe B, Zuin R, Calabrese F, Casoni G, Maestrelli P, Papi A, Fabbri LM, Saetta M: Neutrophilic infiltration within the airway smooth muscle in patients with COPD. Thorax 59;308-312, 2004 https://doi.org/10.1136/thx.2003.012146
  16. Keatings VM, Collins PD, Scott DM, Barnes PJ: Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. Am J Respir Crit Care Med 153;530-534, 1996 https://doi.org/10.1164/ajrccm.153.2.8564092
  17. Keatings VM, Collins PD, Scott DM, Barnes PJ: Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. Am J Respir Crit Care Med 153;530-534, 1996 https://doi.org/10.1164/ajrccm.153.2.8564092
  18. Shapiro SD, Goldstein NM, Houghton AM, Kobayashi DK, Kelley D, Belaaouaj A: Neutrophil elastase contributes to cigarette smoke-induced emphysema in mice. Am J Pathol 163; 2329-2335, 2003 https://doi.org/10.1016/S0002-9440(10)63589-4
  19. Voynow JA, Young LR, Wang Y, Horger T, Rose MC, Fischer BM: Neutrophil elastase increases MUC5AC mRNA and protein expression in respiratory epithelial cells. Am J Physiol 276; L835-843, 1999
  20. Barnes PJ: Alveolar macrophages as orchestrators of COPD. COPD 1;59-70, 2004 https://doi.org/10.1081/COPD-120028701
  21. Churg A, Wright JL: Proteases and emphysema. Curr Opin Pulm Med 11;153-159, 2005 https://doi.org/10.1097/01.mcp.0000149592.51761.e3
  22. Russell RE, Thorley A, Culpitt SV, Dodd S, Donnelly LE, Demattos C, Fitzgerald M, Barnes PJ: Alveolar macrophage- mediated elastolysis: roles of matrix metalloproteinases, cysteine, and serine proteases. Am J Physiol Lung Cell Mol Physiol 283;L867-873, 2002 https://doi.org/10.1152/ajplung.00020.2002
  23. Finlay GA, Russell KJ, McMahon KJ, D'arcy EM, Masterson JB, FitzGerald MX, O'Connor CM: Elevated levels of matrix metalloproteinases in bronchoalveolar lavage fluid of emphysematous patients. Thorax 52;502-506, 1997 https://doi.org/10.1136/thx.52.6.502
  24. Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD: Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277;2002-2004, 1997 https://doi.org/10.1126/science.277.5334.2002
  25. Grumelli S, Corry DB, Song LZ, Song L, Green L, Huh J, Hacken J, Espada R, Bag R, Lewis DE, Kheradmand F: An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Med 1;e8, 2004 https://doi.org/10.1371/journal.pmed.0010008
  26. Fujita M, Shannon JM, Irvin CG, Fagan KA, Cool C, Augustin A, Mason RJ: Overexpression of tumor necrosis factor-alpha produces an increase in lung volumes and pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 280;L39-49, 2001 https://doi.org/10.1152/ajplung.2001.280.1.L39
  27. Aaron SD, Angel JB, Lunau M, Wright K, Fex C, Le Saux N, Dales RE: Granulocyte inflammatory markers and airway infection during acute exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 163;349-355, 2001 https://doi.org/10.1164/ajrccm.163.2.2003122
  28. Dentener MA, Creutzberg EC, Pennings HJ, Rijkers GT, Mercken E, Wouters EF: Effect of infliximab on local and systemic inflammation in chronic obstructive pulmonary disease: a pilot study. Respiration 76;275-282, 2008 https://doi.org/10.1159/000117386
  29. Rennard SI, Fogarty C, Kelsen S, Long W, Ramsdell J, Allison J, Mahler D, Saadeh C, Siler T, Snell P, Korenblat P, Smith W, Kaye M, Mandel M, Andrews C, Prabhu R, Donohue JF, Watt R, Lo KH, Schlenker-Herceg R, Barnathan ES, Murray J; COPD Investigators: The safety and efficacy of infliximab in moderate to severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 175;926-934, 2007 https://doi.org/10.1164/rccm.200607-995OC
  30. Sapey E, Ahmad A, Bayley D, Newbold P, Snell N, Rugman P, Stockley RA: Imbalances between interleukin-1 and tumor necrosis factor agonists and antagonists in stable COPD. J Clin Immunol 29;508-516, 2009 https://doi.org/10.1007/s10875-009-9286-8
  31. 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 https://doi.org/10.1136/thorax.55.2.114
  32. Calabrese F, Baraldo S, Bazzan E, Lunardi F, Rea F, Maestrelli P, Turato G, Lokar-Oliani K, Papi A, Zuin R, Sfriso P, Balestro E, Dinarello CA, Saetta M: IL-32, a novel proinflammatory cytokine in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 178;894-901, 2008 https://doi.org/10.1164/rccm.200804-646OC
  33. Miossec P, Korn T, Kuchroo VK: Interleukin-17 and type 17 helper T cells. N Engl J Med 361;888-898, 2009 https://doi.org/10.1056/NEJMra0707449
