A new short-term mouse model of chronic obstructive pulmonary disease identifies a role for mast cell tryptase in pathogenesis

Journal of Allergy and Clinical Immunology

Volumn 131, Issue 3, 2013, Pages

  Beckett, Emma L ^a   Stevens, Richard L ^b,c   Jarnicki, Andrew G ^a   Kim, Richard Y ^a   Hanish, Irwan ^a   Hansbro, Nicole G ^a   Deane, Andrew ^a   Keely, Simon ^a   Horvat, Jay C ^a   Yang, Ming ^a   Oliver, Brian G ^d   Van Rooijen, Nico ^e   Inman, Mark D ^f   Adachi, Roberto ^g   Soberman, Roy J ^b,h   Hamadi, Sahar ^c   Wark, Peter A ^a,i   Foster, Paul S ^a   Hansbro, Philip M ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

^e VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^f MCMASTER UNIVERSITY   (Canada)

^g UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^h MASSACHUSETTS GENERAL HOSPITAL   (United States)

ⁱ JOHN HUNTER HOSPITAL   (Australia)

Author keywords

airway remodeling; chronic obstructive pulmonary disease; Cigarette smoke; emphysema; htryptase ; inflammation; lung function; macrophage; mast cell; mouse mast cell protease 6; protease

Indexed keywords

CHEMOKINE; CIGARETTE SMOKE; CYTOKINE; DEXAMETHASONE; TRYPTASE;

AIRWAY REMODELING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; DISEASE EXACERBATION; EMPHYSEMA; EXPERIMENTAL MODEL; FEMALE; HEART; INFLAMMATION; LUNG FUNCTION; MACROPHAGE; MAST CELL; MOUSE; MUCUS SECRETION; NONHUMAN; PATHOGENESIS; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; STREPTOCOCCUS PNEUMONIAE;

EID: 84875224340     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2012.11.053     Document Type: Article

References (87)

