Chlamydial respiratory infection during allergen sensitization drives neutrophilic allergic airways disease

Journal of Immunology

Volumn 184, Issue 8, 2010, Pages 4159-4169

  Horvat, Jay C ^a   Starkey, Malcolm R ^a   Kim, Richard Y ^a   Beagley, Kenneth W ^a,b   Preston, Julie A ^a   Gibson, Peter G ^a   Foster, Paul S ^a   Hansbro, Philip M ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 5; METHACHOLINE; OVALBUMIN;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HYPERPLASIA; CHLAMYDIASIS; CONTROLLED STUDY; CYTOKINE RELEASE; EOSINOPHIL; FEMALE; IMMUNOPATHOGENESIS; LYMPHOCYTOPOIESIS; MOUSE; MUCOUS CELL; MUCUS SECRETION; NEUTROPHIL; NEUTROPHILIA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIZATION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; CHLAMYDIA; DISEASE MODEL; IMMUNOLOGY; IMMUNOPHENOTYPING; INFLAMMATION; MICROBIOLOGY; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; RESPIRATORY TRACT ALLERGY;

ALLERGENS; ANIMALS; ASTHMA; CHLAMYDIA INFECTIONS; CHLAMYDIA MURIDARUM; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOPHENOTYPING; INFLAMMATION; MICE; MICE, INBRED BALB C; NEUTROPHIL INFILTRATION; NEUTROPHILS; OVALBUMIN; RESPIRATORY HYPERSENSITIVITY; TH1 CELLS; TH2 CELLS;

EID: 77952746227     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902287     Document Type: Article

References (70)

1. WHO/NHLBI. 1995. Global strategy for asthma management and prevention. National Institutes of Health, National Heart, Lung, and Blood Institute. Publication No, Bethesda, MD, p. 95-3659.
2. Hilman, B. 1997. NHLBI guidelines for diagnosis and management of asthma. National Institutes of Health, National Heart, Lung, and Blood Institute. Publication No, Bethesda, MD, p. 97-4051.
3. Prescott, S. L., C. Macaubas, B. J. Holt, T. B. Smallacombe, R. Loh, P. D. Sly, and P. G. Holt. 1998. Transplacental priming of the human immune system to environmental allergens: universal skewing of initial T cell responses toward the Th2 cytokine profile. J. Immunol. 160: 4730-4737.
4. Jarman, E. R., and J. R. Lamb. 2004. Reversal of established CD4+ type 2 T helper-mediated allergic airway inflammation and eosinophilia by therapeutic treatment with DNA vaccines limits progression towards chronic inflammation and remodelling. Immunology 112: 631-642.
5. Foster, P. S., M. Martinez-Moczygemba, D. P. Huston, and D. B. Corry. 2002. Interleukins-4, -5, and -13: emerging therapeutic targets in allergic disease. Pharmacol. Ther. 94: 253-264.
6. Rogers, D. F. 2004. Airway mucus hypersecretion in asthma: an undervalued pathology? Curr. Opin. Pharmacol. 4: 241-250.
7. O'Byrne, P. M., and M. D. Inman. 2003. Airway hyperresponsiveness. Chest 123 (3, Suppl)411S-416S.
8. Hansbro, P. M., K. W. Beagley, J. C. Horvat, and P. G. Gibson. 2004. Role of atypical bacterial infection of the lung in predisposition/protection of asthma. Pharmacol. Ther. 101: 193-210.
9. Horvat, J. C., K. W. Beagley, M. A. Wade, J. A. Preston, N. G. Hansbro, D. K. Hickey, G. E. Kaiko, P. G. Gibson, P. S. Foster, and P. M. Hansbro. 2007. Neonatal chlamydial infection induces mixed T-cell responses that drive allergic airway disease. Am. J. Respir. Crit. Care Med. 176: 556-564.
