Chlamydia muridarum infection subverts dendritic cell function to promote Th2 immunity and airways hyperreactivity

Journal of Immunology

Volumn 180, Issue 4, 2008, Pages 2225-2232

  Kaiko, Gerard E ^a   Phipps, Simon ^a   Hickey, Danica K ^a   Chuan, En Lam ^a   Hansbro, Philip M ^a   Foster, Paul S ^a,b   Beagley, Kenneth W ^a,b,c  

^a HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

^b Biology and Environment   (Australia)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD86 ANTIGEN; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADOPTIVE TRANSFER; AIRWAY RESISTANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; ASTHMA; BAGG ALBINO MOUSE; BONE MARROW; BRONCHUS HYPERREACTIVITY; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL SECRETION; CELLULAR IMMUNITY; CHLAMYDIA; CHLAMYDIASIS; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; DISEASE EXACERBATION; LUNG COMPLIANCE; LUNG LAVAGE; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TH2 CELL; ANIMAL; BONE MARROW CELL; CELL CULTURE; COCULTURE; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOPHYSIOLOGY; SECRETION; TRANSGENIC MOUSE;

ANIMALS; BONE MARROW CELLS; BRONCHIAL HYPERREACTIVITY; CELLS, CULTURED; CHLAMYDIA INFECTIONS; CHLAMYDIA MURIDARUM; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; IMMUNOPHENOTYPING; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, TRANSGENIC; TH2 CELLS;

EID: 42149111673     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.4.2225     Document Type: Article

References (57)

