The soluble isoform of CTLA-4 as a regulator of T-cell responses

European Journal of Immunology

Volumn 43, Issue 5, 2013, Pages 1274-1285

  Ward, Frank J ^a   Dahal, Lekh N ^a   Wijesekera, Subadra K ^a,b   Abdul Jawad, Sultan K ^a,c   Kaewarpai, Taniya ^a   Xu, Heping ^a,d   Vickers, Mark A ^a   Barker, Robert N ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b OPEN UNIVERSITY OF SRI LANKA   (Sri Lanka)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

CD4+ T cells; Costimulatory molecules; Immune regulation; Treg cells

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERLEUKIN 17; OVALBUMIN;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE RESPONSE; IMMUNOCYTOCHEMISTRY; IMMUNOREGULATION; IN VITRO STUDY; MELANOMA; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ANIMALS; ANTIBODIES, NEUTRALIZING; CELLS, CULTURED; CTLA-4 ANTIGEN; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-17; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; NEOPLASM METASTASIS; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; SOLUBILITY; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, REGULATORY;

EID: 84876832601     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242529     Document Type: Article

References (51)

1. Brunet, J. F., Denizot, F., Luciani, M. F., Roux-Dosseto, M., Suzan, M., Mattei, M. G. and Golstein, P., A new member of the immunoglobulin superfamily: CTLA-4. Nature 1987. 328: 267-270.
2. Lenschow, D. J., Zeng, Y., Thistlethwaite, J. R., Montag, A., Brady, W., Gibson, M. G., Linsley, P. S. et al., Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4lg. Science 1992. 257: 789-792.
3. Linsley, P. S., Wallace, P. M., Johnson, J., Gibson, M. G., Greene, J. L., Ledbetter, J. A., Singh, C. et al., Immunosuppression in vivo by a soluble form of the CTLA-4 T cell activation molecule. Science 1992. 257: 792-795.
4. Krummel, M. F. and Allison, J. P., CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J. Exp. Med. 1995. 182: 459-465.
5. Tivol, E. A., Borriello, F., Schweitzer, A. N., Lynch, W. P., Bluestone, J. A. and Sharpe, A. H., Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 1995. 3: 541-547.
6. Waterhouse, P., Penninger, J. M., Timms, E., Wakeham, A., Shahinian, A., Lee, K. P., Thompson, C. B. et al., Lymphoproliferative disorders with early lethality in mice deficient in CTLA-4. Science 1995. 270: 985-988.
7. Alegre, M. L., Frauwirth, K. A. and Thompson, C. B., T-cell regulation by CD28 and CTLA-4. Nat. Rev. Immunol. 2001. 1: 220-228.
8. Bour-Jordan, H. and Blueston, J. A., CD28 function: a balance of costimulatory and regulatory signals. J. Clin. Immunol. 2002. 22: 1-7.
9. Bachmann, M. F., Kohler, G., Ecabert, B., Mak, T. W. and Kopf, M., Cutting edge: lymphoproliferative disease in the absence of CTLA-4 is not T cell autonomous. J. Immunol. 1999. 163: 1128-1131.
10. Tivol, E. A. and Gorski, J., Re-establishing peripheral tolerance in the absence of CTLA-4: complementation by wild-type T cells points to an indirect role for CTLA-4. J. Immunol. 2002. 169: 1852-1858.
11. 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.
12. Read, S., Malmstrom, 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.
13. Manzotti, C. N., Tipping, H., Perry, L. C., Mead, K. I., Blair, P. J., Zheng, Y. and Sansom, D. M., Inhibition of human T cell proliferation by CTLA-4 utilizes CD80 and requires CD25+ regulatory T cells. Eur. J. Immunol. 2002. 32: 2888-2896. 2-F.
14. 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.
15. Zheng, Y., Manzotti, C. N., Burke, F., Dussably, L., Qureshi, O., Walker, L. S. and Sansom, D. M., Acquisition of suppressive function by activated human CD4 +CD25- T cells is associated with the expression of CTLA-4 not FoxP3. J. Immunol. 2008. 181: 1683-1691.