1. World Health Organization Global burden of disease: 2004 update 2008 World Health Organization Geneva
2. K.F. Rabe, S. Hurd, A. Anzueto, P.J. Barnes, S.A. Buist, and P. Calverley Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary Am J Respir Crit Care Med 176 2007 532 555
3. R. Vlahos, S. Bozinovski, R.C. Gualano, M. Ernst, and G.P. Anderson Modelling COPD in mice Pulm Pharmacol Ther 19 2006 12 17
4. K.R. Bracke, A.I. D'hulst, T. Maes, K.B. Moerloose, I.K. Demedts, and S. Lebecque Cigarette smoke-induced pulmonary inflammation and emphysema are attenuated in CCR6-deficient mice J Immunol 177 2006 4350 4359
5. G.J. Gaschler, C.C.J. Zavitz, C.M.T. Bauer, M. Skrtic, M. Lindahl, and C.S. Robbins Cigarette smoke exposure attenuates cytokine production by mouse alveolar macrophages Am J Respir Cell Mol Biol 38 2007 218 226
6. G.T. Motz, B.L. Eppert, B.W. Wortham, R.M. Amos-Kroohs, J.L. Flury, and S.C. Wesselkamper Chronic cigarette smoke exposure primes NK cell activation in a mouse model of chronic obstructive pulmonary disease J Immunol 184 2010 4460 4469
7. S. Hodge, G. Matthews, V. Mukaro, J. Ahern, A. Shivam, and G. Hodge Cigarette smoke-induced changes to alveolar macrophage phenotype and function are improved by treatment with procysteine Am J Respir Cell Mol Biol 44 2011 673 681
8. J.J. Atkinson, B.A. Lutey, Y. Suzuki, H.M. Toennies, D.G. Kelley, and D.K. Kobayashi The role of matrix metalloproteinase-9 in cigarette smoke-induced emphysema Am J Respir Crit Care Med 183 2011 876 884
9. R.D. Hautamaki, D.K. Kobayashi, R.M. Senior, and S.D. Shapiro Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice Science 277 1997 2002 2004
10. J.L. Wright, and A. Churg Smoking cessation decreases the number of metaplastic secretory cells in the small airways of the guinea pig Inhal Toxicol 14 2002 1153 1159
11. W. Huvenne, C.A. Pérez-Novo, L. Derycke, N. De Ruyck, O. Krysko, and T. Maes Different regulation of cigarette smoke induced inflammation in upper versus lower airways Respir Res 11 2010 100 109
12. S.M. Ruwanpura, L. McLeod, A. Miller, J. Jones, S. Bozinovski, and R. Vlahos Interleukin-6 promotes pulmonary emphysema associated with apoptosis in mice Am J Respir Cell Mol Biol 45 2011 720 730
13. E. Mortaz, G. Folkerts, and F. Redegeld Mast cells and COPD Pulm Pharmacol Ther 24 2011 367 372
14. C.K. Andersson, M. Mori, L. Bjermer, C.G. Lofdahl, and J.S. Erjefalt Alterations in lung mast cell populations in patients with chronic obstructive pulmonary disease Am J Respir Crit Care Med 181 2010 206 217
15. A. Ballarin, E. Bazzan, R.H. Zenteno, G. Turato, S. Baraldo, and D. Zanovello Mast cell infiltration discriminates between histopathological phenotypes of chronic obstructive pulmonary disease Am J Respir Crit Care Med 186 2012 233 239
16. X. Zhang, H. Zheng, W. Ma, F. Wang, X. Zeng, and C. Liu Tryptase enzyme activity is correlated with severity of chronic obstructive pulmonary disease Tohoku J Exp Med 224 2011 179 187
17. E. Mortaz, M.E. Givi, C.A. Da Silva, G. Folkerts, and F.A. Redegeld A relation between TGF-β and mast cell tryptase in experimental emphysema models Biochim Biophys Acta 1822 2012 1154 1160
18. S.M. Thakurdas, E. Melicoff, L. Sansores-Garcia, D.C. Moreira, Y. Petrova, and R.L. Stevens The mast cell-restricted tryptase mMCP-6 has a critical immunoprotective role in bacterial infections J Biol Chem 282 2007 20809 20815
19. A.N. Thorburn, B.J. O'Sullivan, R. Thomas, R.K. Kumar, P.S. Foster, and P.G. Gibson Pneumococcal conjugate vaccine-induced regulatory T cells suppress the development of allergic airways disease Thorax 65 2010 1053 1060
20. A.T. Essilfie, J.L. Simpson, J.C. Horvat, J.A. Preston, M.L. Dunkley, and P.S. Foster Haemophilus influenzae infection drives IL-17-mediated neutrophilic allergic airways disease PLoS Pathog 7 2011 e1002244
21. J.A. Preston, A.T. Essilfie, J.C. Horvat, M.A. Wade, K.W. Beagley, and P.G. Gibson Inhibition of allergic airways disease by immunomodulatory therapy with whole killed Streptococcus pneumoniae Vaccine 25 2007 8154 8162
22. A.N. Thorburn, P.S. Foster, P.G. Gibson, and P.M. Hansbro Streptococcus pneumoniae components suppress allergic airways disease and natural killer T cells by inducing regulatory T cells J Immunol 188 2012 4611 4620
