CTLA-4 and autoimmunity: New insights into the dual regulator of tolerance

Autoimmunity Reviews

Volumn 12, Issue 12, 2013, Pages 1171-1176

  Romo Tena, Jorge ^a   Gómez Martín, Diana ^a   Alcocer Varela, Jorge ^a  

^a INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

Author keywords

Abatacept; Autoimmunity; CTLA 4; Polymorphisms; Systemic lupus erythematosus

Indexed keywords

ABATACEPT; ADAPTOR PROTEIN; B7 ANTIGEN; CD28 ANTIGEN; CD86 ANTIGEN; CLATHRIN; CORTICOSTEROID; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PLACEBO; PROTEIN TYROSINE PHOSPHATASE;

ANTIGEN STRUCTURE; ANTIGENIC MODULATION; AUTOIMMUNITY; CELL MIGRATION; CHEMICAL ANALYSIS; CORTICOSTEROID THERAPY; CYTOPLASM; GENETIC ASSOCIATION; GRAVES DISEASE; HASHIMOTO DISEASE; HUMAN; IMMUNOLOGICAL SYNAPSE; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; LIGAND BINDING; LUPUS ERYTHEMATOSUS NEPHRITIS; NONHUMAN; PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION;

ABATACEPT; AUTOIMMUNITY; CTLA-4; POLYMORPHISMS; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIGENS, CD28; ANTIGENS, CD80; ANTIGENS, CD86; AUTOANTIGENS; AUTOIMMUNE DISEASES; CTLA-4 ANTIGEN; HUMANS; IMMUNE TOLERANCE; IMMUNOCONJUGATES; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION;

EID: 84884704400     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2013.07.002     Document Type: Review

References (58)

