Recipient myeloid-derived immunomodulatory cells induce PD-1 ligand-dependent donor CD4+Foxp3+ regulatory T cell proliferation and donor-recipient immune tolerance after murine nonmyeloablative bone marrow transplantation

Journal of Immunology

Volumn 191, Issue 11, 2013, Pages 5764-5776

  Van Der Merwe, Marie ^a   Abdelsamed, Hossam A ^a   Seth, Aman ^a   Ong, Taren ^a   Vogel, Peter ^a   Pillai, Asha B ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; CD11B ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; GLYCOPROTEIN P 15095; INDUCIBLE NITRIC OXIDE SYNTHASE; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; STAT6 PROTEIN; THYMOCYTE ANTIBODY; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ACUTE GRAFT VERSUS HOST DISEASE; ADOPTIVE TRANSFER; ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; COCULTURE; DONOR; GRAFT RECIPIENT; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE IRRADIATION; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; MYELOID DENDRITIC CELL; NATURAL KILLER T CELL; NONHUMAN; NONMYELOABLATIVE STEM CELL TRANSPLANTATION; POLARIZATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T CELL DEPLETION; T LYMPHOCYTE SUBPOPULATION; TH2 CELL; WHOLE BODY RADIATION; WILD TYPE;

EID: 84888320813     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302191     Document Type: Article

References (48)