16. Peggs, K. S., Quezada, S. A., Chambers, C. A., Korman, A. J. and Allison, J. P., Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J. Exp. Med. 2009. 206: 1717-1725.
17. Grohmann, U., Orabona, C., Fallarino, F., Vacca, C., Calcinaro, F., Falorni, A., Candeloro, P. et al., CTLA-4-ig regulates tryptophan catabolism in vivo. Nat. Immunol. 2002. 3: 1097-1101.
18. Dejean, A. S., Beisner, D. R., Ch'en, I. L., Kerdiles, Y. M., Babour, A., Arden, K. C., Castrillon, D. H. et al., Transcription factor Foxo3 controls the magnitude of T cell immune responses by modulating the function of dendritic cells. Nat. Immunol. 2009. 10: 504-513.
19. 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.
20. Magistrelli, G., Jeannin, P., Herbault, N., Benoit De Coignac, A., Gauchat, J. F., Bonnefoy, J. Y. and Delneste, Y., A soluble form of CTLA-4 generated by alternative splicing is expressed by nonstimulated human T cells. Eur. J. Immunol. 1999. 29: 3596-3602.
21. Oaks, M. K., Hallett, K. M., Penwell, R. T., Stauber, E. C., Warren, S. J. and Tector, A. J., A native soluble form of CTLA-4. Cell. Immunol. 2000. 201: 144-153.
22. Oaks, M. K. and Hallett, K. M., Cutting edge: a soluble form of CTLA-4 in patients with autoimmune thyroid disease. J. Immunol. 2000. 164: 5015-5018.
23. Ueda, H., Howson, J. M., Esposito, L., Heward, J., Snook, H., Chamberlain, G., Rainbow, D. B. et al., Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease. Nature 2003. 423: 506-511.
24. Pearce, S. H. and Merriman, T. R., Genetic progress towards the molecular basis of autoimmunity. Trends Mol. Med. 2006. 12: 90-98.
25. Seddiki, N., Santner-Nanan, B., Martinson, J., Zaunders, J., Sasson, S., Landay, A., Solomon, M. et al., Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J. Exp. Med. 2006. 203: 1693-1700.
26. Liu, W., Putnam, A. L., Xu-Yu, Z., Szot, G. L., Lee, M. R., Zhu, S., Gottlieb, P. A. et al., CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 2006. 203: 1701-1711.
27. Peters, J. H., Preijers, F. W., Woestenenk, R., Hilbrands, L. B., Koenen, H. J. and Joosten, I., Clinical grade Treg: GMP isolation, improvement of purity by CD127 depletion, Treg expansion, and Treg cryopreservation. PLoS One 2008. 3: e3161.
28. Codarri, L., Vallotton, L., Ciuffreda, D., Venetz, J. P., Garcia, M., Hadaya, K., Buhler, L. et al., Expansion and tissue infiltration of an allospecific CD4+CD25+CD45RO+IL-7Ralphahigh cell population in solid organ transplant recipients. J. Exp. Med. 2007. 204: 1533-1541.
29. Finney, O. C., Riley, E. M. and Walther, M., Phenotypic analysis of human peripheral blood regulatory T cells (CD4+FOXP3+CD127lo/-) ex vivo and after in vitro restimulation with malaria antigens. Eur. J. Immunol. 2010. 40: 47-60.
30. van Elsas, A., Hurwitz, A. A. and Allison, J. P., Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J. Exp. Med. 1999. 190: 355-366.
31. Chambers, C. A., Kuhns, M. S., Egen, J. G. and Allison, J. P., CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu. Rev. Immunol. 2001. 19: 565-594.
32. van Elsas, A., Sutmuller, R. P., Hurwitz, A. A., Ziskin, J., Villasenor, J., Medema, J. P., Overwijk, W. W. et al., Elucidating the autoimmune and antitumor effector mechanisms of a treatment based on cytotoxic T lymphocyte antigen-4 blockade in combination with a B16 melanoma vaccine: comparison of prophylaxis and therapy. J. Exp. Med. 2001. 194: 481-489.
33. Pruitt, S. K., Boczkowski, D., de Rosa, N., Haley, N. R., Morse, M. A., Tyler, D. S., Dannull, J. and Nair, S., Enhancement of anti-tumor immunity through local modulation of CTLA-4 and GITR by dendritic cells. Eur. J. Immunol. 2011. 41: 3553-3563.
