Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase

Nature Medicine

Volumn 9, Issue 10, 2003, Pages 1269-1274

  Uyttenhove, Catherine ^a   Pilotte, Luc ^a   Théate, Ivan ^a   Stroobant, Vincent ^a   Colau, Didier ^a   Parmentier, Nicolas ^a   Boon, Thierry ^a   Van den Eynde, Benoît J ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLTRYPTOPHAN; COMPLEMENTARY DNA; ENZYME INHIBITOR; INDOLEAMINE 2,3 DIOXYGENASE; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOLOGY; CELL GROWTH; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFICACY; DRUG MECHANISM; ENZYME INHIBITION; ENZYME MECHANISM; HUMAN; HUMAN CELL; IMMUNIZATION; IMMUNOGENICITY; LYMPHOCYTE PROLIFERATION; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TUMOR CELL; TUMOR GROWTH; TUMOR IMMUNITY; VACCINATION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; FEMALE; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MICE; NEOPLASM TRANSPLANTATION; NEOPLASMS; PLACENTA; PREGNANCY; RNA, MESSENGER; TRYPTOPHAN; TRYPTOPHAN OXYGENASE; TUMOR ESCAPE;

ANIMALIA;

EID: 0142137237     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm934     Document Type: Article

References (38)

1. Mellor, A.L. & Munn, D.H. Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol. Today 20, 469-473 (1999).
2. Munn, D.H, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281, 1191-1193 (1998).
3. Munn, D.H. et al. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med. 189, 1363-1372 (1999).
4. Hwu, P. et al. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J. Immunol. 164, 3596-3599 (2000).
5. Kudo, Y., Boyd, C.A., Sargent, I. L. & Redman, C.W. Tryptophan degradation by human placental indoleamine 2,3-dioxygenase regulates lymphocyte proliferation. J. Physiol. 535, 207-215 (2001).
6. Frumento, G., Rotondo, R., Tonetti, M. & Ferrara, G.B. T cell proliferation is blocked by indoleamine 2.3-dioxygenase. Transplant. Proc. 33, 428-430 (2001).
7. + dendritic cells. Int. Immunol. 14, 65-68 (2002).
8. Takikawa, O., Kuroiwa, T., Yamazaki, F. & Kido, R. Mechanism of interferon-gamma action. Characterization of indoleamine 2,3-dioxygenase in cultured human cells induced by interferon-gamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J. Biol. Chem. 263, 2041-2046 (1988).
9. Habara-Ohkubo, A., Takikawa, O. & Yoshida, R. Cloning and expression of a cDNA encoding mouse indoleamine 2,3- dioxygenase. Gene 105, 221-227 (1991).
10. Munn, D.H. et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297, 1867-1870 (2002).
11. Friberg, M. et al. Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection. Int. J. Cancer 101, 151-155 (2002).
12. Grohmann, U. et al. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nature Immunol. 3, 1097-1101 (2002).
13. Van den Eynde, B., Lethé, B., Van Pel, A., De Plaen, E. & Boon, T. The gene coding for a major tumor rejection antigen of tumor P815 is identical to the normal gene of syngeneic DBA/2 mice. J. Exp. Med. 173, 1373-1384 (1991).
14. Brändle, D. et al. The shared tumor-specific antigen encoded by mouse gene P1A is a target not only for cytolytic T lymphocytes but also for tumor rejection. Eur. J. Immunol. 28, 4010-4019 (1998).
15. Medema, J.P. et al. Blockade of the granzyme B/perforin pathway through overexpression of the serine protease inhibitor PI-9/SPI-6 constitutes a mechanism for immune escape by tumors. Proc. Natl. Acad. Sci. USA 98, 11515-11520 (2001).
