Segregated regulatory CD39 +CD4 + T cell function: TGF-β-producing Foxp3 - and IL-10-producing Foxp3 + cells are interdependent for protection against collagen-induced arthritis

Journal of Immunology

Volumn 187, Issue 9, 2011, Pages 4654-4666

  Kochetkova, Irina ^a   Thornburg, Theresa ^a   Callis, Gayle ^a   Pascual, David W ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APYRASE; BACTERIAL PROTEIN; CD39 ANTIGEN; COLONIZATION FACTOR AG 1; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 10; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTHRITIS; ARTICLE; CD39+ CD4+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE VECTOR; IMMUNIZATION; IN VIVO STUDY; LYMPHOCYTE FUNCTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REGULATORY T LYMPHOCYTE; SALMONELLA TYPHIMURIUM; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD; APYRASE; ARTHRITIS, EXPERIMENTAL; CD4-POSITIVE T-LYMPHOCYTES; COLLAGEN; FIMBRIAE PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SALMONELLA VACCINES; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; VACCINES, DNA;

EID: 80555154833     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100530     Document Type: Article

References (50)

1. Mueller, D. L. 2010. Mechanisms maintaining peripheral tolerance. Nat. Immunol. 11: 21-27.
2. Campbell, D. J., and S. F. Ziegler. 2007. FOXP3 modifies the phenotypic and functional properties of regulatory T cells. Nat. Rev. Immunol. 7: 305-310. (Pubitemid 46480960)
3. + regulatory T cells. Nat. Immunol. 4: 330-336.
4. 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: 1151-1164.
5. Ochoa-Repáraz, J., C. Riccardi, A. Rynda, S. Jun, G. Callis, and D. W. Pascual. 2007. Regulatory T cell vaccination without autoantigen protects against experimental autoimmune encephalomyelitis. J. Immunol. 178: 1791-1799. (Pubitemid 46154651)
6. Kretschmer, K., I. Apostolou, D. Hawiger, K. Khazaie, M. C. Nussenzweig, and H. von Boehmer. 2005. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6: 1219-1227. (Pubitemid 43045633)
7. Rynda, A., M. Maddaloni, D. Mierzejewska, J. Ochoa-Repáraz, T. Maślanka, K. Crist, C. Riccardi, B. Barszczewska, K. Fujihashi, J. R. McGhee, and D. W. Pascual. 2008. Low-dose tolerance is mediated by the microfold cell ligand, reovirus protein s1. J. Immunol. 180: 5187-5200.
8. reg) cells in protein s1-mediated protection against murine experimental autoimmune encephalomyelitis (EAE). PLoS One 5: e8720.
9. Ochoa-Repáraz, J., A. Rynda, M. A. Ascón, X. Yang, I. Kochetkova, C. Riccardi, G. Callis, T. Trunkle, and D. W. Pascual. 2008. IL-13 production by regulatory T cells protects against experimental autoimmune encephalomyelitis independently of autoantigen. J. Immunol. 181: 954-968.
10. Kochetkova, I., T. Trunkle, G. Callis, and D. W. Pascual. 2008. Vaccination without autoantigen protects against collagen II-induced arthritis via immune deviation and regulatory T cells. J. Immunol. 181: 2741-2752.
11. Vieira, P. L., J. R. Christensen, S. Minaee, E. J. O'Neill, F. J. Barrat, A. Boonstra, T. Barthlott, B. Stockinger, D. C. Wraith, and A. O'Garra. 2004. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J. Immunol. 172: 5986-5993. (Pubitemid 38621199)
12. Roncarolo, M. G., and M. Battaglia. 2007. Regulatory T-cell immunotherapy for tolerance to self antigens and alloantigens in humans. Nat. Rev. Immunol. 7: 585-598. (Pubitemid 47123554)
13. Weiner, H. L. 2001. Induction and mechanism of action of transforming growth factor-β-secreting Th3 regulatory cells. Immunol. Rev. 182: 207-214. (Pubitemid 33070220)
14. + Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 110: 1225-1232.
15. Kobie, J. J., P. R. Shah, L. Yang, J. A. Rebhahn, D. J. Fowell, and T. R. Mosmann. 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. (Pubitemid 44715042)
