Antioxidants inhibit indoleamine 2,3-dioxygenase in IFN-γ-activated human macrophages: Posttranslational regulation by pyrrolidine dithiocarbamate

Journal of Immunology

Volumn 166, Issue 10, 2001, Pages 6332-6340

  Thomas, Shane R ^a,c   Salahifar, Houta ^a   Mashima, Ryuichi ^a   Hunt, Nicholas H ^b   Richardson, Des R ^a   Stocker, Roland ^a  

^a HEART RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CARBON 14; EBSELEN; GAMMA INTERFERON; GLUTATHIONE DISULFIDE; HEME; HEMIN; INDOLEAMINE 2,3 DIOXYGENASE; MESSENGER RNA; PORPHOBILINOGEN SYNTHASE; PYRIDOXAL ISONICOTINOYLHYDRAZONE; PYRROLIDINE DITHIOCARBAMATE; SUCCINYLACETONE; TERT BUTYLHYDROQUINONE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEME SYNTHESIS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MACROPHAGE ACTIVATION; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING;

EID: 0035873436     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.166.10.6332     Document Type: Article

References (55)

1. Nathan, C. F., and R. Yoshida. 1988. Cytokines: Interferon-γ. In Inflammation: Basic Principles and Clinical Correlates, J. I. Gallin, I. M. Goldstein, and R. Snyderman, eds. Raven Press, New York, p.229.
2. Nathan, C. F., and J. B. Hibbs, Jr. 1991. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:65.
3. Taylor, M. W., and G. S. Feng. 1991. Relationship between interferon-γ, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 5:2516.
4. 2 into the reaction products. J. Biol. Chem. 252:3548.
5. Thomas, S. R., D. Mohr, and R. Stocker. 1994. Nitric oxide inhibits indoleamine 2,3-dioxygenase activity in interferon-γ-primed mononuclear phagocytes. J. Biol. Chem. 269:14457.
6. Alberati-Giani, D., P. Malherbe, P. Ricciardi-Castagnoli, C. Kohler, S. Denis-Donini, and A. M. Cesura. 1997. Differential regulation of indoleamine 2,3-dioxygenase expression by nitric oxide and inflammatory mediators in IFN-γ-activated murine macrophages and microglial cells. J. Immunol. 159:419.
7. Padgett, E. L., and S. B. Pruett. 1992. Evaluation of nitrite production by human monocyte-derived macrophages. Biochem. Biophys. Res. Commun. 186:775.
8. Werner-Felmayer, G., E. R. Werner, D. Fuchs, A. Hausen, G. Reibnegger, and H. Wachter. 1989. Characteristics of interferon induced tryptophan metabolism in human cells in vitro. Biochim. Biophys. Acta 1012:140.
9. Carlin, J. M., Y. Ozaki, G. I. Byrne, R. R. Brown, and E. C. Borden. 1989. Interferons and indoleamine 2,3-dioxygenase: role in antimicrobial and antitumor effects. Experientia 45:535.
10. 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.
11. Munn, D. H., E. Shafizadeh, J. T. Attwood, I. Bondarev, A. Pashine, and A. L. Mellor. 1999. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med. 189:1363.
12. Schwarcz, R., W. O. Whetsell, Jr., and R. M. Mangano. 1983. Quinolinic acid: an endogenous metabolite that produces axon-sparing lesions in rat brain. Science 219:316.
13. 2-microglobulin in cerebrospinal fluid and serum of HIV-1infected patients. J. Neuroimmunol. 40:71.
14. Sanni, L. A., S. R. Thomas, B. N. Tattam, D. E. Moore, G. Chaudhri, R. Stocker, and N. H. Hunt. 1998. Dramatic changes in oxidative tryptophan metabolism along the kynurenine pathway in experimental cerebral and noncerebral malaria. Am. J. Pathol. 152:611.
15. Heyes, M. P., K. Saito, A. Lackner, C. A. Wiley, C. L. Achim, and S. P. Markey. 1998. Sources of the neurotoxin quinolinic acid in the brain of HIV-1-infected patients and retrovirus-infected macaques. FASEB J. 12:881.
16. Christen, S., E. Peterhans, and R. Stocker. 1990. Antioxidant activities of some tryptophan metabolites: possible implication for inflammatory diseases. Proc. Natl. Acad. Sci. USA 87:2506.