23. J.C. Horvat, K.W. Beagley, M.A. Wade, J.A. Preston, N.G. Hansbro, and D.K. Hickey Neonatal chlamydial infection induces mixed T-cell responses that drive allergic airway disease Am J Respir Crit Care Med 176 2007 556 564
24. M.R. Starkey, A.T. Essilfie, J.C. Horvat, R.Y. Kim, D.H. Nguyen, and K.W. Beagley Constitutive production of IL-13 promotes early-life Chlamydia respiratory infection and allergic airway disease Mucosal Immunol 2012 [Epub ahead of print]
25. J.J. Li, W. Wang, K.J. Baines, N.A. Bowden, P.M. Hansbro, and P.G. Gibson IL-27/IFN-γ induce MyD88-dependent steroid-resistant airway hyperresponsiveness by inhibiting glucocorticoid signaling in macrophages J Immunol 185 2010 4401 4409
26. K.L. Asquith, J.C. Horvat, G.E. Kaiko, A.J. Carey, K.W. Beagley, and P.M. Hansbro Interleukin-13 promotes susceptibility to chlamydial infection of the respiratory and genital tracts PLoS Pathog 7 2011 e1001339
27. M. Zhu, I. Rhee, Y. Liu, and W. Zhang Negative regulation of FceRI-mediated signaling and mast cell function by the adaptor protein LAX J Biol Chem 281 2006 18408 18413
28. J.C. Horvat, M.R. Starkey, R.Y. Kim, S. Phipps, P.G. Gibson, and K.W. Beagley Early-life chlamydial lung infection enhances allergic airways disease through age-dependent differences in immunopathology J Allergy Clin Immunol 125 2010 617 625
29. J.C. Horvat, M.R. Starkey, R.Y. Kim, K.W. Beagley, J.A. Preston, and P.G. Gibson Chlamydial respiratory infection during allergen sensitization drives neutrophilic allergic airways disease J Immunol 184 2010 4159 4169
30. R.K. Kumar, C. Herbert, and M. Kasper Reversibility of airway inflammation and remodelling following cessation of antigenic challenge in a model of chronic asthma Clin Exp Allergy 34 2004 1796 1802
31. R.S. Harris Pressure-volume curves of the respiratory system Respir Care 50 2005 78 98
32. A.T. Essilfie, J.L. Simpson, M.L. Dunkley, L.C. Morgan, B.G. Oliver, and P.G. Gibson Combined Haemophilus influenzae respiratory infection and allergic airways disease drives chronic infection and features of neutrophilic asthma Thorax 67 2012 588 599
33. J.A. Preston, K.W. Beagley, P.G. Gibson, and P.M. Hansbro Genetic background affects susceptibility in nonfatal pneumococcal bronchopneumonia Eur Respir J 23 2004 224 231
34. J.A. Preston, A.N. Thorburn, M.R. Starkey, E.L. Beckett, J.C. Horvat, and M.A. Wade Streptococcus pneumoniae infection suppresses allergic airways disease by inducing regulatory T-cells Eur Respir J 37 2011 53 64
35. A.C. Hsu, I. Barr, P.M. Hansbro, and P.A. Wark Human influenza is more effective than avian influenza at antiviral suppression in airway cells Am J Respir Cell Mol Biol 44 2011 906 913
36. A.C. Hsu, K. Parsons, I. Barr, S. Lowther, D. Middleton, and P.M. Hansbro Critical role of constitutive type I interferon response in bronchial epithelial cell to influenza infection PLoS One 7 2012 e32947
37. J.M. Daley, A.A. Thomay, M.D. Connolly, J.S. Reichner, and J.E. Albina Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice J Leukoc Biol 83 2008 64 70
38. S. Singh, A.V. Amin, and Y.K. Loke Long-term use of inhaled corticosteroids and the risk of pneumonia in chronic obstructive pulmonary disease: a meta-analysis Arch Intern Med 169 2009 21929
39. P.M. Calverley, J.A. Anderson, B. Celli, G.T. Ferguson, C. Jenkins, and P.W. Jones Salmeterol and fluticasone propionate and survival in chronic obstructive pulmonary disease N Engl J Med 356 2007 775 789
40. R.M. Séguin, and N. Ferrari Emerging oligonucleotide therapies for asthma and chronic obstructive pulmonary disease Expert Opin Investig Drugs 18 2009 1505 1517
41. I.A. Yang, K.M. Fong, E.H. Sim, P.N. Black, and T.J. Lasserson Inhaled corticosteroids for stable chronic obstructive pulmonary disease Cochrane Database Syst Rev 2 2007 CD002991
42. P.J. Barnes Glucocorticosteroids: current and future directions Br J Pharmacol 163 2011 29 43
43. P.J. Barnes, and B.R. Celli Systemic manifestations and comorbidities of COPD Eur Respir J 33 2009 1165 1185
44. M. Miravitlles, A. Marín, E. Monsó, S. Vilà, C. de la Roza, and R. Hervás Colour of sputum is a marker for bacterial colonisation in chronic obstructive pulmonary disease Respir Res 11 2010 58 67
