Donor-type CD4+CD25+ Regulatory T Cells Suppress Lethal Acute Graft-Versus-Host Disease after Allogeneic Bone Marrow Transplantation

doi:10.1084/jem.20020399

Published 5 August 2002. doi:10.1084/jem.20020399

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© Rockefeller University Press, 0022-1007/2002/8/389/ $5.00
The Journal of Experimental Medicine, Volume 196, Number 3, August 5, 2002 389-399

Donor-type CD4⁺CD25⁺ Regulatory T Cells Suppress Lethal Acute Graft-Versus-Host Disease after Allogeneic Bone Marrow Transplantation

Petra Hoffmann¹, Joerg Ermann¹, Matthias Edinger², C. Garrison Fathman¹ and Samuel Strober¹

¹ Division of Immunology and Rheumatology, Department of Medicine, Stanford University School of Medicine, Stanford, CA 94305
² Division of Bone Marrow Transplantation, Department of Medicine, Stanford University School of Medicine, Stanford, CA 94305

Address correspondence to Samuel Strober, Division of Immunology and Rheumatology, Department of Medicine, CCSR Building, 2215-C, Stanford University School of Medicine, 300 Pasteur Drive, Stanford, CA 94305. Phone: 650-725-6500; Fax: 650-725-6104; E-mail: sstrober{at}stanford.edu

Acute graft-versus-host disease (aGVHD) is still a major obstaclein clinical allogeneic bone marrow (BM) transplantation. CD4⁺CD25⁺regulatory T (T_reg) cells have recently been shown to suppressproliferative responses of CD4⁺CD25^- T cells to alloantigenicstimulation in vitro and are required for ex vivo tolerizationof donor T cells, which results in their reduced potential toinduce aGVHD. Here we show that CD4⁺CD25⁺ T cells isolated fromthe spleen or BM of donor C57BL/6 (H-2^b) mice that have notbeen tolerized are still potent inhibitors of the alloresponsein vitro and of lethal aGVHD induced by C57BL/6 CD4⁺CD25^- Tcells in irradiated BALB/c (H-2^d) hosts in vivo. The additionof the CD4⁺CD25⁺ T_reg cells at a 1:1 ratio with responder/inducerCD4⁺CD25^- T cells resulted in a >90% inhibition of the mixedleukocyte reaction and marked protection from lethal GVHD. Thisprotective effect depended in part on the ability of the transferredCD4⁺CD25⁺ T cells to secrete interleukin 10 and occurred ifthe T_reg cells were of donor, but not host, origin. Our resultsdemonstrate that the balance of donor-type CD4⁺CD25⁺ T_reg andconventional CD4⁺CD25^- T cells can determine the outcome ofaGVHD.

Key Words: immune regulation • T lymphocytes • IL-10 • mixed leukocyte reaction • alloimmunity

