CD28/CTLA-4/B7 costimulatory pathway blockade affects regulatory T-cell function in autoimmunity

European Journal of Immunology

Volumn 45, Issue 6, 2015, Pages 1832-1841

  Vogel, Isabel ^a   Kasran, Ahmad ^a   Cremer, Jonathan ^a   Kim, Yoo Jin ^b   Boon, Louis ^c   Van Gool, Stefaan W ^a   Ceuppens, Jan L ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b SAARLAND UNIVERSITY   (Germany)

^c BIOCEROS   (Netherlands)

Author keywords

Animal model; CTLA 4Ig; EAE; Suppression; Tolerance

Indexed keywords

ABATACEPT; CD28 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERLEUKIN 17; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY B7; MONOCLONAL ANTIBODY KI 67; MYELIN; UNCLASSIFIED DRUG; B7 ANTIGEN; BLOCKING ANTIBODY; KI 67 ANTIGEN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN (35-55); PEPTIDE FRAGMENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEMYELINATION; DISEASE COURSE; DISEASE EXACERBATION; IMMUNIZATION; IMMUNOMODULATION; INFLAMMATION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, BLOCKING; ANTIBODIES, MONOCLONAL; ANTIGENS, CD28; AUTOIMMUNITY; B7 ANTIGENS; CTLA-4 ANTIGEN; DISEASE PROGRESSION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE EXPRESSION; INTERFERON-GAMMA; INTERLEUKIN-17; KI-67 ANTIGEN; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MICE; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84930416203     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445190     Document Type: Article

References (36)