10. Yang, X., K. T. HayGlass, and R. C. Brunham. 1996. Genetically determined differences in IL-10 and IFN-gamma responses correlate with clearance of Chlamydia trachomatis mouse pneumonitis infection. J. Immunol. 156: 4338-4344. (Pubitemid 26165833)
11. Yang, X., J. Gartner, L. Zhu, S. Wang, and R. C. Brunham. 1999. IL-10 gene knockout mice show enhanced Th1-like protective immunity and absent granuloma formation following Chlamydia trachomatis lung infection. J. Immunol. 162: 1010-1017. (Pubitemid 29035428)
12. Gibson, P. G., J. L. Simpson, and N. Saltos. 2001. Heterogeneity of airway inflammation in persistent asthma : evidence of neutrophilic inflammation and increased sputum interleukin-8. Chest 119: 1329-1336.
13. Wenzel, S. E., L. B. Schwartz, E. L. Langmack, J. L. Halliday, J. B. Trudeau, R. L. Gibbs, and H. W. Chu. 1999. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am. J. Respir. Crit. Care Med. 160: 1001-1008.
14. Ordoñez, C. L., T. E. Shaughnessy, M. A.Matthay, and J. V. Fahy. 2000. Increased neutrophil numbers and IL-8 levels in airway secretions in acute severe asthma: Clinical and biologic significance. Am. J. Respir. Crit. Care Med. 161: 1185-1190.
15. Simpson, J. L., R. Scott, M. J. Boyle, and P. G. Gibson. 2006. Inflammatory subtypes in asthma: assessment and identification using induced sputum. Respirology 11: 54-61.
16. Simpson, J. L., T. V. Grissell, J. Douwes, R. J. Scott, M. J. Boyle, and P. G. Gibson. 2007. Innate immune activation in neutrophilic asthma and bronchiectasis. Thorax 62: 211-218. (Pubitemid 46579799)
17. Shannon, J., P. Ernst, Y. Yamauchi, R. Olivenstein, C. Lemiere, S. Foley, L. Cicora, M. Ludwig, Q. Hamid, and J. G. Martin. 2008. Differences in airway cytokine profile in severe asthma compared to moderate asthma. Chest 133: 420-426. (Pubitemid 351272400)
18. Wark, P. A., S. L. Johnston, I. Moric, J. L. Simpson, M. J. Hensley, and P. G. Gibson. 2002. Neutrophil degranulation and cell lysis is associated with clinical severity in virus-induced asthma. Eur. Respir. J. 19: 68-75.
19. Wark, P. A. B., S. L. Johnston, J. L. Simpson, M. J. Hensley, and P. G. Gibson. 2002. Chlamydia pneumoniae immunoglobulin A reactivation and airway inflammation in acute asthma. Eur. Respir. J. 20: 834-840.
20. Bai, H., J. Yang, H. Qiu, S. Wang, Y. Fan, X. Han, S. Xie, and X. Yang. 2005. Intranasal inoculation of Chlamydia trachomatis mouse pneumonitis agent induces significant neutrophil infiltration which is not efficient in controlling the infection in mice. Immunology 114: 246-254. (Pubitemid 40208941)
21. Rodriguez, N., F. Fend, L. Jennen, M. Schiemann, N. Wantia, C. U. Prazeres da Costa, S. Dürr, U. Heinzmann, H. Wagner, and T. Miethke. 2005. Polymorphonuclear neutrophils improve replication of Chlamydia pneumoniae in vivo upon MyD88-dependent attraction. J. Immunol. 174: 4836-4844. (Pubitemid 40504567)
22. Bilenki, L., S. Wang, Y. Fan, J. Yang, X. Han, and X. Yang. 2002. Chlamydia trachomatis infection inhibits airway eosinophilic inflammation induced by ragweed. Clin. Immunol. 102: 28-36.
23. Han, X., Y. Fan, S. Wang, L. Jiao, H. Qiu, and X. Yang. 2008. NK cells contribute to intracellular bacterial infection-mediated inhibition of allergic responses. J. Immunol. 180: 4621-4628.
24. Bullens, D. M. 2007. Measuring T cell cytokines in allergic upper and lower airway inflammation: can we move to the clinic? Inflamm. Allergy Drug Targets 6: 81-90.
25. Kumar, R. K., D. C. Webb, C. Herbert, and P. S. Foster. 2006. Interferon-γ as a possible target in chronic asthma. Inflamm. Allergy Drug Targets 5: 253-256.