45. 6-mediated TGF-β activation causes MMP12-dependent emphysema Nature 422 2003 169 173
46. A.F. Ofulue, M. Ko, and R.T. Abboud Time course of neutrophil and macrophage elastinolytic activities in cigarette smoke-induced emphysema Am J Physiol Lung Cell Mol Physiol 275 1998 L1134 L1144
47. H.P. McNeil, K. Shin, I.K. Campbell, I.P. Wicks, R. Adachi, and D.M. Lee The mouse mast cell-restricted tetramer-forming tryptases mouse mast cell protease 6 and mouse mast cell protease 7 are critical mediators in inflammatory arthritis Arthritis Rheum 58 2008 2338 2346
48. A.M. Houghton, M. Mouded, and S.D. Shapiro Common origins of lung cancer and COPD Nat Med 14 2008 1023 1024
49. J.C. Hogg Pathophysiology of airflow limitation in chronic obstructive pulmonary disease Lancet 364 2004 709 721
50. S. Battaglia, T. Mauad, A.M. van Schadewijk, A.M. Vignola, K.F. Rabe, and V. Bellia Differential distribution of inflammatory cells in large and small airways in smokers J Clin Pathol 60 2007 907 911
51. J.A. Vanoirbeek, M. Rinaldi, V. De Vooght, S. Haenen, S. Bobic, and G. Gayan-Ramirez Noninvasive and invasive pulmonary function in mouse models of obstructive and restrictive respiratory diseases Am J Respir Cell Mol Biol 42 2010 96 104
52. T. Welte, and T. Köhnlein Global and local epidemiology of community-acquired pneumonia: the experience of the CAPNETZ Network Semin Respir Crit Care Med 30 2009 127 135
53. T. Seemungal, R. Harper-Owen, A. Bhowmik, I. Moric, G. Sanderson, and S. Message Respiratory viruses, symptoms, and inflammatory markers in acute exacerbations and stable chronic obstructive pulmonary disease Am J Respir Crit Care Med 164 2001 1618 1623
54. 1 decline in patients with chronic obstructive pulmonary disease Am J Respir Crit Care Med 167 2003 1090 1095
55. V.M. Keatings, P.D. Collins, D.M. Scott, and P.J. Barnes Differences in interleukin-8 and tumor necrosis factor-α in induced sputum from patients with chronic obstructive pulmonary disease or asthma Am J Respir Crit Care Med 153 1996 530 534
56. S. Keely, N.J. Talley, and P.M. Hansbro Pulmonary-intestinal crosstalk in mucosal inflammatory disease Mucosal Immunol 5 2012 7 18
57. K. Shin, P.A. Nigrovic, J. Crish, E. Boilard, H.P. McNeil, and K.S. Larabee Mast cells contribute to autoimmune inflammatory arthritis via their tryptase/heparin complexes J Immunol 182 2009 647 656
58. M.J. Hamilton, M.J. Sinnamon, G.D. Lyng, J.N. Glickman, X. Wang, and W. Xing Essential role for mast cell tryptase in acute experimental colitis Proc Natl Acad Sci U S A 108 2011 290 295
59. L.B. Schwartz, R.A. Lewis, and K.F. Austen Tryptase from human pulmonary mast cells. Purification and characterization J Biol Chem 256 1981 11939 11943
60. J.S. Miller, G. Moxley, and L.B. Schwartz Cloning and characterization of a second complementary DNA for human tryptase J Clin Invest 86 1990 864 870
61. D.S. Reynolds, R.L. Stevens, W.S. Lane, M.H. Carr, K.F. Austen, and W.E. Serafin Different mouse mast cell populations express various combinations of at least six distinct mast cell serine proteases Proc Natl Acad Sci U S A 87 1990 3230 3234
62. K. Shin, G.F. Watts, H.C. Oettgen, D.S. Friend, A.D. Pemberton, and M.F. Gurish Mouse mast cell tryptase mMCP-6 is a critical link between adaptive and innate immunity in the chronic phase of Trichinella spiralis infection J Immunol 180 2008 4885 4891
63. S.W. Oh, C.I. Pae, D.K. Lee, F. Jones, G.K. Chiang, and H.O. Kim Tryptase inhibition blocks airway inflammation in a mouse asthma model J Immunol 168 2002 1992 2000
64. H.P. McNeil, D.S. Reynolds, V. Schiller, N. Ghildyal, D.S. Gurley, and K.F. Austen Isolation, characterization, and transcription of the gene encoding mouse mast cell protease 7 Proc Natl Acad Sci U S A 89 1992 11174 11178
65. J.E. Hunt, R.L. Stevens, K.F. Austen, J. Zhang, Z. Xia, and N. Ghildyal Natural disruption of the mouse mast cell protease 7 gene in the C57BL/6 mouse J Biol Chem 271 1996 2851 2855
66. S.M. Thakurdas, E. Melicoff, L. Sansores-Garcia, D.C. Moreira, Y. Petrova, and R.L. Stevens The mast cell-restricted tryptase mMCP-6 has a critical immunoprotective role in bacterial infections J Biol Chem 282 2007 20809 20815
