Heme oxygenase-1-mediated CD4+CD25high regulatory T cells suppress allergic airway inflammation

Journal of Immunology

Volumn 177, Issue 9, 2006, Pages 5936-5945

  Xia, Zhen Wei ^a,b   Zhong, Wen Wei ^a   Xu, Li Qing ^a   Sun, Jian Le ^a   Shen, Qing Xiang ^a   Wang, Ji Guang ^a   Shao, Jie ^a   Li, Yun Zhu ^a   Yu, Shan Chang ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; HEME OXYGENASE 1; HEMIN; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; MESSENGER RNA; OVALBUMIN; PROTOPORPHYRIN TIN; TRANSCRIPTION FACTOR FOXP3;

ALLERGY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTHMA; CD4+ CD25+ T LYMPHOCYTE; CELL CULTURE; CELL INFILTRATION; CONTROLLED STUDY; CULTURE MEDIUM; DISEASE MODEL; ENZYME ACTIVITY; EOSINOPHIL; FEMALE; FOXP3 GENE; GENE; GENE EXPRESSION; IFN GAMMA GENE; IL 4 GENE; IMMUNOREGULATION; LUNG LAVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; RESPIRATORY TRACT INFLAMMATION;

EID: 33750375087     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.9.5936     Document Type: Article

References (35)

