A defect in tryptophan catabolism impairs tolerance in nonobese diabetic mice

Journal of Experimental Medicine

Volumn 198, Issue 1, 2003, Pages 153-160

  Grohmann, Ursula ^a   Fallarino, Francesca ^a   Bianchi, Roberta ^a   Orabona, Ciriana ^a   Vacca, Carmine ^a   Fioretti, Maria C ^a   Puccetti, Paolo ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Autoimmunity; Dendritic cells; Indoleamine 2,3 dioxygenase; NOD mice; Tolerance

Indexed keywords

GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; STAT1 PROTEIN; TRYPTOPHAN;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; DIABETES MELLITUS; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; MALE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; DENDRITIC CELLS; DNA-BINDING PROTEINS; FEMALE; GUANIDINES; IMMUNE TOLERANCE; INTERFERON TYPE II; INTERLEUKIN-12; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, INBRED NOD; NITRIC OXIDE; STAT1 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; TRYPTOPHAN; TRYPTOPHAN OXYGENASE;

EID: 0037815119     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20030633     Document Type: Article

References (45)

1. Delovitch, T.L., and B. Singh. 1997. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity. 7:727-738.
2. Atkinson, M.A., and E.H. Leiter. 1999. The NOD mouse model of type 1 diabetes: as good as it gets? Nat. Med. 5:601-604.
3. Kishimoto, H., and J. Sprent. 2001. A defect in central tolerance in NOD mice. Nat. Immunol. 2:1025-1031.
4. Serreze, D.V., H.R. Gaskins, and E.H. Leiter. 1993. Defects in the differentiation and function of antigen presenting cells in NOD/Lt mice. J. Immunol. 150:2534-2543.
5. Liu, J., and D. Beller. 2002. Aberrant production of IL-12 by macrophages from several autoimmune-prone mouse strains is characterized by intrinsic and unique patterns of NF-κB expression and binding to the IL-12 p40 promoter. J. Immunol. 169:581-586.
6. Suarez-Pinzon, W.L., J.G. Mabley, K. Strynadka, R.F. Power, C. Szabo, and A. Rabinovitch. 2001. An inhibitor of inducible nitric oxide synthase and scavenger of peroxynitrite prevents diabetes development in NOD mice. J. Autoimmun. 16:449-455.
7. Christen, U., T. Wolfe, U. Mohrle, A.C. Hughes, E. Rodrigo, E.A. Green, R.A. Flavell, and M.G. von Herrath. 2001. A dual role for TNF-α in type 1 diabetes: islet-specific expression abrogates the ongoing autoimmune process when induced late but not early during pathogenesis. J. Immunol. 166:7023-7032.
8. Sobel, D.O., J. Han, J. Williams, J.W. Yoon, H.S. Jun, and B. Ahvazi. 2002. Gamma interferon paradoxically inhibits the development of diabetes in the NOD mouse. J. Autoimmun. 19:129-137.
9. Shinomiya, M., S.M. Fazle Akbar, H. Shinomiya, and M. Onji. 1999. Transfer of dendritic cells (DC) ex vivo stimulated with interferon-gamma (IFN-γ) down-modulates autoimmune diabetes in non-obese diabetic (NOD) mice. Clin. Exp. Immunol. 117:38-43.
10. Grohmann, U., C. Orabona, F. Fallarino, C. Vacca, F. Calcinaro, A. Falorni, P. Candeloro, M.L. Belladonna, R. Bianchi, M.C. Fioretti, and P. Puccetti. 2002. CTLA-4-Ig regulates trytophan catabolism in vivo. Nat. Immunol. 3: 1097-1101.
11. Finger, E.B., and J.A. Bluestone. 2002. When ligand becomes receptor-tolerance via B7 signaling on DCs. Nat. Immunol. 3:1056-1057.
12. Grohmann, U., F. Fallarino, and P. Puccetti. 2003. Tolerance, DCs and tryptophan: much ado about IDO. Trends Immunol. 24:242-248.
13. + dendritic cells expressing indoleamine 2,3-dioxygenase. J. Immunol. 167:708-714.
14. + T cell response against one peptide/MHC complex in autoimmune diabetes. Proc. Natl. Acad. Sci. USA. 96:9311-9316.
15. Amrani, A., J. Verdaguer, P. Serra, S. Tafuro, R. Tan, and P. Santamaria. 2000. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature. 406:739-742.
16. + subset. J. Immunol. 165: 1357-1363.
17. 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. 166:277-283.
18. + dendritic cells. Int. Immunol. 14:65-68.
19. McDaniel, M.L., G. Kwon, J.R. Hill, C.A. Marshall, and J.A. Corbett. 1996. Cytokines and nitric oxide in islet inflammation and diabetes. Proc. Soc. Exp. Biol. Med. 211: 24-32.
20. + T cells: involvement of a nitric oxide-dependent pathway. J. Immunol. 163:5770-5780.
21. Llovera, M., J.D. Pearson, C. Moreno, and V. Riveros-Moreno. 2001. Impaired response to interferon-γ in activated macrophages due to tyrosine nitration of STAT1 by endogenous nitric oxide. Br. J. Pharmacol. 132:419-426.