67. A.N. Thorburn, B.J. O'Sullivan, R. Thomas, R.K. Kumar, P.S. Foster, and P.G. Gibson Pneumococcal conjugate vaccine-induced regulatory T cells suppress the development of allergic airways disease Thorax 65 2010 1053 1060
68. A.T. Essilfie, J.L. Simpson, J.C. Horvat, J.A. Preston, M.L. Dunkley, and P.S. Foster Haemophilus influenzae infection drives IL-17-mediated neutrophilic allergic airways disease PLoS Pathog 7 2011 e1002244
69. A.N. Thorburn, P.S. Foster, P.G. Gibson, and P.M. Hansbro Streptococcus pneumoniae components suppress allergic airways disease and natural killer T cells by inducing regulatory T cells J Immunol 188 2012 4611 4620
70. J.C. Horvat, K.W. Beagley, M.A. Wade, J.A. Preston, N.G. Hansbro, and D.K. Hickey Neonatal chlamydial infection induces mixed T-cell responses that drive allergic airway disease Am J Respir Crit Care Med 176 2007 556 564
71. J.C. Horvat, M.R. Starkey, R.Y. Kim, S. Phipps, P.G. Gibson, and K.W. Beagley Early-life chlamydial lung infection enhances allergic airways disease through age-dependent differences in immunopathology J Allergy Clin Immunol 125 2010 617 625
72. R.K. Kumar, C. Herbert, and M. Kasper Reversibility of airway inflammation and remodelling following cessation of antigenic challenge in a model of chronic asthma Clin Exp Allergy 34 2004 1796 1802
73. M. O'Reilly, S.B. Hooper, B.J. Allison, S.J. Flecknoe, K. Snibson, and R. Harding Persistent bronchiolar remodeling following brief ventilation of the very immature ovine lung Am J Physiol Lung Cell Mol Physiol 297 2009 L992 L1001
74. S. Braber, K.A. Verheijden, P.A. Henricks, A.D. Kraneveld, and G. Folkerts A comparison of fixation methods on lung morphology in a murine model of emphysema Am J Physiol Lung Cell Mol Physiol 299 2010 L843 L851
75. J.A. Preston, A.T. Essilfie, J.C. Horvat, M.A. Wade, K.W. Beagley, and P.G. Gibson Inhibition of allergic airways disease by immunomodulatory therapy with whole killed Streptococcus pneumoniae Vaccine 25 2007 8154 8162
76. J.J. Li, W. Wang, K.J. Baines, N.A. Bowden, P.M. Hansbro, and P.G. Gibson IL-27/IFN-γ induce MyD88-dependent steroid-resistant airway hyperresponsiveness by inhibiting glucocorticoid signaling in macrophages J Immunol 185 2010 4401 4409
77. R.S. Harris Pressure-volume curves of the respiratory system Respir Care 50 2005 78 98
78. D. Bedoret, H. Wallemacq, T. Marichal, C. Desmet, F. Quesada Calvo, and E. Henry Lung interstitial macrophages alter dendritic cell functions to prevent airway allergy in mice J Clin Invest 119 2009 3723 3738
79. J.A. Preston, K.W. Beagley, P.G. Gibson, and P.M. Hansbro Genetic background affects susceptibility in nonfatal pneumococcal bronchopneumonia Eur Respir J 23 2004 224 231
80. J.A. Preston, A.N. Thorburn, M.R. Starkey, E.L. Beckett, J.C. Horvat, and M.A. Wade Streptococcus pneumoniae infection suppresses allergic airways disease by inducing regulatory T-cells Eur Respir J 37 2011 53 64
81. A.C. Hsu, I. Barr, P.M. Hansbro, and P.A. Wark Human influenza is more effective than avian influenza at antiviral suppression in airway cells Am J Respir Cell Mol Biol 44 2011 906 913
82. A.C. Hsu, K. Parsons, I. Barr, S. Lowther, D. Middleton, and P.M. Hansbro Critical role of constitutive type I interferon response in bronchial epithelial cell to influenza infection PLoS One 7 2012 e32947
83. J.M. Daley, A.A. Thomay, M.D. Connolly, J.S. Reichner, and J.E. Albina Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice J Leukoc Biol 83 2008 64 70
84. K.L. Asquith, J.C. Horvat, G.E. Kaiko, A.J. Carey, K.W. Beagley, and P.M. Hansbro Interleukin-13 promotes susceptibility to chlamydial infection of the respiratory and genital tracts PLoS Pathog 7 2011 e1001339
85. M. Zhu, I. Rhee, Y. Liu, and W. Zhang Negative regulation of FcεRI-mediated signaling and mast cell function by the adaptor protein LAX J Biol Chem 281 2006 18408 18413
86. M.K. Warren, and S.N. Vogel Bone marrow-derived macrophages: development and regulation of differentiation markers by colony-stimulating factor and interferons J Immunol 134 1985 982 989
87. S. Takeshita, K. Kaji, and A. Kudo Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts J Bone Miner Res 15 2000 1477 1488