Impaired lung dendritic cell migration and T cell stimulation induced by immunostimulatory oligonucleotides contribute to reduced allergic airway inflammation

Journal of Immunology

Volumn 183, Issue 5, 2009, Pages 3443-3453

  Constabel, Hannelore ^a   Stankov, Metodi V ^a   Hartwig, Christina ^a   Tschernig, Thomas ^a   Behrens, Georg M N ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD86 ANTIGEN; CPG CONTAINING OLIGONUCLEOTIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OLIGONUCLEOTIDE; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG; ALLERGEN; AUTACOID; CPG OLIGONUCLEOTIDE; CPG-OLIGONUCLEOTIDE; OLIGODEOXYRIBONUCLEOTIDE;

ADOPTIVE TRANSFER; AIRWAY; ALLERGY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; BONE MARROW CELL; CD4 CD8 RATIO; CELL MIGRATION; COMPETITIVE INHIBITION; CONTROLLED STUDY; DENDRITIC CELL; EOSINOPHILIA; FEMALE; IMMUNOSTIMULATION; LUNG ALVEOLUS CELL; LUNG INFILTRATE; LUNG PARENCHYMA; LYMPH NODE; LYMPHOCYTE PROLIFERATION; MEDIASTINUM LYMPH NODE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT INFLAMMATION; T LYMPHOCYTE ACTIVATION; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL DIFFERENTIATION; CELL MOTION; CPG ISLAND; DRUG EFFECT; IMMUNOLOGY; IMMUNOPHENOTYPING; LUNG; LYMPHOCYTE ACTIVATION; PATHOLOGY; PHYSIOLOGY; RESPIRATORY TRACT ALLERGY; T LYMPHOCYTE; TRANSGENIC MOUSE;

ALLERGENS; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CPG ISLANDS; DENDRITIC CELLS; FEMALE; IMMUNOPHENOTYPING; INFLAMMATION MEDIATORS; LUNG; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGODEOXYRIBONUCLEOTIDES; RESPIRATORY HYPERSENSITIVITY; T-LYMPHOCYTES;

EID: 70349233989     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0804223     Document Type: Article

References (53)