26. Truyen, E., L. Coteur, E. Dilissen, L. Overbergh, L. J. Dupont, J. L. Ceuppens, and D. M. A. Bullens. 2006. Evaluation of airway inflammation by quantitative Th1/Th2 cytokine mRNA measurement in sputum of asthma patients. Thorax 61: 202-208.
27. Liu, L., N. N. Jarjour, W. W. Busse, and E. A. B. Kelly. 2004. Enhanced generation of helper T type 1 and 2 chemokines in allergen-induced asthma. Am. J. Respir. Crit. Care Med. 169: 1118-1124.
28. Mattes, J., M. Yang, A. Siqueira, K. Clark, J. MacKenzie, A. N. J. McKenzie, D. C. Webb, K. I. Matthaei, and P. S. Foster. 2001. IL-13 induces airways hyper-reactivity independently of the IL-4R alpha chain in the allergic lung. J. Immunol. 167: 1683-1692. (Pubitemid 32703171)
29. Williams, D. M., B. G. Grubbs, J. Schachter, and D. M. Magee. 1993. Gamma interferon levels during Chlamydia trachomatis pneumonia in mice. Infect. Immun. 61: 3556-3558.
30. Phipps, S., C. E. Lam, S. Mahalingam, M. Newhouse, R. Ramirez, H. F. Rosenberg, P. S. Foster, and K. I. Matthaei. 2007. Eosinophils contribute to innate antiviral immunity and promote clearance of respiratory syncytial virus. Blood 110: 1578-1586. (Pubitemid 47443974)
31. Snelgrove, R. J., J. Goulding, A. M. Didierlaurent, D. Lyonga, S. Vekaria, L. Edwards, E. Gwyer, J. D. Sedgwick, A. N. Barclay, and T. Hussell. 2008. A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat. Immunol. 9: 1074-1083.
32. Huang, J., M.-D. Wang, S. Lenz, D. Gao, and B. Kaltenboeck. 1999. IL-12 administered during Chlamydia psittaci lung infection in mice confers immediate and long-term protection and reduces macrophage inflammatory protein-2 level and neutrophil infiltration in lung tissue. J. Immunol. 162: 2217-2226. (Pubitemid 29288844)
33. Nigg, C., and M. D. Eaton. 1944. Isolation from normal mice of a pneumotropic virus which forms elementary bodies. J. Exp. Med. 79: 497-510.
34. Gogolak, F. M. 1953. The histopathology of murine pneumonitis infection and the growth of the virus in the mouse lung. J. Infect. Dis. 92: 254-272.
35. Fahy, J. V., K. W. Kim, J. Liu, and H. A. Boushey. 1995. Prominent neutrophilic inflammation in sputum from subjects with asthma exacerbation. J. Allergy Clin. Immunol. 95: 843-852.
36. Sur, S., T. B. Crotty, G. M. Kephart, B. A. Hyma, T. V. Colby, C. E. Reed, L. W. Hunt, and G. J. Gleich. 1993. Sudden-onset fatal asthma. A distinct entity with few eosinophils and relatively more neutrophils in the airway submucosa? Am Rev Respir Res 148: 713-719.
37. Friedlander, S. L., and W. W. Busse. 2005. The role of rhinovirus in asthma exacerbations. J. Allergy Clin. Immunol. 116: 267-273.
38. ten Brinke, A., J. T. van Dissel, P. J. Sterk, A. H. Zwinderman, K. F. Rabe, and E. H. Bel. 2001. Persistent airflow limitation in adult-onset nonatopic asthma is associated with serologic evidence of Chlamydia pneumoniae infection. J. Allergy Clin. Immunol. 107: 449-454.
39. Hahn, D. 1998. Chlamydia pneumoniae and asthma. Thorax 53: 1095-1096.
40. van Zandbergen, G., J. Gieffers, H. Kothe, J. Rupp, A. Bollinger, E. Aga, M. Klinger, H. Brade, K. Dalhoff, M. Maass, et al. 2004. Chlamydia pneumoniae multiply in neutrophil granulocytes and delay their spontaneous apoptosis. J. Immunol. 172: 1768-1776.