1. Brunet J.F., Denizot F., Luciani M.F., Roux-Dosseto M., Suzan M., Mattei M.G., et al. A new member of the immunoglobulin superfamily-CTLA-4. Nature 1987, 328:267-270.
2. Linsley P.S., Greene J.L., Tan P., Bradshaw J., Ledbetter J.A., Anasetti C., et al. Coexpression and functional cooperation of CTLA-4 and CD28 on activated T lymphocytes. J Exp Med 1992, 176:1595-1604.
3. Dariavach P., Mattei M.G., Golstein P., Lefranc M.P. Human Ig superfamily CTLA-4 gene: chromosomal localization and identity of protein sequence between murine and human CTLA-4 cytoplasmic domains. Eur J Immunol 1988, 18:1901-1905.
4. Masteller E.L., Chuang E., Mullen A.C., Reiner S.L., Thompson C.B. Structural analysis of CTLA-4 function in vivo. J Immunol 2000, 164:5319-5327.
5. Harper K., Balzano C., Rouvier E., Mattei M.G., Luciani M.F., Golstein P. CTLA-4 and CD28 activated lymphocyte molecules are closely related in both mouse and human as to sequence, message expression, gene structure, and chromosomal location. J Immunol 1991, 147:1037-1044.
6. Yokosuka T., Kobayashi W., Takamatsu M., Sakata-Sogawa K., Zeng H., Hashimoto-Tane A., et al. Spatiotemporal basis of CTLA-4 costimulatory molecule-mediated negative regulation of T cell activation. Immunity 2010, 33:326-339.
7. Walunas T.L., Lenschow D.J., Bakker C.Y., Linsley P.S., Freeman G.J., Green J.M., et al. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1994, 1:405-413.
8. Guntermann C., Alexander D.R. CTLA-4 suppresses proximal TCR signaling in resting human CD4(+) T cells by inhibiting ZAP-70 Tyr(319) phosphorylation: a potential role for tyrosine phosphatases. J Immunol 2002, 168:4420-4429.
9. Krummel M.F., 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.
10. Tivol E.A., Borriello F., Schweitzer A.N., Lynch W.P., Bluestone J.A., 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.
11. Waterhouse P., Penninger J.M., Timms E., Wakeham A., Shahinian A., Lee K.P., et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 1995, 270:985-988.
12. Bachmann M.F., Kohler G., Ecabert B., Mak T.W., Kopf M. Cutting edge: lymphoproliferative disease in the absence of CTLA-4 is not T cell autonomous. J Immunol 1999, 163:1128-1131.
13. Ise W., Kohyama M., Nutsch K.M., Lee H.M., Suri A., Unanue E.R., et al. CTLA-4 suppresses the pathogenicity of self antigen-specific T cells by cell-intrinsic and cell-extrinsic mechanisms. Nat Immunol 2010, 11:129-135.
14. Wing K., Onishi Y., Prieto-Martin P., Yamaguchi T., Miyara M., Fehervari Z., et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science 2008, 322:271-275.
15. Jain N., Nguyen H., Chambers C., Kang J. Dual function of CTLA-4 in regulatory T cells and conventional T cells to prevent multiorgan autoimmunity. Proc Natl Acad Sci U S A 2010, 107:1524-1528.
16. Schneider H., Downey J., Smith A., Zinselmeyer B.H., Rush C., Brewer J.M., et al. Reversal of the TCR stop signal by CTLA-4. Science 2006, 313:1972-1975.
17. Takahashi T., Tagami T., Yamazaki S., Uede T., Shimizu J., Sakaguchi N., 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.
18. Chikuma S., Abbas A.K., Bluestone J.A. B7-independent inhibition of T cells by CTLA-4. J Immunol 2005, 175:177-181.
19. Martin M., Schneider H., Azouz A., Rudd C.E. Cytotoxic T lymphocyte antigen 4 and CD28 modulate cell surface raft expression in their regulation of T cell function. J Exp Med 2001, 194:1675-1681.
20. Darlington P.J., Baroja M.L., Chau T.A., Siu E., Ling V., Carreno B.M., et al. Surface cytotoxic T lymphocyte-associated antigen 4 partitions within lipid rafts and relocates to the immunological synapse under conditions of inhibition of T cell activation. J Exp Med 2002, 195:1337-1347.
21. Chikuma S., Imboden J.B., Bluestone J.A. Negative regulation of T cell receptor-lipid raft interaction by cytotoxic T lymphocyte-associated antigen 4. J Exp Med 2003, 197:129-135.
22. Tai X., Van Laethem F., Pobezinsky L., Guinter T., Sharrow S.O., Adams A., et al. Basis of CTLA-4 function in regulatory and conventional CD4(+) T cells. Blood 2012, 119:5155-5163.
23. Qureshi O.S., Kaur S., Hou T.Z., Jeffery L.E., Poulter N.S., Briggs Z., et al. Constitutive clathrin-mediated endocytosis of CTLA-4 persists during T cell activation. J Biol Chem 2012, 287:9429-9440.
24. Schneider H., Martin M., Agarraberes F.A., Yin L., Rapoport I., Kirchhausen T., et al. Cytolytic T lymphocyte-associated antigen-4 and the TCR zeta/CD3 complex, but not CD28, interact with clathrin adaptor complexes AP-1 and AP-2. J Immunol 1999, 163:1868-1879.
25. Lee K.M., Chuang E., Griffin M., Khattri R., Hong D.K., Zhang W., et al. Molecular basis of T cell inactivation by CTLA-4. Science 1998, 282:2263-2266.
26. Smida M., Cammann C., Gurbiel S., Kerstin N., Lingel H., Lindquist S., et al. PAG/Cbp suppression reveals a contribution of CTLA-4 to setting the activation threshold in T cells. Cell Commun Signal 2013, 11:28.
27. Hoff H., Kolar P., Ambach A., Radbruch A., Brunner-Weinzierl M.C. CTLA-4 (CD152) inhibits T cell function by activating the ubiquitin ligase Itch. Mol Immunol 2010, 47:1875-1881.
28. Teft W.A., Chau T.A., Madrenas J. Structure-Function analysis of the CTLA-4 interaction with PP2A. BMC Immunol 2009, 10:23.
29. Kessel A., Haj T., Peri R., Snir A., Melamed D., Sabo E., et al. Human CD19(+)CD25(high) B regulatory cells suppress proliferation of CD4(+) T cells and enhance Foxp3 and CTLA-4 expression in T-regulatory cells. Autoimmun Rev 2012, 11:670-677.
