CD4 +Foxp3 + regulatory T cell therapy in transplantation

Journal of Molecular Cell Biology

Volumn 4, Issue 1, 2012, Pages 11-21

  Tang, Qizhi ^a   Bluestone, Jeffrey A ^b   Kang, Sang Mo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cell therapy; immune tolerance; regulatory T cells; transplantation

Indexed keywords

ALLOANTIGEN; BASILIXIMAB; CALCINEURIN INHIBITOR; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; INTERLEUKIN 1; INTERLEUKIN 2; INTERLEUKIN 6; LYMPHOCYTE ANTIBODY; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1 ANTIBODY; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3 ANTIBODY; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD20; MONOCLONAL ANTIBODY CD28; MONOCLONAL ANTIBODY CD80; MONOCLONAL ANTIBODY CD86; OKT 3; RAPAMYCIN; THYMOCYTE ANTIBODY; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ACUTE GRAFT REJECTION; ALLOIMMUNITY; ANTIGEN SPECIFICITY; AUTOIMMUNE DISEASE; BLOOD TRANSFUSION; CD4+ T LYMPHOCYTE; CELL THERAPY; CHIMERA; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATORY DISEASE; MYELOABLATIVE CONDITIONING; NONHUMAN; ORGAN TRANSPLANTATION; REGULATORY T LYMPHOCYTE; REGULATORY T LYMPHOCYTE THERAPY; REVIEW; RISK BENEFIT ANALYSIS; SIDE EFFECT; T CELL DEPLETION; TH17 CELL; TRANSPLANTATION; TRANSPLANTATION TOLERANCE; WHOLE BODY RADIATION;

ANIMALS; AUTOIMMUNE DISEASES; CELL TRANSPLANTATION; FORKHEAD TRANSCRIPTION FACTORS; GRAFT VS HOST DISEASE; HUMANS; IMMUNOSUPPRESSION; ISOANTIGENS; MICE; ORGAN TRANSPLANTATION; T-LYMPHOCYTES, REGULATORY; TIME FACTORS; TRANSPLANTATION IMMUNOLOGY; TRANSPLANTATION TOLERANCE;

EID: 84856908569     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjr047     Document Type: Review

References (144)

1. Baan, C.C., van der Mast, B.J., Klepper, M., et al. (2005). Differential effect of calcineurin inhibitors, anti-CD25 antibodies and rapamycin on the induction of FOXP3 in human T cells. Transplantation 80, 110-117. (Pubitemid 40980903)
2. + conventional T cells. Eur. J. Immunol. 37, 2378-2389. (Pubitemid 47423608)
3. + regulatory T cells. Blood 105, 4743-4748. (Pubitemid 40807298)
4. + T cells on the fate of allografts in the absence of immunosuppression. Transplantation 79, 648-654. (Pubitemid 40463170)
5. + antigen-specific regulatory T cells. Proc. Natl Acad. Sci. USA 01(Suppl 2), 14622-14626. (Pubitemid 39346733)
6. Bluestone, J.A., Liu, W., Yabu, J.M., et al. (2008). The effect of costimulatory and interleukin 2 receptor blockade on regulatory T cells in renal transplantation. Am. J. Transplant. 8, 2086-2096.
7. Bolton, E.M. (2005). Regulatory T cells in transplantation: Natural or induced? Transplantation 79, 643-645. (Pubitemid 40463168)
8. Brandt, C., Pavlovic, V., Radbruch, A., et al. (2009). Low-dose cyclosporine a therapy increases the regulatory T cell population in patients with atopic dermatitis. Allergy 64, 1588-1596.
9. Brennan, T.V., Tang, Q., Liu, F.C., et al. (2011). Requirements for prolongation of allograft survival with regulatory T cell infusion in lymphosufficient hosts. J. Surg. Res. 169, e69-75.
10. + T regulatory cells. Blood 114, 5003-5006.
11. Brunstein, C.G., Miller, J.S., Cao, Q., et al. (2010). Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: Safety profile and detection kinetics. Blood 117, 1061-1070.
12. Brusko, T.M., Koya, R.C., Zhu, S., et al. (2010). Human antigen-specific regulatory T cells generated by T cell receptor gene transfer. PLoS One 5, e11726.