1. Beagley, K. W., and P. Timms. 2000. Chlamydia trachomatis infection: incidence, health costs and prospects for vaccine development. J. Reprod. Immunol. 48: 47-68.
2. Kuo, C. C., L. A. Jackson, L. A. Campbell, and J. T. Grayston. 1995. Chlamydia pneumoniae (TWAR). Clin. Microbiol. Rev. 8: 451-461.
3. Gibbs, R. G., N. Carey, and A. H. Davies. 1998. Chlamydia pneumoniae and vascular disease. Br. J. Surg. 85: 1191-1197.
4. Hahn, D. L. 1999. Chlamydia pneumoniae, asthma, and COPD: what is the evidence? Ann. Allergy Asthma Immunol. 83: 271-288.
5. Eugster, A. K. 1980. Chlamydiosis. In CRC Handbook Series in Zoonoses. J. H. Steele, ed. CRC Press, Boca Raton, pp. 357-417.
6. Godzik, K. L., E. R. O'Brien, S. K. Wang, and C. C. Kuo. 1995. In vitro susceptibility of human vascular wall cells to infection with Chlamydia pneumoniae. J. Clin. Microbiol. 33: 2411-2414.
7. Gaydos, C. A., J. T. Summersgill, N. N. Sahney, J. A. Ramirez, and T. C. Quinn. 1996. Replication of Chlamydia pneumoniae in vitro in human macrophages, endothelial cells, and aortic artery smooth muscle cells. Infect. Immun. 64: 1614-1620.
8. Matyszak, M. K., J. L. Young, and J. S. Gaston. 2002. Uptake and processing of Chlamydia trachomatis by human dendritic cells. Eur. J. Immunol. 32: 742-751.
9. Hook, C. E., M. K. Matyszak, and J. S. Gaston. 2005. Infection of epithelial and dendritic cells by Chlamydia trachomatis results in IL-18 and IL-12 production, leading to interferon-γ production by human natural killer cells. FEMS Immunol. Med. Microbiol. 45: 113-120.
10. Ito, J. I., and J. M. Lyons. 1999. Role of γ interferon in controlling murine chlamydial genital tract infection. Infect. Immun. 67: 5518-5521.
11. Rottenberg, M. E., A. C. Gigliotti Rothfuchs, D. Gigliotti, C. Svanholm, L. Bandholtz, and H. Wigzell. 1999. Role of innate and adaptive immunity in the outcome of primary infection with Chlamydia pneumoniae, as analyzed in genetically modified mice. J. Immunol. 162: 2829-2836.
12. Farrar, J. D., H. Asnagli, and K. M. Murphy. 2002. T helper subset development: roles of instruction, selection, and transcription. J. Clin. Invest. 109: 431-435.
13. Lu, H., X. Yang, K. Takeda, D. Zhang, Y. Fan, M. Luo, C. Shen, S. Wang, S. Akira, and R. C. Brunham. 2000. Chlamydia trachomatis mouse pneumonitis lung infection in IL-18 and IL-12 knockout mice: IL-12 is dominant over IL-18 for protective immunity. Mol. Med. 6: 604-612.
14. Shepherd, J. M., D. N. Duddleston, G. S. Hinks, A. K. Low, L. D. Russell, and C. A. Brown. 2002. Asthma: a brief overview. Am. J. Med. Sci. 324: 174-179.
15. Grunig, G., M. Warnock, A. E. Wakil, R. Venkayya, F. Brombacher, D. M. Rennick, D. Sheppard, M. Mohrs, D. D. Donaldson, R. M. Locksley, and D. B. Corry. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282: 2261-2263.
16. Zhu, Z., R. J. Homer, Z. Wang, Q. Chen, G. P. Geba, J. Wang, Y. Zhang, and J. A. Elias. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103: 779-788.
17. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science 282: 2258-2261.
18. + dendritic cells during allergen challenge abrogates the characteristic features of asthma. J. Exp. Med. 201: 981-991.
19. Lambrecht, B. N., B. Salomon, D. Klatzmann, and R. A. Pauwels. 1998. Dendritic cells are required for the development of chronic eosinophilic airway inflammation in response to inhaled antigen in sensitized mice. J. Immunol. 160: 4090-4097.
20. Cunningham, A. F., S. L. Johnston, S. A. Julious, F. C. Lampe, and M. E. Ward. 1998. Chronic Chlamydia pneumoniae infection and asthma exacerbations in children. Eur. Respir. J. 11: 345-349.
21. 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.
22. Wark, P. A., 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.
23. Webley, W. C., P. S. Salva, C. Andrzejewski, F. Cirino, C. A. West, Y. Tilahun, and E. S. Stuart. 2005. The bronchial lavage of pediatric patients with asthma contains infectious Chlamydia. Am. J. Respir. Crit. Care Med. 171: 1083-1088.
24. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R. M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176: 1693-1702.
25. Berry, L. J., D. K. Hickey, K. A. Skelding, S. Bao, A. M. Rendina, P. M. Hansbro, C. M. Gockel, and K. W. Beagley. 2004. Transcutaneous immunization with combined cholera toxin and CpG adjuvant protects against Chlamydia muridarum genital tract infection. Infect. Immun. 72: 1019-1028.
26. Lyons, A. B., and C. R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 171: 131-137.
27. Takeda, K., E. Hamelmann, A. Joetham, L. D. Shultz, G. L. Larsen, C. G. Irvin, and E. W. Gelfand. 1997. Development of eosinophilic airway inflammation and airway hyperresponsiveness in mast cell-deficient mice. J. Exp. Med. 186: 449-454.
28. Horvat, J. C., K. W. Beagley, M. A. Wade, J. A. Preston, N. G. Hansbro, D. K. Hickey, G. Kaiko, P. G. Gibson, P. S. Foster, and P. M. Hansbro. 2007. Neonatal chlamydial infection induces mixed T cell responses that drive allergic airways disease. Am. J. Respir. Crit. Care Med. 176: 556-564.
29. Rey-Ladino, J., X. Jiang, B. R. Gabel, C. Shen, and R. C. Brunham. 2007. Survival of Chlamydia muridarum within dendritic cells. Infect. Immun. 75: 3707-3714.
30. 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.
31. Bell, J. J., B. Min, R. K. Gregg, H. H. Lee, and H. Zaghouani. 2003. Break of neonatal Th1 tolerance and exacerbation of experimental allergic encephalomyelitis by interference with B7 costimulation. J. Immunol. 171: 1801-1808.
