Intravenous infusion of syngeneic apoptotic cells by photopheresis induces antigen-specific regulatory T cells

Journal of Immunology

Volumn 174, Issue 10, 2005, Pages 5968-5976

  Maeda, Akira ^a   Schwarz, Agatha ^a   Kernebeck, Kerstin ^a   Gross, Nicole ^a   Aragane, Yoshinori ^b   Peritt, David ^c   Schwarz, Thomas ^d  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Therakos   (United States)

^d UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 FLUORO 2,4 DINITROBENZENE; CD4 ANTIGEN; HAPTEN; INTERLEUKIN 2 RECEPTOR ALPHA; METHOXSALEN; OXAZOLONE; PHOTOSENSITIZING AGENT;

ANIMAL CELL; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CONTACT ALLERGY; FEMALE; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; LYMPH NODE CELL; MOUSE; NONHUMAN; PALLIATIVE THERAPY; PRIORITY JOURNAL; PUVA; RECIPIENT; RISK BENEFIT ANALYSIS; T CELL LYMPHOMA; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; ULTRAVIOLET A RADIATION;

EID: 18644372264     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.10.5968     Document Type: Article

References (65)

1. Gilchrest, B. A., J. A. Parrish, L. Tanenbaum, H. A. Haynes, and T. B. Fitzpatrick. 1976. Oral methoxsalen photochemotherapy of mycosis fungoides. Cancer 38: 683-689.
2. Efferth, T., U. Fabry, and R. Osieka. 2001. Induction of apoptosis, depletion of glutathione, and DNA damage by extracorporeal photochemotherapy and psoralen with exposure to UV light in vitro. Anticancer Res. 21: 2777-2783.
3. Edelson, R., C. Berger, F. Gasparro, B. Jegasothy, P. Heald, B. Wintroub, E. Vonderheid, R. Knobler, K. Wolff, G. Plewig, et al. 1987. Treatment of cutaneous T-cell lymphoma by extracorporeal photochemotherapy: preliminary results. N. Engl. J. Med. 316: 297-303.
4. Heald, P., A. Rook, M. Perez, B. Wintroub, R. Knobler, B. Jegasothy, F. Gasparro, C. Berger, and R. Edelson. 1992. Treatment of erythrodermic cutaneous T-cell lymphoma with extracorporeal photochemotherapy. J. Am. Acad. Dermatol. 27: 427-433.
5. Laroche, L., R. L. Edelson, M. Perez, and C. L. Berger. 1991. Antigen-specific tolerance induced by autoimmunization with photoinactivated syngeneic effector cells. Ann. NY Acad. Sci. 636: 113-123.
6. Rook, A. H., K. R. Suchin, D. M. Kao, E. K. Yoo, W. H. Macey, B. J. DeNardo, P. G. Bromely, Y. Geng, J. M. Junkins-Hopkins, and S. R. Lessin. 1999. Photopheresis: clinical applications and mechanism of action. J. Investig. Dermatol. Symp. Proc. 4: 85-90.
7. Edelson, R. L. 2001. Cutaneous T cell lymphoma: the helping hand of dendritic cells. Ann. NY Acad. Sci. 941: 1-11.
8. Edelson, R. L. 2002. Transimmunization: the science catches up to the clinical success. Transfus. Apheresis Sci. 26: 177-180.
9. Lim, H. W., and R. L. Edelson. 1995. Photopheresis for the treatment of cutaneous T-cell lymphoma. Hematol. Oncol Clin. North Am. 9: 1117-1126.
10. Suchin, K. R., M. Cassin, R. Washko, G. Nahass, M. Berkson, B. Stouch, B. R. Vowels, and A. H. Rook. 1999. Extracorporeal photochemotherapy does not suppress T- or B-cell responses to novel or recall antigens. J. Am. Acad. Dermatol. 41: 980-986.
11. Aubin, F., and C. Mousson. 2004. Ultraviolet light-induced regulatory (suppressor) T cells: an approach for promoting induction of operational allograft tolerance? Transplantation 77: S29-S31.
12. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389: 737-742.
13. + regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol. Rev. 182: 18-32.
14. Roncarolo, M. G., R. Bacchetta, C. Bordignon, S. Narula, and M. K. Levings. 2001. Type 1 T regulatory cells. Immunol. Rev. 182: 68-79.
15. Chatenoud, L., B. Salomon, and J. A. Bluestone. 2001. Suppressor T cells-they're back and critical for regulation of autoimmunity! Immunol. Rev. 182: 149-163.
16. + regulatory T cells generated ex vivo with IL-2 and TGF-β suppress a stimulatory graft-versus-host disease with a lupus-like syndrome. J. Immunol. 172: 1531-1539.
17. Wood, K. J., and S. Sakaguchi. 2003. Regulatory T cells in transplantation tolerance. Nat. Rev. Immunol. 3: 199-210.
18. Schwarz, A., A. Maeda, M. K. Wild, K. Kernebeck, N. Gross, Y. Aragane, S. Beissert, D. Vestweber, and T. Schwarz. 2004. Ultraviolet radiation-induced regulatory T cells not only inhibit the induction but can suppress the effector phase of contact hypersensitivity. J. Immunol. 172: 1036-1043.
19. Schwarz, T. 1999. Ultraviolet radiation-induced tolerance. Allergy 54: 1252-1261.
20. Mahnke, K., J. Knop, and A. H. Enk. 2003. Induction of tolerogenic DCs: "you are what you eat". Trends Immunol 24: 646-651.
21. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 1: 965-975.
22. Albert, M. L. 2004. Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat. Rev. Immunol. 4: 223-231.
23. Morelli, A. E., A. T. Larregina, W. J. Shufesky, A. F. Zahorchak, A. J. Logar, G. D. Papworth, Z. Wang, S. C. Watkins, L. D. Falo, Jr., and A. W. Thomson. 2003. Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood 101: 611-620.
24. + T cells produce active immune unresponsiveness. J. Immunol. 168: 5589-5595.
25. Huynh, M. L., V. A. Fadok, and P. M. Henson. 2002. Phosphatidylserine- dependent ingestion of apoptotic cells promotes TGF-β1 secretion and the resolution of inflammation. J. Clin. Invest. 109: 41-50.
26. Steinman, R. M., D. Hawiger, K. Liu, L. Bonifaz, D. Bonnyay, K. Mahnke, T. Iyoda, J. Ravetch, M. Dhodapkar, K. Inaba, and M. Nussenzweig. 2003. Dendritic cell function in vivo during the steady state: a role in peripheral tolerance. Ann. NY Acad. Sci. 987: 15-25.
27. Matzinger, P. 2002. The danger model: a renewed sense of self Science 296: 301-305.
28. Barr, M. L. 1998. Photopheresis in transplantation: future research and directions. Transplant Proc. 30: 2248-2250.
29. Greinix, H. T., B. Volc-Platzer, and R. M. Knobler. 2000. Extracorporeal photochemotherapy in the treatment of severe graft-versus-host disease. Lenk. Lymphoma 36: 425-434.
30. Reinisch, W., H. Nahavandi, R. Santella, Y. Zhang, C. Gasche, G. Moser, T. Waldhor, A. Gangl, H. Vogelsang, and R. Knobler. 2001. Extracorporeal photochemotherapy in patients with steroid-dependent Crohn's disease: a prospective pilot study. Aliment Pharmacol. Ther. 15: 1313-1322.
31. Malawista, S. E., D. Trock, and R. L. Edelson. 1991. Photopheresis for rheumatoid arthritis. Ann. NY Acad. Sci. 636: 217-226.
32. Prinz, B., F. Nachbar, and G. Plewig. 1994. Treatment of severe atopic dermatitis with extracorporeal photopheresis. Arch. Dermatol. Res. 287: 48-52.
