Murine plasmacytoid dendritic cells initiate the immunosuppressive pathway of tryptophan catabolism in response to CD200 receptor engagement

Journal of Immunology

Volumn 173, Issue 6, 2004, Pages 3748-3754

  Fallarino, Francesca ^a   Asselin Paturel, Carine ^b   Vacca, Carmine ^a   Bianchi, Roberta ^a   Gizzi, Stefania ^a   Fioretti, Maria Cristina ^a   Trinchieri, Giorgio ^b   Grohmann, Ursula ^a   Puccetti, Paolo ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CD200 ANTIGEN; CELL SURFACE PROTEIN; GLYCOPROTEIN P 15095; INTERFERON RECEPTOR; TRYPTOPHAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; DENDRITIC CELL; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRYPTOPHAN METABOLISM;

EID: 4644220112     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.6.3748     Document Type: Article

References (50)

1. Steinman, R. M., and M. C. Nussenzweig. 2002. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99:351.
2. Gorczynski, R. M., S. Hadidi, G. Yu, and D. A. Clark. 2002. The same immunoregulatory molecules contribute to successful pregnancy and transplantation. Am. J. Reprod. Immunol. 48:18.
3. Grohmann, U., F. Fallarino, and P. Puccetti. 2003. Tolerance, DCs and tryptophan: much ado about IDO. Trends Immunol. 24:242.
4. Munn, D. H., M. Zhou, J. T. Attwood, I. Bondarev, S. J. Conway, B. Marshall, C. Brown, and A. L. Mellor. 1998. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281:1191.
5. Miki, T., H. Sun, Y. Lee, A. Tandin, A. M. Kovscek, V. Subbotin, J. J. Fung, and L. A. Valdivia. 2001. Blockade of tryptophan catabolism prevents spontaneous tolerogenicity of liver allografts. Transplant. Proc. 33:129.
6. Grohmann, U., C. Orabona, F. Fallarino, C. Vacca, F. Calcinaro, A. Falomi, P. Candeloro, M. L. Belladonna, R. Bianchi, M. C. Fioretti, and P. Puccetti. 2002. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 3:1097.
7. Mellor, A. L., B. Baban, P. Chandler, B. Marshall, K. Jhaver, A. Hansen, P. A. Koni, M. Iwashima, and D. H. Munn. 2003. Cutting edge: induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J. Immunol. 171:1652.
8. Sakurai, K., J. P. Zou, J. R. Tschetter, J. M. Ward, and G. M. Shearer. 2002. Effect of indoleamine 2,3-dioxygenase on induction of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 129:186.
9. Grohmann, U., F. Fallarino, R. Bianchi, C. Orabona, C. Vacca, M. C. Fioretti, and P. Puccetti. 2003. A defect in tryptophan catabolism impairs tolerance in nonobese diabetic mice. J. Exp. Med. 198:153.
10. Xiao, B. G., X. C. Wu, J. S. Yang, L. Y. Xu, X. Liu, Y. M. Huang, B. Bjelke, and H. Link. 2004. Therapeutic potential of IFN-γ-modified dendritic cells in acute and chronic experimental allergic encephalomyelitis. Int. Immunol. 16:13.
11. + dendritic cells. Int. Immunol. 14:65.
12. Munn, D. H., M. D. Sharma, J. R. Lee, K. G. Jhaver, T. S. Johnson, D. B. Keskin, B. Marshall, P. Chandler, S. J. Antonia, R. Burgess, et al. 2002. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297:1867.
13. Mellor, A. L., and D. H. Munn. 2003. Tryptophan catabolism and regulation of adaptive immunity. J. Immunol. 170:5809.
14. Grohmann, U., and P. Puccetti. 2003. CTLA-4, T helper lymphocytes and dendritic cells: an internal perspective of T-cell homeostasis. Trends Mol. Med. 9:133.
15. Grohmann, U., R. Bianchi, C. Orabona, F. Fallarino, C. Vacca, A. Micheletti, M. C. Fioretti, and P. Puccetti. 2003. Functional plasticity of dendritic cell subsets as mediated by CD40 versus B7 activation. J. Immunol. 171:2581.
16. Fallarino, F., U. Grohmann, K. W. Hwang, C. Orabona, C. Vacca, R. Bianchi, M. L. Belladonna, M. C. Fioretti, M. L. Alegre, and P. Puccetti. 2003. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol. 4:1206.
17. Von Bubnoff, D., H. Matz, C. Frahnert, M. L. Rao, D. Hanau, H. de la Salle, and T. Bieber. 2002. FcεRI induces the tryptophan degradation pathway involved in regulating T cell responses. J. Immunol. 169:1810.
18. Wright, G. J., M. J. Puklavec, A. C. Willis, R. M. Hoek, J. D. Sedgwick, M. H. Brown, and A. N. Barclay. 2000. Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity 13:233.
19. Wright, G. J., H. Cherwinski, M. Foster-Cuevas, G. Brooke, M. J. Puklavec, M. Bigler, Y. Song, M. Jenmalm, D. Gorman, T. McClanahan, et al. 2003. Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J. Immunol. 171:3034.
20. Hoek, R. M., S. R. Ruuls, C. A. Murphy, G. J. Wright, R. Goddard, S. M. Zurawski, B. Blom, M. E. Homola, W. J. Streit, M. H. Brown, et al. 2000. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 290:1768.
21. Rosenblum, M. D., E. Olasz, J. E. Woodliff, B. D. Johnson, M. C. Konkol, K. A. Gerber, R. J. Orentas, G. Sandford, and R. L. Truitt. 2003. CD200 is a novel p53-target gene involved in apoptosis-associated immune tolerance. Blood 103:2691.