1. + T cells. Biochem. Biophys. Res. Commun. 306: 701-705.
2. Ryter, S. W., and A. M. Choi. 2005. Heme oxygenase-1: redox regulation of a stress protein in lung and cell culture models. Antioxid. Redox. Signal. 7: 80-91.
3. Song, R., R. S. Mahidhara, F. Liu, W. Ning, L. E. Otterbein, and A. M. Choi. 2002. Carbon monoxide inhibits human airway smooth muscle cell proliferation via mitogen-activated protein kinase pathway. Am. J. Respir. Cell Mol. Biol. 27: 603-610.
4. Almolki, A., C. Taille, O. F. Martin, P. J. Jose, C. Zedda, M. Conti, J. Megret, D. Henin, M. Aubier, and J. Boczkowski. 2004. Heme oxygenase attenuates allergen-induced airway inflammation and hyperreactivity in guinea pigs. Am. J. Physiol. 287: L26-L34.
5. Umetsu, D. T., O. Akbari, and R. H. Dekruyff. 2003. Regulatory T cells control the development of allergic disease and asthma. J. Allergy Clin. Immunol. 112: 480-487.
6. + suppressor T cells: more questions than answers. Nat. Rev. Immunol. 3: 331-341.
7. Prescott, S. L., and J. A. Dunstan. 2005. Immune dysregulation in allergic respiratory disease: the role of T regulatory cells. Pulm. Pharmacol. Ther. 18: 217-228.
8. Gambineri, E., T. Torgerson, and H. Ochs. 2003. Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T-cell homeostasis. Curr. Opin. Rheumatol. 15: 430-435.
9. Hadeiba, H., and R. Locksley. 2003. Lung CD25 CD4 regulatory T cells suppress type 2 immune responses but not bronchial hyperreactivity. J. Immunol. 170: 5502-5510.
10. + T cells from the target organ of patients with rheumatoid arthritis. Eur. J. Immunol. 33: 215-223.
11. + T cells. Clin. Immunol. 115: 10-18.
12. + regulatory T cells. Int. Immunol. 16: 249-256.
13. Henderson, W. R., Jr., E. Y. Chi, and C. R. Maliszewski. 2000. Soluble IL-4 receptor inhibits airway inflammation following allergen challenge in a mouse model of asthma. J. Immunol. 164: 1086-1095.
14. Otterbein, L. E., and A. M. K. Choi. 2000. Heme oxygenase: colors of defense against cellular stress. Am. J. Physiol. 279: L1029-L1037.
15. Devesa, I., M. L. Ferrandiz, M. C. Terencio, L. A. Joosten, W. B. van den Berg, and M. J. Alcaraz. 2005. Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. Arthritis Rheum. 52: 3230-3238.
16. van Scott, M. R., J. P. Justice, J. F. Bradfield, E. Enright, A. Sigounas, and S. Sur. 2000. IL-10 reduces Th2 cytokine production and eosinophilia but augments airway reactivity in allergic mice. Am. J. Physiol. 278: L667-L674.
17. Otterbein, L. E., F. H. Bach, J. Alam, M. Soares, L. H. Tao, M. Wysk, R. J. Davis, R. A. Flavell, and A. M. Choi. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6: 422-428.
18. Chapman, J. T., L. E. Otterbein, J. A. Elias, and A. M. Choi. 2001. Carbon monoxide attenuates aeroallergen-induced inflammation in mice. Am. J. Physiol. 281: L209-L216.
19. Choi, B. M., H. O. Pae, Y. R. Jeong, Y. M. Kim, and H. T. Chung. 2005. Critical role of heme oxygenase-1 in Foxp3-mediated immune suppression. Biochem. Biophys. Res. Commun. 327: 1066-1071.
20. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061.
21. Walker, M. R., D. J. Kasprowicz, V. H. Oersuk, A. Benard, M. Van Landeghen, J. H. Buckner, and S. F. Ziegler. 2003. Induction of Foxp3 and acquisition of T regulatory activity by stimulated human CD4. Clin. Invest. 112: 1437-1443.
22. Sardana, M. K., and A. Kappas. 1987. Dual control mechanism for heme oxygenase: tin(IV)-protoporphyrin potently inhibits enzyme activity while markedly increasing content of enzyme protein in liver. Proc. Natl. Acad. Sci. USA 84: 2464-2468.
23. Ricchetti, G. A., L. M. Williams, and B. M. Foxwell. 2004. Heme oxygenase I expression induced by IL-10 requires STAT-3 and phosphoinositol-3 kinase and is inhibited by lipopolysaccharide. J. Leukocyte Biol. 76: 719-726.
24. Ning, W., R. Song, C. Li, E. Park, A. Mohsenin, A. M. Choi, and M. E. Choi. 2002. TGF-β1 stimulates HO-1 via the p38 mitogen-activated protein kinase in A549 pulmonary epithelial cells. Am. J. Physiol. 283: L1094-L1102.
25. Inoue, S., M. Suzuki, Y. Nagashima, S. Suzuki, T. Hashiba, T. Tsuburai, K. Ikehara, T. Matsuse, and Y. Ishigatsubo. 2001. Transfer of heme oxygenase 1 cDNA by a replication-deficient adenovirus enhances interleukin 10 production from alveolar macrophages that attenuates lipopolysaccharide-induced acute lung injury in mice. Hum. Gene Ther. 12: 967-979.
26. + regulatory T cell activity in both humans and mice. J. Immunol. 172: 834-842.
27. Duvernelle, C., V. Freund, and N. Frossard. 2003. Transforming growth factor-β and its role in asthma. Pulm. Pharmacol. Ther. 16: 181-196.
28. Stampfli, M. R., M. Cwiartka, B. U. Gajewska, D. Alvarez, S. A. Ritz, M. D. Inman, Z. Xing, and M. Jordana. 1999. Interleukin-10 gene transfer to the airway regulates allergic mucosal sensitization in mice. Am. J. Respir. Cell Mol. Biol. 21: 586-596.
29. Pae, H. O., G. S. Oh, B. M. Choi, S. C. Chae, Y. M. Kim, K. R. Chung, and H. T. Chung. 2004. Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of IL-2 production. J. Immunol. 172: 4744-4751.
30. Chen, S., M. H. Kapturczak, C. Wasserfall, O. Y. Glushakova, M. Campbell-Thompson, J. S. Deshane, R. Joseph, P. E. Cruz, W. W. Hauswirth, K. M. Madsen, et al. 2005. Interleukin 10 attenuates neointimal proliferation and inflammation in aortic allografts by a heme oxygenase-dependent pathway. Proc. Natl. Acad. Sci. USA 102: 7251-7256.
31. R cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197: 111-119.
32. + regulatory T cells. Semin. Immunol. 16: 89-97.
33. + cells: a naturally occurring population of regulatory T cells. Blood 98: 2736-2744.
34. + regulatory cells in human peripheral blood. J. Immunol. 167: 1245-1253.
35. - T cells through Foxp3 induction and down-regulation of Smad7. J. Immunol. 172: 5149-5153.