33. Legitimo, A., R. Consolini, R. Di Stefano, W. Bencivelli, and F. Mosca. 2002. Psoralen and UVA light: an in vitro investigation of multiple immunological mechanisms underlying the immunosuppression induction in allograft rejection. Blood Cells Mol. Dis. 29: 24-34.
34. Heng, A. E., B. Sauvezie, L. Genestier, F. Demeocq, A. Dosgilbert, and P. Deteix. 2003. PUVA apoptotic response in activated and resting human lymphocytes. Transfus. Apheresis. Sci. 28: 43-50.
35. Stuart, L. M., M. Lucas, C. Simpson, J. Lamb, J. Savill, and A. Lacy-Hulbert. 2002. Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J. Immunol. 168: 1627-1635.
36. Fadok, V. A. 2003. The sirens' call. Nat. Cell Biol. 5: 697-699.
37. Byrne, A., and D. J. Reen. 2002. Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J. Immunol. 168: 1968-1977.
38. Newman, S. L., J. E. Henson, and P. M. Henson. 1982. Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages. J. Exp. Med. 156: 430-442.
39. 3/CD36/thrombospondin recognition mechanism and lack of phlogistic response. Am. J. Pathol. 149: 911-921.
40. Meagher, L. C., J. S. Savill, A. Baker, R. W. Fuller, and C. Haslett. 1992. Phagocytosis of apoptotic neutrophils does not induce macrophage release of thromboxane B2. J. Leukocyte Biol. 52: 269-273.
41. Fast, L. D. 2003. The effect of exposing murine splenocytes to UVB light, psoralen plus UVA light, or γ-irradiation on in vitro and in vivo immune responses. Transfusion 43: 576-583.
42. Steinman, R. M., S. Turley, I. Mellman, and K. Inaba. 2000. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191: 411-416.
43. Bittencourt, M. C., S. Perruche, E. Contassot, S. Fresnay, M. H. Baron, R. Angonin, F. Aubin, P. Herve, P. Tiberghien, and P. Saas. 2001. Intravenous injection of apoptotic leukocytes enhances bone marrow engraftment across major histocompatibility barriers. Blood 98: 224-230.
44. Kleinclauss, F., S. Perruche, J. Y. Cahn, P. Tiberghien, and P. Saas. 2003. Administration of donor apoptotic cells: an alternative cell-based therapy to induce tolerance? Transplantation 75(Suppl. 9): 43S-45S.
45. Saas, P., P. Tiberghien, and M. de Carvalho Bittencourt. 2002. Cell-based therapy approaches using dying cells: from tumour immunotherapy to transplantation tolerance induction. Expert Opin. Biol. Ther. 2: 249-263.
46. Barker, R. N., L. P. Erwig, K. S. Hill, A. Devine, W. P. Pearce, and A. J. Rees. 2002. Antigen presentation by macrophages is enhanced by the uptake of necrotic, but not apoptotic, cells. Clin. Exp. Immunol. 127: 220-225.
47. Fadok, V. A., D. L. Bratton, L. Guthrie, and P. M. Henson. 2001. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J. Immunol. 166: 6847-6854.
48. Voll, R. E., M. Herrmann, E. A. Roth, C. Stach, J. R. Kalden, and I. Girkontaite. 1997. Immunosuppressive effects of apoptotic cells. Nature 390: 350-351.
49. Vink, A. A., F. M. Strickland, C. Bucana, P. A. Cox, L. Roza, D. B. Yarosh, and M. L. Kripke. 1996. Localization of DNA damage and its role in altered antigen-presenting cell function in ultraviolet-irradiated mice. J. Exp. Med. 183: 1491-1500.
50. Greene, M. I., M. S. Sy, M. Kripke, and B. Benacerraf. 1979. Impairment of antigen-presenting cell function by ultraviolet radiation. Proc. Natl. Acad. Sci. USA 76: 6591-6595.
