Inhibition of allogeneic T-cell responses by dendritic cells expressing transduced indoleamine 2,3-dioxygenase

Journal of Gene Medicine

Volumn 7, Issue 5, 2005, Pages 565-575

  Funeshima, Naoko ^a   Fujino, Masayuki ^a   Kitazawa, Yusuke ^a   Hara, Yuko ^a   Hara, Yoshiaki ^a   Hayakawa, Kou ^b   Okuyama, Torayuki ^a   Kimura, Hiromitus ^a   Li, Xiao Kang ^a  

^a NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^b National Center for Child Health and Development   (Japan)

Author keywords

Adenovirus vector; Cell cycle arrest; Dendritic cells; Indoleamine 2,3 dioxygenase; Proliferation

Indexed keywords

ADENOVIRUS VECTOR; B7 ANTIGEN; CD86 ANTIGEN; COMPLEMENTARY DNA; IA ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CELL CULTURE; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; DENDRITIC CELL; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; FLUORESCENCE ACTIVATED CELL SORTING; GENE OVEREXPRESSION; GENETIC TRANSFECTION; GRAFT REJECTION; GROWTH INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING;

ADENOVIRIDAE; ANIMALS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; COCULTURE TECHNIQUES; DENDRITIC CELLS; DNA, COMPLEMENTARY; FEMALE; GENE THERAPY; IMMUNOHISTOCHEMISTRY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KYNURENINE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED A; MICE, INBRED C57BL; PREGNANCY; SPLEEN; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; TRYPTOPHAN OXYGENASE;

ADENOVIRIDAE;

EID: 19744361967     PISSN: 1099498X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jgm.698     Document Type: Article

References (49)

