Ethylenecarbodiimide-coupled allogeneic antigen presenting cells induce human CD4+ regulatory T cells

Clinical Immunology

Volumn 129, Issue 3, 2008, Pages 381-393

  Albert, Michael H ^a   Yu, Xue Zhong ^b   Magg, Thomas ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

ECDI; GVHD; Rapamycin; Treg

Indexed keywords

ALLOANTIGEN; B7 ANTIGEN; CD27 ANTIGEN; CD40 ANTIGEN; ETHYLENECARBODIIMIDE; IMIDE; INTERLEUKIN 7 RECEPTOR; L SELECTIN; MESSENGER RNA; RAPAMYCIN; RECOMBINANT INTERLEUKIN 2; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ADOPTIVE IMMUNOTHERAPY; ALLOIMMUNITY; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL ISOLATION; CELL POPULATION; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOSTIMULATION; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; UPREGULATION;

ANTIGEN-PRESENTING CELLS; CARBODIIMIDES; COCULTURE TECHNIQUES; CYTOKINES; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNE TOLERANCE; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE CULTURE TEST, MIXED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIROLIMUS; T-LYMPHOCYTES, REGULATORY; UP-REGULATION;

EID: 55549130238     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2008.07.027     Document Type: Article

References (46)

1. Gershon R.K., Lance E.M., and Kondo K. Immuno-regulatory role of spleen localizing thymocytes. J. Immunol. 112 (1974) 546-554
2. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., and Toda M. 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 (1995) 1151-1164
3. Sakaguchi S., Ono M., Setoguchi R., Yagi H., Hori S., Fehervari Z., Shimizu J., Takahashi T., and Nomura T. Foxp3+CD25+CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol. Rev. 212 (2006) 8-27
4. Albert M.H., Anasetti C., and Yu X.Z. T regulatory cells as an immunotherapy for transplantation. Expert Opin. Biol. Ther. 6 (2006) 315-324
5. Hoffmann P., and Edinger M. CD4+CD25+ regulatory T cells and graft-versus-host disease. Semin. Hematol. 43 (2006) 62-69
6. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4 (2003) 330-336
7. Hori S., Nomura T., and Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 299 (2003) 1057-1061
8. Shimizu J., Yamazaki S., Takahashi T., Ishida Y., and Sakaguchi S. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 3 (2002) 135-142
9. Albert M.H., Liu Y., Anasetti C., and Yu X.Z. Antigen-dependent suppression of alloresponses by Foxp3-induced regulatory T cells in transplantation. Eur. J. Immunol. 35 (2005) 2598-2607
10. Edinger M., Hoffmann P., Ermann J., Drago K., Fathman C.G., Strober S., and Negrin R.S. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat. Med. 9 (2003) 1144-1150
11. Taylor P.A., Lees C.J., and Blazar B.R. The infusion of ex vivo activated and expanded CD4(+)CD25(+) immune regulatory cells inhibits graft-versus-host disease lethality. Blood 99 (2002) 3493-3499
12. Koenen H.J., Fasse E., and Joosten I. CD27/CFSE-based ex vivo selection of highly suppressive alloantigen-specific human regulatory T cells. J. Immunol. 174 (2005) 7573-7583
13. Ermann J., Hoffmann P., Edinger M., Dutt S., Blankenberg F.G., Higgins J.P., Negrin R.S., Fathman C.G., and Strober S. Only the CD62L+ subpopulation of CD4+CD25+ regulatory T cells protects from lethal acute GVHD. Blood 105 (2005) 2220-2226
14. Ochando J.C., Yopp A.C., Yang Y., Garin A., Li Y., Boros P., Llodra J., Ding Y., Lira S.A., Krieger N.R., and Bromberg J.S. Lymph node occupancy is required for the peripheral development of alloantigen-specific Foxp3+ regulatory T cells. J. Immunol. 174 (2005) 6993-7005
15. June C.H., and Blazar B.R. Clinical application of expanded CD4+25+ cells. Semin. Immunol. 18 (2006) 78-88
16. Hoffmann P., Eder R., Kunz-Schughart L.A., Andreesen R., and Edinger M. Large-scale in vitro expansion of polyclonal human CD4(+)CD25 high regulatory T cells. Blood 104 (2004) 895-903
17. Godfrey W.R., Ge Y.G., Spoden D.J., Levine B.L., June C.H., Blazar B.R., and Porter S.B. In vitro-expanded human CD4(+)CD25(+) T-regulatory cells can markedly inhibit allogeneic dendritic cell-stimulated MLR cultures. Blood 104 (2004) 453-461
18. Battaglia M., Stabilini A., Migliavacca B., Horejs-Hoeck J., Kaupper T., and Roncarolo M.G. Rapamycin promotes expansion of functional CD4+CD25+FOXP3+ regulatory T cells of both healthy subjects and type 1 diabetic patients. J. Immunol. 177 (2006) 8338-8347
19. Battaglia M., Stabilini A., and Roncarolo M.G. Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood 105 (2005) 4743-4748
20. Elliott C., Wang K., Miller S., and Melvold R. Ethylcarbodiimide as an agent for induction of specific transplant tolerance. Transplantation 58 (1994) 966-968
21. Masteller E.L., Tang Q., and Bluestone J.A. Antigen-specific regulatory T cells-ex vivo expansion and therapeutic potential. Semin. Immunol. 18 (2006) 103-110
22. Jenkins M.K., and Schwartz R.H. Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J. Exp. Med. 165 (1987) 302-319
23. Miller S.D., Wetzig R.P., and Claman H.N. The induction of cell-mediated immunity and tolerance with protein antigens coupled to syngeneic lymphoid cells. J. Exp. Med. 149 (1979) 758-773