41. Hellings, P. W., A. Kasran, Z. Liu, P. Vandekerckhove, A. Wuyts, L. Overbergh, C. Mathieu, and J. L. Ceuppens. 2003. Interleukin-17 orchestrates the granulocyte influx into airways after allergen inhalation in a mouse model of allergic asthma. Am. J. Respir. Cell Mol. Biol. 28: 42-50.
42. Manetti, R., P. Parronchi, M. G. Giudizi, M. P. Piccinni, E. Maggi, G. Trinchieri, and S. Romagnani. 1993. Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med. 177: 1199-1204.
43. Lindén, A., M. Laan, and G. P. Anderson. 2005. Neutrophils, interleukin-17A and lung disease. Eur. Respir. J. 25: 159-172.
44. Molet, S., Q. Hamid, F. Davoine, E. Nutku, R. Taha, N. Pagé, R. Olivenstein, J. Elias, and J. Chakir. 2001. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J. Allergy Clin. Immunol. 108: 430-438.
45. Bullens, D. M., E. Truyen, L. Coteur, E. Dilissen, P. W. Hellings, L. J. Dupont, and J. L. Ceuppens. 2006. IL-17 mRNA in sputum of asthmatic patients: linking T cell driven inflammation and granulocytic influx? Respir. Res. 7: 135.
46. Cui, J., S. Pazdziorko, J. S. Miyashiro, P. Thakker, J. W. Pelker, C. Declercq, A. Jiao, J. Gunn, L. Mason, J. P. Leonard, et al. 2005. TH1-mediated airway hyperresponsiveness independent of neutrophilic inflammation. J. Allergy Clin. Immunol. 115: 309-315.
47. McKinley, L., J. F. Alcorn, A. Peterson, R. B. Dupont, S. Kapadia, A. Logar, A. Henry, C. G. Irvin, J. D. Piganelli, A. Ray, and J. K. Kolls. 2008. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J. Immunol. 181: 4089-4097.
48. Macdowell, A. L., and S. P. Peters. 2007. Neutrophils in asthma. Curr. Allergy Asthma Rep. 7: 464-468.
49. Green, R. H., C. E. Brightling, G. Woltmann, D. Parker, A. J. Wardlaw, and I. D. Pavord. 2002. Analysis of induced sputum in adults with asthma: identification of subgroup with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax 57: 875-879.
50. Hauber, H. P., M. Gotfried, K. Newman, R. Danda, R. J. Servi, P. Christodoulopoulos, and Q. Hamid. 2003. Effect of HFA-flunisolide on peripheral lung inflammation in asthma. J. Allergy Clin. Immunol. 112: 58-63.
51. Meagher, L. C., J. M. Cousin, J. R. Seckl, and C. Haslett. 1996. Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J. Immunol. 156: 4422-4428.
52. Cox, G. 1995. Glucocorticoid treatment inhibits apoptosis in human neutrophils. Separation of survival and activation outcomes. J. Immunol. 154: 4719-4725.
53. Tsumura, N., U. Emre, P. Roblin, and M. R. Hammerschlag. 1996. Effect of hydrocortisone succinate on growth of Chlamydia pneumoniae in vitro. J. Clin. Microbiol. 34: 2379-2381.
54. Laitinen, K., A. L. Laurila, M. Leinonen, and P. Saikku. 1996. Reactivation of Chlamydia pneumoniae infection in mice by cortisone treatment. Infect. Immun. 64: 1488-1490.
55. Black, P. N., R. Scicchitano, C. R. Jenkins, F. Blasi, L. Allegra, J. Wlodarczyk, and B. C. Cooper. 2000. Serological evidence of infection with Chlamydia pneumoniae is related to the severity of asthma. Eur. Respir. J. 15: 254-259.
56. Cho, Y. S., T. B. Kim, T. H. Lee, K. A. Moon, J. Lee, Y. K. Kim, K. Y. Lee, and H. B. Moon. 2005. Chlamydia pneumoniae infection enhances cellular proliferation and reduces steroid responsiveness of human peripheral blood mononuclear cells via a tumor necrosis factor-alpha-dependent pathway. Clin. Exp. Allergy 35: 1625-1631.
57. Lee, J., G. Cacalano, T. Camerato, K. Toy, M. W. Moore, and W. I. Wood. 1995. Chemokine binding and activities mediated by the mouse IL-8 receptor. J. Immunol. 155: 2158-2164.
