Selective targeting of regulatory T cells with CD28 superagonists allows effective therapy of experimental autoimmune encephalomyelitis

Journal of Experimental Medicine

Volumn 202, Issue 3, 2005, Pages 445-455

  Beyersdorf, Niklas ^a   Gaupp, Stefanie ^b,e   Balbach, Karen ^a   Schmidt, Jens ^b   Toyka, Klaus V ^b   Lin, Chia Huey ^a   Hanke, Thomas ^c   Hünig, Thomas ^a   Kerkau, Thomas ^a   Gold, Ralf ^b,d  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^c TeGenero ImmunoTherapeutics AG   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD28 ANTIGEN SUPERAGONIST; CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; JJ 316; MONOCLONAL ANTIBODY; MYELIN BASIC PROTEIN; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CELL ISOLATION; CELL TRANSFER; CELLULAR IMMUNITY; CONTROLLED STUDY; DATA ANALYSIS; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; FEMALE; IN VIVO STUDY; LOW DRUG DOSE; LYMPHOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; REGULATORY MECHANISM; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD28; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOSUPPRESSION; INJECTIONS, INTRAVENOUS; LYMPHOCYTE ACTIVATION; MULTIPLE SCLEROSIS; RATS; RATS, INBRED LEW; RECEPTORS, INTERLEUKIN-2;

EID: 23744517125     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20051060     Document Type: Article

References (44)

