Spleen tyrosine kinase inhibition attenuates airway hyperresponsiveness and pollution-induced enhanced airway response in a chronic mouse model of asthma

Journal of Allergy and Clinical Immunology

Volumn 131, Issue 2, 2013, Pages

  Penton, Patricia Castellanos ^a   Wang, Xiaomin ^a   Amatullah, Hajera ^b   Cooper, Josephine ^c   Godri, Krystal ^c   North, Michelle L ^a,b   Khanna, Nivedita ^a,b   Scott, Jeremy A ^d   Chow, Chung Wai ^a,c,e  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d LAKEHEAD UNIVERSITY   (Canada)

^e UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Airways hyperresponsiveness; asthma; mouse; pollution; Syk

Indexed keywords

METHACHOLINE; NVP QAB 205; OVALBUMIN; OZONE; PHOSPHATE BUFFERED SALINE; PROTEIN KINASE SYK; PROTEIN KINASE SYK INHIBITOR; UNCLASSIFIED DRUG;

AIR POLLUTANT; AIR POLLUTION; ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BREATHING MECHANICS; CELL COUNT; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; INFLAMMATORY CELL; LUNG LAVAGE; MOUSE; NEBULIZATION; NONHUMAN; PARTICLE SIZE; PARTICULATE MATTER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT ALLERGY; SENSITIZATION; SINGLE DRUG DOSE;

EID: 84873406511     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2012.07.039     Document Type: Article

References (55)

