Human regulatory macrophages are potent in suppression of the xenoimmune response via indoleamine-2,3-dioxygenase-involved mechanism(s)

Xenotransplantation

Volumn 24, Issue 5, 2017, Pages

  Guo, Fei ^a,b   Hu, Min ^a   Huang, Dandan ^a   Zhao, Yuanfei ^a   Heng, Benjamin ^c   Guillemin, Gilles ^c   Lim, Chai K ^c   Hawthorne, Wayne J ^a   Yi, Shounan ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b THE THIRD XIANGYA HOSPITAL OF CENTRAL SOUTH UNIVERSITY   (China)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

indoleamine 2,3 dioxygenase; regulatory macrophages; transplantation tolerance; xenotransplantation

Indexed keywords

CD14 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; COLONY STIMULATING FACTOR 1; HLA DR ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; MACROPHAGE; MIXED LYMPHOCYTE REACTION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; UPREGULATION; XENOTRANSPLANTATION; ANIMAL; CELL CULTURE; CELL PROLIFERATION; DRUG EFFECT; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; METABOLISM; MONOCYTE; MONONUCLEAR CELL; PIG; PROCEDURES; T LYMPHOCYTE; XENOGRAFT;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; HUMANS; IMMUNOSUPPRESSION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; MONOCYTES; SWINE; T-LYMPHOCYTES; TRANSPLANTATION, HETEROLOGOUS;

EID: 85026664020     PISSN: 0908665X     EISSN: 13993089     Source Type: Journal    
DOI: 10.1111/xen.12326     Document Type: Article

References (51)