30. Bacchetta R., Gregori S., Roncarolo M.G. CD4+ regulatory T cells: mechanisms of induction and effector function. Autoimmun Rev 2005, 4:491-496.
31. Schmidt E.M., Wang C.J., Ryan G.A., Clough L.E., Qureshi O.S., Goodall M., et al. Ctla-4 controls regulatory T cell peripheral homeostasis and is required for suppression of pancreatic islet autoimmunity. J Immunol 2009, 182:274-282.
32. Qureshi O.S., Zheng Y., Nakamura K., Attridge K., Manzotti C., Schmidt E.M., et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 2011, 332:600-603.
33. Verhagen J., Genolet R., Britton G.J., Stevenson B.J., Sabatos-Peyton C.A., Dyson J., et al. CTLA-4 controls the thymic development of both conventional and regulatory T cells through modulation of the TCR repertoire. Proc Natl Acad Sci U S A 2013, 110:E221-E230.
34. Verhagen J., Gabrysova L., Minaee S., Sabatos C.A., Anderson G., Sharpe A.H., et al. Enhanced selection of FoxP3+ T-regulatory cells protects CTLA-4-deficient mice from CNS autoimmune disease. Proc Natl Acad Sci U S A 2009, 106:3306-3311.
35. Watanabe N., Nakajima H. Coinhibitory molecules in autoimmune diseases. Clin Dev Immunol 2012, 2012:269756.
36. Lessard C.J., Ice J.A., Adrianto I., Wiley G.B., Kelly J.A., Gaffney P.M., et al. The genomics of autoimmune disease in the era of genome-wide association studies and beyond. Autoimmun Rev 2012, 11:267-275.
37. Ghaderi A. CTLA4 gene variants in autoimmunity and cancer: a comparative review. Iran J Immunol 2011, 8:127-149.
38. Zhu J.M., Li B.K., Chen G.M., Feng C.C., Cen H., Fan Y.G., et al. CTLA-4-1722T/C polymorphism and systemic lupus erythematosus susceptibility: a meta-analysis involving ten separate studies. Immunol Invest 2013, 42:91-105.
39. Jury E.C., Flores-Borja F., Kalsi H.S., Lazarus M., Isenberg D.A., Mauri C., et al. Abnormal CTLA-4 function in T cells from patients with systemic lupus erythematosus. Eur J Immunol 2010, 40:569-578.
40. Pawlak E., Kochanowska I.E., Frydecka I., Kielbinski M., Potoczek S., Bilinska M. The soluble CTLA-4 receptor: a new marker in autoimmune diseases. Arch Immunol Ther Exp (Warsz) 2005, 53:336-341.
41. Merrill J.T., Burgos-Vargas R., Westhovens R., Chalmers A., D'Cruz D., Wallace D.J., et al. The efficacy and safety of abatacept in patients with non-life-threatening manifestations of systemic lupus erythematosus: results of a twelve-month, multicenter, exploratory, phase IIb, randomized, double-blind, placebo-controlled trial. Arthritis Rheum 2010, 62:3077-3087.
42. Mok C.C. Abatacept for systemic lupus erythematosus: the outlook. Expert Opin Biol Ther 2012, 12:1559-1561.
43. Diamanti A.P., Rosado M.M., Carsetti R., Valesini G. B cells in SLE: different biological drugs for different pathogenic mechanisms. Autoimmun Rev 2007, 7:143-148.
44. Caporali R., Bugatti S., Cavagna L., Antivalle M., Atzeni F., Puttini P.S. Abatacept as a first-line biological therapy. Autoimmun Rev Jun 24 2013, http://dx.doi.org/1568-9972(13)00114-6.
45. Caporali R., Bugatti S., Cavagna L., Antivalle M., Sarzi-Puttini P. Modulating the co-stimulatory signal for T cell activation in rheumatoid arthritis: could it be the first step of the treatment?. Autoimmun Rev Jun 15 2013, http://dx.doi.org/S1568-9972(13)00109-2.
46. Cutolo M., Nadler S.G. Advances in CTLA-4-Ig-mediated modulation of inflammatory cell and immune response activation in rheumatoid arthritis. Autoimmun Rev 2013, 12:758-767.
47. Fiocco U., Sfriso P., Oliviero F., Pagnin E., Scagliori E., Campana C., et al. Co-stimulatory modulation in rheumatoid arthritis: the role of (CTLA4-Ig) abatacept. Autoimmun Rev 2008, 8:76-82.
48. Atzeni F., Puttini P.S., Mutti A., Bugatti S., Cavagna L., Caporali R. Long-term safety of abatacept in patients with rheumatoid arthritis. Autoimmun Rev Jun 22 2013, http://dx.doi.org/S1568-9972(13)00115-8.
49. Jordan N., Lutalo P.M., D'Cruz D.P. Novel therapeutic agents in clinical development for systemic lupus erythematosus. BMC Med 2013, 11:120.
50. Wofsy D., Hillson J.L., Diamond B. Abatacept for lupus nephritis: alternative definitions of complete response support conflicting conclusions. Arthritis Rheum 2012, 64:3660-3665.
51. Liu J., Zhang H.X. CTLA-4 polymorphisms and systemic lupus erythematosus: a comprehensive meta-analysis. Genet Test Mol Biomarkers 2013, 17:226-231.
52. Liu J., Zhang H. 1722T/C polymorphism (rs733618) of CTLA-4 significantly associated with systemic lupus erythematosus (SLE): a comprehensive meta-analysis. Hum Immunol 2013, 74:341-347.
53. Lee Y.H., Harley J.B., Nath S.K. CTLA-4 polymorphisms and systemic lupus erythematosus (SLE): a meta-analysis. Hum Genet 2005, 116:361-367.
54. Liu C.P., Jiang J.A., Wang T., Liu X.M., Gao L., Zhu R.R., et al. CTLA-4 and CD86 genetic variants and haplotypes in patients with rheumatoid arthritis in southeastern China. Genet Mol Res 2013, 12:1373-1382.
55. Lee Y.H., Bae S.C., Choi S.J., Ji J.D., Song G.G. Association between the CTLA-4+49 A/G polymorphism and susceptibility to rheumatoid arthritis: a meta-analysis. Mol Biol Rep 2012, 39:5599-5605.
56. Si X., Zhang X., Tang W., Luo Y. Association between the CTLA-4+49A/G polymorphism and Graves' disease: a meta-analysis. Exp Ther Med 2012, 4:538-544.
57. Du L., Yang J., Huang J., Ma Y., Wang H., Xiong T., et al. The associations between the polymorphisms in the CTLA-4 gene and the risk of Graves' disease in the Chinese population. BMC Med Genet 2013, 14:46.
58. Si X., Zhang X., Luo Y., Tang W. Association between the CTLA-4+49A/G polymorphism and type 1 diabetes: a meta-analysis. Genet Test Mol Biomarkers 2012, 16:1336-1342.