Decreased protein nitration in macrophages that overexpress indoleamine 2, 3-dioxygenase

Cellular and Molecular Biology Letters

Volumn 12, Issue 1, 2007, Pages 82-102

  Keskin, Derin B ^a,c   Marshall, Brendan ^a   Munn, David ^a   Mellor, Andrew L ^a   Gearhart, Debra A ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Indoleamine 2, 3 dioxygenase; Oxidative stress; Protein oxidation; RAW 264.7 macrophages; Superoxide anion

Indexed keywords

ARYLFORMAMIDASE; CARBONYL DERIVATIVE; HYDROGEN PEROXIDE; HYPOXANTHINE; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; MESSENGER RNA; NITRIC OXIDE; PURINE; SUPEROXIDE; TRYPTOPHAN; XANTHINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; CELL LYSATE; CELL PROTECTION; CELL STRESS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPRESSION VECTOR; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MACROPHAGE; MOUSE; NITRATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 34249003035     PISSN: 14258153     EISSN: 16891392     Source Type: Journal    
DOI: 10.2478/s11658-006-0048-9     Document Type: Article

References (92)

1. Hayaishi, O. Properties and function of indoleamine 2,3-dioxygenase. J. Biochem. 79 (1976) 13P-21P.
2. Shimizu, T., Nomiyama, S., Hirata, F. and Hayaishi, O. Indoleamine 2,3-dioxygenase. Purification and some properties. J. Biol. Chem. 253 (1978) 4700-4706.
3. Yoshida, R., Nukiwa, T., Watanabe, Y., Fujiwara, M., Hirata, F. and Hayaishi, O. Regulation of indoleamine 2,3-dioxygenase activity in the small intestine and the epididymis of mice. Arch. Biochem. Biophys. 203 (1980) 343-351.
4. Watanabe, Y., Yoshida, R., Sono, M. and Hayaishi, O. Immunohistochemical localization of indoleamine 2,3-dioxygenase in the argyrophilic cells of rabbit duodenum and thyroid gland. J. Histochem. Cytochem. 29 (1981) 623-632.
5. Yoshida, R., Imanishi, J., Oku, T., Kishida, T. and Hayaishi, O. Induction of pulmonary indoleamine 2,3-dioxygenase by interferon. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 129-132.
6. Pfefferkorn, E.R., Rebhun, S. and Eckel, M. Characterization of an indoleamine 2,3-dioxygenase induced by gamma-interferon in cultured human fibroblasts. J. Interferon Res. 6 (1986) 267-279.
7. Yoshida, R. and Hayaishi, O. Indoleamine 2,3-dioxygenase. Methods Enzymol. 142 (1987) 188-195.
8. Carlin, J.M., Borden, E.C., Sondel, P.M. and Byrne, G.I. Interferon-induced indoleamine 2,3-dioxygenase activity in human mononuclear phagocytes. J. Leukoc. Biol. 45 (1989) 29-34.
9. Saito, K., Markey, S.P. and Heyes, M.P. Chronic effects of gamma-interferon on quinolinic acid and indoleamine-2,3-dioxygenase in brain of C57BL6 mice. Brain Res. 546 (1991) 151-154.
10. Gupta, S.L., Carlin, J.M., Pyati, P., Dai, W., Pfefferkorn, E.R. and Murphy, M.J., Jr. Antiparasitic and antiproliferative effects of indoleamine 2,3-dioxygenase enzyme expression in human fibroblasts. Infect Immun. 62 (1994) 2277-2284.
11. Malina, H.Z. and Martin, X.D. Indoleamine 2,3-dioxygenase: antioxidant enzyme in the human eye. Graefes Arch. Klin. Exp. Ophthalmol. 234 (1996) 457-462.
12. Hansen, A.M., Driussi, C., Turner, V., Takikawa, O. and Hunt, N.H. Tissue distribution of indoleamine 2,3-dioxygenase in normal and malaria-infected tissue. Redox Rep. 5 (2000) 112-115.
