Inhibition of NF-κB and oxidative pathways in human dendritic cells by antioxidative vitamins generates regulatory T cells

Journal of Immunology

Volumn 174, Issue 12, 2005, Pages 7633-7644

  Tan, Peng H ^a   Sagoo, Pervinder ^a,c   Chan, Cliburn ^a,d   Yates, John B ^a,c   Campbell, Jamie ^b,e   Beutelspacher, Sven C ^a,f   Foxwell, Brian M J ^b   Lombardi, Giovanna ^a,c   George, Andrew J T ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e GLAXOSMITHKLINE   (United Kingdom)

^f UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; AUTOANTIGEN; B7 ANTIGEN; CD4 ANTIGEN; CD45RO ANTIGEN; CYTOKINE; DEXAMETHASONE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HLA DR ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 2ALPHA; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 8; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PROSTAGLANDIN E2; PROTEASOME INHIBITOR; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; SN 50; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; OXIDATION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; WESTERN BLOTTING;

EID: 20444426900     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.12.7633     Document Type: Article

References (82)

1. Evans, H. M., and K. S. Bishop. 1922. On the existence of hitherto unrecognized dietary factor essential for reproduction. Nature 56: 650-651.
2. Ouahchi, K., M. Arita, H. Kayden, F. Hentati, M. Ben Hamida, R. Sokol, H. Arai, K. Inoue, J. L. Mandel, and M. Koenig. 1995. Ataxia with isolated vitamin E deficiency is caused by mutations in the α-tocopherol transfer protein. Nat. Genet. 9: 141-145.
3. Gotoda, T., M. Arita, H. Arai, K. Inoue, T. Yokota, Y. Fukuo, Y. Yazaki, and N. Yamada. 1995. Adult-onset spinocerebellar dysfunction caused by a mutation in the gene for the α-tocopherol-transfer protein. N. Engl. J. Med. 333: 1313-1318.
4. Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto miocardico. 1999. Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Lancet 354: 447-455.
5. Yusuf, S., G. Dagenais, J. Pogue, J. Bosch, and P. Sleight. 2000. Vitamin E supplementation and cardiovascular events in high-risk patients: The Heart Outcomes Prevention Evaluation Study Investigators. N. Engl. J. Med. 342: 154-160.
6. Constantinescu, A., D. Han, and L. Packer. 1993. Vitamin E recycling in human erythrocyte membranes. J. Biol. Chem. 268: 10906-10913.
7. Cederberg, I., C. M. Siman, and U. J. Eriksson. 2001. Combined treatment with vitamin E and vitamin C decreases oxidative stress and improves fetal outcome in experimental diabetic pregnancy. Pediatr. Res. 49: 755-762.
8. Jha, P., M. Flather, E. Lonn, M. Farkouh, and S. Yusuf. 1995. The antioxidant vitamins and cardiovascular disease: a critical review of epidemiologic and clinical trial data. Ann. Intern. Med. 123: 860-872.
9. Martin, A., K. Youdim, A. Szprengiel, B. Shukitt-Hale, and I. Joseph. 2002. Roles of vitamins E and C on neurodegenerative diseases and cognitive performance. Nutr. Rev. 60: 308-326.
10. Fang, J. C., S. Kinlay, J. Beltrame, H. Hikiti, M. Wainstein, D. Behrendt, J. Suh, B. Frei, G. H. Mudge, A. P. Selwyn, and P. Ganz. 2002. Effect of vitamins C and E on progression of transplant-associated arteriosclerosis: a randomized trial. Lancet 359: 1108-1113.
11. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18: 767-811.
12. Guermonprez, P., I. Valladeau, L. Zitvogel, C. Thery, and S. Amigorena. 2002. Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol. 20: 621-667.
13. Lechler, R., W. F. Ng, and R. M. Steinman. 2001. Dendritic cells in transplantation: friend or foe? Immunity 14: 357-368.
14. Frasca, L., P. Carmichael, R. Lechler, and G. Lombardi. 1997. Anergic T cells affect linked suppression. Eur. J. Immunol. 27: 3191-3197.
15. + T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192: 1213-1222.
16. Lu, L., and A. W. Thomson. 2002. Manipulation of dendritic cells for tolerance induction in transplantation and autoimmune disease. Transplantation 73: S19-S22.