13. Bumgardner, G.L., Hardie, I., Johnson, R.W., et al. (2001). Results of 3-year phase III clinical trials with daclizumab prophylaxis for prevention of acute rejection after renal transplantation. Transplantation 72, 839-845. (Pubitemid 32879855)
14. Callaghan, C.J., Rouhani, F.J., Negus, M.C., et al. (2007). Abrogation of antibody-mediated allograft rejection by regulatory CD4T cells with indirect allospecificity. J. Immunol. 178, 2221-2228. (Pubitemid 46233420)
15. Calvo-Turrubiartes, M., Romano-Moreno, S., Garcia-Hernandez, M., et al. (2009). Quantitative analysis of regulatory T cells in kidney graft recipients: A relationship with calcineurin inhibitor level. Transpl. Immunol. 21, 43-49.
16. + regulatory T cells. Nat. Rev. Immunol. 11, 119-130.
17. Chen, T.C., Waldmann, H., and Fairchild, P.J. (2004). Induction of dominant transplantation tolerance by an altered peptide ligand of the male antigen Dby. J. Clin. Invest. 113, 1754-1762. (Pubitemid 39071667)
18. + regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J. Immunol. 172, 6003-6010. (Pubitemid 38621201)
19. + T cells. Bone Marrow Transplant. 39, 537-545. (Pubitemid 46629589)
20. + immunoregulatory T cells: New therapeutics for graft-versus-host disease. J. Exp. Med. 196, 401-406. (Pubitemid 34875668)
21. Cosimi, A.B., and Sachs, D.H. (2004). Mixed chimerism and transplantation tolerance. Transplantation 77, 943-946. (Pubitemid 38436841)
22. D'Addio, F., Yuan, X., Habicht, A., et al. (2010). A novel clinically relevant approach to tip the balance toward regulation in stringent transplant model. Transplantation 90, 260-269.
23. + CD45RB low-density cells from untreated mice prevent acute allograft rejection. J. Immunol. 163, 5353-5357.
24. Deeks, E.D., and Keating, G.M. (2009). Rabbit antithymocyte globulin (thymoglobulin): A review of its use in the prevention and treatment of acute renal allograft rejection. Drugs 69, 1483-1512.
25. Delgoffe, G.M., Kole, T.P., Zheng, Y., et al. (2009). The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity 30, 832-844.
26. + regulatory T cells: Does in vitro evidence translate to the clinical setting? Transplantation 85, 783-789. (Pubitemid 351440740)
27. + regulatory T cells. Transplantation 87, 1062-1068.
28. Di Ianni, M., Falzetti, F., Carotti, A., et al. (2011). Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood 117, 3921-3928.
29. Dorf, M.E., and Benacerraf, B. (1984). Suppressor cells and immunoregulation. Annu. Rev. Immunol. 2, 127-157.
30. + regulatory T cells suppress effector T cell proliferation. Clin. Immunol. 115, 3-9. (Pubitemid 40616162)
31. + regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat. Med. 9, 1144-1150. (Pubitemid 37173698)
32. Fan, Z., Spencer, J.A., Lu, Y., et al. (2010). In vivo tracking of 'color-coded' effector, natural and induced regulatory T cells in the allograft response. Nat. Med. 16, 718-722.
33. Feng, S. (2008). Long-term management of immunosuppression after pediatric liver transplantation: Is minimization or withdrawal desirable or possible or both? Curr. Opin. Organ. Transplant. 13, 506-512.
34. Floess, S., Freyer, J., Siewert, C., et al. (2007). Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol. 5, e38.
35. + regulatory T cells. Nat. Immunol. 4, 330-336. (Pubitemid 36432314)
36. Fourtounas, C., Dousdampanis, P., Sakellaraki, P., et al. (2010). Different immunosuppressive combinations on T-cell regulation in renal transplant recipients. Am. J. Nephrol. 32, 1-9.
37. Gao, W., Lu, Y., El Essawy, B., et al. (2007). Contrasting effects of cyclosporine and rapamycin in de novo generation of alloantigen-specific regulatory T cells. Am. J. Transplant. 7, 1722-1732. (Pubitemid 46905432)
38. Gokmen, M.R., Lombardi, G., and Lechler, R.I. (2008). The importance of the indirect pathway of allorecognition in clinical transplantation. Curr. Opin. Immunol. 20, 568-574.
39. + regulatory T cells promote experimental transplantation tolerance. Blood 109, 827-835. (Pubitemid 46105988)
40. Gupta, S., Balasubramanian, S., Thornley, T.B., et al. (2011). Direct pathway T-cell alloactivation is more rapid than indirect pathway alloactivation. Transplantation 91, e65-e67.