17. Christen, S., S. R. Thomas, B. Garner, and R. Stocker. 1994. Inhibition by interferon-γ of human mononuclear cell-mediated low density lipoprotein oxidation: participation of tryptophan metabolism along the kynurenine pathway. J. Clin. Invest. 93:2149.
18. Thomas, S. R., and R. Stocker. 1999. Redox reactions related to indoleamine 2,3-dioxygenase and tryptophan metabolism along the kynurenine pathway. Redox Rep. 4:199.
19. Schreck, R., K. Albermann, and P. A. Baeuerle. 1992. Nuclear factor κB: an oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radic. Res. Commun. 17:221.
20. Allen, R. G., and M. Tresini. 2000. Oxidative stress and gene regulation. Free Radic. Biol. Med. 28:463.
21. Lander, H. M. 1997. An essential role for free radicals and derived species in signal transduction. FASEB J. 11:118.
22. 2 and antioxidants have opposite effects on activation of NF-κB and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J. 12:2005.
23. Schenk, H., M. Klein, W. Erdbrugger, W. Droge, and K. Schulze-Osthoff. 1994. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-κB and AP-1. Proc. Natl. Acad. Sci. USA 91:1672.
24. Wu, H. H., and J. Momand. 1998. Pyrrolidine dithiocarbamate prevents p53 activation and promotes p53 cysteine residue oxidation. J. Biol. Chem. 273:18898.
25. Xie, Q. W., Y. Kashiwabara, and C. Nathan. 1994. Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269:4705.
26. Weber, C., W. Erl, A. Pietsch, M. Strobel, H. W. Ziegler-Heitbrock, and P. C. Weber. 1994. Antioxidants inhibit monocyte adhesion by suppressing nuclear factor-κB mobilization and induction of vascular cell adhesion molecule-1 in endothelial cells stimulated to generate radicals. Arterioscler. Thromb. 14: 1665.
27. Sunderman, F. W., Sr. 1991. Therapeutic properties of sodium diethyldithiocarbamate: its role as an inhibitor in the progression of AIDS. Ann. Clin. Lab. Sci. 21:70.
28. Lang, J. M., J. L. Touraine, C. Trepo, P. Choutet, M. Kirstetter, A. Falkenrodt, L. Herviou, J. M. Livrozet, G. Retomaz, F. Touraine, et al. 1988. Randomised, double-blind, placebo-controlled trial of dithiocarb sodium ('Imuthiol') in human immunodeficiency virus infection. Lancet 2:702.
29. Liu, S. F., X. Ye, and A. B. Malik. 1999. Inhibition of NF-κB activation by pyrrolidine dithiocarbamate prevents in vivo expression of proinflammatory genes. Circulation 100:1330.
30. Richardson, D. R., and E. Baker. 1992. Intermediate steps in cellular iron uptake from transferrin: detection of a cytoplasmic pool of iron, free of transferrin. J. Biol. Chem. 267:21384.
31. Ponka, P., J. Borova, J. Neuwirt, and O. Fuchs. 1979. Mobilization of iron from reticulocytes: identification of pyridoxal isonicotinoyl hydrazone as a new iron chelating agent. FEBS Lett. 97:317.
32. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156.
33. Musso, T., G. L. Gusella, A. Brooks, D. L. Longo, and L. Varesio. 1994. Interleukin-4 inhibits indoleamine 2,3-dioxygenase expression in human monocytes. Blood 83:1408.
34. Sono, M. 1989. The roles of superoxide anion and methylene blue in the reductive activation of indoleamine 2,3-dioxygenase by ascorbic acid or by xanthine oxidase-hypoxanthine. J. Biol. Chem. 264:1616.
35. Jones, D. P., J. L. Carlson, P. S. Samiec, P. Sternberg, Jr., V. C. Mody, Jr., R. L. Reed, and L. A. Brown. 1998. Glutathione measurement in human plasma: evaluation of sample collection, storage and derivatization conditions for analysis of dansyl derivatives by HPLC. Clin. Chim. Acta 275:175.
36. Heyes, M. P., K. Saito, and S. P. Markey. 1992. Human macrophages convert L-tryptophan into the neurotoxin quinolinic acid. Biochem. J. 283:633.
37. Liu, J., M. K. Shigenaga, L. J. Yan, A. Mori, and B. N. Ames. 1996. Antioxidant activity of diethyldithiocarbamate. Free Radical Res. 24:461.
