An integral role for heme oxygenase-1 and carbon monoxide in maintaining peripheral tolerance by CD4+CD25+ regulatory T cells

Journal of Immunology

Volumn 174, Issue 9, 2005, Pages 5181-5186

  Brusko, Todd M ^a   Wasserfall, Clive H ^a   Agarwal, Anupam ^b   Kapturczak, Matthias H ^b   Atkinson, Mark A ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; CD4 ANTIGEN; HEME OXYGENASE 1; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 2 RECEPTOR ALPHA;

AUTOIMMUNITY; CELL INTERACTION; ENZYME ACTIVITY; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; IMMUNOREGULATION; LYMPHOCYTE FUNCTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; T LYMPHOCYTE SUBPOPULATION;

EID: 17844374374     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.9.5181     Document Type: Short Survey

References (78)

1. Getshon, R. K., and K. Kondo. 1971. Infectious immunological tolerance. Immunology 21:903.
2. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, and M. Toda. 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155:1151.
3. + suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2:389.
4. high regulatory cells in human peripheral blood. J. Immunol. 167:1245.
5. Annacker, O., R. Pimenta-Araujo, O. Burlen-Defranoux, and A. Bandeira. 2001. On the ontogeny and physiology of regulatory T cells. Immunol. Rev. 182:5.
6. + regulatory T-lymphocytes: current concepts and therapeutic potential]. J. Soc. Biol. 196:263.
7. + immunoregulatory T cells: central players in the arena of peripheral rolerance. Semin. Immunol. 16:81.
8. Fontenot, J. D., and A. Y. Rudensky. 2004. Molecular aspects of regulatory T cell development. Semin. Immunol. 16:73.
9. Wildin, R. S., F. Ramsdell, J. Peake, F. Faravelli, J. L. Casanova, N. Buist, E. Levy-Lahad, M. Mazzella, O. Goulet, L. Perroni, et al. 2001. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat. Genet. 27:18.
10. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188:287.
11. + naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int. Immunol. 10:1969.
12. + T cells with regulatory properties from human blood. J. Exp. Med. 193:1303.
13. + T cells with regulatory properties isolated from peripheral blood. J. Exp. Med. 193:1285.
14. + thymocytes and peripheral T cells have immune suppressive activity in vitro. Eur. J. Immunol. 31:1247.
15. + cells: a naturally occurring population of regulatory T cells. Blood 98:2736.
16. Chen, W., W. Jin, N. Hardegen, K. J. Lei, L. Li, N. Marinos, G. McGrady, and S. M. Wahl. 2003.
17. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198:1875.
18. + regulatory T cells from human peripheral blood. J. Immunol. 166:7282.
19. + regulatory T cells is mediated by cell surface-bound transforming growth factor β. J. Exp. Med. 194:629.
20. + regulatory T cell activity in both humans and mice. J. Immunol. 172: 834.
21. + regulatory T cells independent of autocrine TGF-β1. Blood 103:4594.
22. + regulatory T cells can mediate suppressor function, in the absence of transforming growth factor β1 production and responsiveness. J. Exp. Med. 196:237.
23. Lucas, P. J., S. J. Kim, S. J. Melby, and R. E. Gress. 2000. Disruption of T cell homeostasis in mice expressing a T cell-specific dominant negative transforming growth factor β II receptor. J. Exp. Med. 191:1187.
24. Dong, Z., Y. Lavrovsky, M. A. Venkatachalam, and A. K. Roy. 2000. Heme oxygenase-1 in tissue pathology: the Yin and Yang. Am. J. Pathol. 156:1485.
25. Ryter, S. W., L. E. Otterbein, D. Motse, and A. M. Choi. 2002. Heme oxygenase/ carbon monoxide signaling pathways: regulation and functional significance. Mol. Cell Biochem. 234-235:249.