1. Lambrecht, B. N., and H. Hammad. 2003. Taking our breath away: dendritic cells in the pathogenesis of asthma. Nat. Rev. Immunol. 3: 994-1003.
2. Wills-Karp, M., J. Santeliz, and C. L. Karp. 2001. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat. Rev. Immunol. 1: 69-75.
3. Kline, J. N. 2007. Eat dirt: CpG DNA and immunomodulation of asthma. Proc. Am. Thorac. Soc. 4: 283-288.
4. Akira, S., K. Takeda, and T. Kaisho. 2001. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2: 675-680. (Pubitemid 32747155)
5. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995.
6. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
7. Krieg, A. M. 2002. CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20: 709-760.
8. Klinman, D. M. 2004. Immunotherapeutic uses of CpG oligodeoxynucleotides. Nat. Rev. Immunol. 4: 249-258.
9. Broide, D., J. Schwarze, H. Tighe, T. Gifford, M. D. Nguyen, S. Malek, J. Van Uden, E. Martin-Orozco, E. W. Gelfand, and E. Raz. 1998. Immunostimulatory DNA sequences inhibit IL-5, eosinophilic inflammation, and airway hyperresponsiveness in mice. J. Immunol. 161: 7054-7062.
10. Kline, J. N., T. J. Waldschmidt, T. R. Businga, J. E. Lemish, J. V. Weinstock, P. S. Thorne, and A. M. Krieg. 1998. Modulation of airway inflammation by CpG oligodeoxynucleotides in a murine model of asthma. J. Immunol. 160: 2555-2559.
11. Sur, S., J. S. Wild, B. K. Choudhury, N. Sur, R. Alam, and D. M. Klinman. 1999. Long term prevention of allergic lung inflammation in a mouse model of asthma by CpG oligodeoxynucleotides. J. Immunol. 162: 6284-6293. (Pubitemid 29314994)
12. Serebrisky, D., A. A. Teper, C. K. Huang, S. Y. Lee, T. F. Zhang, B. H. Schofield, M. Kattan, H. A. Sampson, and X. M. Li. 2000. CpG oligodeoxynucleotides can reverse Th2-associated allergic airway responses and alter the B7.1/B7.2 expression in a murine model of asthma. J. Immunol. 165: 5906-5912.
13. Broide, D. H., G. Stachnick, D. Castaneda, J. Nayar, M. Miller, J. Y. Cho, M. Roman, J. Zubeldia, T. Hayashi, and E. Raz. 2001. Systemic administration of immunostimulatory DNA sequences mediates reversible inhibition of Th2 responses in a mouse model of asthma. J. Clin. Immunol. 21: 175-182.
14. Jahn-Schmid, B., U. Wiedermann, B. Bohle, A. Repa, D. Kraft, and C. Ebner. 1999. Oligodeoxynucleotides containing CpG motifs modulate the allergic TH2 response of BALB/c mice to Bet v 1, the major birch pollen allergen. J. Allergy Clin. Immunol. 104: 1015-1023.
15. Kohama, Y., O. Akizuki, K. Hagihara, E. Yamada, and H. Yamamoto. 1999. Immunostimulatory oligodeoxynucleotide induces TH1 immune response and inhibition of IgE antibody production to cedar pollen allergens in mice. J. Allergy Clin. Immunol. 104: 1231-1238.
16. Hirose, I., H. Tanaka, G. Takahashi, K. Wakahara, M. Tamari, T. Sakamoto, S. Kojima, N. Inagaki, and H. Nagai. 2008. Immunomodulatory effects of CpG oligodeoxynucleotides on house dust mite-induced airway inflammation in mice. Int. Arch. Allergy Immunol. 147: 6-16.
17. Kline, J. N., K. Kitagaki, T. R. Businga, and V. V. Jain. 2002. Treatment of established asthma in a murine model using CpG oligodeoxynucleotides. Am. J. Physiol. 283: L170-L179.
18. Jain, V. V., K. Kitagaki, T. Businga, I. Hussain, C. George, P. O'Shaughnessy, and J. N. Kline. 2002. CpG-oligodeoxynucleotides inhibit airway remodeling in a murine model of chronic asthma. J. Allergy Clin. Immunol. 110: 867-872.
19. Hessel, E. M., M. Chu, J. O. Lizcano, B. Chang, N. Herman, S. A. Kell, M. Wills-Karp, and R. L. Coffman. 2005. Immunostimulatory oligonucleotides block allergic airway inflammation by inhibiting Th2 cell activation and IgE-mediated cytokine induction. J. Exp. Med. 202: 1563-1573.
