An IL-2 paradox: Blocking CD25 on T cells induces IL-2-driven activation of CD56bright NK cells

Journal of Immunology

Volumn 185, Issue 2, 2010, Pages 1311-1320

  Martin, Jayne F ^a   Perry, Justin S A ^a   Jakhete, Neha R ^a   Wang, Xiang ^a   Bielekova, Bibiana ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD56 ANTIGEN; DACLIZUMAB; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; TRANSCRIPTION FACTOR FOXP3; CD15 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; IMMUNOGLOBULIN G; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7 RECEPTOR ALPHA; MONOCLONAL ANTIBODY;

ARTICLE; CD25+ T LYMPHOCYTE; CELL POPULATION; CELL SURVIVAL; CYTOTOXICITY; EX VIVO STUDY; HUMAN; HUMAN CELL; IMMUNOREGULATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; NATURAL KILLER CELL; OBSERVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; CELL CULTURE; CELL LINE; CELL PROLIFERATION; CELL STRAIN K 562; CYTOLOGY; DRUG EFFECT; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; T LYMPHOCYTE;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD15; ANTIGENS, CD56; CELL LINE; CELL PROLIFERATION; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOGLOBULIN G; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTERLEUKIN-7; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; K562 CELLS; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 77955506880     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902238     Document Type: Article

References (31)