24. Vandenbark A.A., Barnes D., Finn T., Bourdette D.N., Whitham R., Robey I., Kaleeba J., Bebo Jr. B.F., Miller S.D., Offner H., and Chou Y.K. Differential susceptibility of human T(h)1 versus T(h) 2 cells to induction of anergy and apoptosis by ECDI/antigen-coupled antigen-presenting cells. Int. Immunol. 12 (2000) 57-66
25. Smith C.E., and Miller S.D. Multi-peptide coupled-cell tolerance ameliorates ongoing relapsing EAE associated with multiple pathogenic autoreactivities. J. Autoimmun. 27 (2006) 218-231
26. Kaneko K., Morelli A.E., Wang Z., and Thomson A.W. Alloantigen presentation by ethylcarbodiimide-treated dendritic cells induces T cell hyporesponsiveness, and prolongs organ graft survival. Clin. Immunol. 108 (2003) 190-198
27. Magg T., and Albert M.H. Tracking cell proliferation using the far red fluorescent dye SNARF-1. Cytometry B. Clin. Cytom. 72 (2007) 458-464
28. Seddiki N., Santner-Nanan B., Martinson J., Zaunders J., Sasson S., Landay A., Solomon M., Selby W., Alexander S.I., Nanan R., Kelleher A., and Fazekas de St Groth B. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J. Exp. Med. 203 (2006) 1693-1700
29. Keir M.E., Butte M.J., Freeman G.J., and Sharpe A.H. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26 (2008) 677-704
30. Strauss L., Whiteside T.L., Knights A., Bergmann C., Knuth A., and Zippelius A. Selective survival of naturally occurring human CD4+CD25+Foxp3+ regulatory T cells cultured with rapamycin. J. Immunol. 178 (2007) 320-329
31. Valmori D., Tosello V., Souleimanian N.E., Godefroy E., Scotto L., Wang Y., and Ayyoub M. Rapamycin-mediated enrichment of T cells with regulatory activity in stimulated CD4+ T cell cultures is not due to the selective expansion of naturally occurring regulatory T cells but to the induction of regulatory functions in conventional CD4+ T cells. J. Immunol. 177 (2006) 944-949
32. Turley D.M., and Miller S.D. Peripheral tolerance induction using ethylenecarbodiimide-fixed APCs uses both direct and indirect mechanisms of antigen presentation for prevention of experimental autoimmune encephalomyelitis. J. Immunol. 178 (2007) 2212-2220
33. Chen W., Jin W., Hardegen N., Lei K.J., Li L., Marinos N., McGrady G., and Wahl S.M. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198 (2003) 1875-1886
34. Lopez M., Clarkson M.R., Albin M., Sayegh M.H., and Najafian N. A novel mechanism of action for anti-thymocyte globulin: induction of CD4+CD25+Foxp3+ regulatory T cells. J. Am. Soc. Nephrol. 17 (2006) 2844-2853
35. Allan S.E., Crome S.Q., Crellin N.K., Passerini L., Steiner T.S., Bacchetta R., Roncarolo M.G., and Levings M.K. Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int. Immunol. 19 (2007) 345-354
36. Gavin M.A., Torgerson T.R., Houston E., DeRoos P., Ho W.Y., Stray-Pedersen A., Ocheltree E.L., Greenberg P.D., Ochs H.D., and Rudensky A.Y. Single-cell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 6659-6664
37. Pillai V., Ortega S.B., Wang C.K., and Karandikar N.J. Transient regulatory T-cells: a state attained by all activated human T-cells. Clin. Immunol. 123 (2007) 18-29
38. Basu S., Golovina T., Mikheeva T., June C.H., and Riley J.L. Cutting edge: foxp3-mediated induction of pim 2 allows human T regulatory cells to preferentially expand in rapamycin. J. Immunol. 180 (2008) 5794-5798
39. Tran D.Q., Ramsey H., and Shevach E.M. Induction of FOXP3 expression in naive human CD4+ FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 110 (2007) 2983-2990
40. Taylor P.A., Panoskaltsis-Mortari A., Swedin J.M., Lucas P.J., Gress R.E., Levine B.L., June C.H., Serody J.S., and Blazar B.R. L-Selectin(hi) but not the L-selectin(lo) CD4+25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection. Blood 104 (2004) 3804-3812
41. Duggleby R.C., Shaw T.N., Jarvis L.B., Kaur G., and Hill Gaston J.S. CD27 expression discriminates between regulatory and non-regulatory cells after expansion of human peripheral blood CD4(+) CD25(+) cells. Immunology 121 (2007) 129-139
42. Liu W., Putnam A.L., Xu-Yu Z., Szot G.L., Lee M.R., Zhu S., Gottlieb P.A., Kapranov P., Gingeras T.R., Fazekas de St Groth B., Clayberger C., Soper D.M., Ziegler S.F., and Bluestone J.A. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 203 (2006) 1701-1711
43. Wan Y.Y., and Flavell R.A. The roles for cytokines in the generation and maintenance of regulatory T cells. Immunol. Rev. 212 (2006) 114-130
44. Walker M.R., Carson B.D., Nepom G.T., Ziegler S.F., and Buckner J.H. De novo generation of antigen-specific CD4+CD25+ regulatory T cells from human CD4+CD25- cells. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 4103-4108
45. Gao W., Lu Y., El Essawy B., Oukka M., Kuchroo V.K., and Strom T.B. Contrasting effects of cyclosporine and rapamycin in de novo generation of alloantigen-specific regulatory T cells. Am. J. Transplant 7 (2007) 1722-1732
46. Haxhinasto S., Mathis D., and Benoist C. The AKT-mTOR axis regulates de novo differentiation of CD4+Foxp3+ cells. J. Exp. Med. 205 (2008) 565-574