26. Otterbein, L. E., M. P. Soares, K. Yamashita, and F. H. Bach. 2003. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24:449.
27. Poss, K. D., and S. Tonegawa. 1997. Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci. USA 94:10919.
28. Kapturczak, M. H., C. Wasserfall, T. Brusko, M. Campbell-Thompson, T. M. Ellis, M. A. Atkinson, and A. Agarwal. 2004. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am. J. Pathol. 165:1045.
29. Kawashima, A., Y. Oda, A. Yachie, S. Koizumi, and I. Nakanishi. 2002. Heme oxygenase-1 deficiency: the first autopsy case. Hum. Pathol. 33:125.
30. Akamatsu, Y., M. Haga, S. Tyagi, K. Yamashita, A. V. Graca-Souza, R. Ollinger, E. Czismadia, G. A. May, E. Ifedigbo, L. E. Otterbein, et al. 2004. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J. 18:771.
31. Sato, K., J. Balla, L. Otterbein, R. N. Smith, S. Brouard, Y. Lin, E. Csizmadia, J. Sevigny, S. C. Robson, G. Vercellotti, et al. 2001. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J. Immunol. 166:4185.
32. Katoti, M., R. W. Busuttil, and J. W. Kupiec-Weglinski. 2002. Heme oxygenase-1 system in organ transplantation. Transplantation 74:905.
33. Braudeau, C., D. Bouchet, L. Tesson, S. Iyer, S. Remy, R. Buelow, I. Anegon, and C. Chauveau. 2004. Induction of long-term cardiac allograft survival by heme oxygenase-1 gene transfer. Gene Ther. 11:701.
34. McDaid, J., K. Yamashita, A. Chora, R. Ollinger, T. B. Strom, X. C. Li, F. H. Bach, and M. P. Soares. 2005. Heme oxygenase-1 modulates the allo-immune response by promoting activation-induced cell death of T cells. FASEB J. 19:458.
35. Pae, H. O., G. S. Oh, B. M. Choi, S. C. Chae, and H. T. Chung. 2003. Differential expressions of heme oxygenase-1 gene in. Biochem. Biophys. Res. Commun. 306:701.
36. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057.
37. +. J. Clin. Invest. 112:1437.
38. 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.
39. Otterbein, L. E., B. S. Zuckerbraun, M. Hagal, F. Liu, R. Song, A. Usheva, C. Stachulak, N. Bodyak, R. N. Smith, E. Csizmadia, et al. 2003. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat. Med. 9:183.
40. 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.
41. + immunoregulatory T cells is antigen nonspecific. J. Immunol. 164:183.
42. Otterbein, L. E., and A. M. Choi. 2000. Heme oxygenase: colors of defense against cellular stress. Am. J. Physiol. 279:11029.
43. Medina, J. H., and I. Izquierdo. 1995. Retrograde messengers, long-term potentiation and memory. Brain Res. Rev. 21:185.
44. + regulatory T cells. J. Immunol. 173:2428.
45. + T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J. Exp. Med. 199:1479.
46. Kumanogoh, A., X. Wang, I. Lee, C. Watanabe, M. Kamanaka, W. Shi, K. Yoshida, T. Sato, S. Habu, M. Itoh, et al. 2001. Increased T cell auto reactivity in the absence of CD40-CD40 ligand interactions: a role of CD40 in regulatory T cell development. J. Immunol. 166:353.
47. + immunoregulatory T cells that control autoimmune diabetes. Immunity 12:431.
48. + regulatory T cells. Semin. Immunol. 16:89.
49. + regulatory T cells constitutive expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 192:303.
50. + regulatory cells that control intestinal inflammation. J. Exp. Med. 192:295.
51. Alegre, M. L., K. A. Frauwirth, and C. B. Thompson. 2001. T-cell regulation by CD28 and CTLA-4. Nat. Rev. Immunol. 1:220.
52. Fallarino, F., U. Grohmann, K. W. Hwang, C. Orabona, C. Vacca, R. Bianchi, M. L. Belladonna, M. C. Fioretti, M. L. Alegre, and P. Puccetri. 2003. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol. 4:1206.