20. Kitagaki, K., V. V. Jain, T. R. Businga, I. Hussain, and J. N. Kline. 2002. Immunomodulatory effects of CpG oligodeoxynucleotides on established Th2 responses. Clin. Diagn. Lab. Immunol. 9: 1260-1269.
21. Kline, J. N., A. M. Krieg, T. J. Waldschmidt, Z. K. Ballas, V. Jain, and T. R. Businga. 1999. CpG oligodeoxynucleotides do not require TH1 cytokines to prevent eosinophilic airway inflammation in a murine model of asthma. J. Allergy Clin. Immunol. 104: 1258-1264.
22. Chiaramonte, M. G., M. Hesse, A. W. Cheever, and T. A. Wynn. 2000. CpG oligonucleotides can prophylactically immunize against Th2-mediated schistosome egg-induced pathology by an IL-12-independent mechanism. J. Immunol. 164: 973-985.
23. Broide, D. H., G. Stachnick, D. Castaneda, J. Nayar, M. Miller, J. Cho, M. Rodriquez, M. Roman, and E. Raz. 2001. Immunostimulatory DNA mediates inhibition of eosinophilic inflammation and airway hyperreactivity independent of natural killer cells in vivo. J. Allergy Clin. Immunol. 108: 759-763.
24. Ashino, S., D. Wakita, Y. Zhang, K. Chamoto, H. Kitamura, and T. Nishimura. 2008. CpG-ODN inhibits airway inflammation at effector phase through down-regulation of antigen-specific Th2-cell migration into lung. Int. Immunol. 20: 259-266.
25. Wilson, N. S., G. M. Behrens, R. J. Lundie, C. M. Smith, J. Waithman, L. Young, S. P. Forehan, A. Mount, R. J. Steptoe, K. D. Shortman, et al. 2006. Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat. Immunol. 7: 165-172.
26. Young, L. J., N. S. Wilson, P. Schnorrer, A. Mount, R. J. Lundie, N. L. La Gruta, B. S. Crabb, G. T. Belz, W. R. Heath, and J. A. Villadangos. 2007. Dendritic cell preactivation impairs MHC class II presentation of vaccines and endogenous viral antigens. Proc. Natl. Acad. Sci. USA 104: 17753-17758.
27. Cohn, L., R. J. Homer, A. Marinov, J. Rankin, and K. Bottomly. 1997. Induction of airway mucus production by T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production. J. Exp. Med. 186: 1737-1747.
28. Bandukwala, H. S., B. S. Clay, J. Tong, P. D. Mody, J. L. Cannon, R. A. Shilling, J. S. Verbeek, J. V. Weinstock, J. Solway, and A. I. Sperling. 2007. Signaling through FcγRIII is required for optimal T helper type (Th)2 responses and Th2- mediated airway inflammation. J. Exp. Med. 204: 1875-1889.
29. Henri, S., D. Vremec, A. Kamath, J. Waithman, S. Williams, C. Benoist, K. Burnham, S. Saeland, E. Handman, and K. Shortman. 2001. The dendritic cell populations of mouse lymph nodes. J. Immunol. 167: 741-748.
30. Vremec, D., J. Pooley, H. Hochrein, L. Wu, and K. Shortman. 2000. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164: 2978-2986. (Pubitemid 30148956)
31. Wilson, N. S., D. El Sukkari, G. T. Belz, C. M. Smith, R. J. Steptoe, W. R. Heath, K. Shortman, and J. A. Villadangos. 2003. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102: 2187-2194.
32. Belz, G. T., C. M. Smith, L. Kleinert, P. Reading, A. Brooks, K. Shortman, F. R. Carbone, and W. R. Heath. 2004. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. USA 101: 8670-8675.
33. Mueller, S. N., K. A. Hosiawa-Meagher, B. T. Konieczny, B. M. Sullivan, M. F. Bachmann, R. M. Locksley, R. Ahmed, and M. Matloubian. 2007. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science 317: 670-674.
34. Suzuki, K., T. Suda, T. Naito, K. Ide, K. Chida, and H. Nakamura. 2005. Impaired Toll-like receptor 9 expression in alveolar macrophages with no sensitivity to CpG DNA. Am. J. Respir. Crit. Care Med. 171: 707-713.
35. Chen, L., M. Arora, M. Yarlagadda, T. B. Oriss, N. Krishnamoorthy, A. Ray, and P. Ray. 2006. Distinct responses of lung and spleen dendritic cells to the TLR9 agonist CpG oligodeoxynucleotide. J. Immunol. 177: 2373-2383.
36. Wilson, N. S., and J. A. Villadangos. 2005. Regulation of antigen presentation and cross-presentation in the dendritic cell network: facts, hypothesis, and immunological implications. Adv. Immunol. 86: 241-305.