17. Morelli, A. E., H. Hackstein, and A. W. Thomson. 2001. Potential of tolerogenic dendritic cells for transplantation. Semin. Immunol. 13: 323-335.
18. Kitajima, T., K. Ariizumi, P. R. Bergstresser, and A. Takashima. 1996. A novel mechanism of glucocorticoid-induced immune suppression: the inhibiton of T cell-mediated terminal maturation of a murine dendritic cell line. J. Clin. Invest. 98: 142-147.
19. Penna, G., and L. Adorini. 2000. 1α,25-Dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J. Immunol. 164: 2405-2411.
20. Yoshimura, S., I. Bondeson, F. M. Brennan, B. M. Foxwell, and M. Feldmann. 2001. Role of NFκB in antigen presentation and development of regulatory T cells elucidated by treatment of dendritic cells with the proteasome inhibitor PSI. Eur. J. Immunol. 31: 1883-1893.
21. Steinbnnk, K., M. Wolfl, H. Jonuleit, J. Knop, and A. H. Enk. 1997. Induction of tolerance by IL-10-treated dendritic cells. J. Immunol. 159: 4772-4780.
22. Lu, L., W. C. Lee, T. Takayama, S. Qian, A. Gambotto, P. D. Robbins, and A. W. Thomson. 1999. Genetic engineering of dendritic cells to express immunosuppressive molecules (viral IL-10, TGF-β, and CTLA4Ig). J. Leukocyte Biol. 66: 293-296.
23. Rutault, K., C. Alderman, B. M. Chain, and D. R. Katz. 1999. Reactive oxygen species activate human peripheral blood dendritic cells. Free Radical Biol. Med. 26: 232-238.
24. Mazzeo, D., S. Sacco, P. Di Lucia, G. Penna, L. Adorini, P. Panina-Bordignon. and P. Ghezzi. 2002. Thiol antioxidants inhibit the formation of the interleukin-12 heterodimer: a novel mechanism for the inhibition of IL-12 production. Cytokine 17: 285-293.
25. Islam, K. N., S. Devaraj, and I. Jialal. 1998. α-Tocopherol enrichment of monocytes decreases agonist-induced adhesion to human endothelial cells. Circulation 98: 2255-2261.
26. Mitsiades, N., C. S. Mitsiades, V. Poulaki, D. Chauhan, P. G. Richardson, T. Hideshima, N. Munshi, S. P. Treon, and K. C. Anderson. 2002. Biologic sequelae of nuclear factor-κB blockade in multiple myeloma: therapeutic applications. Blood 99: 4079-4086.
27. + dendritic cells. Proc. Natl. Acad. Sci. USA 93: 2588-2592.
28. Tan, P. H., C. Chan, S. A. Xue, D. Dong, B. Ananthesayanan, M. Manunta, C. Kerouedan, C. Cheshire, J. Wolfe, D. O. Haskard, et al. 2004. Phenotypic and functional differences between human saphenous vein (HSVEC) and umbilical vein (HUVEC) endothelial cells. Atherosclerosis 173: 171-183.
29. Tan, P. H., S. C. Beutelspacher, S. A. Xue, Y. H. Wang, P. Mitchell, J. C. McAlister, D. F. Larkin, M. O. McClure, H. J. Stauss, M. A. Ritter, et al. 2005. Modulation of human dendritic cell function following transduction with viral vectors; implications for gene therapy. Blood, in press.
30. pos T cells by human mature autologous dendritic cells. Eur. J. Immunol. 34: 762-772.
31. Devaraj, S., D. Li, and I. Jialal. 1996. The effects of a tocopherol supplementation on monocyte function: decreased lipid oxidation, interleukin 1β secretion, and monocyte adhesion to endothelium. J. Clin. Invest. 98: 756-763.
32. Harcourt, J. L., M. K. Hagan, and M. K. Offermann. 2000. Modulation of double-stranded RNA-mediated gene induction by interferon in human umbilical vein endothelial cells. J. Interferon Cytokine Res. 20: 1007-1113.
33. Cho, D., E. Hahm, J. S. Kang, Y. I. Kim, Y. Yang, J. H. Park, D. Kim, S. Kim, Y. S. Kim, D. Hur, et al. 2003. Vitamin C down-regulates interleukin-18 production by increasing reactive oxygen intermediate and mitogen-activated protein kinase signalling in B16F10 murine melanoma cells. Melanoma Res. 13: 549-554.