16. Deaglio, S., K. M. Dwyer, W. Gao, D. Friedman, A. Usheva, A. Erat, J. F. Chen, K. Enjyoji, J. Linden, M. Oukka, et al. 2007. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204: 1257-1265. (Pubitemid 46919862)
17. + regulatory T cells confers protection against collagen II-induced arthritis via the production of IL-10. J. Immunol. 184: 7144-7153.
18. + T cell-mediated immunosuppression involves extracellular nucleotide catabolism. Trends Immunol. 29: 99-102.
19. Ferrari, D., P. Chiozzi, S. Falzoni, S. Hanau, and F. Di Virgilio. 1997. Purinergic modulation of interleukin-1 β release from microglial cells stimulated with bacterial endotoxin. J. Exp. Med. 185: 579-582. (Pubitemid 27078376)
20. Hu, Y., P. L. Fisette, L. C. Denlinger, A. G. Guadarrama, J. A. Sommer, R. A. Proctor, and P. J. Bertics. 1998. Purinergic receptor modulation of lipopolysaccharide signaling and inducible nitric-oxide synthase expression in RAW 264.7 macrophages. J. Biol. Chem. 273: 27170-27175. (Pubitemid 28500425)
21. Tonetti, M., L. Sturla, M. Giovine, U. Benatti, and A. De Flora. 1995. Extracellular ATP enhances mRNA levels of nitric oxide synthase and TNF-α in lipopolysaccharide-treated RAW 264.7 murine macrophages. Biochem. Biophys. Res. Commun. 214: 125-130.
22. Brand, D. D., A. H. Kang, and E. F. Rosloniec. 2004. The mouse model of collagen-induced arthritis. Methods Mol. Med. 102: 295-312.
23. Inglis, J. J., G. Criado, M. Medghalchi, M. Andrews, A. Sandison, M. Feldmann, and R. O. Williams. 2007. Collagen-induced arthritis in C57BL/6 mice is associated with a robust and sustained T-cell response to type II collagen. Arthritis Res. Ther. 9: R113.
24. Kai, H., K. Shibuya, Y. Wang, H. Kameta, T. Kameyama, S. Tahara-Hanaoka, A. Miyamoto, S. Honda, I. Matsumoto, A. Koyama, et al. 2006. Critical role of M. tuberculosis for dendritic cell maturation to induce collagen-induced arthritis in H-2b background of C57BL/6 mice. Immunology 118: 233-239. (Pubitemid 43727428)
25. Nakae, S., A. Nambu, K. Sudo, and Y. Iwakura. 2003. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171: 6173-6177. (Pubitemid 37467240)
26. Myers, L. K., B. Tang, J. M. Stuart, and A. H. Kang. 2002. The role of IL-4 in regulation of murine collagen-induced arthritis. Clin. Immunol. 102: 185-191. (Pubitemid 34171518)
27. Kuruvilla, A. P., R. Shah, G. M. Hochwald, H. D. Liggitt, M. A. Palladino, and G. J. Thorbecke. 1991. Protective effect of transforming growth factor beta 1 on experimental autoimmune diseases in mice. Proc. Natl. Acad. Sci. USA 88: 2918-2921. (Pubitemid 21916531)
28. Schramm, C., J. Kriegsmann, M. Protschka, S. Huber, T. Hansen, E. Schmitt, P. R. Galle, and M. Blessing. 2004. Susceptibility to collagen-induced arthritis is modulated by TGFbeta responsiveness of T cells. Arthritis Res. Ther. 6: R114-R119.
29. Jun, S., W. Gilmore, G. Callis, A. Rynda, A. Haddad, and D.W. Pascual. 2005. A live diarrheal vaccine imprints a Th2 cell bias and acts as an anti-inflammatory vaccine. J. Immunol. 175: 6733-6740. (Pubitemid 41598917)
30. Liao, H., M. C. Hyman, A. E. Baek, K. Fukase, and D. J. Pinsky. 2010. cAMP/ CREB-mediated transcriptional regulation of ectonucleoside triphosphate diphosphohydrolase 1 (CD39) expression. J. Biol. Chem. 285: 14791-14805.
31. Kamiya, K., K. Sakakibara, E. J. Ryer, R. P. Hom, E. B. Leof, K. C. Kent, and B. Liu. 2007. Phosphorylation of the cyclic AMP response element binding protein mediates transforming growth factor β-induced downregulation of cyclin A in vascular smooth muscle cells. Mol. Cell. Biol. 27: 3489-3498. (Pubitemid 46685223)
32. Holmdahl, R., R. Bockermann, J. Bäcklund, and H. Yamada. 2002. The molecular pathogenesis of collagen-induced arthritis in mice: a model for rheumatoid arthritis. Ageing Res. Rev. 1: 135-147. (Pubitemid 38344149)