32. Elloso, M. M., and P. Scott. 1999. Expression and contribution of B7-1 (CD80) and B7-2 (CD86) in the early immune response to Leishmania major infection. J. Immunol. 162: 6708-6715.
33. Zhong, G., T. Fan, and L. Liu. 1999. Chlamydia inhibits interferon γ-inducible major histocompatibility complex class II expression by degradation of upstream stimulatory factor 1. J. Exp. Med. 189: 1931-1938.
34. Prebeck, S., C. Kirschning, S. Durr, C. da Costa, B. Donath, K. Brand, V. Redecke, H. Wagner, and T. Miethke. 2001. Predominant role of toll-like receptor 2 versus 4 in Chlamydia pneumoniae-induced activation of dendritic cells. J. Immunol. 167: 3316-3323.
35. Opitz, B., S. Forster, A. C. Hocke, M. Maass, B. Schmeck, S. Hippenstiel, N. Suttorp, and M. Krull. 2005. Nod1-mediated endothelial cell activation by Chlamydophila pneumoniae. Circ Res. 96: 319-326.
36. Derbigny, W. A., M. S. Kerr, and R. M. Johnson. 2005. Pattern recognition molecules activated by Chlamydia muridarum infection of cloned murine oviduct epithelial cell lines. J. Immunol. 175: 6065-6075.
37. Kanneganti, T. D., M. Lamkanfi, and G. Nunez. 2007. Intracellular NOD-like receptors in host defense and disease. Immunity 27: 549-559.
38. Bobryshev, Y. V., W. Cao, M. C. Phoon, D. Tran, V. T. Chow, R. S. Lord, and J. Lu. 2004. Detection of Chlamydophila pneumoniae in dendritic cells in atherosclerotic lesions. Atherosclerosis 173: 185-195.
39. Gervassi, A., M. R. Alderson, R. Suchland, J. F. Maisonneuve, K. H. Grabstein, and P. Probst. 2004. Differential regulation of inflammatory cytokine secretion by human dendritic cells upon Chlamydia trachomatis infection. Infect. Immun. 72: 7231-7239.
40. Wittkop, U., B. Krausse-Opatz, T. C. Gust, T. Kirsch, G. Hollweg, L. Kohler, M. Zenke, H. C. Gerard, A. P. Hudson, H. Zeidler, and A. D. Wagner. 2006. Fate of Chlamydophila pneumoniae in human monocyte-derived dendritic cells: long lasting infection. Microb. Pathog. 40: 101-109.
41. + Treg development and function during allergic airway inflammation in vivo. J. Clin. Invest. 115: 313-325.
42. Morrison, R. P., and H. D. Caldwell. 2002. Immunity to murine chlamydial genital infection. Infect. Immun. 70: 2741-2751.
43. 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.
44. Hogan, R. J., S. A. Mathews, S. Mukhopadhyay, J. T. Summersgill, and P. Timms. 2004. Chlamydial persistence: beyond the biphasic paradigm. Infect. Immun. 72: 1843-1855.
45. Dodge, I. L., M. W. Carr, M. Cernadas, and M. B. Brenner. 2003. IL-6 production by pulmonary dendritic cells impedes Th1 immune responses. J. Immunol. 170: 4457-4464.
46. 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.
47. Igietseme, J. U., G. A. Ananaba, J. Bolier, S. Bowers, T. Moore, T. Belay, F. O. Eko, D. Lyn, and C. M. Black. 2000. Suppression of endogenous IL-10 gene expression in dendritic cells enhances antigen presentation for specific Th1 induction: potential for cellular vaccine development. J. Immunol. 164: 4212-4219.
48. Yin, Z., J. Braun, L. Neure, P. Wu, L. Liu, U. Eggens, and J. Sieper. 1997. Crucial role of interleukin-10/interleukin-12 balance in the regulation of the type 2 T helper cytokine response in reactive arthritis. Arthritis Rheum. 40: 1788-1797.
49. Ohman, H., A. Tiitinen, M. Halttunen, S. Birkelund, G. Christiansen, P. Koskela, M. Lehtinen, J. Paavonen, and H. M. Surcel. 2006. IL-10 polymorphism and cell-mediated immune response to Chlamydia trachomatis. Genes Immun. 7: 243-249.
50. Redecke, V., H. Hacker, S. K. Datta, A. Fermin, P. M. Pitha, D. H. Broide, and E. Raz. 2004. Cutting edge: activation of toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J. Immunol. 172: 2739-2743.
51. Bellinghausen, I., P. Brand, I. Bottcher, B. Klostermann, J. Knop, and J. Saloga. 2003. Production of interleukin-13 by human dendritic cells after stimulation with protein allergens is a key factor for induction of T helper 2 cytokines and is associated with activation of signal transducer and activator of transcription-6. Immunology 108: 167-176.
52. McKenzie, A. N., J. A. Culpepper, R. de Waal Malefyt, F. Briere, J. Punnonen, G. Aversa, A. Sato, W. Dang, B. G. Cocks, S. Menon, et al. 1993. Interleukin 13, a T-cell-derived cytokine that regulates human monocyte and B-cell function. Proc. Natl. Acad. Sci. USA 90: 3735-3739.
53. Doherty, T. M., R. Kastelein, S. Menon, S. Andrade, and R. L. Coffman. 1993. Modulation of murine macrophage function by IL-13. J. Immunol. 151: 7151-7160.
54. Davidson, C., N. D. Verma, C. M. Robinson, K. M. Plain, G. T. Tran, S. J. Hodgkinson, and B. M. Hall. 2007. IL-13 prolongs allograft survival: association with inhibition of macrophage cytokine activation. Transpl. Immunol. 17: 178-186.
55. Chaves, A. C., I. P. Ceravolo, J. A. Gomes, C. L. Zani, A. J. Romanha, and R. T. Gazzinelli. 2001. IL-4 and IL-13 regulate the induction of indoleamine 2,3-dioxygenase activity and the control of Toxoplasma gondii replication in human fibroblasts activated with IFN-γ. Eur. J. Immunol. 31: 333-344.
56. Muzio, M., F. Re, M. Sironi, N. Polentarutti, A. Minty, D. Caput, P. Ferrara, A. Mantovani, and F. Colotta. 1994. Interleukin-13 induces the production of interleukin-1 receptor antagonist (IL-1ra) and the expression of the mRNA for the intracellular (keratinocyte) form of IL-1ra in human myelomonocytic cells. Blood 83: 1738-1743.
57. Zurawski, G., and J. E. de Vries. 1994. Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells. Immunol. Today 15: 19-26.