41. Gurkan, S., Luan, Y., Dhillon, N., et al. (2010). Immune reconstitution following rabbit antithymocyte globulin. Am. J. Transplant. 10, 2132-2141.
42. + suppressor cell and its mechanisms of action. J. Exp. Med. 171, 141-157. (Pubitemid 20040605)
43. Hara, M., Kingsley, C.I., Niimi, M., et al. (2001). IL-10 is required for regulatory T cells to mediate tolerance to alloantigens in vivo. J. Immunol. 166, 3789-3796. (Pubitemid 32224903)
44. Hippen, K.L., Merkel, S.C., Schirm, D.K., et al. (2011). Massive ex vivo expansion of human natural regulatory T cells (T(regs)) with minimal loss of in vivo functional activity. Sci. Transl. Med. 3, 83ra41.
45. +CD25 high regulatory T cells. Blood 104, 895-903. (Pubitemid 38970590)
46. + regulatory T cells upon repetitive in vitro stimulation. Eur. J. Immunol. 39, 1088-1097.
47. Hori, S. (2011). Regulatory T cell plasticity: Beyond the controversies. Trends Immunol. 32, 295-300.
48. Hori, S., Nomura, T., and Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061. (Pubitemid 36222930)
49. + T lymphocytes. Blood 103, 4216-4221. (Pubitemid 38685366)
50. + regulatory T lymphocytes. Nat. Med. 14, 88-92.
51. Kandus, A., Arnol, M., Omahen, K., et al. (2010). Basiliximab versus daclizumab combined with triple immunosuppression in deceased donor renal transplantation: A prospective, randomized study. Transplantation 89, 1022-1027.
52. + regulatory T cells in transplantation: Progress, challenges and prospects. Am. J. Transplant. 7, 1457-1463. (Pubitemid 46776267)
53. Kawai, T., Cosimi, A.B., Spitzer, T.R., et al. (2008). HLA-mismatched renal transplantation without maintenance immunosuppression. N. Engl. J. Med. 358, 353-361. (Pubitemid 351159234)
54. + T regulatory cells. Nat. Immunol. 4, 337-342. (Pubitemid 36432315)
55. Kirk, A.D. (2006). Induction immunosuppression. Transplantation 82, 593-602. (Pubitemid 44395228)
56. Knoechel, B., Lohr, J., Kahn, E., et al. (2005). Sequential development of interleukin 2-dependent effector and regulatory T cells in response to endogenous systemic antigen. J. Exp. Med. 202, 1375-1386. (Pubitemid 41668740)
57. Koch, M.A., Tucker-Heard, G., Perdue, N.R., et al. (2009). The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10, 595-602.
58. + T cells: A committed regulatory T-cell lineage and an uncommitted minor population retaining plasticity. Proc. Natl Acad. Sci. USA 106, 1903-1908.
59. + T regulatory cells. Int. Immunopharmacol. 7, 1819-1824. (Pubitemid 350046435)
60. Kurtz, J., Wekerle, T., and Sykes, M. (2004). Tolerance in mixed chimerism: A role for regulatory cells? Trends Immunol. 25, 518-523. (Pubitemid 39208349)
61. Lakkis, F.G., Arakelov, A., Konieczny, B.T., et al. (2000). Immunologic 'ignorance' of vascularized organ transplants in the absence of secondary lymphoid tissue. Nat. Med. 6, 686-688. (Pubitemid 30398793)
62. Leslie, M. (2011). Immunology. Regulatory T cells get their chance to shine. Science 332, 1020-1021.
63. + T regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J. Exp. Med. 193, 1295-1302.
64. Li, Y., Li, X.C., Zheng, X.X., et al. (1999). Blocking both signal 1 and signal 2 of T-cell activation prevents apoptosis of alloreactive T cells and induction of peripheral allograft tolerance. Nat. Med. 5, 1298-1302. (Pubitemid 29535608)
65. + T cell function but not expansion. Nat. Immunol. 3, 1208-1213. (Pubitemid 35469706)
66. Lin, Y.J., Hara, H., Tai, H.C., et al. (2008). Suppressive efficacy and proliferative capacity of human regulatory T cells in allogeneic and xenogeneic responses. Transplantation 86, 1452-1462.
67. + T reg cells. J. Exp. Med. 203, 1701-1711. (Pubitemid 44036276)
68. LoCascio, S.A., Morokata, T., Chittenden, M., et al. (2010). Mixed chimerism, lymphocyte recovery, and evidence for early donor-specific unresponsiveness in patients receiving combined kidney and bone marrow transplantation to induce tolerance. Transplantation 90, 1607-1615.