1. Taylor MW, Feng GS. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J 1991; 5: 2516-2522.
2. Widner B, Weiss G, Fuchs D. Tryptophan degradation to control T-cell responsiveness. Immunol Today 2000; 21: 250.
3. Mellor AL, Munn DH. Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol Today 1999; 20: 469-473.
4. Munn DH, Zhou M, Attwood JT, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998; 281: 1191-1193.
5. Mellor AL, Sivakumar J, Chandler P, et al. Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat Immunol 2001; 2: 64-68.
6. Munn DH, Shafizadeh E, Attwood JT, et al. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med 1999; 189: 1363-1372.
7. Hwu P, Du MX, Lapointe R, et al. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J Immunol 2000; 164: 3596-3599.
8. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252.
9. Steinman RM. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 1991; 9: 271-296.
10. Bhardwaj N. Interactions of viruses with dendritic cells: a double-edged sword. J Exp Med 1997; 186: 795-799.
11. Johnson LL, Sayles PC. Interleukin-12, dendritic cells, and the initiation of host-protective mechanisms against Toxoplasma gondii. J Exp Med 1997; 186: 1799-1802.
12. Chambers C A, Allison JP. Co-stimulation in T cell responses. Curr Opin Immunol 1997; 9: 396-404.
13. Fallarino F, Vacca C, Orabona C, et al. Functional expression of indoleamine 2,3-dioxygenase by murine CD8 alpha(+) dendritic cells. Int Immunol 2002; 14: 65-68.
14. Grohmann U, Fallarino F, Silla S, et al. CD40 ligation ablates the tolerogenic potential of lymphoid dendritic cells. J Immunol 2001; 166: 277-283.
15. Grohmann U, Fallarino F, Bianchi R, et al. IL-6 inhibits the tolerogenic function of CD8 alpha+ dendritic cells expressing indoleamine 2,3-dioxygenase. J Immunol 2001; 167: 708-714.
16. Xu S, Ariizumi K, Caceres-Dittmar G, et al. Successive generation of antigen-presenting, dendritic cell lines from murine epidermis. J Immunol 1995; 154: 2697-2705.
17. Xu S, Ariizumi K, Edelbaum D, et al. Cytokine-dependent regulation of growth and maturation in murine epidermal dendritic cell lines. Eur J Immunol 1995; 25: 1018-1024.
18. Xu S, Bergstresser PR, Takashima A. Phenotypic and functional heterogeneity among murine epidermal-derived dendritic cell clones. J Invest Dermatol 1995; 105: 831-836.
19. Takashima A, Edelbaum D, Kitajima T, et al. Colony-stimulating factor-1 secreted by fibroblasts promotes the growth of dendritic cell lines (XS series) derived from murine epidermis. J Immunol 1995; 154: 5128-5135.
20. Kitajima T, Caceres-Dittmar G, Tapia FJ, et al. T cell-mediated terminal maturation of dendritic cells: loss of adhesive and phagocytotic capacities. J Immunol 1996; 157: 2340-2347.
21. Kitajima T, Ariizumi K, Bergstresser PR, et al. T cell-dependent loss of proliferative responsiveness to colony-stimulating factor-1 by a murine epidermal-derived dendritic cell line, XS52. J Immunol 1995; 155: 5190-5197.
22. Timares L, Takashima A, Johnston SA. Quantitative analysis of the immunopotency of genetically transfected dendritic cells. Proc Natl Acad Sci U S A 1998; 95: 13 147-13 152.
23. Matsue H, Bergstresser PR, Takashima A. Keratinocyte-derived IL-7 serves as a growth factor for dendritic epidermal T cells in mice. J Immunol 1993; 151: 6012-6019.
24. Habara-Ohkubo A, Takikawa O, Yoshida R. Cloning and expression of a cDNA encoding mouse indoleamine 2,3-dioxygenase. Gene 1991; 105: 221-227.
25. Miyake S, Makimura M, Kanegae Y, et al. Efficient generation of recombinant adenoviruses using adenovirus DNA-terminal protein complex and a cosmid bearing the full-length virus genome. Proc Natl Acad Sci U S A 1996; 93: 1320-1324.
26. Fujino M, Li XK, Suda T, et al. In vitro prevention of cell-mediated xeno-graft rejection via the Fas/FasL-pathway in CrmA-transducted porcine kidney cells. Xenotransplantation 2001; 8: 115-124.
27. Cady SG, Sono M. 1-Methyl-DL-tryptophan, beta-(3-benzofuranyl)-DL-alanine (the oxygen analog of tryptophan), and beta-[3-benzo(b)thienyl]-DL-alanine (the sulfur analog of tryptophan) are competitive inhibitors for indoleamine 2,3-dioxygenase. Arch Biochem Biophys 1991; 291: 326-333.
28. Southan MD, Truscott RJ, Jamie JF, et al. Structural requirements of the competitive binding site of recombinant human indoleamine 2,3-dioxygenase. Med Chem Res 1996; 343-352.
29. Moffett JR, Espey MG, Namboodiri MA. Antibodies to quinolinic acid and the determination of its cellular distribution within the rat immune system. Cell Tissue Res 1994; 278: 461-469.
30. Grohmann U, Bianchi R, Belladonna ML, et al. IFN-gamma inhibits presentation of a tumor/self peptide by CD8 alpha-dendritic cells via potentiation of the CD8 alpha+ subset. J Immunol 2000; 165: 1357-1363.
31. Grohmann U, Orabona C, Fallarino F, et al. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol 2002; 3: 1097-1101.
32. Mellor AL, Keskin DB, Johnson T, et al. Cells expressing indoleamine 2,3-dioxygenase inhibit T cell responses. J Immunol 2002; 168: 3771-3776.
33. Mellor AL, Baban B, Chandler P, et al. Cutting edge: induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J Immunol 2003; 171: 1652-1655.
34. Fallarino F, Grohmann U, Hwang KW, et al. Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol 2003; 4: 1206-1212. Epub 2003 Oct 1226.
35. Grohmann U, Fallarino F, Bianchi R, et al. A defect in tryptophan catabolism impairs tolerance in nonobese diabetic mice. J Exp Med 2003; 198: 153-160. Epub 2003 Jun 2030.
36. Xiao BG, Wu XC, Yang JS, et al. Therapeutic potential of IFN-gamma-modified dendritic cells in acute and chronic experimental allergic encephalomyelitis. Int Immunol 2004; 16: 13-22.
37. Terness P, Bauer TM, Rose L, et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med 2002; 196: 447-457.
38. Frumento G, Rotondo R, Tonetti M, et al. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med 2002; 196: 459-468.
39. Fallarino F, Grohmann U, Vacca C, et al. T cell apoptosis by tryptophan catabolism. Cell Death Differ 2002; 9: 1069-1077.
40. Matsue H, Matsue K, Walters M, et al. Induction of antigen-specific immunosuppression by CD95L cDNA-transfected 'killer' dendritic cells. Nat Med 1999; 5: 930-937.
41. Matsue H, Matsue K, Kusuhara M, et al. Immunosuppressive properties of CD95L-transduced "killer" hybrids created by fusing donor- and recipient-derived dendritic cells. Blood 2001; 98: 3465-3472.
42. Wolfe T, Asseman C, Hughes A, et al. Reduction of antiviral CD8 lymphocytes in vivo with dendritic cells expressing Fas ligand increased survival of viral (lymphocytic choriomeningitis virus) central nervous system infection. J Immunol 2002; 169: 4867-4872.
43. Ozawa H, Ding W, Torii H, et al. Granulocyte-macrophage colony-stimulating factor gene transfer to dendritic cells or epidermal cells augments their antigen-presenting function including induction of anti-tumor immunity. J Invest Dermatol 1999; 113: 999-1005.
44. Min WP, Gorczynski R, Huang XY, et al. Dendritic cells genetically engineered to express Fas ligand induce donor-specific hyporesponsiveness and prolong allograft survival. J Immunol 2000; 164: 161-167.
45. Uyttenhove C, Pilotte L, Theate I, et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med 2003; 9: 1269-1274. Epub 2003 Sep 1221.
46. Kudo Y, Boyd CA. Human placental indoleamine 2,3-dioxygenase: cellular localization and characterization of an enzyme preventing fetal rejection. Biochim Biophys Acta 2000; 1500: 119-124.
47. Kudo Y, Boyd CA. Characterisation of L-tryptophan transporters in human placenta: a comparison of brush border and basal membrane vesicles. J Physiol 2001; 531: 405-416.
48. Praetorius-Ibba M, Stange-Thomann N, Kitabatake M, et al. Ancient adaptation of the active site of tryptophanyl-tRNA synthetase for tryptophan binding. Biochemistry 2000; 39: 13 136-13 143.
49. Jorgensen R, Sogaard TM, Rossing AB, et al. Identification and characterization of human mitochondrial tryptophanyl-tRNA synthetase. J Biol Chem 2000; 275: 16 820-16 826.