Inhalation of sulfur mustard causes long-term T cell-dependent inflammation: Possible role of Th17 cells in chronic lung pathology

International Immunopharmacology

Volumn 13, Issue 1, 2012, Pages 101-108

  Mishra, Neerad C ^a   Rir Sima Ah, Jules ^a   Grotendorst, Gary R ^a   Langley, Raymond J ^a   Singh, Shashi P ^a   Gundavarapu, Sravanthi ^a   Weber, Waylon M ^a   Pena Philippides, Juan C ^a   Duncan, Matthew R ^a   Sopori, Mohan L ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

Author keywords

Apoptosis; Cytokine; Fibrosis; Inflammation; Sulfur mustard

Indexed keywords

COLLAGEN; CXCL1 CHEMOKINE; EOTAXIN; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; MUSTARD GAS; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CHRONIC LUNG DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HAPLORHINI; HISTOPATHOLOGY; LUNG FIBROSIS; LYMPHOCYTIC INFILTRATION; MYOFIBROBLAST; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; T LYMPHOCYTE; TH17 CELL; TOXIC INHALATION; UPREGULATION;

ANIMALS; APOPTOSIS; BRONCHOALVEOLAR LAVAGE FLUID; CHEMICAL WARFARE AGENTS; CHEMOTAXIS, LEUKOCYTE; CYTOKINES; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INHALATION EXPOSURE; LUNG; LUNG INJURY; LYMPHOCYTE COUNT; MACACA FASCICULARIS; MUSTARD GAS; PULMONARY FIBROSIS; RATS; RATS, INBRED F344; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; TH17 CELLS;

EID: 84859507616     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2012.03.010     Document Type: Article

References (70)