38. Moellering, D., J. McAndrew, H. Jo, and V. M. Darley-Usmar. 1999. Effects of pyrrolidine dithiocarbamate on endothelial cells: protection against oxidative stress. Free Radical Biol. Med. 26:1138.
39. Pinkus, R., L. M. Weiner, and V. Daniel. 1996. Role of oxidants and antioxidants in the induction of AP-1, NF-κB, and glutathione S-transferase gene expression. J. Biol. Chem. 271:13422.
40. Nobel, C. S., D. H. Burgess, B. Zhivotovsky, M. J. Burkitt, S. Orrenius, and A. F. G. Slater. 1997. Mechanism of dithiocarbamate inhibition of apoptosis: thiol oxidation by dithiocarbamate disulfides directly inhibits processing of the caspase-3 proenzyme. Chem. Res. Toxicol. 10:636.
41. Kirlin, W. G., J. Cai, S. A. Thompson, D. Diaz, T. J. Kavanagh, and D. P. Jones. 1999. Glutathione redox potential in response to differentiation and enzyme inducers. Free Radic. Biol. Med. 27:1208.
42. Nobel, C. S. I., M. Kimland, B. Lind, S. Orrenius, and A. F. G. Slater. 1995. Dithiocarbamates induce apoptosis in thymocytes by raising the intracellular level of redox-active copper. J. Biol. Chem. 270:26202.
43. Taetle, R., and J. M. Honeysett. 1988. γ-interferon modulates human monocyte/ macrophage transferrin receptor expression. Blood 71:1590.
44. McMillan, K., D. S. Bredt, D. J. Hirsch, S. H. Snyder, J. E. Clark, and B. S. Siler Master. 1992. Cloned, expressed rat cerebellar nitric oxide synthase contains stoichiometric amounts of heme, which binds carbon monoxide. Proc. Natl. Acad. Sci. USA 89:11141.
45. Sen, C. K., and L. Packer. 1996. Antioxidant and redox regulation of gene transcription. FASEB J. 10:709.
46. Tetsuka, T., L. D. Baier, and A. R. Morrison. 1996. Antioxidants inhibit interleukin-1-induced cyclooxygenase and nitric-oxide synthase expression in rat mesangial cells: evidence for post-transcriptional regulation. J. Biol. Chem. 271: 11689.
47. 2 generated at the apical surface of thyroid cells in autocatalytic covalent heme binding. J. Biol. Chem. 274:10533.
48. Albakri, Q. A., and D. J. Stuehr. 1996. Intracellular assembly of inducible NO synthase is limited by nitric oxide-mediated changes in heme insertion and availability. J. Biol. Chem. 271:5414.
49. Pinnix, I. B., G. S. Guzman, H. L. Bonkovsky, S. R. Zaki, and J. M. Kinkade, Jr. 1994. The post-translational processing of myeloperoxidase is regulated by the availability of heme. Arch. Biochem. Biophys. 312:447.
50. Weiss, G., D. Fuchs, A. Hausen, G. Reibnegger, E. R. Werner, G. Werner-Felmayer, and H. Wachter. 1992. Iron modulates interferon-γ effects in the human myelomonocytic cell line THP-1. Exp. Hematol. 20:605.
51. Weiss, G., J. D. Lutton, D. Fuchs, G. Werner-Felmayer, G. Bock, N. G. Abraham, A. Kappas, R. D. Levere, and H. Wachter. 1993. Comparative effects of heme and metalloporphyrins on interferon-γ-mcdiated pathways in monocytic cells (THP-1). Proc. Soc. Exp. Biol. Med. 202:470.
52. Weiss, G., G. Werner-Felmayer, E. R. Werner, K. Grunewald, H. Wachter, and M. W. Hentze. 1994. Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J. Exp. Med. 180:969.
53. Ponka, P., J. Borova, J. Neuwirt, O. Fuchs, and E. Necas. 1979. A study of intracellular iron metabolism using pyridoxal isonicotinoyl hydrazone and other synthetic chelating agents. Biochim. Biophys. Acta 586:278.
54. Hentze, M. W., and L. C. Kuhn. 1996. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA 93:8175.
55. Aune, T. M., and S. L. Pogue. 1989. Inhibition of tumor cell growth by interferon-γ is mediated by two distinct mechanisms dependent upon oxygen tension: induction of tryptophan degradation and depletion of intracellular nicotinamide adenine dinucleotide. J. Clin. Invest. 84:863.