69. Long, E., and Wood, K.J. (2009). Regulatory T cells in transplantation: Transferring mouse studies to the clinic. Transplantation 88, 1050-1056.
70. + regulatory T cells. J. Am. Soc. Nephrol. 17, 2844-2853. (Pubitemid 44484674)
71. Luo, X., Pothoven, K.L., McCarthy, D., et al. (2008). ECDI-fixed allogeneic splenocytes induce donor-specific tolerance for long-term survival of islet transplants via two distinct mechanisms. Proc. Natl Acad. Sci. USA 105, 14527-14532.
72. McClymont, S.A., Putnam, A.L., Lee, M.R., et al. (2010). Plasticity of human regulatory T cells in healthy subjects and patients with type 1 diabetes. J. Immunol. 186, 3918-3926.
73. Morelon, E., Lefrancois, N., Besson, C., et al. (2010). Preferential increase in memory and regulatory subsets during T-lymphocyte immune reconstitution after Thymoglobulin induction therapy with maintenance sirolimus vs cyclosporine. Transpl. Immunol. 23, 53-58.
74. Moxham, V.F., Karegli, J., Phillips, R.E., et al. (2008). Homeostatic proliferation of lymphocytes results in augmented memory-like function and accelerated allograft rejection. J. Immunol. 180, 3910-3918.
75. Nadig, S.N., Wieckiewicz, J., Wu, D.C., et al. (2010). In vivo prevention of transplant arteriosclerosis by ex vivo-expanded human regulatory T cells. Nat. Med. 16, 809-813.
76. Neujahr, D.C., Chen, C., Huang, X., et al. (2006). Accelerated memory cell homeostasis during T cell depletion and approaches to overcome it. J. Immunol. 176, 4632-4639.
77. Noris, M., Casiraghi, F., Todeschini, M., et al. (2007). Regulatory T cells and T cell depletion: Role of immunosuppressive drugs. J. Am. Soc. Nephrol. 18, 1007-1018. (Pubitemid 46434518)
78. + regulatory T cells. J. Immunol. 174, 6993-7005. (Pubitemid 40705664)
79. Ochando, J.C., Homma, C., Yang, Y., et al. (2006). Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 7, 652-662. (Pubitemid 43797347)
80. + Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 31, 772-786.
81. Padberg, W.M., Lord, R.H., Kupiec-Weglinski, J.W., et al. (1987). Two phenotypically distinct populations of T cells have suppressor capabilities simultaneously in the maintenance phase of immunologic enhancement. J. Immunol. 139, 1751-1757. (Pubitemid 17141598)
82. Pascual, J., Bloom, D., Torrealba, J., et al. (2008). Calcineurin inhibitor withdrawal after renal transplantation with alemtuzumab: Clinical outcomes and effect on T-regulatory cells. Am. J. Transplant. 8, 1529-1536. (Pubitemid 351989487)
83. Penaranda, C., Tang, Q., and Bluestone, J.A. (2011). Anti-CD3 therapy promotes tolerance by selectively depleting pathogenic cells while preserving regulatory T cells. J. Immunol. 187, 2015-2022.
84. Polansky, J.K., Schreiber, L., Thelemann, C., et al. (2010). Methylation matters: Binding of Ets-1 to the demethylated Foxp3 gene contributes to the stabilization of Foxp3 expression in regulatory T cells. J. Mol. Med. 88, 1029-1040.
85. Posselt, A.M., Szot, G.L., Frassetto, L.A., et al. (2010). Islet transplantation in type 1 diabetic patients using calcineurin inhibitor-free immunosuppressive protocols based on T-cell adhesion or costimulation blockade. Transplantation 90, 1595-1601.
86. Putnam, A.L., Brusko, T.M., Lee, M.R., et al. (2009). Expansion of human regulatory T-cells from patients with type 1 diabetes. Diabetes 58, 652-662.
87. Quezada, S.A., Fuller, B., Jarvinen, L.Z., et al. (2003). Mechanisms of donorspecific transfusion tolerance: Preemptive induction of clonal T-cell exhaustion via indirect presentation. Blood 102, 1920-1926. (Pubitemid 37022594)
88. Rubtsov, Y.P., Niec, R.E., Josefowicz, S., et al. (2010). Stability of the regulatory T cell lineage in vivo. Science 329, 1667-1671.
