The development and immunosuppressive functions of CD4+ CD25+ FoxP3+ regulatory T cells are under influence of the adenosine-A2A adenosine receptor pathway

Frontiers in Immunology

Volumn 3, Issue JUL, 2012, Pages

  Ohta, Akio ^a   Kini, Radhika ^a   Ohta, Akiko ^a   Subramanian, Meenakshi ^a   Madasu, Manasa ^a   Sitkovsky, Michail ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

A2A adenosine receptor; Adenosine; Autoimmune; Cancer; Immunosuppression; Regulatory T cells

Indexed keywords

EID: 84871299189     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00190     Document Type: Article

References (46)

1. + T helper cells and hindered by naturally occurring T regulatory cells. J. Immunol. 174, 2591-2601.
2. Belikoff, B., Hatfield, S., Sitkovsky, M., and Remick, D. G. (2011). Adenosine negative feedback on A2A adenosine receptors mediates hyporesponsiveness in chronically septic mice. Shock 35, 382-387.
3. Blay, J., White, T. D., and Hoskin, D. W. (1997). The extracellular fluid of solid carcinomas contains immunosuppressive concentrations of adenosine. Cancer Res. 57, 2602-2605.
4. Cadieux, J. S., Leclerc, P., St-Onge, M., Dussault, A. A., Laflamme, C., Picard, S., Ledent, C., Borgeat, P., and Pouliot, M. (2005). Potentiation of neutrophil cyclooxygenase-2 by adenosine: an early anti-inflammatory signal. J. Cell Sci. 118, 1437-1447.
5. Chen, J. F., Huang, Z., Ma, J., Zhu, J., Moratalla, R., Standaert, D., Moskowitz, M. A., Fink, J. S., and Schwarzschild, M. A. (1999). A(2A) adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. J. Neurosci. 19, 9192-9200.
6. Deaglio, S., Dwyer, K. M., Gao, W., Friedman, D., Usheva, A., Erat, A., Chen, J. F., Enjyoji, K., Linden, J., Oukka, M., Kuchroo, V. K., Strom, T. B., and Robson, S. C. (2007). Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204, 1257-1265.
7. Facciabene, A., Peng, X., Hagemann, I. S., Balint, K., Barchetti, A., Wang, L. P., Gimotty, P. A., Gilks, C. B., Lal, P., Zhang, L., and Coukos, G. (2011). Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 475, 226-230.
8. + T lymphocytes against activation-induced cell death. FASEB J. 24,2631-2640.
9. + regulatory T cells upon repetitive in vitro stimulation. Eur. J. Immunol. 39, 1088-1097.
10. Huang, S., Apasov, S., Koshiba, M., and Sitkovsky, M. (1997). Role of A2a extracellular adenosine receptor-mediated signaling in adenosine-mediated inhibition of T-cell activation and expansion. Blood 90, 1600-1610.
11. Kobie, J. J., Shah, P. R., Yang, L., Rebhahn, J. A., Fowell, D. J., and Mosmann, T. R. (2006). T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5;-adenosine monophosphate to adenosine. J. Immunol. 177, 6780-6786.
12. Linnemann, C., Schildberg, F. A., Schurich, A., Diehl, L., Hegenbarth, S. I., Endl, E., Lacher, S., Müller, C. E., Frey, J., Simeoni, L., Schraven, B., Stabenow, D., and Knolle, P. A. (2009). Adenosine regulates CD8 T-cell priming by inhibition of membrane-proximal T-cell receptor signaling. Immunology 128, e728-e737.
13. Lu, L. F., and Rudensky, A. (2009). Molecular orchestration of differentiation and function of regulatory T cells. Genes Dev. 23, 1270-1282.
14. Lukashev, D., Ohta, A., Apasov, S., Chen, J. F., and Sitkovsky, M. (2004). Cutting edge: physiologic attenuation of proinflammatory transcription by the Gs protein-coupled A2A adenosine receptor in vivo. J. Immunol. 173, 21-24.
15. + lymphopenia following allogeneic hematopoietic stem cell transplantation. J. Clin. Invest. 120, 1479-1493.
16. Miller, S. L. (1953). A production of amino acids under possible primitive earth conditions. Science 117, 528-529.
17. Miller, S. L., and Urey, H. C. (1959). Organic compound synthesis on the primitive earth. Science 130, 245-251.
18. Nagahama, K., Nishimura, E., and Sakaguchi, S. (2007). Induction of tolerance by adoptive transfer of Treg cells. Methods Mol. Biol. 380, 431-442.
19. Ohkura, N., and Sakaguchi, S. (2011). Maturation of effector regulatory T cells. Nat. Immunol. 12, 283-284.
20. Ohta, A., and Sitkovsky, M. (2001). Role of G-protein-coupled adeno-sine receptors in downregulation of inflammation and protection from tissue damage. Nature 414, 916-920.
21. Ohta, A., Gorelik, E., Prasad, S. J., Ronchese, F., Lukashev, D., Wong, M. K., Huang, X., Caldwell, S., Liu, K., Smith, P., Chen, J. F., Jackson, E. K., Apasov, S., Abrams, S., and Sitkovsky, M. (2006). A2A adeno-sine receptor protects tumors from antitumor T cells. Proc. Natl. Acad. Sci. U.S.A. 103, 13132-13137.