1. Walker, L.S., and A.K. Abbas. 2002. The enemy within: keeping self-reactive T cells at bay in the periphery. Nat. Rev. Immunol. 2:11-19.
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 alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155:1151-1164.
3. Suri-Payer, E., A.Z. Amar, A.M. Thornton, and E.M. Shevach. 1998. CD4+CD25+ T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells. J. Immunol. 160:1212-1218.
4. Dieckmann, D., C.H. Bruett, H. Ploettner, M.B. Lutz, and G. Schuler. 2002. Human CD4(+)CD25(+) regulatory, contact-dependent T cells induce interleukin 10-producing, contact-independent type 1-like regulatory T cells. J. Exp. Med. 196:247-253.
5. Jonuleit, H., E. Schmitt, M. Stassen, A. Tuettenberg, J. Knop, and A.H. Enk. 2001. Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood. J. Exp. Med. 193:1285-1294.
6. Sakaguchi, S. 2000. Regulatory T cells: key controllers of immunologic self-tolerance. Cell. 101:455-458.
7. Kukreja, A., G. Cost, J. Marker, C. Zhang, Z. Sun, K. Lin-Su, S. Ten, M. Sanz, M. Exley, B. Wilson, et al. 2002. Multiple immuno-regulatory defects in type-1 diabetes. J. Clin. Invest. 109:131-140.
8. Viglietta, V., C. Baecher-Allan, H.L. Weiner, and D.A. Hafler. 2004. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis. J. Exp. Med. 199:971-979.
9. Ehrenstein, M.R., J.G. Evans, A. Singh, S. Moore, G. Warnes, D.A. Isenberg, and C. Mauri. 2004. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J. Exp. Med. 200:277-285.
10. Kriegel, M.A., T. Lohmann, C. Gabler, N. Blank, J.R. Kalden, and H.M. Lorenz. 2004. Defective suppressor function of human CD4+CD25+ regulatory T cells in autoimmune polyglandular syndrome type II. J. Exp. Med. 199:1285-1291.
11. Tacke, M., G. Hanke, T. Hanke, and T. Hunig. 1997. CD28-mediated induction of proliferation in resting T cells in vitro and in vivo without engagement of the T cell receptor: evidence for functionally distinct forms of CD28. Eur. J. Immunol. 27:239-247.
12. Luhder, F., Y. Huang, K.M. Dennehy, C. Guntermann, I. Muller, E. Winkler, T. Kerkau, S. Ikemizu, S.J. Davis, T. Hanke, and T. Hunig. 2003. Topological requirements and signaling properties of T cell-activating, anti-CD28 antibody superagonists. J. Exp. Med. 197:955-966.
13. Evans, E.J., R.M. Esnouf, R. Manso-Sancho, R.J. Gilbert, J.R. James, C. Yu, J.A. Fennelly, C. Vowles, T. Hanke, B. Walse, et al. 2005. Crystal structure of a soluble CD28-Fab complex. Nat. Immunol. 6:271-279.
14. Rodriguez-Palmero, M., T. Hara, A. Thumbs, and T. Hunig. 1999. Triggering of T cell proliferation through CD28 induces GATA-3 and promotes T helper type 2 differentiation in vitro and in vivo. Eur. J. Immunol. 29:3914-3924.
15. Lin, C.H., and T. Hunig. 2003. Efficient expansion of regulatory T cells in vitro and in vivo with a CD28 superagonist. Eur. J. Immunol. 33:626-638.
16. Fontenot, J.D., M.A. Gavin, and A.Y. Rudensky. 2003. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4:330-336.
17. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science. 299:1057-1061.
18. Khattri, R., T. Cox, S.A. Yasayko, and F. Ramsdell. 2003. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol. 4:337-342.
19. Fontenot, J.D., J.P. Rasmussen, L.M. Williams, J.L. Dooley, A.G. Farr, and A.Y. Rudensky. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 22:329-341.
20. Takahashi, T., T. Tagami, S. Yamazaki, T. Uede, J. Shimizu, N. Sakaguchi, T.W. Mak, and S. Sakaguchi. 2000. Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 192:303-310.
21. Read, S., V. Malmstrom, and F. Powrie. 2000. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J. Exp. Med. 192:295-302.
22. high regulatory cells in human peripheral blood. J. Immunol. 167:1245-1253.
23. Levings, M.K., R. Sangregorio, C. Sartirana, A.L. Moschin, M. Battaglia, P.C. Orban, and M.G. Roncarolo. 2002. Human CD25+CD4+ T suppressor cell clones produce transforming growth factor beta, but not interleukin 10, and are distinct from type 1 T regulatory cells. J. Exp. Med. 196:1335-1346.
24. Pozzilli, C., F. Marinelli, S. Romano, and F. Bagnato. 2004. Corticosteroids treatment. J. Neurol. Sci. 223:47-51.
25. Swanborg, R.H. 2001. Experimental autoimmune encephalomyelitis in the rat: lessons in T-cell immunology and autoreactivity. Immunol. Rev. 184:129-135.
26. Hsieh, C.S., Y. Liang, A.J. Tyznik, S.G. Self, D. Liggitt, and A.Y. Rudensky. 2004. Recognition of the peripheral self by naturally arising CD25+ CD4+ T cell receptors. Immunity. 21:267-277.
27. Salomon, B., D.J. Lenschow, L. Rhee, N. Ashourian, B. Singh, A. Sharpe, and J.A. Bluestone. 2000. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity. 12:431-440.
28. Tang, Q., K.J. Henriksen, E.K. Boden, A.J. Tooley, J. Ye, S.K. Subudhi, X.X. Zheng, T.B. Strom, and J.A. Bluestone. 2003. Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells. J. Immunol. 171:3348-3352.
29. Kerstan, A., and T. Hunig. 2004. Cutting edge: distinct TCR- and CD28-derived signals regulate CD95L, Bcl-xL, and the survival of primary T cells. J. Immunol. 172:1341-1345.
30. Cobbold, S.P., R. Castejon, E. Adams, D. Zelenika, L. Graca, S. Humm, and H. Waldmann. 2004. Induction of foxP3+ regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J. Immunol. 172:6003-6010.
31. Peng, Y., Y. Laouar, M.O. Li, E.A. Green, and R.A. Flavell. 2004. TGF-beta regulates in vivo expansion of Foxp3-expressing CD4+CD25+ regulatory T cells responsible for protection against diabetes. Proc. Natl. Acad. Sci. USA. 101:4572-4577.
32. Maloy, K.J., and F. Powrie. 2001. Regulatory T cells in the control of immune pathology. Nat. Immunol. 2:816-822.
33. Paust, S., L. Lu, N. McCarty, and H. Cantor. 2004. Engagement of B7 on effector T cells by regulatory T cells prevents autoimmune disease. Proc. Natl. Acad. Sci. USA. 101:10398-10403.
34. Fallarino, F., U. Grohmann, K.W. Hwang, C. Orabona, C. Vacca, R. Bianchi, M.L. Belladonna, M.C. Fioretti, M.L. Alegre, and P. Puccetti. 2003. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol. 4:1206-1212.
35. O'Garra, A., P.L. Vieira, P. Vieira, and A.E. Goldfeld. 2004. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J. Clin. Invest. 114:1372-1378.
36. Furtado, G.C., M.A. Curotto de Lafaille, N. Kutchukhidze, and J.J. Lafaille. 2002. Interleukin 2 signaling is required for CD4(+) regulatory T cell function. J. Exp. Med. 196:851-857.
37. Thornton, A.M., E.E. Donovan, C.A. Piccirillo, and E.M. Shevach. 2004. Cutting edge: IL-2 is critically required for the in vitro activation of CD4+CD25+ T cell suppressor function. J. Immunol. 172:6519-6523.
38. Schmidt, J., K. Elflein, M. Stienekemeier, M. Rodriguez-Palmero, C. Schneider, K.V. Toyka, R. Gold, and T. Hunig. 2003. Treatment and prevention of experimental autoimmune neuritis with superagonistic CD28-specific monoclonal antibodies. J. Neuroimmunol. 140:143-152.
39. Hori, S., M. Haury, A. Coutinho, and J. Demengeot. 2002. Specificity requirements for selection and effector functions of CD25+4+ regulatory T cells in anti-myelin basic protein T cell receptor transgenic mice. Proc. Natl. Acad. Sci. USA. 99:8213-8218.
40. Reddy, J., Z. Illes, X. Zhang, J. Encinas, J. Pyrdol, L. Nicholson, R.A. Sobel, K.W. Wucherpfennig, and V.K. Kuchroo. 2004. Myelin proteolipid protein-specific CD4+CD25+ regulatory cells mediate genetic resistance to experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 101:15434-15439.
41. Kohm, A.P., P.A. Carpentier, H.A. Anger, and S.D. Miller. 2002. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J. Immunol. 169:4712-4716.
42. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3:23-35.
43. Weishaupt, A., S. Jander, W. Bruck, T. Kuhlmann, M. Stienekemeier, T. Hartung, K.V. Toyka, G. Stoll, and R. Gold. 2000. Molecular mechanisms of high-dose antigen therapy in experimental autoimmune encephalomyelitis: rapid induction of Th1-type cytokines and inducible nitric oxide synthase. J. Immunol. 165:7157-7163.
44. Gold, R., G. Giegerich, H.P. Hartung, and K.V. Toyka. 1995. T-cell receptor (TCR) usage in Lewis rat experimental autoimmune encephalomyelitis: TCR beta-chain-variable-region V beta 8.2-positive T cells are not essential for induction and course of disease. Proc. Natl. Acad. Sci. USA. 92:5850-5854.