89. Rudensky, A.Y., Gavin, M., and Zheng, Y. (2006). FOXP3 and NFAT: Partners in tolerance. Cell 126, 253-256. (Pubitemid 44092973)
90. Sagoo, P., Lombardi, G., and Lechler, R.I. (2008). Regulatory T cells as therapeutic cells. Curr. Opin. Organ. Transplant. 13, 645-653.
91. Sagoo, P., Ali, N., Garg, G., et al. (2011). Human regulatory T cells with alloantigen specificity are more potent inhibitors of alloimmune skin graft damage than polyclonal regulatory T cells. Sci. Transl. Med. 3, 83ra42.
92. Sakaguchi, S., Sakaguchi, N., Asano, M., et al. (1995). Immunologic selftolerance maintained by activated T cells expressing IL-2 receptor alphachains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155, 1151-1164.
93. Sawitzki, B., Kingsley, C.I., Oliveira, V., et al. (2005). IFN-gamma production by alloantigen-reactive regulatory T cells is important for their regulatory function in vivo. J. Exp. Med. 201, 1925-1935. (Pubitemid 41002929)
94. Scandling, J.D., Busque, S., Dejbakhsh-Jones, S., et al. (2008). Tolerance and chimerism after renal and hematopoietic-cell transplantation. N. Engl. J. Med. 358, 362-368. (Pubitemid 351159235)
95. + regulatory T cells in renal transplant recipients. Transplantation 82, 550-557. (Pubitemid 44290262)
96. Sener, A., Tang, A.L., and Farber, D.L. (2009). Memory T-cell predominance following T-cell depletional therapy derives from homeostatic expansion of naive T cells. Am. J. Transplant. 9, 2615-2623.
97. + T cell priming in naive mice. Immunity 33, 942-954.
98. Sho, M., Kishimoto, K., Harada, H., et al. (2005). Requirements for induction and maintenance of peripheral tolerance in stringent allograft models. Proc. Natl. Acad. Sci. USA 102, 13230-13235. (Pubitemid 41325006)
99. Snanoudj, R., Zuber, J., and Legendre, C. (2010). Co-stimulation blockade as a new strategy in kidney transplantation: Benefits and limits. Drugs 70, 2121-2131.
100. Spitzer, T.R., Sykes, M., Tolkoff-Rubin, N., et al. (2011). Long-term follow-up of recipients of combined human leukocyte antigen-matched bone marrow and kidney transplantation for multiple myeloma with end-stage renal disease. Transplantation 91, 672-676.
101. Sykes, M. (2009). Hematopoietic cell transplantation for tolerance induction: Animal models to clinical trials. Transplantation 87, 309-316.
102. Tang, Q., and Bluestone, J.A. (2006). Regulatory T-cell physiology and application to treat autoimmunity. Immunol. Rev. 212, 217-237. (Pubitemid 44116711)
103. + regulatory T cells. J. Immunol. 171, 3348-3352. (Pubitemid 37254533)
104. + regulatory T cell function. Eur. J. Immunol. 34, 2996-3005. (Pubitemid 39549379)
105. Tang, Q., Henriksen, K.J., Bi, M., et al. (2004b). In vitro-expanded antigenspecific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199, 1455-1465. (Pubitemid 38780401)
106. + immune regulatory cells are required for induction of tolerance to alloantigen via costimulatory blockade. J. Exp. Med. 193, 1311-1318.
107. + immune regulatory cells inhibits graft-versus-host disease lethality. Blood 99, 3493-3499. (Pubitemid 34534513)
108. Thomson, A.W., Turnquist, H.R., and Raimondi, G. (2009). Immunoregulatory functions of mTOR inhibition. Nat. Rev. Immunol. 9, 324-337.
109. Tone, Y., Furuuchi, K., Kojima, Y., et al. (2008). Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat. Immunol. 9, 194-202.
110. Toso, C., Edgar, R., Pawlick, R., et al. (2009). Effect of different induction strategies on effector, regulatory and memory lymphocyte sub-populations in clinical islet transplantation. Transpl. Int. 22, 182-191.
111. +FOXP32 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 110, 2983-2990. (Pubitemid 350006952)
112. + regulatory T cells favor immune reconstitution and control graft-versus-host disease while maintaining graft-versus-leukemia. J. Clin. Invest. 112, 1688-1696. (Pubitemid 38063726)
113. + T regulatory cells. Haematologica 96, 1357-1365.
114. - T regulatory cells. Clin. Immunol. 133, 22-26.
115. + Tregs by TCR gene transfer favors transplantation tolerance in mice. J. Clin. Invest. 118, 3619-3628.