16. Pawelec, G. et al. Escape mechanisms in tumor immunity: a year 2000 update. Crit. Rev. Oncog. 11, 97-133 (2000).
17. Marincola, F., Jaffee, E. M., Hicklin, D.J. & Ferrone, S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv. Immunol. 74, 181-273 (2000).
18. Cady, S.G. & Sono, M. 1-Methyl-DL-tryptophan, β -(3-benzofuranyl)-DL-alanine (the oxygen analog of tryptophan), and β-[3-benzo(b)thienyl]-DL-alanine (the sulfur analog of tryptophan) are competitive inhibitors for indoleamine 2,3-dioxygenase. Arch. Biochem. Biophys. 291, 326-333 (1991).
19. Kudo, Y. & Boyd, C.A. Human placental indoleamine 2,3-dioxygenase: cellular localization and characterization of an enzyme preventing fetal rejection. Biochim. Biophys. Acta 1500, 119-124 (2000).
20. Kudo, Y. & Boyd, C.A. Characterisation of L-tryptophan transporters in human placenta: a comparison of brush border and basal membrane vesicles. J. Physiol. 531, 405-416 (2001).
21. Prætorius-Ibba, M. et al. Ancient adaptation of the active site of tryptophanyl-tRNA synthetase for tryptophan binding. Biochemistry 39, 13136-13143 (2000).
22. Jorgensen, R., Sogaard, T.M.M., Rossing, A.B., Martensen, P.M. & Justesen, J. Identification and characterization of human mitochondrial tryptophanyl-tRNA synthetase. J. Biol. Chem. 275, 16820-16826 (2000)
23. Terness, P. 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. 196, 447-457 (2002).
24. Fallarino, F. et al. T cell apoptosis by tryptophan catabolism. Cell Death Differ. 9, 1069-1077 (2002).
25. Van den Eynde, B. & van der Bruggen, P. T cell-defined tumor antigens. Curr. Opin. Immunol. 9, 684-693 (1997).
26. Boon, T. & Van den Eynde, B. Tumor immunology-editorial overview. Curr. Opin. Immunol. 15, 129-130 (2003).
27. Nestle, F.O. et al. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat. Med. 4, 328-332 (1998).
28. Rosenberg, S.A. et al. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 4, 321-327 (1998).
29. Marchand, M. et al. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int. J. Cancer 80, 219-230 (1999).
30. Thurner, B. et al. Vaccination with MAGE-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J. Exp. Med. 190, 1669-1678 (1999).
31. + cancers. Proc. Natl. Acad. Sci. USA 97, 12198-12203 (2000).
32. Suzuki, S. et al. Expression of indoleamine 2,3-dioxygenase and tryptophan 2,3-dioxygenase in early concepti. Biochem. J. 355, 425-429 (2001).
33. Uno, T., Chen, P.W., Murray, T.G., Podack, E.R. & Ksander, B.R. Gene transfer of the CD80 costimulatory molecule into ocular melanoma cells using a novel episomal vector. Invest. Ophtalmol. Vis. Sci. 38, 2531-2539 (1997).
34. Wenkel, H., Chen, P.W., Ksander, B.R. & Streilein, J.W. Immune privilege is extended, then withdrawn, from allogeneic tumor cell grafts placed in the subretinal space. Invest. Opthalmol. Vis. Sci. 40, 3202-3208 (1999).
35. Lethé, B., Van den Eynde, B., Van Pel, A., Corradin, G. & Boon, T. Mouse tumor rejection antigens P815A and P815B: two epitopes carried by a single peptide. Eur. J. Immunol. 22, 2283-2288 (1992).
36. Van Pel, A., De Plaen, E. & Boon, T. Selection of a highly transfectable variant from mouse mastocytoma P815. Som. Cell Genet. 11, 467-475 (1985).
37. + T cells following immunization of mice with a tumor-specific peptide. J. Immunol. 169, 3053-3060 (2002).
38. Van den Eynde, B. et al. A new family of genes coding for an antigen recognized by autologous cytolytic T lymphocytes on a human melanoma. J. Exp. Med. 182, 689-698 (1995).