1. K. Kehe, and L. Szinicz Medical aspects of sulphur mustard poisoning Toxicology 214 3 2005 198 209
2. M. Ghanei, M. Naderi, A.M. Kosar, A.A. Harandi, N.S. Hopkinson, and Z. Poursaleh Long-term pulmonary complications of chemical warfare agent exposure in Iraqi Kurdish civilians Inhal Toxicol 22 9 2010 719 724
3. M. Wattana, and T. Bey Mustard gas or sulfur mustard: an old chemical agent as a new terrorist threat Prehosp Disaster Med 24 1 2009 19 29 [discussion 30-1]
4. K. Ghabili, P.S. Agutter, M. Ghanei, K. Ansarin, Y. Panahi, and M.M. Shoja Sulfur mustard toxicity: history, chemistry, pharmacokinetics, and pharmacodynamics Crit Rev Toxicol 41 5 2011 384 403
5. M. Balali-Mood, and M. Hefazi Comparison of early and late toxic effects of sulfur mustard in Iranian veterans Basic Clin Pharmacol Toxicol 99 4 2006 273 282
6. M. Hefazi, D. Attaran, M. Mahmoudi, and M. Balali-Mood Late respiratory complications of mustard gas poisoning in Iranian veterans Inhal Toxicol 17 11 2005 587 592
7. M. Balali-Mood, R. Afshari, R. Zojaji, H. Kahrom, M. Kamrani, and D. Attaran Delayed toxic effects of sulfur mustard on respiratory tract of Iranian veterans Hum Exp Toxicol 30 9 2010 1141 1149
8. M. Adelipour, A.A. Imani Fooladi, S. Yazdani, E. Vahedi, M. Ghanei, and M.R. Nourani Smad molecules expression pattern in human bronchial airway induced by sulfur mustard Iran J Allergy Asthma Immunol 10 3 2011 147 154
9. F. Taghaddosinejad, A.F. Fayyaz, and B. Behnoush Pulmonary complications of mustard gas exposure: a study on cadavers Acta Med Iran 49 4 2011 233 236
10. L. Ghotbi, and Z. Hassan The immunostatus of natural killer cells in people exposed to sulfur mustard Int Immunopharmacol 2 7 2002 981 985
11. A. Emad, and Y. Emad Levels of cytokine in bronchoalveolar lavage (BAL) fluid in patients with pulmonary fibrosis due to sulfur mustard gas inhalation J Interferon Cytokine Res 27 1 2007 38 43
12. A. Emad, and Y. Emad CD4/CD8 ratio and cytokine levels of the BAL fluid in patients with bronchiectasis caused by sulfur mustard gas inhalation J Inflamm (London, England) 4 2007 2
13. A. Emad, and Y. Emad Increased in CD8 T lymphocytes in the BAL fluid of patients with sulfur mustard gas-induced pulmonary fibrosis Respir Med 101 4 2007 786 792
14. X. Gao, D.R. Anderson, A.W. Brown, H. Lin, J. Amnuaysirikul, and A.L. Chua Pathological studies on the protective effect of a macrolide antibiotic, roxithromycin, against sulfur mustard inhalation toxicity in a rat model Toxicol Pathol 39 7 2011 1056 1064
15. R. Malaviya, V.R. Sunil, J. Cervelli, D.R. Anderson, W.W. Holmes, and M.L. Conti Inflammatory effects of inhaled sulfur mustard in rat lung Toxicol Appl Pharmacol 248 2 2010 89 99
16. J. Emmler, M.I. Hermanns, D. Steinritz, H. Kreppel, C.J. Kirkpatrick, and W. Bloch Assessment of alterations in barrier functionality and induction of proinflammatory and cytotoxic effects after sulfur mustard exposure of an in vitro coculture model of the human alveolo-capillary barrier Inhal Toxicol 19 8 2007 657 665
17. J. Seagrave, W.M. Weber, and G.R. Grotendorst Sulfur mustard vapor effects on differentiated human lung cells Inhal Toxicol 22 11 2010 896 902
18. E. Wigenstam, D. Rocksen, B. Ekstrand-Hammarstrom, and A. Bucht Treatment with dexamethasone or liposome-encapsuled vitamin E provides beneficial effects after chemical-induced lung injury Inhal Toxicol 21 11 2009 958 964
19. B. Ekstrand-Hammarstrom, E. Wigenstam, and A. Bucht Inhalation of alkylating mustard causes long-term T cell-dependent inflammation in airways and growth of connective tissue Toxicology 280 3 2011 88 97
20. N.C. Mishra, J. Rir-Sima-Ah, T. March, W. Weber, J. Benson, and R. Jaramillo Sulfur mustard induces immune sensitization in hairless guinea pigs Int Immunopharmacol 10 2 2010 193 199
21. C. Nembrini, B.J. Marsland, and M. Kopf IL-17-producing T cells in lung immunity and inflammation J Allergy Clin Immunol 123 5 2009 986 994 [quiz 95-6]
22. G. Han, F. Li, T.P. Singh, P. Wolf, and X.J. Wang The pro-inflammatory role of TGFbeta1: a paradox? Int J Biol Sci 8 2 2012 228 235
23. W.M. Weber, D.A. Kracko, M.R. Lehman, C.M. Irvin, L.F. Blair, and R.K. White Inhalation exposure systems for the development of rodent models of sulfur mustard-induced pulmonary injury Toxicol Mech Methods 20 1 2010 14 24
24. N.C. Mishra, J. Rir-Sima-Ah, R.J. Langley, S.P. Singh, J.C. Pena-Philippides, and T. Koga Nicotine primarily suppresses lung Th2 but not goblet cell and muscle cell responses to allergens J Immunol 180 11 2008 7655 7663