13. Kudo, Y. and Boyd, C.A. Human placental indoleamine 2,3-dioxygenase: cellular localization and characterization of an enzyme preventing fetal rejection. Biochim. Biophys. Acta 1500 (2000) 119-124.
14. Daubener, W., Spors, B., Hucke, C., Adam, R., Stins, M., Kwang Sik, K. and Schroten, H. Restriction of Toxoplasma gondii growth in human brain microvascular endothelial cells by activation of indoleamine 2,3-dioxygenase. Infect. Immun. 69 (2001) 6527-6531.
15. Sedlmayr, P., Blaschitz, A., Wintersteiger, R., Semlitsch, M., Hammer, A., MacKenzie, C.R., Walcher, W., Reich, O., Takikawa, O. and Dohr, G. Localization of indoleamine 2,3-dioxygenase in human female reproductive organs and the placenta. Mol. Hum. Reprod. 8 (2002) 385-391.
16. de la Maza, L.M. and Peterson, E.M. Dependence of the in vitro antiproliferative activity of recombinant human gamma-interferon on the concentration of tryptophan in culture media. Cancer Res. 48 (1988) 346-350.
17. Schroten, H., Spors, B., Hucke, C., Stins, M., Kim, K.S., Adam, R. and Daubener, W. Potential role of human brain microvascular endothelial cells in the pathogenesis of brain abscess: inhibition of Staphylococcus aureus by activation of indoleamine 2,3-dioxygenase. Neuropediatrics 32 (2001) 206-210.
18. Hayashi, T., Rao, S.P., Takabayashi, K., Van Uden, J.H., Kornbluth, R.S., Baird, S.M., Taylor, M.W., Carson, D.A. Catanzaro, A. and Raz, E. Enhancement of innate immunity against Mycobacterium avium infection by immunostimulatory DNA is mediated by indoleamine 2,3-dioxygenase. Infect. Immun. 69 (2001) 6156-6164.
19. Rottenberg, M.E., Gigliotti Rothfuchs, A., Gigliotti, D., Ceausu, M., Une, C., Levitsky, V. and Wigzell, H. Regulation and role of IFN-gamma in the innate resistance to infection with Chlamydia pneumoniae. J. Immunol. 164 (2000) 4812-4818.
20. Ceravolo, I.P., Chaves, A.C., Bonjardim, C.A., Sibley, D., Romanha, A.J. and Gazzinelli, R.T. Replication of Toxoplasma gondii, but not Trypanosoma cruzi, is regulated in human fibroblasts activated with gamma interferon: requirement of a functional JAK/STAT pathway. Infect. Immun. 67 (1999) 2233-2240.
21. Jacoby, D.B. and Choi, A.M. Influenza virus induces expression of antioxidant genes in human epithelial cells. Free Radic. Biol. Med. 16 (1994) 821-824.
22. Heyes, M.P., Saito, K., Crowley, J.S., Davis, L.E., Demitrack, M.A., Der, M., Dilling, L.A., Elia, J., Kruesi, M.J., Lackner, A. and et al. Quinolinic acid and kynurenine pathway metabolism in inflammatory and non-inflammatory neurological disease. Brain 115 (1992) 1249-1273.
23. Mellor, A.L., Keskin, D.B., Johnson, T., Chandler, P. and Munn, D.H. Cells expressing indoleamine 2,3-dioxygenase inhibit T cell responses. J. Immunol. 168 (2002) 3771-3776.
24. Munn, D.H., Shafizadeh, E., Attwood, J.T., Bondarev, I., Pashine, A. and Mellor, A.L. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med. 189 (1999) 1363-1372.
25. Sun, Y. Indoleamine 2,3-dioxygenase-a new antioxidant enzyme. Mater Med. Pol. 21 (1989) 244-250.
26. Christen, S., Peterhans, E. and Stocker, R. Antioxidant activities of some tryptophan metabolites: possible implication for inflammatory diseases. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 2506-2510.