22. Ohta, A., Lukashev, D., Jackson, E. K., Fredholm, B. B., and Sitkovsky, M. (2007). 1, 3, 7-trimethylxanthine (caffeine) may exacerbate acute inflammatory liver injury by weakening the physiological immunosuppressive mechanism. J. Immunol. 179, 7431-7438.
23. Ohta, A., Ohta, A., Madasu, M., Kini, R., Subramanian, M., Goel, N., and Sitkovsky, M. (2009). A2A adeno-sine receptor may allow expansion of T cells lacking effector functions in extracellular adenosine-rich microenvironments. J. Immunol. 183, 5487-5493.
24. Oró, J., and Kimball, A. P. (1961). Synthesis of purines under possible primitive earth conditions. I. Adenine from hydrogen cyanide. Arch. Biochem. Biophys. 94, 217-227.
25. + T cells. Nat. Immunol. 8, 1353-1362.
26. Pandiyan, P., Zheng, L., and Lenardo, M. J. (2011). The molecular mechanisms of regulatory T cell immuno-suppression. Front. Immun. 2:60. doi: 10.3389/fimmu.2011.00060
27. Pouliot, M., Fiset, M. E., Masse, M., Naccache, P. H., and Borgeat, P. (2002). Adenosine up-regulates cyclooxygenase-2 in human gran-ulocytes: impact on the balance of eicosanoid generation. J. Immunol. 169, 5279-5286.
28. Riley, J. L., June, C. H., and Blazar, B. R. (2009). Human T regulatory cell therapy: take a billion or so and call me in the morning. Immunity 30, 656-665.
29. Rudensky, A. Y. (2011). Regulatory T cells and Foxp3. Immunol. Rev. 241, 260-268.
30. Sakaguchi, S. (2011). Regulatory T cells: history and perspective. Methods Mol. Biol. 707, 3-17.
31. Sakaguchi, S., Fukuma, K., Kuribayashi, K., and Masuda, T. (1985). Organ-specific autoimmune diseases induced in mice by elimination of T cell subset. I. Evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J. Exp. Med. 161, 72-87.
32. Sakaguchi, S., Takahashi, T., and Nishizuka, Y. (1982). Study on cellular events in post-thymectomy autoimmune oophoritis in mice. II. Requirement of Lyt-1 cells in normal female mice for the prevention of oophoritis. J. Exp. Med. 156, 1577-1586.
33. Sakaguchi, S., Wing, K., Onishi, Y., Prieto-Martin, P., and Yamaguchi, T. (2009). Regulatory T cells: how do they suppress immune responses? Int. Immunol. 21, 1105-1111.
34. Sitkovsky, M. V. (2009). T regulatory cells: hypoxia-adenosinergic suppression and re-direction of the immune response. Trends Immunol. 30, 102-108.
35. Sitkovsky, M., and Lukashev, D. (2005). Regulation of immune cells by local-tissue oxygen tension: HIF1alpha and adenosine receptors. Nat. Rev. Immunol. 5, 712-721.
36. Sitkovsky, M. V., and Ohta, A. (2005). The 'danger' sensors that STOP the immune response: the A2 adeno-sine receptors? Tr e n d s Im m u n o l. 26, 299-304.
37. Sitkovsky, M. V., Kjaergaard, J., Lukashev, D., and Ohta, A. (2008). Hypoxia-adenosinergic immuno-suppression: tumor protection by T regulatory cells and cancerous tissue hypoxia. Clin. Cancer Res. 14, 5947-5952.
38. Sitkovsky, M. V., Lukashev, D., Apasov, S., Kojima, H., Koshiba, M., Caldwell, C., Ohta, A., and Thiel, M. (2004). Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu. Rev. Immunol. 22, 657-682.
39. +Foxp3+regulatory T cells cultured with rapamycin. J. Immunol. 178, 320-329.
40. Thiel, M., Chouker, A., Ohta, A., Jackson, E., Caldwell, C., Smith, P., Lukashev, D., Bittmann, I., and Sitkovsky, M. V. (2005). Oxygenation inhibits the physiological tissue-protecting mechanism and thereby exac erbates acute inflammatory lung injury. PLoS Biol. 3:e174. doi: 10.1371/journal.pbio.0030174
41. Turk, M. J., Guevara-Patiño, J. A., Rizzuto, G. A., Engelhorn, M. E., Sakaguchi, S., and Houghton, A. N. (2004). Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J. Exp. Med. 200, 771-782.
42. Vang, T., Torgersen, K. M., Sundvold, V., Saxena, M., Levy, F. O., Skalhegg, B. S., Hansson, V., Mustelin, T., and Tasken, K. (2001). Activation of the COOH-terminal Src kinase (Csk) by cAMP-dependent protein kinase inhibits signaling through the T cell receptor. J. Exp. Med. 193, 497-507.
43. Whiteside, T. L. (2012). Disarming suppressor cells to improve immunotherapy. Cancer Immunol. Immunother. 61, 283-288.
44. Wing, K., Onishi, Y., Prieto-Martin, P., Yamaguchi, T., Miyara, M., Fehervari, Z., Nomura, T., and Sakaguchi, S. (2008). CTLA-4 control over Foxp3+ regulatory T cell function. Science 322, 271-275.
45. + regulatory T cells by dendritic cells during the mixed leukocyte reaction. Proc. Natl. Acad. Sci. U.S.A. 103, 2758-2763.
46. Zarek, P. E., Huang, C. T., Lutz, E. R., Kowalski, J., Horton, M. R., Linden, J., Drake, C. G., and Powell, J. D. (2008). A2A receptor signaling promotes peripheral tolerance by inducing T-cell anergy and the generation of adaptive regulatory T cells. Blood 111, 251-259.