25. M.S. Wilson, and T.A. Wynn Pulmonary fibrosis: pathogenesis, etiology and regulation Mucosal Immunol 2 2 2009 103 121
26. M. Ghanei, I. Adibi, F. Farhat, and J. Aslani Late respiratory effects of sulfur mustard: how is the early symptoms severity involved? Chron Respir Dis 5 2 2008 95 100
27. M. Ponticos, A.M. Holmes, X. Shi-wen, P. Leoni, K. Khan, and V.S. Rajkumar Pivotal role of connective tissue growth factor in lung fibrosis: MAPK-dependent transcriptional activation of type I collagen Arthritis Rheum 60 7 2009 2142 2155
28. L.A. Murray, Q. Chen, M.S. Kramer, D.P. Hesson, R.L. Argentieri, and X. Peng TGF-beta driven lung fibrosis is macrophage dependent and blocked by Serum amyloid P Int J Biochem Cell Biol 43 1 2011 154 162
29. M. Balali-Mood, R. Afshari, R. Zojaji, H. Kahrom, M. Kamrani, and D. Attaran Delayed toxic effects of sulfur mustard on respiratory tract of Iranian veterans Hum Exp Toxicol 30 9 2011 1141 1149
30. A. Emad, and G.R. Rezaian Immunoglobulins and cellular constituents of the BAL fluid of patients with sulfur mustard gas-induced pulmonary fibrosis Chest 115 5 1999 1346 1351
31. F. Balkwill Cancer and the chemokine network Nat Rev 4 7 2004 540 550
32. I.F. Charo, and M.B. Taubman Chemokines in the pathogenesis of vascular disease Circ Res 95 9 2004 858 866
33. M.N. Ajuebor, R.J. Flower, R. Hannon, M. Christie, K. Bowers, and A. Verity Endogenous monocyte chemoattractant protein-1 recruits monocytes in the zymosan peritonitis model J Leukoc Biol 63 1 1998 108 116
34. J. Zhang, L. Patel, and K.J. Pienta Targeting chemokine (C-C motif) ligand 2 (CCL2) as an example of translation of cancer molecular biology to the clinic Prog Mol Biol Transl Sci 95 2010 31 53
35. B.B. Moore, R. Paine III, P.J. Christensen, T.A. Moore, S. Sitterding, and R. Ngan Protection from pulmonary fibrosis in the absence of CCR2 signaling J Immunol 167 8 2001 4368 4377
36. C.D. Ramos, C. Canetti, J.T. Souto, J.S. Silva, C.M. Hogaboam, and S.H. Ferreira MIP-1alpha[CCL3] acting on the CCR1 receptor mediates neutrophil migration in immune inflammation via sequential release of TNF-alpha and LTB4 J Leukoc Biol 78 1 2005 167 177
37. A.M. Das, M.N. Ajuebor, R.J. Flower, M. Perretti, and S.R. McColl Contrasting roles for RANTES and macrophage inflammatory protein-1 alpha (MIP-1 alpha) in a murine model of allergic peritonitis Clin Exp Immunol 117 2 1999 223 229
38. J.M. Schroder Chemoattractants as mediators of neutrophilic tissue recruitment Clin Dermatol 18 3 2000 245 263
39. A.E. Koch, S.L. Kunkel, M.R. Shah, S. Hosaka, M.M. Halloran, and G.K. Haines Growth-related gene product alpha. A chemotactic cytokine for neutrophils in rheumatoid arthritis J Immunol 155 7 1995 3660 3666
40. R.P. MacDermott Chemokines in the inflammatory bowel diseases J Clin Immunol 19 5 1999 266 272
41. F.M. Graziano, E.B. Cook, and J.L. Stahl Cytokines, chemokines, RANTES, and eotaxin Allergy Asthma Proc 20 3 1999 141 146
42. T.A. Wynn IL-13 effector functions Annu Rev Immunol 21 2003 425 456
43. M. Ghanei, and A.A. Harandi Molecular and cellular mechanism of lung injuries due to exposure to sulfur mustard: a review Inhal Toxicol 23 7 2011 363 371
44. N. Allon, A. Amir, E. Manisterski, I. Rabinovitz, S. Dachir, and T. Kadar Inhalation exposure to sulfur mustard in the guinea pig model: clinical, biochemical and histopathological characterization of respiratory injuries Toxicol Appl Pharmacol 241 2 2009 154 162
45. S.J. Fairhall, B.J. Jugg, R.W. Read, S.J. Stubbs, S.J. Rutter, and A.J. Smith Exposure-response effects of inhaled sulfur mustard in a large porcine model: a 6-h study Inhal Toxicol 22 14 2010 1135 1143
46. M.B. Torchinsky, J. Garaude, and J.M. Blander Infection and apoptosis as a combined inflammatory trigger Curr Opin Immunol 22 1 2010 55 62
47. V.M. Borges, H. Falcao, J.H. Leite-Junior, L. Alvim, G.P. Teixeira, and M. Russo Fas ligand triggers pulmonary silicosis J Exp Med 194 2 2001 155 164
48. W.D. Huang, J.Z. Wang, Y.Q. Lu, Y.M. Di, J.K. Jiang, and Q. Zhang Lysine acetylsalicylate ameliorates lung injury in rats acutely exposed to paraquat Chin Med J 124 16 2011 2496 2501
49. Y. Imazu, S. Yanagi, K. Miyoshi, H. Tsubouchi, S. Yamashita, and N. Matsumoto Ghrelin ameliorates bleomycin-induced acute lung injury by protecting alveolar epithelial cells and suppressing lung inflammation Eur J Pharmacol 672 1-3 2011 153 158