1. Ekser B, Ezzelarab M, Hara H, et al. Clinical xenotransplantation: the next medical revolution? Lancet. 2012;379:672-683.
2. Cooper DK, Bottino R. Recent advances in understanding xenotransplantation: implications for the clinic. Exp Rev Clin Immunol. 2015;11:1379-1390.
3. Satyananda V, Hara H, Ezzelarab MB, Phelps C, Ayares D, Cooper DK. New concepts of immune modulation in xenotransplantation. Transplantation. 2013;96:937-945.
4. Vadori M, Cozzi E. The immunological barriers to xenotransplantation. Tissue Antigens. 2015;86:239-253.
5. Higginbotham L, Ford ML, Newell KA, Adams AB. Preventing T cell rejection of pig xenografts. Int J Surg. 2015;23:285-290.
6. Griesemer A, Yamada K, Sykes M. Xenotransplantation: immunological hurdles and progress toward tolerance. Immunol Rev. 2014;258:241-258.
7. Scalea J, Hanecamp I, Robson SC, Yamada K. T-cell-mediated immunological barriers to xenotransplantation. Xenotransplantation. 2012;19:23-30.
8. Yamada K, Sachs DH, DerSimonian H. Human anti-porcine xenogeneic T cell response. Evidence for allelic specificity of mixed leukocyte reaction and for both direct and indirect pathways of recognition. J Immunol. 1995;155:5249-5256.
9. Dorling A, Lombardi G, Binns R, Lechler RI. Detection of primary direct and indirect human anti-porcine T cell responses using a porcine dendritic cell population. Eur J Immunol. 1996;26:1378-1387.
10. Hering BJ, Cooper DK, Cozzi E, et al. The international xenotransplantation association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes– executive summary. Xenotransplantation. 2009;16:196-202.
11. Lin YJ, Hara H, Tai HC, et al. Suppressive efficacy and proliferative capacity of human regulatory T cells in allogeneic and xenogeneic responses. Transplantation. 2008;86:1452-1462.
12. June CH, Riddell SR, Schumacher TN. Adoptive cellular therapy: a race to the finish line. Sci Transl Med. 2015;7:280 ps287.
13. Zhou X, Tang J, Cao H, Fan H, Li B. Tissue resident regulatory T cells: novel therapeutic targets for human disease. Cell Mol Immunol. 2015;12:543-552.
14. Raker VK, Domogalla MP, Steinbrink K. Tolerogenic dendritic cells for regulatory T cell induction in man. Front Immunol. 2015;6:569.
15. Yi S, Ji M, Wu J, et al. Adoptive transfer with in vitro expanded human regulatory T cells protects against porcine islet xenograft rejection via interleukin-10 in humanized mice. Diabetes. 2012;61:1180-1191.
16. Sato K, Yamashita N, Baba M, Matsuyama T. Regulatory dendritic cells protect mice from murine acute graft-versus-host disease and leukemia relapse. Immunity. 2003;18:367-379.
17. Lund FE, Randall TD. Effector and regulatory B cells: modulators of CD4+ T cell immunity. Nat Rev Immunol. 2010;10:236-247.
18. Hutchinson JA, Riquelme P, Geissler EK, Fandrich F. Human regulatory macrophages. Methods Mol Biol. 2011;677:181-192.
19. Riquelme P, Tomiuk S, Kammler A, et al. IFN-gamma-induced iNOS expression in mouse regulatory macrophages prolongs allograft survival in fully immunocompetent recipients. Mol Ther. 2013;21:409-422.
20. Hutchinson JA, Riquelme P, Sawitzki B, et al. Cutting edge: immunological consequences and trafficking of human regulatory macrophages administered to renal transplant recipients. J Immunol. 2011;187:2072-2078.
21. Riquelme P, Geissler EK, Hutchinson JA. Alternative approaches to myeloid suppressor cell therapy in transplantation: comparing regulatory macrophages to tolerogenic DCs and MDSCs. Transplant Res. 2012;1:17.
22. Sahu D, Dey S, Pathak T, Ganguly B. Regioselectivity of vinyl sulfone based 1,3-dipolar cycloaddition reactions with sugar azides by computational and experimental studies. Org Lett. 2014;16:2100-2103.
23. Arnold L, Henry A, Poron F, et al. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med. 2007;204:1057-1069.
24. Wahl SM, McCartney-Francis N, Allen JB, Dougherty EB, Dougherty SF. Macrophage production of TGF-beta and regulation by TGF-beta. Ann N Y Acad Sci. 1990;593:188-196.
25. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol. 2004;4:762-774.
26. Ostrand-Rosenberg S, Horn LA, Haile ST. The programmed death-1 immune-suppressive pathway: barrier to antitumor immunity. J Immunol. 2014;193:3835-3841.
27. Grohmann U, Fallarino F, Puccetti P. Tolerance, DCs and tryptophan: much ado about IDO. Trends Immunol. 2003;24:242-248.