1. R. Halwani, S. Al-Muhsen, and Q. Hamid Airway remodeling in asthma Curr Opin Pharmacol 10 2010 236 245
2. H.Y. Kim, R.H. DeKruyff, and D.T. Umetsu The many paths to asthma: phenotype shaped by innate and adaptive immunity Nat Immunol 11 2010 577 584
3. D.M. Murphy, and P.M. O'Byrne Recent advances in the pathophysiology of asthma Chest 137 2010 1417 1426
4. P.J. Barnes New therapies for asthma: is there any progress? Trends Pharmacol Sci 31 2010 335 343
5. U. Gehring, A.H. Wijga, M. Brauer, P. Fischer, J.C. de Jongste, and M. Kerkhof Traffic-related air pollution and the development of asthma and allergies during the first 8 years of life Am J Respir Crit Care Med 181 2010 596 603
6. C. Penard-Morand, C. Raherison, D. Charpin, C. Kopferschmitt, F. Lavaud, and D. Caillaud Long-term exposure to close-proximity air pollution and asthma and allergies in urban children Eur Respir J 36 2010 33 40
7. N.A. Clark, P.A. Demers, C.J. Karr, M. Koehoorn, C. Lencar, and L. Tamburic Effect of early life exposure to air pollution on development of childhood asthma Environ Health Perspect 118 2010 284 290
8. C. Carlsten, A. Dybuncio, A. Becker, M. Chan-Yeung, and M. Brauer Traffic-related air pollution and incident asthma in a high-risk birth cohort Occup Environ Med 68 2011 291 295
9. R. Dales, A. Wheeler, M. Mahmud, A.M. Frescura, M. Smith-Doiron, and E. Nethery The influence of living near roadways on spirometry and exhaled nitric oxide in elementary schoolchildren Environ Health Perspect 116 2008 1423 1427
10. R. Dales, L. Chen, A.M. Frescura, L. Liu, and P.J. Villeneuve Acute effects of outdoor air pollution on FEV1: a panel study of schoolchildren with asthma Eur Respir J 34 2009 316 323
11. L. Liu, R. Poon, L. Chen, A.M. Frescura, P. Montuschi, and G. Ciabattoni Acute effects of air pollution on pulmonary function, airway inflammation, and oxidative stress in asthmatic children Environ Health Perspect 117 2009 668 674
12. R. Dales, A.J. Wheeler, M. Mahmud, A.M. Frescura, and L. Liu The influence of neighborhood roadways on respiratory symptoms among elementary schoolchildren J Occup Environ Med 51 2009 654 660
13. M.E. Weinblatt, A. Kavanaugh, M.C. Genovese, T.K. Musser, E.B. Grossbard, and D.B. Magilavy An oral spleen tyrosine kinase (Syk) inhibitor for rheumatoid arthritis N Engl J Med 363 2010 1303 1312
14. E.O. Meltzer, R.B. Berkowitz, and E.B. Grossbard An intranasal Syk-kinase inhibitor (R112) improves the symptoms of seasonal allergic rhinitis in a park environment J Allergy Clin Immunol 115 2005 791 796
15. E.S. Masuda, and J. Schmitz Syk inhibitors as treatment for allergic rhinitis Pulm Pharmacol Ther 21 2008 461 467
16. A. Mocsai, J. Ruland, and V.L. Tybulewicz The Syk tyrosine kinase: a crucial player in diverse biological functions Nat Rev Immunol 10 2010 387 402
17. D. Proud, and C.W. Chow Role of viral infections in asthma and COPD Am J Respir Cell Mol Biol 35 2006 513 518
18. D.J. Jackson, and S.L. Johnston The role of viruses in acute exacerbations of asthma J Allergy Clin Immunol 125 2010 1178 1187
19. X. Wang, C. Lau, S. Wiehler, A. Pow, T. Mazzulli, and D. Proud Syk is downstream of ICAM-1 and mediates human rhinovirus (HRV) activation of p38 MAP kinase in airway epithelial cells J Immunol 177 2006 6859 6870
20. C. Lau, X. Wang, L. Song, M. North, S. Wiehler, and D. Proud Syk associates with clathrin and mediates phosphatidylinositol 3-kinase activation during human rhinovirus internalization J Immunol 180 2008 870 880
21. C. Lau, P. Castellanos, D. Ranev, X. Wang, and C.W. Chow HRV signaling in airway epithelial cells is regulated by ITAM-mediated recruitment and activation of Syk Protein Pept Lett 18 2011 518 529
22. G.R. Stenton, M. Ulanova, R.E. Dery, S. Merani, M.K. Kim, and M. Gilchrist Inhibition of allergic inflammation in the airways using aerosolized antisense to Syk kinase J Immunol 169 2002 1028 1036
23. G.R. Stenton, M.K. Kim, O. Nohara, C.F. Chen, N. Hirji, and F.L. Wills Aerosolized Syk antisense suppresses Syk expression, mediator release from macrophages, and pulmonary inflammation J Immunol 164 2000 3790 3797
24. S. Matsubara, G. Li, K. Takeda, J.E. Loader, P. Pine, and E.S. Masuda Inhibition of spleen tyrosine kinase prevents mast cell activation and airway hyperresponsiveness Am J Respir Crit Care Med 173 2006 56 63
25. S. Matsubara, T. Koya, K. Takeda, A. Joetham, N. Miyahara, and P. Pine Syk activation in dendritic cells is essential for airway hyperresponsiveness and inflammation Am J Respir Cell Mol Biol 34 2006 426 433
26. J.A. Hirota, R. Ellis, and M.D. Inman Regional differences in the pattern of airway remodeling following chronic allergen exposure in mice Respir Res 7 2006 120
27. M. Ilies, C.L. Di, M.L. North, J.A. Scott, and D.W. Christianson 2-aminoimidazole amino acids as inhibitors of the binuclear manganese metalloenzyme human arginase I J Med Chem 53 2010 4266 4276
28. M.L. North, N. Khanna, P.A. Marsden, H. Grasemann, and J.A. Scott Functionally important role for arginase 1 in the airway hyperresponsiveness of asthma Am J Physiol Lung Cell Mol Physiol 296 2009 L911 L920
29. M.L. North, H. Amatullah, N. Khanna, B. Urch, H. Grasemann, and F. Silverman Augmentation of arginase 1 expression by exposure to air pollution exacerbates the airways hyperresponsiveness in murine models of asthma Respir Res 12 2011 19