51. Vink, A. A., A. M. Moodycliffe, V. Shreedhar, S. E. Ullrich, L. Roza, D. B. Yarosh, and M. L. Kripke. 1997. The inhibition of antigen-presenting activity of dendritic cells resulting from UV irradiation of murine skin is restored by in vitro photorepair of cyclobutane pyrimidine dimers. Proc. Natl. Acad. Sci. USA 94: 5255-5260.
52. Schwarz, A., S. Grabbe, Y. Aragane, K. Sandkuhl, H. Riemann, T. A. Luger, M. Kubin, G. Trinchieri, and T. Schwarz. 1996. Interleukin-12 prevents ultraviolet B-induced local immunosuppression and overcomes UVB-induced tolerance. J. Invest. Dermatol. 106: 1187-1191.
53. Schwarz, A., S. Stander, M. Berneburg, M. Bohm, D. Kulms, H. van Steeg, K. Grosse-Heitmeyer, J. Krutmann, and T. Schwarz. 2002. Interleukin-12 suppresses ultraviolet radiation-induced apoptosis by inducing DNA repair. Nat. Cell Biol. 4: 26-31.
54. Schwarz, A., A. Maeda, K. Kernebeck, H. van Steeg, S. Beissert, and T. Schwarz. 2005. Prevention of UV radiation-induced immunosuppression by IL-12 is dependent on DNA repair. J. Exp. Med. 201: 173-179.
55. Gorgun, G., K. B. Miller, and F. M. Foss. 2002. Immunologic mechanisms of extracorporeal photochemotherapy in chronic graft-versus-host disease. Blood 100: 941-947.
56. Plumas, J., O. Manches, and L. Chaperot. 2003. Mechanism of action of extracorporeal photochemotherapy in the control of GVHD: involvement of dendritic cells. Leukemia 17: 2061-2062.
57. Craciun, L. I., P. Stordeur, L. Schandene, H. Duvillier, D. Bron, M. Lambermont, M. Goldman, and E. Dupont. 2002. Increased production of interleukin-10 and interleukin-1 receptor antagonist after extracorporeal photochemotherapy in chronic graft-versus-host disease. Transplantation 74: 995-1000.
58. Bladon, J., and P. C. Taylor. 1999. Extracorporeal photopheresis induces apoptosis in the lymphocytes of cutaneous T-cell lymphoma and graft-versus-host disease patients. Br. J. Haematol. 107: 707-711.
59. Bladon, J., and P. C. Taylor. 2003. Early reduction in number of T cells producing proinflammatory cytokines, observed after extracorporeal photopheresis, is not linked to apoptosis induction. Transplant Proc. 35: 1328-1332.
60. Barr, M. L., B. M. Meiser, H. J. Eisen, R. F. Roberts, U. Livi, R. Dall'Amico, R. Dorent, J. G. Rogers, B. Radovancevic, D. O. Taylor, V. Jeevanandam, and C. C. Marboe. 1998. Photopheresis for the prevention of rejection in cardiac transplantation: Photopheresis Transplantation Study Group. N. Engl. J. Med. 339: 1744-1751.
61. Darvay, A., N. Salooja, and R. Russell-Jones. 2004. The effect of extracorporeal photopheresis on intracellular cytokine expression in chronic cutaneous graft-versus-host disease. J. Eur. Acad. Dermatol. Venereol. 18: 279-284.
62. Toews, G. B., P. R. Bergstresser, and J. W. Streilein. 1980. Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J. Immunol. 124: 445-453.
63. Aragane, Y., A. Maeda, A. Schwarz, T. Tezuka, K. Ariizumi, and T. Schwarz. 2003. Involvement of dectin-2 in ultraviolet radiation-induced tolerance. J. Immunol. 171: 3801-3807.
64. Schwarz, A., S. Beissert, K. Grosse-Heitmeyer, M. Gunzer, J. A. Bluestone, S. Grabbe, and T. Schwarz. 2000. Evidence for functional relevance of CTLA-4 in ultraviolet-radiation-induced tolerance. J. Immunol. 165: 1824-1831.
65. Aubin, F. 2003. Mechanisms involved in ultraviolet light-induced immunosuppression. Eur. J. Dermatol. 13: 515-523.