1. Shlomchik, W. D. 2007. Graft-versus-host disease. Nat. Rev. Immunol. 7: 340-352.
2. Welniak, L. A., B. R. Blazar, and W. J. Murphy. 2007. Immunobiology of allogeneic hematopoietic stem cell transplantation. Annu. Rev. Immunol. 25: 139-170.
3. Storb, R. F., R. Champlin, S. R. Riddell, M. Murata, S. Bryant, and E. H. Warren. 2001. Non-myeloablative transplants for malignant disease. Hematology Am. Soc. Hematol. Educ. Program 375-391.
4. Pillai, A., C. Hartford, C. Wang, D. Pei, J. Yang, A. Srinivasan, B. Triplett, M. Dallas, and W. Leung. 2011. Favorable preliminary results using TLI/ATG-based immunomodulatory conditioning for matched unrelated donor allogeneic hematopoietic stem cell transplantation in pediatric severe aplastic anemia. Pediatr. Transplant. 15: 628-634.
5. Lowsky, R., T. Takahashi, Y. P. Liu, S. Dejbakhsh-Jones, F. C. Grumet, J. A. Shizuru, G. G. Laport, K. E. Stockerl-Goldstein, L. J. Johnston, R. T. Hoppe, et al. 2005. Protective conditioning for acute graft-versus-host disease. N. Engl. J. Med. 353: 1321-1331.
6. Kohrt, H. E., B. B. Turnbull, K. Heydari, J. A. Shizuru, G. G. Laport, D. B. Miklos, L. J. Johnston, S. Arai, W. K. Weng, R. T. Hoppe, et al. 2009. TLI and ATG conditioning with low risk of graft-versus-host disease retains antitumor reactions after allogeneic hematopoietic cell transplantation from related and unrelated donors. Blood 114: 1099-1109.
7. Lan, F., D. Zeng, M. Higuchi, J. P. Higgins, and S. Strober. 2003. Host conditioning with total lymphoid irradiation and antithymocyte globulin prevents graft-versus-host disease: the role of CD1-reactive natural killer T cells. Biol. Blood Marrow Transplant. 9: 355-363.
8. Rigby, S. M., T. Rouse, and E. H. Field. 2003. Total lymphoid irradiation nonmyeloablative preconditioning enriches for IL-4-producing CD4+-TNK cells and skews differentiation of immunocompetent donor CD4+ cells. Blood 101: 2024-2032.
9. Pillai, A. B., T. I. George, S. Dutt, P. Teo, and S. Strober. 2007. Host NKT cells can prevent graft-versus-host disease and permit graft antitumor activity after bone marrow transplantation. J. Immunol. 178: 6242-6251.
10. Yao, Z., Y. Liu, J. Jones, and S. Strober. 2009. Differences in Bcl-2 expression by T-cell subsets alter their balance after in vivo irradiation to favor CD4+Bcl-2hi NKT cells. Eur. J. Immunol. 39: 763-775.
11. Pillai, A. B., T. I. George, S. Dutt, and S. Strober. 2009. Host natural killer T cells induce an interleukin-4-dependent expansion of donor CD4+CD25 +Foxp3+ T regulatory cells that protects against graft-versus-host disease. Blood 113: 4458-4467.
12. Mantel, P. Y., H. Kuipers, O. Boyman, C. Rhyner, N. Ouaked, B. Rückert, C. Karagiannidis, B. N. Lambrecht, R. W. Hendriks, R. Crameri, et al. 2007. GATA3-driven Th2 responses inhibit TGF-beta1-induced FOXP3 expression and the formation of regulatory T cells. PLoS Biol. 5: e329.
13. Prochazkova, J., J. Fric, K. Pokorna, A. Neuwirth, M. Krulova, A. Zajicova, and V. Holan. 2009. Distinct regulatory roles of transforming growth factor-beta and interleukin-4 in the development and maintenance of natural and induced CD4+ CD25+ Foxp3+ regulatory T cells. Immunology 128(1, Suppl.)e670-e678.
14. Wang, Y., M. A. Su, and Y. Y. Wan. 2011. An essential role of the transcription factor GATA-3 for the function of regulatory T cells. Immunity 35: 337-348.
15. Campbell, D. J. 2011. Regulatory T cells GATA have it. Immunity 35: 313-315.
16. Akbari, O., P. Stock, E. Meyer, M. Kronenberg, S. Sidobre, T. Nakayama, M. Taniguchi, M. J. Grusby, R. H. DeKruyff, and D. T. Umetsu. 2003. Essential role of NKT cells producing IL-4 and IL-13 in the development of allergeninduced airway hyperreactivity. Nat. Med. 9: 582-588.
17. Higuchi, M., D. Zeng, J. Shizuru, J. Gworek, S. Dejbakhsh-Jones, M. Taniguchi, and S. Strober. 2002. Immune tolerance to combined organ and bone marrow transplants after fractionated lymphoid irradiation involves regulatory NK T cells and clonal deletion. J. Immunol. 169: 5564-5570.
18. Daley, J. M., A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina. 2008. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83: 64-70.
19. Thornton, A. M., P. E. Korty, D. Q. Tran, E. A. Wohlfert, P. E. Murray, Y. Belkaid, and E. M. Shevach. 2010. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 184: 3433-3441.
20. Gabrilovich, D. I., and S. Nagaraj. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9: 162-174.
21. Youn, J. I., S. Nagaraj, M. Collazo, and D. I. Gabrilovich. 2008. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 181: 5791-5802.
22. Peranzoni, E., S. Zilio, I. Marigo, L. Dolcetti, P. Zanovello, S. Mandruzzato, and V. Bronte. 2010. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr. Opin. Immunol. 22: 238-244.
23. Gehrie, E., W. Van der Touw, J. S. Bromberg, and J. C. Ochando. 2011. Plasmacytoid dendritic cells in tolerance. Methods Mol. Biol. 677: 127-147.