37. Garrett, W. S., L. M. Chen, R. Kroschewski, M. Ebersold, S. Turley, S. Trombetta, J. E. Galan, and I. Mellman. 2000. Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102: 325-334.
38. West, M. A., A. R. Prescott, E. L. Eskelinen, A. J. Ridley, and C. Watts. 2000. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its down-regulation. Curr. Biol. 10: 839-848.
39. Cella, M., A. Engering, V. Pinet, J. Pieters, and A. Lanzavecchia. 1997. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388: 782-787.
40. Askew, D., R. S. Chu, A. M. Krieg, and C. V. Harding. 2000. CpG DNA induces maturation of dendritic cells with distinct effects on nascent and recycling MHC-II antigen-processing mechanisms. J. Immunol. 165: 6889-6895. (Pubitemid 32001158)
41. Villadangos, J. A., M. Cardoso, R. J. Steptoe, D. van Berkel, J. Pooley, F. R. Carbone, and K. Shortman. 2001. MHC class II expression is regulated in dendritic cells independently of invariant chain degradation. Immunity 14: 739-749.
42. Wilson, N. S., D. El Sukkari, and J. A. Villadangos. 2004. Dendritic cells constitutively present self antigens in their immature state in vivo and regulate antigen presentation by controlling the rates of MHC class II synthesis and endocytosis. Blood 103: 2187-2195.
43. Shin, J. S., M. Ebersold, M. Pypaert, L. Delamarre, A. Hartley, and I. Mellman. 2006. Surface expression of MHC class II in dendritic cells is controlled by regulated ubiquitination. Nature 444: 115-118.
44. Van Niel, G., R. Wubbolts, T. Ten Broeke, S. I. Buschow, F. A. Ossendorp, C. J. Melief, G. Raposo, B. W. van Balkom, and W. Stoorvogel. 2006. Dendritic cells regulate exposure of MHC class II at their plasma membrane by oligoubiquitination. Immunity 25: 885-894.
45. Ohmura-Hoshino, M., Y. Matsuki, M. Aoki, E. Goto, M. Mito, M. Uematsu, T. Kakiuchi, H. Hotta, and S. Ishido. 2006. Inhibition of MHC class II expression and immune responses by c-MIR. J. Immunol. 177: 341-354.
46. Villadangos, J. A., P. Schnorrer, and N. S. Wilson. 2005. Control of MHC class II antigen presentation in dendritic cells: a balance between creative and destructive forces. Immunol. Rev. 207: 191-205.
47. Jirmo, A. C., C. H. Nagel, C. Bohnen, B. Sodeik, and G. M. Behrens. 2009. Contribution of direct and cross-presentation to CTL immunity against herpes simplex virus 1. J. Immunol. 182: 283-292.
48. Hayashi, T., L. Beck, C. Rossetto, X. Gong, O. Takikawa, K. Takabayashi, D. H. Broide, D. A. Carson, and E. Raz. 2004. Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J. Clin. Invest. 114: 270-279.
49. Legge, K. L., and T. J. Braciale. 2003. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18: 265-277.
50. Youn, C. J., M. Miller, K. J. Baek, J. W. Han, J. Nayar, S. Y. Lee, K. McElwain, S. McElwain, E. Raz, and D. H. Broide. 2004. Immunostimulatory DNA reverses established allergen-induced airway remodeling. J. Immunol. 173: 7556-7564.
51. Cho, J. Y., M. Miller, K. J. Baek, J. W. Han, J. Nayar, M. Rodriguez, S. Y. Lee, K. McElwain, S. McElwain, E. Raz, and D. H. Broide. 2004. Immunostimulatory DNA inhibits transforming growth factor-β expression and airway remodeling. Am. J. Respir. Cell Mol. Biol. 30: 651-661.
52. Fanucchi, M. V., E. S. Schelegle, G. L. Baker, M. J. Evans, R. J. McDonald, L. J. Gershwin, E. Raz, D. M. Hyde, C. G. Plopper, and L. A. Miller. 2004. Immunostimulatory oligonucleotides attenuate airways remodeling in allergic monkeys. Am. J. Respir. Crit. Care Med. 170: 1153-1157.
53. Eisenbarth, S. C., A. Zhadkevich, P. Ranney, C. A. Herrick, and K. Bottomly. 2004. IL-4-dependent Th2 collateral priming to inhaled antigens independent of Toll-like receptor 4 and myeloid differentiation factor 88. J. Immunol. 172: 4527-4534.