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Kojima, H., Kanno, Y., Hase, H., Kobata, T. (2005). CD4+CD25+ Regulatory T Cells Attenuate the Phosphatidylinositol 3-Kinase/Akt Pathway in Antigen-Primed Immature CD8+ CTLs during Functional Maturation. J. Immunol. 174: 5959-5967 [Abstract] [Full Text]
Haeryfar, S. M. M., DiPaolo, R. J., Tscharke, D. C., Bennink, J. R., Yewdell, J. W. (2005). Regulatory T Cells Suppress CD8+ T Cell Responses Induced by Direct Priming and Cross-Priming and Moderate Immunodominance Disparities. J. Immunol. 174: 3344-3351 [Abstract] [Full Text]
Zhang, Y., Joe, G., Hexner, E., Zhu, J., Emerson, S. G. (2005). Alloreactive Memory T Cells Are Responsible for the Persistence of Graft-versus-Host Disease. J. Immunol. 174: 3051-3058 [Abstract] [Full Text]
Ermann, J., Hoffmann, P., Edinger, M., Dutt, S., Blankenberg, F. G., Higgins, J. P., Negrin, R. S., Fathman, C. G., Strober, S. (2005). Only the CD62L+ subpopulation of CD4+CD25+ regulatory T cells protects from lethal acute GVHD. Blood 105: 2220-2226 [Abstract] [Full Text]
Lombardi, G. (2005). CD4+CD25+ T cells, transplant engraftment, and allospecific tolerance. Blood 105: 1375-1376 [Full Text]
Hanash, A. M., Levy, R. B. (2005). Donor CD4+CD25+ T cells promote engraftment and tolerance following MHC-mismatched hematopoietic cell transplantation. Blood 105: 1828-1836 [Abstract] [Full Text]
Rao, P. E., Petrone, A. L., Ponath, P. D. (2005). Differentiation and Expansion of T Cells with Regulatory Function from Human Peripheral Lymphocytes by Stimulation in the Presence of TGF-{beta}. J. Immunol. 174: 1446-1455 [Abstract] [Full Text]
Godfrey, W. R., Spoden, D. J., Ge, Y. G., Baker, S. R., Liu, B., Levine, B. L., June, C. H., Blazar, B. R., Porter, S. B. (2005). Cord blood CD4+CD25+-derived T regulatory cell lines express FoxP3 protein and manifest potent suppressor function. Blood 105: 750-758 [Abstract] [Full Text]
Taylor, P. A., Panoskaltsis-Mortari, A., Swedin, J. M., Lucas, P. J., Gress, R. E., Levine, B. L., June, C. H., Serody, J. S., Blazar, B. R. (2004). L-Selectinhi but not the L-selectinlo CD4+25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection. Blood 104: 3804-3812 [Abstract] [Full Text]
Colson, Y. L., Christopher, K., Glickman, J., Taylor, K. N., Wright, R., Perkins, D. L. (2004). Absence of clinical GVHD and the in vivo induction of regulatory T cells after transplantation of facilitating cells. Blood 104: 3829-3835 [Abstract] [Full Text]
Zou, L., Barnett, B., Safah, H., LaRussa, V. F., Evdemon-Hogan, M., Mottram, P., Wei, S., David, O., Curiel, T. J., Zou, W. (2004). Bone Marrow Is a Reservoir for CD4+CD25+ Regulatory T Cells that Traffic through CXCL12/CXCR4 Signals. Cancer Res. 64: 8451-8455 [Abstract] [Full Text]
Nardelli, D. T., Burchill, M. A., England, D. M., Torrealba, J., Callister, S. M., Schell, R. F. (2004). Association of CD4+ CD25+ T Cells with Prevention of Severe Destructive Arthritis in Borrelia burgdorferi-Vaccinated and Challenged Gamma Interferon-Deficient Mice Treated with Anti-Interleukin-17 Antibody. CVI 11: 1075-1084 [Abstract] [Full Text]
Su, L., Creusot, R. J., Gallo, E. M., Chan, S. M., Utz, P. J., Fathman, C. G., Ermann, J. (2004). Murine CD4+CD25+ Regulatory T Cells Fail to Undergo Chromatin Remodeling Across the Proximal Promoter Region of the IL-2 Gene. J. Immunol. 173: 4994-5001 [Abstract] [Full Text]
Foster, A. E., Marangolo, M., Sartor, M. M., Alexander, S. I., Hu, M., Bradstock, K. F., Gottlieb, D. J. (2004). Human CD62L- memory T cells are less responsive to alloantigen stimulation than CD62L+ naive T cells: potential for adoptive immunotherapy and allodepletion. Blood 104: 2403-2409 [Abstract] [Full Text]
Moseman, E. A., Liang, X., Dawson, A. J., Panoskaltsis-Mortari, A., Krieg, A. M., Liu, Y.-J., Blazar, B. R., Chen, W. (2004). Human Plasmacytoid Dendritic Cells Activated by CpG Oligodeoxynucleotides Induce the Generation of CD4+CD25+ Regulatory T Cells. J. Immunol. 173: 4433-4442 [Abstract] [Full Text]
Edinger, M. (2004). Immunoregulation in human bone marrow transplantation?. Blood 104: 1920-1920 [Full Text]
Lee, S. J., Zahrieh, D., Agura, E., MacMillan, M. L., Maziarz, R. T., McCarthy, P. L. Jr, Ho, V. T., Cutler, C., Alyea, E. P., Antin, J. H., Soiffer, R. J. (2004). Effect of up-front daclizumab when combined with steroids for the treatment of acute graft-versus-host disease: results of a randomized trial. Blood 104: 1559-1564 [Abstract] [Full Text]
Anderson, B. E., McNiff, J. M., Matte, C., Athanasiadis, I., Shlomchik, W. D., Shlomchik, M. J. (2004). Recipient CD4+ T cells that survive irradiation regulate chronic graft-versus-host disease. Blood 104: 1565-1573 [Abstract] [Full Text]
Hoffmann, P., Eder, R., Kunz-Schughart, L. A., Andreesen, R., Edinger, M. (2004). Large-scale in vitro expansion of polyclonal human CD4+CD25high regulatory T cells. Blood 104: 895-903 [Abstract] [Full Text]
Muriglan, S. J., Ramirez-Montagut, T., Alpdogan, O., van Huystee, T. W., Eng, J. M., Hubbard, V. M., Kochman, A. A., Tjoe, K. H., Riccardi, C., Pandolfi, P. P., Sakaguchi, S., Houghton, A. N., van den Brink, M. R.M. (2004). GITR Activation Induces an Opposite Effect on Alloreactive CD4+ and CD8+ T Cells in Graft-Versus-Host Disease. JEM 200: 149-157 [Abstract] [Full Text]
Godfrey, W. R., Ge, Y. G., Spoden, D. J., Levine, B. L., June, C. H., Blazar, B. R., Porter, S. B. (2004). In vitro-expanded human CD4+CD25+ T-regulatory cells can markedly inhibit allogeneic dendritic cell-stimulated MLR cultures. Blood 104: 453-461 [Abstract] [Full Text]
Graca, L., Le Moine, A., Lin, C.-Y., Fairchild, P. J., Cobbold, S. P., Waldmann, H. (2004). Donor-specific transplantation tolerance: The paradoxical behavior of CD4+CD25+ T cells. Proc. Natl. Acad. Sci. USA 101: 10122-10126 [Abstract] [Full Text]