1. Caligiuri, M. A. 2008. Human natural killer cells. Blood 112: 461-469.
2. Cooper, M. A., T. A. Fehniger, S. C. Turner, K. S. Chen, B. A. Ghaheri, T. Ghayur, W. E. Carson, and M. A. Caligiuri. 2001. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 97: 3146-3151.
3. Bratke, K., M. Kuepper, B. Bade, J. C. Virchow, Jr., and W. Luttmann. 2005. Differential expression of human granzymes A, B, and K in natural killer cells and during CD8+ T cell differentiation in peripheral blood. Eur. J. Immunol. 35: 2608-2616.
4. Della Chiesa, M., M. Vitale, S. Carlomagno, G. Ferlazzo, L. Moretta, and A. Moretta. 2003. The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors. Eur. J. Immunol. 33: 1657-1666.
5. Bielekova, B., M. Catalfamo, S. Reichert-Scrivner, A. Packer, M. Cerna, T. A. Waldmann, H. McFarland, P. A. Henkart, and R. Martin. 2006. Regulatory CD56(bright) natural killer cells mediate immunomodulatory effects of IL-2Ralpha-targeted therapy (daclizumab) in multiple sclerosis. Proc. Natl. Acad. Sci. USA 103: 5941-5946.
6. Benczur, M., G. G. Petrányl, G. Pálffy, M. Varga, M. Tálas, B. Kotsy, I. Földes, and S. R. Hollán. 1980. Dysfunction of natural killer cells in multiple sclerosis: a possible pathogenetic factor. Clin. Exp. Immunol. 39: 657-662.
7. Kastrukoff, L. F., A. Lau, R. Wee, D. Zecchini, R. White, and D. W. Paty. 2003. Clinical relapses of multiple sclerosis are associated with 'novel' valleys in natural killer cell functional activity. J. Neuroimmunol. 145: 103-114.
8. Zhang, B., T. Yamamura, T. Kondo, M. Fujiwara, and T. Tabira. 1997. Regulation of experimental autoimmune encephalomyelitis by natural killer (NK) cells. J. Exp. Med. 186: 1677-1687.
9. Segal, B. M. 2007. The role of natural killer cells in curbing neuroinflammation. J. Neuroimmunol. 191: 2-7. (Pubitemid 350060993)
10. Shi, F. D., and L. Van Kaer. 2006. Reciprocal regulation between natural killer cells and autoreactive T cells. Nat. Rev. Immunol. 6: 751-760.
11. Hafler, D. A., A. Compston, S. Sawcer, E. S. Lander, M. J. Daly, P. L. De Jager, P. I. de Bakker, S. B. Gabriel, D. B. Mirel, A. J. Ivinson, et al; International Multiple Sclerosis Genetics Consortium. 2007. Risk alleles for multiple sclerosis identified by a genomewide study. N. Engl. J. Med. 357: 851-862.
12. Wang, X., M. Rickert, and K. C. Garcia. 2005. Structure of the quaternary complex of interleukin-2 with its alpha, beta, and gammac receptors. Science 310: 1159-1163.
13. Waldmann, T. A. 2002. The IL-2/IL-15 receptor systems: targets for immunotherapy. J. Clin. Immunol. 22: 51-56.
14. Nussenblatt, R. B., E. Fortin, R. Schiffman, L. Rizzo, J. Smith, P. Van Veldhuisen, P. Sran, A. Yaffe, C. K. Goldman, T. A. Waldmann, and S. M. Whitcup. 1999. Treatment of noninfectious intermediate and posterior uveitis with the humanized anti-Tac mAb: a phase I/II clinical trial. Proc. Natl. Acad. Sci. USA 96: 7462-7466.
15. Bielekova, B., N. Richert, T. Howard, G. Blevins, S. Markovic-Plese, J. McCartin, J. A. Frank, J. Würfel, J. Ohayon, T. A. Waldmann, et al. 2004. Humanized anti-CD25 (daclizumab) inhibits disease activity in multiple sclerosis patients failing to respond to interferon beta. Proc. Natl. Acad. Sci. USA 101: 8705-8708.
16. Rose, J. W., H. E. Watt, A. T. White, and N. G. Carlson. 2004. Treatment of multiple sclerosis with an anti-interleukin-2 receptor monoclonal antibody. Ann. Neurol. 56: 864-867.
17. Bielekova, B., T. Howard, A. N. Packer, N. Richert, G. Blevins, J. Ohayon, T. A. Waldmann, H. F. McFarland, and R. Martin. 2009. Effect of anti-CD25 antibody daclizumab in the inhibition of inflammation and stabilization of disease progression in multiple sclerosis. Arch. Neurol. 66: 483-489.
18. Rose, J. W., J. B. Burns, J. Bjorklund, J. Klein, H. E. Watt, and N. G. Carlson. 2007. Daclizumab phase II trial in relapsing and remitting multiple sclerosis: MRI and clinical results. Neurology 69: 785-789.
19. Fehniger, T. A., E. M. Bluman, M. M. Porter, E. Mrózek, M. A. Cooper, J. B. VanDeusen, S. R. Frankel, W. Stock, and M. A. Caligiuri. 2000. Potential mechanisms of human natural killer cell expansion in vivo during low-dose IL-2 therapy. J. Clin. Invest. 106: 117-124.
20. Oh, U., G. Blevins, C. Griffith, N. Richert, D. Maric, C. R. Lee, H. McFarland, and S. Jacobson. 2009. Regulatory T cells are reduced during anti-CD25 antibody treatment of multiple sclerosis. Arch. Neurol. 66: 471-479.
21. Setoguchi, R., S. Hori, T. Takahashi, and S. Sakaguchi. 2005. Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J. Exp. Med. 201: 723-735.
22. Perez, O. D., and G. P. Nolan. 2006. Phospho-proteomic immune analysis by flow cytometry: from mechanism to translational medicine at the single-cell level. Immunol. Rev. 210: 208-228.
23. Alter, G., J. M. Malenfant, and M. Altfeld. 2004. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294: 15-22. (Pubitemid 39626587)
24. Bayer, A. L., J. Y. Lee, A. de la Barrera, C. D. Surh, and T. R. Malek. 2008. A function for IL-7R for CD4+CD25+Foxp3+ T regulatory cells. J. Immunol. 181: 225-234.
25. Michel, L., L. Berthelot, S. Pettré, S. Wiertlewski, F. Lefrère, C. Braudeau, S. Brouard, J. P. Soulillou, and D. A. Laplaud. 2008. Patients with relapsing-remitting multiple sclerosis have normal Treg function when cells expressing IL-7 receptor alpha-chain are excluded from the analysis. J. Clin. Invest. 118: 3411-3419.
26. Huntington, N. D., N. Legrand, N. L. Alves, B. Jaron, K. Weijer, A. Plet, E. Corcuff, E. Mortier, Y. Jacques, H. Spits, and J. P. Di Santo. 2009. IL-15 transpresentation promotes human NK cell development and differentiation in vivo. J. Exp. Med. 206: 25-34.
27. Saraste, M., H. Irjala, and L. Airas. 2007. Expansion of CD56Bright natural killer cells in the peripheral blood of multiple sclerosis patients treated with interferon-beta. Neurol. Sci. 28: 121-126.
28. Smyth, C. M., S. L. Ginn, C. T. Deakin, G. J. Logan, and I. E. Alexander. 2007. Limiting gammac expression differentially affects signaling via the interleukin (IL)-7 and IL-15 receptors. Blood 110: 91-98.
29. Xue, H. H., P. E. Kovanen, C. A. Pise-Masison, M. Berg, M. F. Radovich, J. N. Brady, and W. J. Leonard. 2002. IL-2 negatively regulates IL-7 receptor alpha chain expression in activated T lymphocytes. Proc. Natl. Acad. Sci. USA 99: 13759-13764.
30. Wuest, T. Y., J. Willette-Brown, S. K. Durum, and A. A. Hurwitz. 2008. The influence of IL-2 family cytokines on activation and function of naturally occurring regulatory T cells. J. Leukoc. Biol. 84: 973-980.
31. Joffre, O., M. A. Nolte, R. Spörri, and C. Reis e Sousa. 2009. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol. Rev. 227: 234-247.