30. J. Hayer, D. Le Grand, H. Bammerlin, X-L Cockcroft, S. Collingwood, and H. Mattes Novel 2,6-disubstituted purines-the synthesis of potent and selective inhibitors of the protein tyrosine kinase Syk Drugs Future 27 2002 280 284
31. F. Duta, M. Ulanova, D. Seidel, L. Puttagunta, S. Musat-Marcu, and K.S. Harrod Differential expression of spleen tyrosine kinase Syk isoforms in tissues: effects of the microbial flora Histochem Cell Biol 126 2006 495 505
32. J.Q. He, A.J. Sandford, I.M. Wang, S. Stepaniants, D.A. Knight, and A. Kicic Selection of housekeeping genes for real-time PCR in atopic human bronchial epithelial cells Eur Respir J 32 2008 755 762
33. P.J. Plant, M.L. North, A. Ward, M. Ward, N. Khanna, and J. Correa Hypertrophic airway smooth muscle mass correlates with increased airways responsiveness in a mouse model of asthma Am J Respir Cell Mol Biol 46 2012 532 540
34. X. Wang, M. Mychajlowycz, C. Lau, C. Gutierrez, J. Scott, and C.W. Chow Syk mediates BEAS-2B cell migration and proliferation, and HRV-induced expression of VEGF and IL-8 J Pharmacol Exp Ther 340 2012 277 282
35. W.R. Roche Inflammatory and structural changes in the small airways in bronchial asthma Am J Respir Crit Care Med 157 suppl 1998 S191 S194
36. P. Pohunek, J.O. Warner, J. Turzikova, J. Kudrmann, and W.R. Roche Markers of eosinophilic inflammation and tissue re-modelling in children before clinically diagnosed bronchial asthma Pediatr Allergy Immunol 16 2005 43 51
37. S. Baraldo, G. Turato, E. Bazzan, A. Ballarin, M. Damin, and E. Balestro Noneosinophilic asthma in children: relation with airway remodeling Eur Respir J 38 2011 575 583
38. N.R. Locke, S.G. Royce, J.S. Wainewright, C.S. Samuel, and M.L. Tang Comparison of airway remodeling in acute, subacute, and chronic models of allergic airways disease Am J Respir Cell Mol Biol 36 2007 625 632
39. E.M. Thomson, A. Williams, C.L. Yauk, and R. Vincent Impact of nose-only exposure system on pulmonary gene expression Inhal Toxicol 21 suppl 1 2009 74 82
40. P. Ruzza, B. Biondi, and A. Calderan Therapeutic prospect of Syk inhibitors Expert Opin Ther Pat 19 2009 1361 1376
41. J.W. Friedberg, J. Sharman, J. Sweetenham, P.B. Johnston, J.M. Vose, and A. Lacasce Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia Blood 115 2010 2578 2585
42. W.J. Moore, D. Richard, and A. Thorarensen An analysis of the diaminopyrimidine patent estates describing spleen tyrosine kinase inhibitors by Rigel and Portola Expert Opin Ther Pat 20 2010 1703 1722
43. M. Ilies, C.L. Di, M.L. North, J.A. Scott, and D.W. Christianson 2-aminoimidazole amino acids as inhibitors of the binuclear manganese metalloenzyme human arginase I J Med Chem 53 2010 4266 4276
44. M.L. North, N. Khanna, P.A. Marsden, H. Grasemann, and J.A. Scott Functionally important role for arginase 1 in the airway hyperresponsiveness of asthma Am J Physiol Lung Cell Mol Physiol 296 2009 L911 L920
45. M.L. North, H. Amatullah, N. Khanna, B. Urch, H. Grasemann, and F. Silverman Augmentation of arginase 1 expression by exposure to air pollution exacerbates the airways hyperresponsiveness in murine models of asthma Respir Res 12 2011 19
46. S. Tomioka, J.H. Bates, and C.G. Irvin Airway and tissue mechanics in a murine model of asthma: alveolar capsule vs. forced oscillations J Appl Physiol 93 2002 263 270
47. Z. Hantos, B. Daroczy, B. Suki, S. Nagy, and J.J. Fredberg Input impedance and peripheral inhomogeneity of dog lungs J Appl Physiol 72 1992 168 178
48. P. Ruzza, B. Biondi, and A. Calderan Therapeutic prospect of Syk inhibitors Expert Opin Ther Pat 19 2009 1361 1376
49. M. Riccaboni, I. Bianchi, and P. Petrillo Spleen tyrosine kinases: biology, therapeutic targets and drugs Drug Discov Today 15 2010 517 530
50. F. Duta, M. Ulanova, D. Seidel, L. Puttagunta, S. Musat-Marcu, and K.S. Harrod Differential expression of spleen tyrosine kinase Syk isoforms in tissues: effects of the microbial flora Histochem Cell Biol 126 2006 495 505
51. J.Q. He, A.J. Sandford, I.M. Wang, S. Stepaniants, D.A. Knight, and A. Kicic Selection of housekeeping genes for real-time PCR in atopic human bronchial epithelial cells Eur Respir J 32 2008 755 762
52. U.S. Akhtar, J.A. Scott, A. Chu, and G.J. Evans In vivo and in vitro assessment of particulate matter toxicology F. Zereini, C.L.S. Wiseman, Urban airborne particulate matter: origins, chemistry, fate and health impacts 2010 Springer Verlag Berlin
53. U.S. Akhtar, R.D. McWhinney, N. Rastogi, J.P. Abbatt, G.J. Evans, and J.A. Scott Cytotoxic and proinflammatory effects of ambient and source-related particulate matter (PM) in relation to the production of reactive oxygen species (ROS) and cytokine adsorption by particles Inhal Toxicol 22 suppl 2 2010 37 47
54. X. Wang, C. Lau, S. Wiehler, A. Pow, T. Mazzulli, and D. Proud Syk is downstream of ICAM-1 and mediates human rhinovirus (HRV) activation of p38 MAP kinase in airway epithelial cells J Immunol 177 2006 6859 6870
55. C. Lau, X. Wang, L. Song, M. North, S. Wiehler, and D. Proud Syk associates with clathrin and mediates phosphatidylinositol 3-kinase activation during human rhinovirus internalization J Immunol 180 2008 870 880