24. Segura, E., J. Wong, and J. A. Villadangos. 2009. Cutting edge: B220+CCR9-dendritic cells are not plasmacytoid dendritic cells but are precursors of conventional dendritic cells. J. Immunol. 183: 1514-1517.
25. Shi, C., and E. G. Pamer. 2011. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11: 762-774.
26. Pan, P. Y., G. Ma, K. J. Weber, J. Ozao-Choy, G. Wang, B. Yin, C. M. Divino, and S. H. Chen. 2010. Immune stimulatory receptor CD40 is required for T-cell suppression and T regulatory cell activation mediated by myeloid-derived suppressor cells in cancer. Cancer Res. 70: 99-108.
27. Guiducci, C., B. Valzasina, H. Dislich, and M. P. Colombo. 2005. CD40/CD40L interaction regulates CD4+CD25+ T reg homeostasis through dendritic cellproduced IL-2. Eur. J. Immunol. 35: 557-567.
28. Varol, C., A. Vallon-Eberhard, E. Elinav, T. Aychek, Y. Shapira, H. Luche, H. J. Fehling, W. D. Hardt, G. Shakhar, and S. Jung. 2009. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31: 502-512.
29. Herman, S., D. Krenbek, M. Klimas, M. Bonelli, C. W. Steiner, P. Pietschmann, J. S. Smolen, and C. Scheinecker. 2012. Regulatory T cells form stable and longlasting cell cluster with myeloid dendritic cells (DC). Int. Immunol. 24: 417-426.
30. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19: 59-70.
31. Bosschaerts, T., M. Guilliams, B. Stijlemans, Y. Morias, D. Engel, F. Tacke, M. Hérin, P. De Baetselier, and A. Beschin. 2010. Tip-DC development during parasitic infection is regulated by IL-10 and requires CCL2/CCR2, IFN-gamma and MyD88 signaling. PLoS Pathog. 6: e1001045.
32. Gorelik, L., and R. A. Flavell. 2000. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12: 171-181.
33. Serafini, P., S. Mgebroff, K. Noonan, and I. Borrello. 2008. Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res. 68: 5439-5449.
34. Highfill, S. L., P. C. Rodriguez, Q. Zhou, C. A. Goetz, B. H. Koehn, R. Veenstra, P. A. Taylor, A. Panoskaltsis-Mortari, J. S. Serody, D. H. Munn, et al. 2010. Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graft-versus-host disease (GVHD) via an arginase-1-dependent mechanism that is up-regulated by interleukin-13. Blood 116: 5738-5747.
35. Huang, C., G. Yang, T. Jiang, K. Huang, J. Cao, and Z. Qiu. 2010. Effects of IL-6 and AG490 on regulation of Stat3 signaling pathway and invasion of human pancreatic cancer cells in vitro. J. Exp. Clin. Cancer Res. 29: 51.
36. Yi, T., X. Li, S. Yao, L. Wang, Y. Chen, D. Zhao, H. F. Johnston, J. S. Young, H. Liu, I. Todorov, et al. 2011. Host APCs augment in vivo expansion of donor natural regulatory T cells via B7H1/B7.1 in allogeneic recipients. J. Immunol. 186: 2739-2749.
37. Fukaya, T., H. Takagi, Y. Sato, K. Sato, K. Eizumi, H. Taya, T. Shin, L. Chen, C. Dong, M. Azuma, et al. 2010. Crucial roles of B7-H1 and B7-DC expressed on mesenteric lymph node dendritic cells in the generation of antigen-specific CD4+Foxp3+ regulatory T cells in the establishment of oral tolerance. Blood 116: 2266-2276.
38. Keir, M. E., M. J. Butte, G. J. Freeman, and A. H. Sharpe. 2008. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26: 677-704.
39. Wölfle, S. J., J. Strebovsky, H. Bartz, A. Sähr, C. Arnold, C. Kaiser, A. H. Dalpke, and K. Heeg. 2011. PD-L1 expression on tolerogenic APCs is controlled by STAT-3. Eur. J. Immunol. 41: 413-424.
40. Bronte, V., and P. Zanovello. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5: 641-654.
41. Karp, C. L., and P. J. Murray. 2012. Non-canonical alternatives: what a macrophage is 4. J. Exp. Med. 209: 427-431.
42. Geissmann, F., M. G. Manz, S. Jung, M. H. Sieweke, M. Merad, and K. Ley. 2010. Development of monocytes, macrophages, and dendritic cells. Science 327: 656-661.
43. Hume, D. A. 2008. Macrophages as APC and the dendritic cell myth. J. Immunol. 181: 5829-5835.
44. Ouabed, A., H. X. Hubert, D. Chabannes, L. Gautreau, M. Heslan, and R. Josien. 2008. Differential control of T regulatory cell proliferation and suppressive activity by mature plasmacytoid versus conventional spleen dendritic cells. J. Immunol. 180: 5862-5870.
45. Kuwana, M. 2002. Induction of anergic and regulatory T cells by plasmacytoid dendritic cells and other dendritic cell subsets. Hum. Immunol. 63: 1156-1163.
46. Mahnke, K., and A. H. Enk. 2005. Dendritic cells: key cells for the induction of regulatory T cells? Curr. Top. Microbiol. Immunol. 293: 133-150.
47. Ochando, J. C., C. Homma, Y. Yang, A. Hidalgo, A. Garin, F. Tacke, V. Angeli, Y. Li, P. Boros, Y. Ding, et al. 2006. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 7: 652-662.
48. Zou, T., A. J. Caton, G. A. Koretzky, and T. Kambayashi. 2010. Dendritic cells induce regulatory T cell proliferation through antigen-dependent and -independent interactions. J. Immunol. 185: 2790-2799.