50. E. Lappi-Blanco, Y. Soini, and P. Paakko Apoptotic activity is increased in the newly formed fibromyxoid connective tissue in bronchiolitis obliterans organizing pneumonia Lung 177 6 1999 367 376
51. S.I. Cha, S.D. Groshong, S.K. Frankel, B.L. Edelman, G.P. Cosgrove, and J.L. Terry-Powers Compartmentalized expression of c-FLIP in lung tissues of patients with idiopathic pulmonary fibrosis Am J Respir Cell Mol Biol 42 2 2010 140 148
52. M.W. Wynes, B.L. Edelman, A.G. Kostyk, M.G. Edwards, C. Coldren, and S.D. Groshong Increased cell surface Fas expression is necessary and sufficient to sensitize lung fibroblasts to Fas ligation-induced apoptosis: implications for fibroblast accumulation in idiopathic pulmonary fibrosis J Immunol 187 1 2011 527 537
53. T.E. Quan, S.E. Cowper, and R. Bucala The role of circulating fibrocytes in fibrosis Curr Rheumatol Rep 8 2 2006 145 150
54. M. Emura, S. Nagai, M. Takeuchi, M. Kitaichi, and T. Izumi In vitro production of B cell growth factor and B cell differentiation factor by peripheral blood mononuclear cells and bronchoalveolar lavage T lymphocytes from patients with idiopathic pulmonary fibrosis Clin Exp Immunol 82 1 1990 133 139
55. W.A. Wallace, E.A. Ramage, D. Lamb, and S.E. Howie A type 2 (Th2-like) pattern of immune response predominates in the pulmonary interstitium of patients with cryptogenic fibrosing alveolitis (CFA) Clin Exp Immunol 101 3 1995 436 441
56. A.E. Elovic, H. Ohyama, A. Sauty, J. McBride, T. Tsuji, and M. Nagai IL-4-dependent regulation of TGF-alpha and TGF-beta1 expression in human eosinophils J Immunol 160 12 1998 6121 6127
57. T.C. O'Shaughnessy, T.W. Ansari, N.C. Barnes, and P.K. Jeffery Inflammation in bronchial biopsies of subjects with chronic bronchitis: inverse relationship of CD8 + T lymphocytes with FEV1 Am J Respir Crit Care Med 155 3 1997 852 857
58. M. Saetta, A. Di Stefano, G. Turato, F.M. Facchini, L. Corbino, and C.E. Mapp CD8 + T-lymphocytes in peripheral airways of smokers with chronic obstructive pulmonary disease Am J Respir Crit Care Med 157 3 Pt 1 1998 822 826
59. J. Nadigel, D. Prefontaine, C.J. Baglole, F. Maltais, J. Bourbeau, and D.H. Eidelman Cigarette smoke increases TLR4 and TLR9 expression and induces cytokine production from CD8 + T cells in chronic obstructive pulmonary disease Respir Res 12 2011 149
60. S.A. Papiris, A. Kollintza, M. Karatza, E.D. Manali, C. Sotiropoulou, and J. Milic-Emili CD8 + T lymphocytes in bronchoalveolar lavage in idiopathic pulmonary fibrosis J Inflamm (London, England) 4 2007 14
61. S. Nagai, T. Handa, Y. Ito, M. Takeuchi, and T. Izumi Bronchoalveolar lavage in idiopathic interstitial lung diseases Semin Respir Crit Care Med 28 5 2007 496 503
62. P. Kopinski, G. Przybylski, B. Balicka-Slusarczyk, J. Chorostowska-Wynimko, G. Pinis, and M. Plato Cigarette smoking results in the number of CD8+Fas Ligand + T cytotoxic lymphocytes in bronchoalveolar lavage (BAL) fluid of patients with idiopathic pulmonary fibrosis (IPF) Przegl Lek 64 10 2007 689 694
63. S. Hodge, G. Hodge, J. Ahern, C.L. Liew, P. Hopkins, and D.C. Chambers Increased levels of T cell granzyme b in bronchiolitis obliterans syndrome are not suppressed adequately by current immunosuppressive regimens Clin Exp Immunol 158 2 2009 230 236
64. M. Rowell, K. Kehe, F. Balszuweit, and H. Thiermann The chronic effects of sulfur mustard exposure Toxicology 263 1 2009 9 11
65. A. Awasthi, and V.K. Kuchroo Th17 cells: from precursors to players in inflammation and infection Int Immunol 21 5 2009 489 498
66. H.L. Tan, N. Regamey, S. Brown, A. Bush, C.M. Lloyd, and J.C. Davies The Th17 pathway in cystic fibrosis lung disease Am J Respir Crit Care Med 184 2 2011 252 258
67. P.K. Dagur, A. Biancotto, L. Wei, H.N. Sen, M. Yao, and W. Strober MCAM-expressing CD4(+) T cells in peripheral blood secrete IL-17A and are significantly elevated in inflammatory autoimmune diseases J Autoimmun 37 4 2011 319 327
68. E. Hsu, H. Shi, R.M. Jordan, J. Lyons-Weiler, J.M. Pilewski, and C.A. Feghali-Bostwick Lung tissues in systemic sclerosis have gene expression patterns unique to pulmonary fibrosis and pulmonary hypertension Arthritis Rheum Nov. 19 2010 [epub ahead of print]
69. M.S. Wilson, S.K. Madala, T.R. Ramalingam, B.R. Gochuico, I.O. Rosas, and A.W. Cheever Bleomycin and IL-1beta-mediated pulmonary fibrosis is IL-17A dependent J Exp Med 207 3 2010 535 552
70. L. Yang, D.E. Anderson, C. Baecher-Allan, W.D. Hastings, E. Bettelli, and M. Oukka IL-21 and TGF-beta are required for differentiation of human T(H)17 cells Nature 454 7202 2008 350 352