22. Nathan, C., and W. A. Muller. 2001. Putting the brakes on innate immunity: a regulatory role for CD200? Nat. Immunol. 2:17.
23. Barclay, A. N., G. J. Wright, G. Brooke, and M. H. Brown. 2002. CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol. 23:285.
24. Gorczynski, R. M., Z. Chen, K. Yu, and J. Hu. 2001. CD200 immunoadhesin suppresses collagen-induced arthritis in mice. Clin. Immunol. 101:328.
25. Gorczynski, R. M., M. S. Cattral, Z. Chen, J. Hu, J. Lei, W. P. Min, G. Yu, and J. Ni. 1999. An immunoadhesin incorporating the molecule OX-2 is a potent immunosuppressant that prolongs allo- and xenograft survival. J. Immunol. 163:1654.
26. Kaufman, K. A., J. A. Bowen, A. F. Tsai, J. A. Bluestone, J. S. Hunt, and C. Ober. 1999. The CTLA-4 gene is expressed in placental fibroblasts. Mol. Hum. Reprod. 5:84.
27. Petroff, M. G., L. Chen, T. A. Phillips, D. Azzola, P. Sedlmayr, and J. S. Hunt. 2003. B7 family molecules are favorably positioned at the human maternal-fetal interface. Biol. Reprod. 68:1496.
28. Clark, D. A., A. Keil, Z. Chen, U. Markert, J. Manuel, and R. M. Gorczynski. 2003. Placental trophoblast from successful human pregnancies expresses the tolerance signaling molecule, CD200 (OX-2). Am. J. Reprod. Immunol. 50:187.
29. Grouard, G., M. C. Rissoan, L. Filgueira, I. Durand, J. Banchereau, and Y. J. Liu. 1997. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J. Exp. Med. 185:1101.
30. Asselin-Paturel, C., A. Boonstra, M. Dalod, I. Durand, N. Yessaad, C. Dezutter-Dambuyant, A. Vicari, A. O'Garra, C. Biron, F. Briere, and G. Trinchieri. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2:1144.
31. Del Hoyo, G. M., P. Martin, H. H. Vargas, S. Ruiz, C. F. Arias, and C. Ardavin, 2002. Characterization of a common precursor population for dendritic cells. Nature 415:1043.
32. + cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J. Exp. Med. 194:1171.
33. Shortman, K., and Y. J. Liu. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2:151.
34. Asselin-Paturel, C., G. Brizard, J. J. Pin, F. Briere, and G. Trinchieri. 2003. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal Ab. J. Immunol. 171:6466.
35. Belladonna, M. L., J. C. Renauld, R. Bianchi, C. Vacca, F. Fallarino, C. Orabona. M. C. Fioretti, U. Grohmann, and P. Puccetti, 2002. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J. Immunol. 168:5448.
36. Grohmann, U., F. Fallarino, S. Silla, R. Bianchi, M. L. Belladonna, C. Vacca, A. Micheletti, M. C. Fioretti, and P. Puccetti. 2001. CD40 ligation ablates the tolerogenic potential of lymphoid dendritic cells. J. Immunol. 166:277.
37. Dalod, M., T. P. Salazar-Mather, L. Malmgaard, C. Lewis, C. Asselin-Paturel, F. Briere, G. Trinchieri, and C. A. Biron. 2002. Interferon α/β and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J. Exp. Med. 195:517.
38. Barchet, W., M. Cella, B. Odermatt, C. Asselin-Paturel, M. Colonna, and U. Kalinke. 2002. Virus-induced interferon-α production by a dendritic cell subset in the absence of feedback signaling in vivo. J. Exp. Med. 195:507.
39. + dendritic cells to produce type I IFN. J. Immunol. 166:2291.
40. + dendritic cells expressing indoleamine 2,3-dioxygenase. J. Immunol. 167:708.
41. Mellor, A. L., and D. H. Munn. 1999. Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol. Today 20:469.
42. Taylor, M. W., and G. S. Feng. 1991. Relationship between interferon-γ, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 5:2516.
43. Aluvihare, V. R., M. Kallikourdis, and A. G. Betz. 2004. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5:266.
44. Gurtner, G. J., R. D. Newberry, S. R. Schloemann, K. G. McDonald, and W. F. Stenson. 2003. Inhibition of indoleamine 2,3-dioxygenase augments trinitrobenzene sulfonic acid colitis in mice. Gastroenterology 125:1762.
45. Bjorck, P. 2001. Isolation and characterization of plasmacytoid dendritic cells from Flt3 ligand and granulocyte-macrophage colony-stimulating factor-treated mice. Blood 98:3520.
46. Kerkmann, M., S. Rothenfusser, V. Hornung, A. Towarowski, M. Wagner, A. Sarris, T. Giese, S. Endres, and G. Hartmann. 2003. Activation with CpG-A and CpG-B oligonucleotides reveals two distinct regulatory pathways of type I IFN synthesis in human plasmacytoid dendritic cells. J. Immunol. 170:4465.
47. Megjugorac, N. J., H. A. Young, S. B. Amrute, S. L. Olshalsky, and P. Fitzgerald-Bocarsly. 2004. Virally stimulated plasmacytoid dendritic cells produce chemokines and induce migration of T and NK cells. J. Leukocyte Biol. 75:504.
48. + subset. J. Immunol. 165:1357.
49. Colonna, M. 2004. Viral immunosuppression: disabling the guards. J. Clin. Invest. 113:660.
50. Adams, O., K. Besken, C. Oberdorfer, C. R. MacKenzie, O. Takikawa, and W. Daubener. 2004. Role of indoleamine-2,3-dioxygenase in α/β and γ interferon-mediated antiviral effects against herpes simplex virus infections. J. Virol. 78:2632.