34. Tan, P. H., S. Beutelspacher, Y. H. Wang, M. A. Ritter, M. O. McClure, G. Lombardi, and A. J. George. 2005. Immunolipoplexes: an efficient, non-viral alternative for transfection of human dendritic cells with potential for clinical vaccination. Mol. Ther. 11: 790-800.
35. Hempel, S. L., G. R. Buettner, Y. Q. O'Malley, D. A. Wessels, and D. M. Flaherty. 1999. Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: comparison with 2′,7′- dichlorodihydrofluorescein diacetate, 5(and 6)-carboxy-2′,7′- dichlorodihydrofluorescein diacetate, and dihydrorhodamine 123. Free Radical Biol. Med. 27: 146-159.
36. Sanlioglu, S., C. M. Williams, L. Samavati, N. S. Butler, G. Wang, P. B. McCray, Jr., T. C. Ritchie, G. W. Hunninghake, E. Zandi, and J. F. Engelhardt. 2001. Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-α secretion through IKK regulation of NF-κB. J. Biol. Chem. 276: 30188-30198.
37. Tan, P. H., M. Manunta, N. Ardjomand, S. A. Xue, D. F. P. Larkin, D. O. Haskard, K. M. Taylor, and A. J. T. George. 2003. Antibody targeted gene transfer to endothelium. J. Gene Med. 5: 311-323.
38. + regulatory T cells ex vivo. Blood 102: 2180-2186.
39. Vieira, P. L., P. Kalinski, E. A. Wierenga, M. L. Kapsenberg, and E. C. de Jong. 1998. Glucocorticoids inhibit bioactive IL-12p70 production by in vitro-generated human dendritic cells without affecting their T cell stimulatory potential. J. Immunol. 161: 5245-5251.
40. Rea, D., C. van Kooten, K. E. van Meijgaarden, T. H. Ottenhoff, C. J. Melief, and R. Offringa. 2000. Glucocorticoids transform CD40-triggering of dendritic cells into an alternative activation pathway resulting in antigen-presenting cells that secrete IL-10. Blood 95: 3162-3167.
41. Devaraj, S., and I. Jialal. 2000. α Tocopherol supplementation decreases serum C-reactive protein and monocyte interleukin-6 levels in normal volunteers and type 2 diabetic patients. Free Radical Biol. Med. 29: 790-792.
42. Devaraj, S., and I. Jialal. 1999. α-Tocopherol decreases interleukin-1β release from activated human monocytes by inhibition of 5-lipoxygenase. Arterioscler. Thromb. Vasc. Biol 19: 1125-1133.
43. kip1 functions as an anergy factor inhibiting interleukin 2 transcription and clonal expansion of alloreactive human and mouse helper T lymphocytes. Nat. Med. 6: 290-297.
44. + Treg cells. Blood 105: 1162-1169.
45. + regulatory T cells by targeting of antigens to immature dendritic cells. Blood 101: 4862-4869.
46. Bach, J. F., and J. Francois Bach. 2003. Regulatory T cells under scrutiny. Nat. Rev. Immunol. 3: 189-198.
47. Selenko-Gebauer, N., O. Majdic, A. Szekeres, G. Hofler, E. Guthann, U. Korthauer, G. Zlabinger, P. Steinberger, W. F. Pickl, H. Stockinger, et al. 2003. B7-H1 (programmed death-1 ligand) on dendritic cells is involved in the induction and maintenance of T cell anergy. J. Immunol. 170: 3637-3644.
48. Moser, M., T. De Smedt, T. Sornasse, F. Tielemans, A. A. Chentoufi, E. Muraille, M. Van Mechelen, J. Urbain, and O. Leo. 1995. Glucocorticoids down-regulate dendritic cell function in vitro and in vivo. Eur. J. Immunol. 25: 2818-2824.
49. Yoshimura, S., J. Bondeson, B. M. Foxwell, F. M. Brennan, and M. Feldmann. 2001. Effective antigen presentation by dendritic cells is NF-κB dependent: coordinate regulation of MHC, co-stimulatory molecules and cytokines. Int. Immunol. 13: 675-683.
50. Neuzil, J., T. Weber, A. Schroder, M. Lu, G. Ostermann, N. Geliert, G. C. Mayne, B. Olejnicka, A. Negre-Salvayre, M. Sticha, et al. 2001. Induction of cancer cell apoptosis by α-tocopheryl succinate: molecular pathways and structural requirements. FASEB J. 15: 403-415.