  34. Louten J, Boniface K, de Waal Malefyt R: Development and function of TH17 cells in health and disease. J Allergy Clin Immunol 123;1004-1011, 2009 https://doi.org/10.1016/j.jaci.2009.04.003
  35. Jones CE, Chan K: Interleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-alpha, and granulocytecolony- stimulating factor by human airway epithelial cells. Am J Respir Cell Mol Biol 26;748-753, 2002 https://doi.org/10.1165/ajrcmb.26.6.4757
  36. Kao CY, Huang F, Chen Y, Thai P, Wachi S, Kim C, Tam L, Wu R: Up-regulation of CC chemokine ligand 20 expression in human airway epithelium by IL-17 through a JAK-independent but MEK/NF-kappaB-dependent signaling pathway. J Immunol 175;6676-6685, 2005 https://doi.org/10.4049/jimmunol.175.10.6676
  37. Chen Y, Thai P, Zhao YH, Ho YS, DeSouza MM, Wu R: Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J Biol Chem 278;17036-17043, 2003 https://doi.org/10.1074/jbc.M210429200
  38. 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. Nat Immunol 6;1133-1141, 2005 https://doi.org/10.1038/ni1261
  39. Harrison OJ, Foley J, Bolognese BJ, Long E 3rd, Podolin PL, Walsh PT: Airway infiltration of CD4+ CCR6+ Th17 type cells associated with chronic cigarette smoke induced airspace enlargement. Immunol Lett 121;13-21, 2008 https://doi.org/10.1016/j.imlet.2008.07.011
  40. Barczyk A, Pierzchala W, Sozanska E: Interleukin-17 in sputum correlates with airway hyperresponsiveness to methacholine. Respir Med 97;726-733, 2003 https://doi.org/10.1053/rmed.2003.1507
  41. Ikeuchi H, Kuroiwa T, Hiramatsu N, Kaneko Y, Hiromura K, Ueki K, Nojima Y: Expression of interleukin-22 in rheumatoid arthritis: potential role as a proinflammatory cytokine. Arthritis Rheum 52;1037-1046, 2005 https://doi.org/10.1002/art.20965
  42. Wolk K, Witte E, Warszawska K, Schulze-Tanzil G, Witte K, Philipp S, Kunz S, Docke WD, Asadullah K, Volk HD, Sterry W, Sabat R: The Th17 cytokine IL-22 induces IL-20 production in keratinocytes: a novel immunological cascade with potential relevance in psoriasis. Eur J Immunol 39;3570-3581, 2009 https://doi.org/10.1002/eji.200939687
  43. Aujla SJ, Chan YR, Zheng M, Fei M, Askew DJ, Pociask DA, Reinhart TA, McAllister F, Edeal J, Gaus K, Husain S, Kreindler JL, Dubin PJ, Pilewski JM, Myerburg MM, Mason CA, Iwakura Y, Kolls JK: IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 14;275-281, 2008 https://doi.org/10.1038/nm1710
  44. 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 https://doi.org/10.1111/j.1365-2249.2009.03965.x
  45. Sonnenberg GF, Nair MG, Kirn TJ, Zaph C, Fouser LA, Artis D: Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A. J Exp Med 207;1293- 1305, 2010 https://doi.org/10.1084/jem.20092054
  46. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, Zurawski S, Wiekowski M, Lira SA, Gorman D, Kastelein RA, Sedgwick JD: Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421;744-748, 2003 https://doi.org/10.1038/nature01355
  47. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ: Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198;1951-1957, 2003 https://doi.org/10.1084/jem.20030896
  48. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ: IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201;233-240, 2005 https://doi.org/10.1084/jem.20041257
  49. Voelkel N, Taraseviciene-Stewart L: Emphysema: an autoimmune vascular disease? Proc Am Thorac Soc 2;23-25, 2005 https://doi.org/10.1513/pats.200405-033MS
  50. Agusti A, MacNee W, Donaldson K, Cosio M: Hypothesis: does COPD have an autoimmune component? Thorax 58;832-834, 2003 https://doi.org/10.1136/thorax.58.10.832
  51. 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. Science Translational Medicine 1;4ra10, 2009 https://doi.org/10.1126/scitranlsmed.3000154
  52. Cottin V, Fabien N, Khouatra C, Moreira A, Cordier JF: Anti-elastin autoantibodies are not present in combined pulmonary fibrosis and emphysema. Eur Respir J 33;219-221, 2009 https://doi.org/10.1183/09031936.00140208
  53. Greene CM, Low TB, O'Neill SJ, McElvaney NG: Anti-proline- glycine-proline or antielastin autoantibodies are not evident in chronic inflammatory lung disease. Am J Respir Crit Care Med 181;31-35, 2010 https://doi.org/10.1164/rccm.200904-0545OC

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