28. Metz R, Rust S, Duhadaway JB, et al. IDO inhibits a tryptophan sufficiency signal that stimulates mTOR: a novel IDO effector pathway targeted by D-1-methyl-tryptophan. Oncoimmunology. 2012;1:1460-1468.
29. Carlin JM, Borden EC, Sondel PM, Byrne GI. Interferon-induced indoleamine 2,3-dioxygenase activity in human mononuclear phagocytes. J Leukoc Biol. 1989;45:29-34.
30. Murray HW, Szuro-Sudol A, Wellner D, et al. Role of tryptophan degradation in respiratory burst-independent antimicrobial activity of gamma interferon-stimulated human macrophages. Infect Immun. 1989;57:845-849.
31. Yi S, Feng X, Hawthorne WJ, Patel AT, Walters SN, O'Connell PJ. CD4+ T cells initiate pancreatic islet xenograft rejection via an interferon-gamma-dependent recruitment of macrophages and natural killer cells. Transplantation. 2002;73:437-446.
32. Pierson RN 3rd, Winn HJ, Russell PS, Auchincloss H Jr. Xenogeneic skin graft rejection is especially dependent on CD4+ T cells. J Exp Med. 1989;170:991-996.
33. Morris CF, Simeonovic CJ, Fung MC, Wilson JD, Hapel AJ. Intragraft expression of cytokine transcripts during pig proislet xenograft rejection and tolerance in mice. J Immunol. 1995;154:2470-2482.
34. Yi S, Hawthorne WJ, Lehnert AM, et al. T cell-activated macrophages are capable of both recognition and rejection of pancreatic islet xenografts. J Immunol. 2003;170:2750-2758.
35. Loudovaris T, Mandel TE, Charlton B. CD4+ T cell mediated destruction of xenografts within cell-impermeable membranes in the absence of CD8+ T cells and B cells. Transplantation. 1996;61:1678-1684.
36. Chen G, Kheradmand T, Bryant J, et al. Intragraft CD11b(+) IDO(+) cells mediate cardiac allograft tolerance by ECDI-fixed donor splenocyte infusions. Am J Transplant. 2012;12:2920-2929.
37. Li Y, Tredget EE, Ghaffari A, Lin X, Kilani RT, Ghahary A. Local expression of indoleamine 2,3-dioxygenase protects engraftment of xenogeneic skin substitute. J Invest Dermatol. 2006;126:128-136.
38. Miller ML, Daniels MD, Wang T, et al. Tracking of TCR-Tg T cells reveals multiple mechanisms maintain cardiac transplant tolerance in mice. Am J Transplant. 2016;16:2854-2864.
39. Moravej A, Geramizadeh B, Azarpira N, et al. Mesenchymal stem cells increase skin graft survival time and up-regulate PD-L1 expression in splenocytes of mice. Immunol Lett. 2017;182:39-49.
40. Ma D, Duan W, Li Y, et al. PD-L1 deficiency within islets reduces allograft survival in mice. PLoS ONE. 2016;11:e0152087.
41. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity. 2010;32:593-604.
42. Ottonello L, Epstein AL, Mancini M, Dapino P, Dallegri F. Monoclonal LYM-1 antibody-dependent cytolysis by human neutrophils exposed to GM-CSF: auto-regulation of target cell attack by cathepsin G. J Leukoc Biol. 2004;75:99-105.
43. Yu FS, Yang JS, Yu CS, et al. Safrole suppresses murine myelomonocytic leukemia WEHI-3 cells in vivo, and stimulates macrophage phagocytosis and natural killer cell cytotoxicity in leukemic mice. Environ Toxicol. 2013;28:601-608.
44. Taylor MW, Feng GS. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 1991;5:2516-2522.
45. Munn DH, Shafizadeh E, Attwood JT, Bondarev I, Pashine A, Mellor AL. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med. 1999;189:1363-1372.
46. Masteller EL, Tang Q, Bluestone JA. Antigen-specific regulatory T cells–ex vivo expansion and therapeutic potential. Semin Immunol. 2006;18:103-110.
47. Sagoo P, Ali N, Garg G, Nestle FO, Lechler RI, Lombardi G. Human regulatory T cells with alloantigen specificity are more potent inhibitors of alloimmune skin graft damage than polyclonal regulatory T cells. Sci Transl Med 2011;3:83ra42.
48. Peters JH, Hilbrands LB, Koenen HJ, Joosten I. Ex vivo generation of human alloantigen-specific regulatory T cells from CD4(pos)CD25(high) T cells for immunotherapy. PLoS ONE. 2008;3:e2233.
49. Ge W, Jiang J, Arp J, Liu W, Garcia B, Wang H. Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2,3-dioxygenase expression. Transplantation. 2010;90:1312-1320.
50. Bock F, Rossner S, Onderka J, et al. Topical application of soluble CD83 induces IDO-mediated immune modulation, increases Foxp3+ T cells, and prolongs allogeneic corneal graft survival. J Immunol. 2013;191:1965-1975.
51. He Y, Zhou S, Liu H, et al. Indoleamine 2, 3-dioxgenase transfected mesenchymal stem cells induce kidney allograft tolerance by increasing the production and function of regulatory T cells. Transplantation. 2015;99:1829-1838.