Requirement for interactions of natural killer T cells and myeloid-derived suppressor cells for transplantation tolerance

American Journal of Transplantation

Volumn 14, Issue 11, 2014, Pages 2467-2477

  Hongo, D ^a   Tang, X ^a   Baker, J ^a   Engleman, E G ^a   Strober, S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basic (laboratory) research science; bone marrow hematopoietic stem cell transplantation; immunosuppression immune modulation; immunosuppressive regimens; induction; macrophage monocyte biology: activation; tolerance: chimerism; tolerance: mechanisms

Indexed keywords

ARGINASE 1; CD11B ANTIGEN; GAMMA INTERFERON RECEPTOR 1; INTERLEUKIN 4; INTERLEUKIN 4 ALPHA; PROGRAMMED DEATH 1 LIGAND 1; T LYMPHOCYTE ANTIBODY; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CD4+ CD25+ T LYMPHOCYTE; CELL INTERACTION; CHIMERA; CONTROLLED STUDY; CYTOKINE RELEASE; HEART GRAFT; HEART TRANSPLANTATION; LYMPH NODE IRRADIATION; LYMPHOID TISSUE; MALE; MICROENVIRONMENT; MIXED LYMPHOCYTE REACTION; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER T CELL; NONHUMAN; NONMYELOABLATIVE CONDITIONING; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; TRANSPLANTATION TOLERANCE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; NATURAL KILLER CELL;

ANIMALS; BONE MARROW TRANSPLANTATION; HEART TRANSPLANTATION; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYELOID CELLS;

EID: 84901589082     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12914     Document Type: Article

References (46)