34. Hodi, F. S., O'Day, S. J., McDermott, D. F., Weber, R. W., Sosman, J. A., Haanen, J. B., Gonzalez, R. et al., Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 2010. 363: 711-723.
35. Walker, L. S. and Sansom, D. M., The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses. Nat. Rev. Immunol. 2011. 11: 852-863.
36. Wing, K., Yamaguchi, T. and Sakaguchi, S., Cell-autonomous and -non-autonomous roles of CTLA-4 in immune regulation. Trends Immunol. 2011. 32: 428-433.
37. Takahashi, T., Kuniyasu, Y., Toda, M., Sakaguchi, N., Itoh, M., Iwata, M., Shimizu, J. and Sakaguchi, S., Immunologic self-tolerance maintained by CD25+CD4 +naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int. Immunol. 1998. 10: 1969-1980.
38. Thornton, A. M. and Shevach, E. M., CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 1998. 188: 287-296.
39. Krummel, M. F. and Allison, J. P., CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J. Exp. Med. 1996. 183: 2533-2540.
40. Walunas, T. L., Bakker, C. Y. and Bluestone, J. A., CTLA-4 ligation blocks CD28-dependent T cell activation. J. Exp. Med. 1996. 183: 2541-2550.
41. Blair, P. J., Riley, J. L., Levine, B. L., Lee, K. P., Craighead, N., Francomano, T., Perfetto, S. J. et al., CTLA-4 ligation delivers a unique signal to resting human CD4 T cells that inhibits interleukin-2 secretion but allows bcl-X(L) induction. J. Immunol. 1998. 160: 12-15.
42. Brunner, M. C., Chambers, C. A., Chan, F. K., Hanke, J., Winoto, A. and Allison, J. P., CTLA-4-mediated inhibition of early events of T cell proliferation. J. Immunol. 1999. 162: 5813-5820.
43. Griffin, M. D., Hong, D. K., Holman, P. O., Lee, K. M., Whitters, M. J., O'Herrin, S. M., Fallarino, F. et al., Blockade of T cell activation using a surface-linked single-chain antibody to CTLA-4 (CD152). J. Immunol. 2000. 164: 4433-4442.
44. Fife, B. T., Griffin, M. D., Abbas, A. K., Locksley, R. M. and Bluestone, J. A., Inhibition of T cell activation and autoimmune diabetes using a B cell surface-linked CTLA-4 agonist. J. Clin. Invest. 2006. 116: 2252-2261.
45. Karman, J., Jiang, J. L., Gumlaw, N., Zhao, H., Campos-Rivera, J., Sancho, J., Zhang, J. et al., Ligation of cytotoxic T lymphocyte antigen-4 to the TCR inhibits T cell activation and directs differentiation into FOXP3+ regulatory T cells. J. Biol. Chem. 2012. 287: 11098-11107.
46. Tivol, E. A., Boyd, S. D., McKeon, S., Borriello, F., Nickerson, P., Strom, T. B. and Sharpe, A. H., CTLA4Ig prevents lymphoproliferation and fatal multiorgan tissue destruction in CTLA-4-deficient mice. J. Immunol. 1997. 158: 5091-5094.
47. Shevach, E. M., Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 2009. 30: 636-645.
48. Laurent, S., Carrega, P., Saverino, D., Piccioli, P., Camoriano, M., Morabito, A., Dozin, B. et al., CTLA-4 is expressed by human monocyte-derived dendritic cells and regulates their functions. Hum. Immunol. 2010. 71: 934-941.
49. Gerold, K. D., Zheng, P., Rainbow, D. B., Zernecke, A., Wicker, L. S. and Kissler, S., The soluble CTLA-4 splice variant protects from type 1 diabetes and potentiates regulatory T-cell function. Diabetes 2011. 60: 1955-1963.
50. Hall, A. M., Ward, F. J., Vickers, M. A., Stott, L. M., Urbaniak, S. J. and Barker, R. N., Interleukin-10-mediated regulatory T-cell responses to epitopes on a human red blood cell autoantigen. Blood 2002. 100: 4529-4536.
51. Barker, R. N., Hall, A. M., Standen, G. R., Jones, J. and Elson, C. J., Identification of T-cell epitopes on the rhesus polypeptides in autoimmune hemolytic anemia. Blood 1997. 90: 2701-2715.