53. Fallarino, F., R. Bianchi, C., Orabona, C. Vacca, M. L. Belladonna, M. C. Fioretti, D. V. Serreze, U. Grohmann, and P. Puccetri. 2004. CTLA-4-Ig activates forkhead transcription factors and protects dendritic cells from oxidative stress in nonobese diabetic mice. J. Exp. Med. 200:1051.
54. Grohmann, U., F. Fallarino, and P. Puccetri. 2003. Tolerance, DCs and tryprophan: much ado abour IDO. Trends Immunol. 24:242.
55. Mofferr, J. R., and M. A. Namboodiri. 2003. Tryptophan and the immune response. Immunol. Cell Biol. 81:247.
56. Oh, G. S., H. O. Pae, B. M. Choi, S. C. Chae, H. S. Lee, D. G. Ryu, and H. T. Chung. 2004. 3-Hydroxyanthranilic acid, one of metabolites of tryptophan via indoleamine 2,3-dioxygenase pathway, suppresses inducible nitric oxide synthase expression by enhancing heme oxygenase-1 expression. Biochem. Biophys. Res. Commun. 320:1156.
57. Pae, H. O., B. M. Choi, G. S. Oh, M. S. Lee, D. G. Ryu, H. Y. Rhew, Y. M. Kim, and H. T. Chung. 2004. Roles of heme oxygenase-1 in the antiproliferative and antiapoptotic effects of nitric oxide on Jurkat cells. Mol. Pharmacol. 66:122. 2002.
58. Frumento, G., R. Rotondo, M. Torletti, G. Damonte, U. Benatti, G.B. Ferrara. 2002. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J. Exp. Med. 196: 459.
59. King, C., A. Ilic, K. Koelsch, and N. Sarvetnick. 2004. Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 117:265.
60. Klebanoff, C. A., H. T. Khong, P. A. Antony, D. C. Palmer, and N. P. Restifo. 2005. Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends Immunol 26:111.
61. Nath, K. A., J. J. Haggard, A. J. Croatt, J. P. Grande, K. D. Poss, and J. Alam. 2000. The indispensability of heme oxygenase-1 in protecting against acute heme protein-induced toxicity in vivo. Am. J. Pathol. 156:1527.
62. Choi, A. M., and J. Alam. 1996. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Respir. Cell Mol. Biol. 15:9.
63. Platt, J. L. and K. A. Nath. 1998. Heme oxygenase: protective gene or Trojan horse. Nat. Med. 4:1364.
64. Cavicchi, M., L. Gibbs, and B. J. Whittle. 2000. Inhibition of inducible nitric oxide synthase in the human intestinal epithelial cell line, DLD-1, by the inducers of heme oxygenase 1, bismuth salts, heme, and nitric oxide donors. Gut 47:771.
65. Agarwal, A., Y. Kim, A. J. Matas, J. Alam, and K. A. Nath. 1996. Gas-generating and nitric oxide synthase. Transplantation 61:93.
66. + antigen-specific regulatory T cells. Proc. Natl. Acad. Sci. USA 101(Suppl. 2):14622.
67. + regulatory T cell function. Eur. J. Immunol 34:2996.
68. Huang, C. T., C. J. Workman, D. Flies, X. Pan, A. L. Marson, G. Zhou, E. L. Hipkiss, S. Ravi, J. Kowalski, H. I. Levitsky, et al. 2004. Role of TAG-3 in regulatory T cells. Immunity 21:503.
69. Workman, C. J., L. S. Cauley, I. J. Kim, M. A. Blackman, D. L. Woodland, and D. A. Vignali. 2004. Lymphocyte activation gene-3 (CD223) regulates the size of the expanding T cell population following antigen activation in vivo. J. Immunol. 172: 5450.
70. Workman, C. J., and D. A, Vignali. 2003. The CD4-related molecule, LAG-3 (CD223), regulates the expansion of activated T cells. Eur. J. Immunol. 33:970.
71. + regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 3:135.
72. + immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 16:311.
73. + T cells. J. Immunol. 172:7306.
74. + regulatory T cell subsets. J. Leukocyte Biol. 74:471.
75. + regulatory T cell function. Eur. J. Immunol. 34:2480.
76. + T cells. J. Exp. Med. 183:2669.
77. Asseman, C., S, Fowler, and F. Powrie. 2000. Control of experimental inflammatory bowel disease by regulatory T cells. Am. J. Respir. Crit. Care Med. 162:S185.
78. + T cells. J. Autoimmun. 16:115.