116. van Loosdregt, J., Brunen, D., Fleskens, V., et al. (2011). Rapid temporal control of Foxp3 protein degradation by sirtuin-1. PLoS One 6, e19047.
117. + T cells on CD40-CD154 costimulation is determined by nature and microenvironment of primary contact with alloantigen. J. Immunol. 172, 2163-2170. (Pubitemid 38182362)
118. Verginis, P., McLaughlin, K.A., Wucherpfennig, K.W., et al. (2008). Induction of antigen-specific regulatory T cells in wild-type mice: Visualization and targets of suppression. Proc. Natl Acad. Sci. USA 105, 3479-3484. (Pubitemid 351723578)
119. Vincenti, F., and Kirk, A.D. (2008). What's next in the pipeline. Am. J. Transplant. 8, 1972-1981.
120. + regulatory T cells in humans. Proc.NatlAcad. Sci. USA106, 4793-4798.
121. + regulatory cells? Immunity 14, 399-406. (Pubitemid 32441592)
122. Waldmann, H., Adams, E., Fairchild, P., et al. (2008). Regulation and privilege in transplantation tolerance. J. Clin. Immunol. 28, 716-725.
123. - T cells. J. Clin. Invest. 112, 1437-1443. (Pubitemid 38057697)
124. Walsh, P.T., Taylor, D.K., and Turka, L.A. (2004). Tregs and transplantation tolerance. J. Clin. Invest. 114, 1398-1403. (Pubitemid 40385567)
125. + regulatory T cells. Nat. Rev. Drug Discov. 8, 969-981.
126. Weclawiak, H., Kamar, N., Ould-Mohamed, A., et al. (2010). Biological agents in kidney transplantation: Belatacept is entering the field. Expert Opin. Biol. Ther. 10, 1501-1508.
127. Wells, A.D., Li, X.C., Li, Y., et al. (1999). Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance. Nat. Med. 5, 1303-1307. (Pubitemid 29535609)
128. Wieczorek, G., Asemissen, A., Model, F., et al. (2009). Quantitative DNA methylation analysis of FOXP3 as a new method for counting regulatory T cells in peripheral blood and solid tissue. Cancer Res. 69, 599-608.
129. Wise, M.P., Bemelman, F., Cobbold, S.P., et al. (1998). Linked suppression of skin graft rejection can operate through indirect recognition. J. Immunol. 161, 5813-5816. (Pubitemid 28535944)
130. Wood, K.J., and Sakaguchi, S. (2003). Regulatory T cells in transplantation tolerance. Nat. Rev. Immunol. 3, 199-210. (Pubitemid 37323205)
131. Wu, Z., Bensinger, S.J., Zhang, J., et al. (2004). Homeostatic proliferation is a barrier to transplantation tolerance. Nat. Med. 10, 87-92. (Pubitemid 38524703)
132. + regulatory T cells synergize with host T-cell depletion to promote long-term survival of allografts. Am. J. Transplant. 8, 298-306.
133. Xiao, Y., Li, B., Zhou, Z., et al. (2010).Histone acetyltransferasemediated regulation of FOXP3 acetylation and Treg function. Curr. Opin. Immunol. 22, 583-591.
134. Yamada, A., Chandraker, A., Laufer, T.M., et al. (2001). Recipient MHC class II expression is required to achieve long-term survival of murine cardiac allografts after costimulatory blockade. J. Immunol. 167, 5522-5526. (Pubitemid 33062737)
135. + regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 198, 235-247. (Pubitemid 37009740)
136. Yang, X.O., Nurieva, R., Martinez, G.J., et al. (2008). Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 29, 44-56.
137. + T cells. Blood 111, 453-462.
138. Zhang, N., Schroppel, B., Lal, G., et al. (2009). Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity 30, 458-469.
139. Zheng, Y., Chaudhry, A., Kas, A., et al. (2009). Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control TH2 responses. Nature 458, 351-356.
140. Zheng, Y., Josefowicz, S., Chaudhry, A., et al. (2010). Role of conserved noncoding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 463, 808-812.
141. Zhou, P., Hwang, K.W., Palucki, D., et al. (2003). Secondary lymphoid organs are important but not absolutely required for allograft responses. Am. J. Transplant. 3, 259-266. (Pubitemid 36407042)
142. + T cell lineage differentiation. Immunity 30, 646-655.
143. + T cells. Curr. Opin. Immunol. 21, 281-285.
144. Zhou, X., Bailey-Bucktrout, S.L., Jeker, L.T., et al. (2009c). Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 10, 1000-1007.