58. Maus, U., S. Herold, H. Muth, R. Maus, L. Ermert, M. Ermert, N. Weissmann, S. Rosseau, W. Seeger, F. Grimminger, and J. Lohmeyer. 2001. Monocytes recruited into the alveolar air space of mice show a monocytic phenotype but upregulate CD14. Am. J. Physiol. Lung Cell. Mol. Physiol. 280: L58-L68.
59. Imai, T., M. Nagira, S. Takagi, M. Kakizaki, M. Nishimura, J. Wang, P. W. Gray, K. Matsushima, and O. Yoshie. 1999. Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine andmacrophage-derived chemokine. Int. Immunol. 11: 81-88.
60. Zingoni, A., H. Soto, J. A. Hedrick, A. Stoppacciaro, C. T. Storlazzi, F. Sinigaglia, D. D'Ambrosio, A. O'Garra, D. Robinson, M. Rocchi, et al. 1998. The chemokine receptor CCR8 is preferentially expressed in Th2 but not Th1 cells. J. Immunol. 161: 547-551.
61. Kuchroo, V. K., M. P. Das, J. A. Brown, A. M. Ranger, S. S. Zamvil, R. A. Sobel, H. L. Weiner, N. Nabavi, and L. H. Glimcher. 1995. B7-1 and B7-2 costimulatory molecules activate differentially the Th1/Th2 developmental pathways: application to autoimmune disease therapy. Cell 80: 707-718.
62. Rutkowski, R., T. Moniuszko, A. Stasiak-Barmuta, B. Kosztyła- Hojna, M. Alifier, K. Rutkowski, and A. Tatarczuk-Krawiel. 2003. CD80 and CD86 expression on LPS-stimulated monocytes and the effect of CD80 and CD86 blockade on IL-4 and IFN-gamma production in nonatopic bronchial asthma. Arch. Immunol. Ther. Exp. (Warsz.) 51: 421-428.
63. Odobasic, D., M. T. Leech, J. R. Xue, and S. R. Holdsworth. 2008. Distinct in vivo roles of CD80 and CD86 in the effector T-cell responses inducing antigen-induced arthritis. Immunology 124: 503-513. (Pubitemid 351962546)
64. Megiovanni, A. M., F. Sanchez, M. Robledo-Sarmiento, C. Morel, J. C. Gluckman, and S. Boudaly. 2006. Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J. Leukoc. Biol. 79: 977-988.
65. Bennouna, S., S. K. Bliss, T. J. Curiel, and E. Y. Denkers. 2003. Cross-talk in the innate immune system: neutrophils instruct recruitment and activation of dendritic cells during microbial infection. J. Immunol. 171: 6052-6058. (Pubitemid 37467225)
66. Alemán, M., S. de la Barrera, P. Schierloh, N. Yokobori, M. Baldini, R. Musella, E. Abbate, and M. Sasiain. 2007. Spontaneous or Mycobacterium tuberculosis-induced apoptotic neutrophils exert opposite effects on the dendritic cell-mediated immune response. Eur. J. Immunol. 37: 1524-1537.
67. Culshaw, S., O. R. Millington, J. M. Brewer, and I. B. McInnes. 2008. Murine neutrophils present Class II restricted antigen. Immunol. Lett. 118: 49-54.
68. Moser, M. 2001. Regulation of Th1/Th2 development by antigen-presenting cells in vivo. Immunobiology 204: 551-557. (Pubitemid 34134167)
69. Sozzani, S., W. Luini, A. Borsatti, N. Polentarutti, D. Zhou, L. Piemonti, G. D'Amico, C. A. Power, T. N. Wells, M. Gobbi, et al. 1997. Receptor expression and responsiveness of human dendritic cells to a defined set of CC and CXC chemokines. J. Immunol. 159: 1993-2000.
70. Zhou, X., Q. Chen, J. Moore, J. K. Kolls, S. Halperin, and J.Wang. 2009. Critical role of the interleukin-17/interleukin-17 receptor axis in regulating host susceptibility to respiratory infection with Chlamydia species. Infect. Immun. 77: 5059-5070.