1. Kawai T, Cosimi AB, Spitzer TR, et al. HLA-mismatched renal transplantation without maintenance immunosuppression. N Engl J Med 2008; 358: 353-361.
2. Farris AB, Taheri D, Kawai T, et al. Acute renal endothelial injury during marrow recovery in a cohort of combined kidney and bone marrow allografts. Am J Transplant 2011; 11: 1464-1477.
3. Scandling JD, Busque S, Dejbakhsh-Jones S, et al. Tolerance and chimerism after renal and hematopoietic-cell transplantation. N Engl J Med 2008; 358: 362-368.
4. Scandling JD, Busque S, Dejbakhsh-Jones S, et al. Tolerance and withdrawal of immunosuppressive drugs in patients given kidney and hematopoietic cell transplants. Am J Transplant 2012; 12: 1133-1145.
5. Leventhal J, Abecassis M, Miller J, et al. Chimerism and tolerance without GVHD or engraftment syndrome in HLA-mismatched combined kidney and hematopoietic stem cell transplantation. Sci Transl Med 2012; 4: 124ra128.
6. Leventhal J, Abecassis M, Miller J, et al. Tolerance induction in HLA disparate living donor kidney transplantation by donor stem cell infusion: Durable chimerism predicts outcome. Transplantation 2013; 95: 169-176.
7. Hayamizu K, Lan F, Huie P, Sibley RK, Strober S., Comparison of chimeric and non-chimeric tolerance using posttransplant total lymphoid irradiation: Cytokine expression and chronic rejection. Transplantation 1999; 68: 1036-1044.
8. Lan F, Hayamizu K, Strober S., Cyclosporine facilitates chimeric and inhibits nonchimeric tolerance after posttransplant total lymphoid irradiation. Transplantation 2000; 69: 649-655.
9. Nador RG, Hongo D, Baker J, Yao Z, Strober S., The changed balance of regulatory and naive T cells promotes tolerance after TLI and anti-T-cell antibody conditioning. Am J Transplant 2010; 10: 262-272.
10. Hongo D, Tang X, Dutt S, Nador RG, Strober S., Interactions between NKT cells and Tregs are required for tolerance to combined bone marrow and organ transplants. Blood 2012; 119: 1581-1589.
11. Lan F, Zeng D, Higuchi M, Huie P, Higgins JP, Strober S., Predominance of NK1.1+ TCR alpha beta+ or DX5+ TCR alpha beta+ T cells in mice conditioned with fractionated lymphoid irradiation protects against graft-versus-host disease: "Natural suppressor" cells. J Immunol 2001; 167: 2087-2096.
12. Pillai AB, George TI, Dutt S, Strober S., 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 2009; 113: 4458-4467.
13. van der Merwe M, Abdelsamed HA, Seth A, Ong T, Vogel P, Pillai AB., 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. J Immunol 2013; 191: 5764-5776.
14. Gallina G, Dolcetti L, Serafini P, et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest 2006; 116: 2777-2790.
15. Huang B, Pan PY, Li Q, et al. Gr-1+ CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res 2006; 66: 1123-1131.
16. Dolcetti L, Peranzoni E, Ugel S, et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 2010; 40: 22-35.
17. Gabrilovich DI, Nagaraj S., Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9: 162-174.
18. Garcia MR, Ledgerwood L, Yang Y, et al. Monocytic suppressive cells mediate cardiovascular transplantation tolerance in mice. J Clin Invest 2010; 120: 2486-2496.
19. Terabe M, Matsui S, Noben-Trauth N, et al. NKT cell-mediated repression of tumor immunosurveillance by IL-13 and the IL-4R-STAT6 pathway. Nat Immunol 2000; 1: 515-520.
20. Terabe M, Matsui S, Park JM, et al. Transforming growth factor-beta production and myeloid cells are an effector mechanism through which CD1d-restricted T cells block cytotoxic T lymphocyte-mediated tumor immunosurveillance: Abrogation prevents tumor recurrence. J Exp Med 2003; 198: 1741-1752.
21. Terabe M, Swann J, Ambrosino E, et al. A nonclassical non-Valpha14Jalpha18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J Exp Med 2005; 202: 1627-1633.
22. Izhak L, Ambrosino E, Kato S, et al. Delicate balance among three types of T cells in concurrent regulation of tumor immunity. Cancer Res 2013; 73: 1514-1523.
23. Smiley ST, Kaplan MH, Grusby MJ., Immunoglobulin E production in the absence of interleukin-4-secreting CD1-dependent cells. Science 1997; 275: 977-979.
24. Cui J, Shin T, Kawano T, et al. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 1997; 278: 1623-1626.
25. Trager DK, Banks BA, Rosenbaum GE, et al. Cardiac allograft prolongation in mice treated with combined posttransplantation total-lymphoid irradiation and anti-L3T4 antibody therapy. Transplantation 1989; 47: 587-591.
26. Lan F, Zeng D, Higuchi M, Higgins JP, Strober S., 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 2003; 9: 355-363.
27. Higuchi M, Zeng D, Shizuru J, et al. Immune tolerance to combined organ and bone marrow transplants after fractionated lymphoid irradiation involves regulatory NK T cells and clonal deletion. J Immunol 2002; 169: 5564-5570.
28. Shirota Y, Shirota H, Klinman DM., Intratumoral injection of CpG oligonucleotides induces the differentiation and reduces the immunosuppressive activity of myeloid-derived suppressor cells. J Immunol 2012; 188: 1592-1599.
29. Gumley TP, McKenzie IF, Sandrin MS., Tissue expression, structure and function of the murine Ly-6 family of molecules. Immunol Cell Biol 1995; 73: 277-296.
30. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI., Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181: 5791-5802.
31. Ochando JC, Chen SH., Myeloid-derived suppressor cells in transplantation and cancer. Immunol Res 2012; 54: 275-285.
32. Basso D, Fogar P, Falconi M, et al. Pancreatic tumors and immature immunosuppressive myeloid cells in blood and spleen: Role of inhibitory co-stimulatory molecules PDL1 and CTLA4. An in vivo and in vitro study. PLoS ONE 2013; 8: e54824.
33. Rodriguez PC, Ochoa AC., Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: Mechanisms and therapeutic perspectives. Immunol Rev 2008; 222: 180-191.
34. Bronte V, Serafini P, De Santo C, et al. IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J Immunol 2003; 170: 270-278.
35. Brigl M, Brenner MB., CD1: Antigen presentation and T cell function. Annu Rev Immunol 2004; 22: 817-890.
36. Kronenberg M., Toward an understanding of NKT cell biology: Progress and paradoxes. Annu Rev Immunol 2005; 23: 877-900.
37. Blank C, Brown I, Marks R, Nishimura H, Honjo T, Gajewski TF., Absence of programmed death receptor 1 alters thymic development and enhances generation of CD4/CD8 double-negative TCR-transgenic T cells. J Immunol 2003; 171: 4574-4581.
38. Hamanishi J, Mandai M, Iwasaki M, et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci U S A 2007; 104: 3360-3365.
39. Konishi J, Yamazaki K, Azuma M, Kinoshita I, Dosaka-Akita H, Nishimura M., B7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expression. Clin Cancer Res 2004; 10: 5094-5100.
40. Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK, Anderson AC., Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med 2010; 207: 2187-2194.
41. Ahn GO, Brown JM., Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: Role of bone marrow-derived myelomonocytic cells. Cancer Cell 2008; 13: 193-205.
42. Keir ME, Butte MJ, Freeman GJ, Sharpe AH., PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008; 26: 677-704.
43. Keir ME, Liang SC, Guleria I, et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med 2006; 203: 883-895.
44. Bronte V, Zanovello P., Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 2005; 5: 641-654.
45. Wells AD, Li XC, Li Y, et al. Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance. Nat Med 1999; 5: 1303-1307.
46. Highfill SL, Rodriguez PC, Zhou Q, et al. 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 2010; 116: 5738-5747.