22. Matata, B.M., and M. Galinanes. 2002. Peroxynitrite is an essential component of cytokines production mechanism in human monocytes through modulation of nuclear factor-κB DNA binding activity. J. Biol. Chem. 277:2330-2335.
23. Serreze, D.V., H.D. Chapman, C.M. Post, E.A. Johnson, W.L. Suarez-Pinzon, and A. Rabinovitch. 2001. Th1 to Th2 cytokine shifts in nonobese diabetic mice: sometimes an outcome, rather than the cause, of diabetes resistance elicited by immunostimulation. J. Immunol. 166:1352-1359.
24. Kishimoto, K., S. Sandner, J. Imitola, M. Sho, Y. Li, P.B. Langmuir, D.M. Rothstein, T.B. Strom, L.A. Turka, and M.H. Sayegh. 2002. Th1 cytokines, programmed cell death, and alloreactive T cell clone size in transplant tolerance. J. Clin. Invest. 109:1471-1479.
25. 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. 281:1191-1193.
26. Mellor, A.L., D.B. Keskin, T. Johnson, P. Chandler, and D.H. Munn. 2002. Cells expressing indoleamine 2,3-dioxygenase inhibit T cell responses. J. Immunol. 168:3771-3776.
27. Fallarino, F., U. Grohmann, C. Vacca, R. Bianchi, C. Orabona, A. Spreca, M.C. Fioretti, and P. Puccetti. 2002. T cell apoptosis by tryptophan catabolism. Cell Death Differ, 9:1069-1077.
28. Rosmalen, J.G., W. van Ewijk, and P.J. Leenen. 2002. T-cell education in autoimmune diabetes: teachers and students. Trends Immunol. 23:40-46.
29. Marrack, P., J. Kappler, and B.L. Kotzin. 2001. Autoimmune disease: why and where it occurs. Nat. Med. 7:899-905.
30. Poligone, B., D.J. Weaver, Jr., P. Sen, A.S. Baldwin, Jr., and R. Tisch. 2002. Elevated NF-κB activation in nonobese diabetic mouse dendritic cells results in enhanced APC function. J. Immunol. 168:188-196.
31. Hayashi, T., and D. Faustman. 1999. NOD mice are defective in proteasome production and activation of NF-κB. Mol. Cell. Biol. 19:8646-8659.
32. Deb, A., S.J. Haque, T. Mogensen, R.H. Silverman, and B.R. Williams. 2001. RNA-dependent protein kinase PKR is required for activation of NF-κB by IFN-γ in a STAT1-independent pathway. J. Immunol. 166:6170-6180.
33. Grohmann, U., M.L. Belladonna, R. Bianchi, C. Orabona, E. Ayroldi, M.C. Fioretti, and P. Puccetti. 1998. IL-12 acts directly on DC to promote nuclear localization of NF-κB and primes DC for IL-12 production. Immunity. 9:315-323.
34. Alderton, W.K., C.E. Cooper, and R.G. Knowles. 2001. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357:593-615.
35. Thomas, H.E., R. Darwiche, J.A. Corbett, and T.W. Kay. 2002. Interleukin-1 plus γ-interferon-induced pancreatic β-cell dysfunction is mediated by β-cell nitric oxide production. Diabetes. 51:311-316.
36. Beckman, J.S., T.W. Beckman, J. Chen, P.A. Marshall, and B.A. Freeman. 1990. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA. 87: 1620-1624.
37. Pryor, W.A., and G.L. Squadrito. 1995. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am. J. Physiol. 268:L699-722.
38. Suarez-Pinzon, W.L., C. Szabo, and A. Rabinovitch. 1997. Development of autoimmune diabetes in NOD mice is associated with the formation of peroxynitrite in pancreatic islet β-cells. Diabetes. 46:907-911.
39. Delaney, C.A., B. Tyrberg, L. Bouwens, H. Vaghef, B. Hellman, and D.L. Eizirik. 1996. Sensitivity of human pancreatic islets to peroxynitrite-induced cell dysfunction and death. FEBS Lett. 394:300-306.
40. Szabo, C., J.G. Mabley, S.M. Moeller, R. Shimanovich, P. Pacher, L. Virag, F.G. Soriano, J.H. Van Duzer, W. Williams, A.L. Salzman, and J.T. Groves. 2002. Part I: Pathogenetic role of peroxynitrite in the development of diabetes and diabetic vascular complications: studies with FP15, a novel potent peroxynitrite decomposition catalyst. Mol. Med. 8:571-580.
41. Murata, Y., M. Amao, and J. Hamuro. 2003. Sequential conversion of the redox status of macrophages dictates the pathological progression of autoimmune diabetes. Eur. J. Immunol. 33:1001-1011.
42. Papaccio, G., S. Frascatore, F.A. Pisanti, M.V. Latronico, and T. Linn. 1995. Superoxide dismutase in the nonobese diabetic (NOD) mouse: a dynamic time-course study. Life Sci. 56:2223-2228.
43. Boonstra, A., C. Asselin-Paturel, M. Gilliet, C. Crain, G. Trinchieri, Y.J. Liu, and A. O'Garra. 2003. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J. Exp. Med. 197:101-109.
44. Shortman, K., and W.R. Heath. 2001. Immunity or tolerance? That is the question for dendritic cells. Nat. Immunol. 2:988-989.
45. 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. 99:351-358.