1. Sharpe, A. H. and Freeman, G. J., The B7-CD28 superfamily. Nat. Rev. Immunol. 2002. 2: 116-126.
2. Appleman, L. J., Tzachanis, D., Grader-Beck, T., Van Puijenbroek, A. A. F. L. and Boussiotis, V. A., Induction of immunologic tolerance for allogeneic hematopoietic cell transplantation. Leuk. Lymphoma. 2002. 43: 1159-1167.
3. Linsley, P. S., Bradshaw, J., Greene, J., Peach, R., Bennett, K. L. and Mittler, R. S., Intracellular trafficking of CTLA-4 and focal localization towards sites of TCR engagement. Immunity 1996. 4: 535-543.
4. Thompson, C. B., and Allison, J. P., The emerging role of CTLA-4 as an immune attenuator. Immunity 1997. 7: 445-450.
5. Wing, K., Onishi, Y., Prieto-Martin, P., Yamaguchi, T., Miyara, M., Fehervari, Z., Nomura, T. et al., CTLA-4 control over Foxp3+ regulatory T cell function. Science 2008. 322: 271-275.
6. Takahashi, T., Tagami, T., Yamazaki, S., Uede, T., Shimizu, J., Sakaguchi, N., Mak, T. W. et al., Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 2000. 192: 303-310.
7. Read, S., Malmström, V., and Powrie, F., 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. 2000. 192: 295-302.
8. Qureshi, O. S., Zheng, Y., Nakamura, K., Attridge, K., Manzotti, C., Schmidt, E. M., Baker, J. et al., Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 2011. 332: 600-603.
9. Kremer, J. M., Westhovens, R., Leon, M., Di Giorgio, E., Alten, R., Steinfeld, S., Russell, A. et al., Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N. Engl. J. Med. 2003. 349: 1907-1915.
10. Genovese, M. C., Becker J.-C., Schiff, M., Luggen, M., Sherrer, Y., Kremer, J., Birbara, C. et al., Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N. Engl. J. Med. 2005. 353: 1114-1123.
11. Larsen, C. P., Pearson, T. C., Adams, A. B., Tso, P., Shirasugi, N., Strobert, E., Anderson, D. et al., Rational development of LEA29Y (belatacept), a high-affinity variant of CTLA4-Ig with potent immunosuppressive properties. Am. J. Transplant. 2005. 5: 443-453.
12. Charpentier, B., Belatacept: a novel immunosuppressive agent for kidney transplant recipients. Expert. Rev. Clin. Immunol. 2012. 8: 719-728.
13. McAdam, A. J., Schweitzer, A. N. and Sharpe, A. H., The role of B7 co-stimulation in activation and differentiation of CD4+ and CD8+ T cells. Immunol. Rev. 1998. 165: 231-247.
14. Riella, L. V., Liu, T., Yang, J., Chock, S., Shimizu, T., Mfarrej, B., Batal, I. et al., Deleterious effect of CTLA4-Ig on a Treg-dependent transplant model. Am. J. Transplant. 2012. 12: 846-855.
15. Charbonnier, L.-M., Vokaer, B., Lemaître, P. H., Field, K. A., Leo, O., and LeMoine, A., CTLA4-Ig restores rejection of MHC class-II mismatched allografts by disabling IL-2-expanded regulatory T cells. Am. J. Transplant. 2012. 12: 2313-2321.
16. Tang, Q., Henriksen, K. J., Boden, E. K., Tooley, A. J., Ye, J., Subudhi, S. K., Zheng, X. X. et al., Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells. J. Immunol. 2003. 171: 3348-3352.
17. Salomon, B., Lenschow, D. J., Rhee, L., Ashourian, N., Singh, B., Sharpe, A., and Bluestone, J. A., B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 2000. 12: 431-440.
18. Zhang, R., Huynh, A., Whitcher, G., Chang, J., Maltzman, J. S. and Turka, L. A., An obligate cell-intrinsic function for CD28 in Tregs. J. Clin. Invest. 2013. 123: 580-593.
19. Gogishvili, T., Lühder, F., Goebbels, S., Beer-Hammer, S., Pfeffer, K., and Hünig, T., Cell-intrinsic and -extrinsic control of Treg-cell homeostasis and function revealed by induced CD28 deletion. Eur. J. Immunol. 2013. 43: 188-193.
20. Compston, A. and Coles, A., Multiple sclerosis. Lancet 2002. 359: 1221-1231.
21. Khoury, S. J., Akalin, E., Chandraker, A., Turka, L. A., Linsley, P. S., Sayegh, M. H. and Hancock, W. W., CD28-B7 costimulatory blockade by CTLA4Ig prevents actively induced experimental autoimmune encephalomyelitis and inhibits Th1 but spares Th2 cytokines in the central nervous system. J. Immunol. 1995. 155: 4521-4524.
22. Arima, T., Rehman, A., Hickey, W. F. and Flye, M. W., Inhibition by CTLA4Ig of experimental allergic encephalomyelitis. J. Immunol. 1996. 156: 4916-4924.
23. Perrin, P. J., Scott, D., Quigley, L., Albert, P. S., Feder, O., Gray, G. S., Abe, R. et al., Role of B7:CD28/CTLA-4 in the induction of chronic relapsing experimental allergic encephalomyelitis. J. Immunol. 1995. 154: 1481-1490.
24. Cross, A. H., Girard, T. J., Giacoletto, K. S., Evans, R. J., Keeling, R. M., Lin, R. F., Trotter, J. L. et al., Long-term inhibition of murine experimental autoimmune encephalomyelitis using CTLA-4-Fc supports a key role for CD28 costimulation. J. Clin. Invest. 1995. 95: 2783-2789.
25. Juedes, A. E., Hjelmström, P., Bergman, C. M., Neild, A. L. and Ruddle, N. H., Kinetics and cellular origin of cytokines in the central nervous system: insight into mechanisms of myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis. J. Immunol. 2000. 164: 419-426.
26. Petermann, F. and Korn, T., Cytokines and effector T cell subsets causing autoimmune CNS disease. FEBS Lett. 2011. 585: 3747-3757.
27. McGeachy, M. J., GM-CSF: the secret weapon in the T(H)17 arsenal. Nat. Immunol. 2011. 12: 521-522.
28. Moore, K. W., deWaal Malefyt, R., Coffman, R. L. and O'Garra, A., Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 2001. 19: 683-765.
29. Murphy, A. C., Lalor, S. J., Lynch, M. A. and Mills, K. H. G., Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis. Brain Behav. Immun. 2010. 24: 641-651.
30. Codarri, L., Gyülvészi, G., Tosevski, V., Hesske, L., Fontana, A., Magnenat, L., Suter, T. et al., RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 2011. 12: 560-567.
31. Ma, Y., Lin, B., Lin, B., Hou, S., Qian, W., Li, J., Tan, M. et al., Pharmacokinetics of CTLA4Ig fusion protein in healthy volunteers and patients with rheumatoid arthritis. Acta Pharmacol. Sin. 2009. 30: 364-371.
32. Bouguermouh, S., Fortin, G., Baba, N., Rubio, M. and Sarfati, M., CD28 co-stimulation down regulates Th17 development. PLoS One 2009. 4: e5087.
33. Ying, H., Yang, L., Qiao, G., Li, Z., Zhang, L., Yin, F., Xie, D. et al., Cutting edge: CTLA-4-B7 interaction suppresses Th17 cell differentiation. J. Immunol. 2010. 185: 1375-1378.
34. Galicia, G., Kasran, A., Uyttenhove, C., DeSwert, K., VanSnick, J. and Ceuppens, J. L., ICOS deficiency results in exacerbated IL-17 mediated experimental autoimmune encephalomyelitis. J. Clin. Immunol. 2009. 29: 426-433.
35. Shindler, K. S., Kenyon, L. C., Dutt, M., Hingley, S. T. and Sarma, J. D., Experimental optic neuritis induced by a demyelinating strain of mouse hepatitis virus. J. Virol. 2008. 82: 8882-8886.
36. Das Sarma, J., Kenyon, L. C., Hingley, S. T. and Shindler, K. S., Mechanisms of primary axonal damage in a viral model of multiple sclerosis. J. Neurosci. 2009. 29: 10272-10280.