51. Griffin, M. D., W. Lutz, V. A. Phan, L. A. Bachman, D. J. McKean, and R. Kumar. 2001. Dendritic cell modulation by 1α,25 dihydroxyvitamin D3 and its analogs: a vitamin D receptor-dependent pathway that promotes a persistent state of immaturity in vitro and in vivo. Proc. Natl. Acad. Sci. USA 98: 6800-6805.
52. Griffin, M. D., W. H. Lutz, V. A. Phan, L. A. Bachman, D. J. McKean, and R. Kumar. 2000. Potent inhibition of dendritic cell differentiation and maturation by vitamin D analogs. Biochem. Biophys. Res. Commun. 270: 701-708.
53. Gauzzi, M. C., C. Purificato, K. Donato, Y. Jin, L. Wang, K. C. Daniel, A. A. Maghazachi, F. Belardelli, L. Adorini, and S. Gessani. 2005. Suppressive effect of 1α,25-dihydroxyvitamin D3 on type I IFN-mediated monocyte differentiation into dendritic cells: impairment of functional activities and chemotaxis. J. Immunol. 174: 270-276.
54. + dendritic cells. J. Immunol. 174: 2061-2070.
55. Piemonti, L., P. Monti, M. Sironi, P. Fraticelli, B. E. Leone, E. Dal Cin, P. Allavena, and V. Di Carlo. 2000. Vitamin D3 affects differentiation, maturation, and function of human monocyte-derived dendritic cells. J. Immunol. 164: 4443-4451.
56. Dong, X., T. Craig, N. Xing, L. A. Bachman, C. V. Paya, F. Weih, D. J. McKean, R. Kumar, and M. D. Griffin. 2003. Direct transcriptional regulation of RelB by 1α,25-dihydroxyvitamin D3 and its analogs: physiologic and therapeutic implications for dendritic cell function. J. Biol. Chem. 278: 49378-49385.
57. D'Ambrosio, D., M. Cippitelli, M. G. Cocciolo, D. Mazzeo, P. Di Lucia, R. Lang, F. Sinigaglia, and P. Panina-Bordignon. 1998. Inhibition of IL-12 production by 1,25-dihydroxyvitamin D3: involvement of NF-κB; down-regulation in transcriptional repression of the p40 gene. J. Clin. Invest. 101: 252-262.
58. Pedersen, A. E., M. Gad, M. R. Walter, and M. H. Claesson. 2004. Induction of regulatory dendritic cells by dexamethasone and 1α,25-dihydroxyvitamin D(3). Immunol. Lett. 91: 63-69.
59. Adorini, L., N. Giarratana, and G. Penna. 2004. Pharmacological induction of tolerogenic dendritic cells and regulatory T cells. Semin. Immunol. 16: 127-134.
60. Van Halteren, A. G., O. M. Tysma, E. van Etten, C. Mathieu, and B. O. Roep, 2004. 1α,25-Dihydroxyvitamin D3 or analogue treated dendritic cells modulate human autoreactive T cells via the selective induction of apoptosis. J. Autoimmun. 23: 233-239.
61. Dong, X., L. A. Bachman, R. Kumar, and M. D. Griffin. 2003. Generation of antigen-specific, interleukin-10-producing T-cells using dendritic cell stimulation and steroid hormone conditioning. Transplant Immunol. 11: 323-333.
62. Tasinato, A., D. Boscoboinik, G. M. Bartoli, P. Maroni, and A. Azzi. 1995. D-α-tocopherol inhibition of vascular smooth muscle cell proliferation occurs at physiological concentrations, correlates with protein kinase C inhibition, and is independent of its antioxidant properties. Proc. Natl. Acad. Sci. USA 92: 12190-12194.
63. Freedman, J. E., J. H. Farhat, J. Loscalzo, and J. F. Keaney, Jr. 1996. α-Tocopherol inhibits aggregation of human platelets by a protein kinase C-dependent mechanism. Circulation 94: 2434-2440.
64. Kanno, T., T. Utsumi, H. Kobuchi, Y. Takehara, J. Akiyama, T. Yoshioka, A. A. Horton, and K. Utsumi. 1995. Inhibition of stimulus-specific neutrophil superoxide generation by α-tocopherol. Free Radical Res. 22: 431-440.