33. Luross, J. A., T. Heaton, T. R. Hirst, M. J. Day, and N. A. Williams. 2002. Escherichia coli heat-labile enterotoxin B subunit prevents autoimmune arthritis through induction of regulatory CD4+ T cells. Arthritis Rheum. 46: 1671-1682. (Pubitemid 34620216)
34. Sugihara, R., M. Yoshimura, M. Mori, N. Kanayama, M. Hikida, and H. Ohmori. 2000. Prevention of collagen-induced arthritis in DBA/1 mice by oral administration of AZ-9, a bacterial polysaccharide from Klebsiella oxytoca. Immunopharmacology 49: 325-333.
35. + T cells in collagen-induced arthritis. Immunol. Lett. 117: 16-25.
36. Koenders, M. I., J. K. Kolls, B. Oppers-Walgreen, L. van den Bersselaar, L. A. B. Joosten, J. R. Schurr, P. Schwarzenberger, W. B. van den Berg, and E. Lubberts. 2005. Interleukin-17 receptor deficiency results in impaired synovial expression of interleukin-1 and matrix metalloproteinases 3, 9, and 13 and prevents cartilage destruction during chronic reactivated streptococcal cell wall-induced arthritis. Arthritis Rheum. 52: 3239-3247. (Pubitemid 41447107)
37. + precursors. J. Immunol. 175: 6107-6116.
38. Finnegan, A., C. D. Kaplan, Y. Cao, H. Eibel, T. T. Glant, and J. Zhang. 2003. Collagen-induced arthritis is exacerbated in IL-10-deficient mice. Arthritis Res. Ther. 5: R18-R24.
39. + regulatory T cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J. Immunol. 183: 7602-7610.
40. Labasi, J. M., N. Petrushova, C. Donovan, S. McCurdy, P. Lira, M. M. Payette, W. Brissette, J. R. Wicks, L. Audoly, and C. A. Gabel. 2002. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J. Immunol. 168: 6436-6445. (Pubitemid 34620068)
41. Moncrieffe, H., K. Nistala, Y. Kamhieh, J. Evans, A. Eddaoudi, S. Eaton, and L. R. Wedderburn. 2010. High expression of the ectonucleotidase CD39 on T cells from the inflamed site identifies two distinct populations, one regulatory and one memory T cell population. J. Immunol. 185: 134-143.
42. Langston, H. P., Y. Ke, A. T. Gewirtz, K. E. Dombrowski, and J. A. Kapp. 2003. Secretion of IL-2 and IFN-γ, but not IL-4, by antigen-specific T cells requires extracellular ATP. J. Immunol. 170: 2962-2970. (Pubitemid 36302168)
43. Mandapathil, M., M. J. Szczepanski, M. Szajnik, J. Ren, E. K. Jackson, J. T. Johnson, E. Gorelik, S. Lang, and T. L. Whiteside. 2010. Adenosine and prostaglandin E2 cooperate in the suppression of immune responses mediated by adaptive regulatory T cells. J. Biol. Chem. 285: 27571-27580.
44. Bopp, T., C. Becker, M. Klein, S. Klein-Hessling, A. Palmetshofer, E. Serfling, V. Heib, M. Becker, J. Kubach, S. Schmitt, et al. 2007. Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. J. Exp. Med. 204: 1303-1310. (Pubitemid 46919868)
45. low adaptive T regulatory cells suppress delayed-type hypersensitivity during transplant tolerance. J. Immunol. 178: 3983-3995.
46. Nistala, K., and L. R. Wedderburn. 2009. Th17 and regulatory T cells: rebalancing pro- and anti-inflammatory forces in autoimmune arthritis. Rheumatology 48: 602-606.
47. Arce, F., K. Breckpot, H. Stephenson, K. Karwacz, M. R. Ehrenstein, M. Collins, and D. Escors. 2011. Selective ERK activation differentiates mouse and human tolerogenic dendritic cells, expands antigen-specific regulatory T cells, and suppresses experimental inflammatory arthritis. Arthritis Rheum. 63: 84-95.
48. Gregg, R. K., R. Jain, S. J. Schoenleber, R. Divekar, J. J. Bell, H. H. Lee, P. Yu, and H. Zaghouani. 2004. A sudden decline in active membrane-bound TGF-βimpairs both T regulatory cell function and protection against autoimmune diabetes. J. Immunol. 173: 7308-7316. (Pubitemid 39628168)
49. + T cells denotes both regulatory and memory populations. Am. J. Transplant. 9: 2303-2311.
50. + T cells denotes a regulatory memory phenotype. Am. J. Transplant. 10: 2410-2420.