65. Hehenberger, K., and A. Hansson. 1997. High glucose-induced growth factor resistance in human fibroblasts can be reversed by antioxidants and protein kinase C-inhibitors. Cell Biochem. Funct. 15: 197-201.
66. Studer, R. K., P. A. Craven, and F. R. DeRubertis. 1997. Antioxidant inhibition of protein kinase C-signaled increases in transforming growth factor-β in mesangial cells. Metabolism 46: 918-925.
67. Clement, S., A. Tasinato, D. Boscoboinik, and A. Azzi. 1997. The effect of α-tocopherol on the synthesis, phosphorylation and activity of protein kinase C in smooth muscle cells after phorbol 12-myristate 13-acetate down-regulation. Eur. J. Biochem. 246: 745-749.
68. Leitges, M., C. Schmedt, R. Guinamard, J. Davoust, S. Schaal, S. Stabel, and A. Tarakhovsky. 1996. Immunodeficiency in protein kinase Cβ-deficient mice. Science 273: 788-791.
69. Sun, Z., C. W. Arendt, W. Ellmeier, E. M. Schaeffer, M. J. Sunshine, L. Gandhi, J. Annes, D. Petrzilka, A. Kupfer, P. L. Schwartzberg, and D. R. Littman. 2000. PKC-θ is required for TCR-induced NF-κB activation in mature but not immature T lymphocytes. Nature 404: 402-407.
70. Valledor, A. F., J. Xaus, M. Comalada, C. Soler, and A. Celada. 2000. Protein kinase Cε is required for the induction of mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages. J. Immunol. 164: 29-37.
71. Aksoy, E., Z. Amraoui, S. Goriely, M. Goldman, and F. Willems. 2002. Critical role of protein kinase Cε for lipopolysaccharide-induced IL-12 synthesis in monocyte-derived dendritic cells. Eur. J. Immunol. 32: 3040-3049.
72. Carcamo, J. M., A. Pedraza, O. Borquez-Ojeda, and D. W. Golde. 2002. Vitamin C suppresses TNFα-induced NFκB activation by inhibiting IκBα phosphorylation. Biochemistry 41: 12995-13002.
73. Kyaw, M., M. Yoshizumi, K. Tsuchiya, K. Kirima, and T. Tamaki. 2001. Anti-oxidants inhibit JNK and p38 MAPK activation but not ERK 1/2 activation by angiotensin II in rat aortic smooth muscle cells. Hypertens. Res. 24: 251-261.
74. Seanor, K. L., J. V. Cross, S. M. Nguyen, M. Van, and D. J. Templeton. 2003. Reactive quinones differentially regulate SAPK/JNK and p38/mHOG stress kinases. Antioxid. Redox. Signal 5: 103-113.
75. Stephens, N. G., A. Parsons, P. M. Schofield, F. Kelly, K. Cheeseman, and M. J. Mitchinson. 1996. Randomized controlled trial of vitamin E in patients with coronary disease: Cambridge Heart Antioxidant Study (CHAOS). Lancet 347: 781-786.
76. The α-Tocopherol, β Carotene Cancer Prevention Study Group. 1994. The effect of vitamin E and β carotene on the incidence of lung cancer and other cancers in male smokers. N. Engl. J. Med. 330: 1029-1035.
77. Goh, K. C., M. J. deVeer, and B. R. Williams. 2000. The protein kinase PKR is required for p38 MAPK activation and the innate immune response to bacterial endotoxin. EMBO J. 19: 4292-4297.
78. D'Acquisto, F., and S. Ghosh. 2001. PACT and PKR: turning on NF-κB in the absence of virus. Sci. STKE 2001: RE1.
79. Williams, B. R. 2001. Signal integration via PKR. Sci. STKE 2001: RE2.
80. phox membrane translocation and phosphorylation. J. Biol. Chem. 273: 32801-32805.
81. Auphan, N., J. A. DiDonato, C. Rosette, A. Helmberg, and M. Karin. 1995. Immunosuppression by glucocorticoids: inhibition of NF-κB activity through induction of IκB synthesis. Science 270: 286-290.
82. De Bosscher, K., M. L. Schmitz, W. Vanden Berghe, S. Plaisance, W. Fiers, and G. Haegeman. 1997. Glucocorticoid-mediated repression of nuclear factor-κB-dependent transcription involves direct interference with transactivation. Proc. Natl. Acad. Sci. USA 94: 13504-13509.