27. Thomas, S.R. and Stocker, R. Redox reactions related to indoleamine 2,3-dioxygenase and tryptophan metabolism along the kynurenine pathway. Redox Rep. 4 (1999) 199-220.
28. Hirata, F. and Hayaishi, O. Studies on indoleamine 2,3-dioxygenase. I. Superoxide anion as substrate. J. Biol. Chem. 250 (1975) 5960-5966.
29. Sono, M. 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 (1989) 1616-1622.
30. Kobayashi, K., Hayashi, K. and Sono, M. Effects of tryptophan and pH on the kinetics of superoxide radical binding to indoleamine 2,3-dioxygenase studied by pulse radiolysis. J. Biol. Chem. 264 (1989) 15280-15283.
31. Ozaki, Y., Nichol, C.A. and Duch, D.S. Utilization of dihydroflavin mononucleotide and superoxide anion for the decyclization of L-tryptophan by murine epididymal indoleamine 2,3-dioxygenase. Arch. Biochem. Biophys. 257 (1987) 207-216.
32. Taniguchi, T., Hirata, F. and Hayaishi, O. Intracellular utilization of superoxide anion by indoleamine 2,3-dioxygenase of rabbit enterocytes. J. Biol. Chem. 252 (1977) 2774-2776.
33. Halliwell, B. The biological effects of the superoxide radical and its products. Bull. Eur. Physiopathol. Respir. 17 (1981) 21-29.
34. Halliwell, B. Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Amer. J. Med. 91 (1991) 14S-22S.
35. Halliwell, B. Mechanisms involved in the generation of free radicals. Pathol. Biol. (Paris) 44 (1996) 6-13.
36. Halliwell, B. and Chirico, S. Lipid peroxidation: its mechanism, measurement, and significance. Am. J. Clin. Nutr. 57 (1993) 715S-724S; discussion 724S-725S.
37. Halliwell, B. and Aruoma, O.I. DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems. FEBS Lett. 281 (1991) 9-19.
38. Levine, R.L. and Stadtman, E.R. Oxidative modification of proteins during aging. Exp. Gerontol. 36 (2001) 1495-1502.
39. Stadtman, E.R. and Levine, R.L. Protein oxidation. Ann. N. Y. Acad. Sci. 899 (2000) 191-208.
40. Tien, M., Berlett, B.S., Levine, R.L., Chock, P.B. and Stadtman, E.R. Peroxynitrite-mediated modification of proteins at physiological carbon dioxide concentration: pH dependence of carbonyl formation, tyrosine nitration, and methionine oxidation. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7809-7814.
41. Stadtman, E.R. and Berlett, B.S. Reactive oxygen-mediated protein oxidation in aging and disease. Drug Metab. Rev. 30 (1998) 225-243.
42. Griffiths, H.R. Antioxidants and protein oxidation. Free Radic. Res. 33 (2000) S47-S58.
43. Levine, R.L., Wehr, N., Williams, J.A., Stadtman, E.R. and Shacter, E. Determination of carbonyl groups in oxidized proteins. Meth. Mol. Biol. 99 (2000) 15-24.
44. Levine, R.L. Carbonyl modified proteins in cellular regulation, aging, and disease. Free Radic. Biol. Med. 32 (2002) 790-796.
45. Betteridge, D.J. What is oxidative stress? Metabolism 49 (2000) 3-8.
46. Lehucher-Michel, M.P., Lesgards, J.F., Delubac, O., Stocker, P., Durand, P. and Prost, M. Oxidative stress and human disease: Current knowledge and perspectives for prevention. Presse Med. 30 (2001) 1076-1081.
47. Witztum, J.L. and Steinberg, D. The oxidative modification hypothesis of atherosclerosis: does it hold for humans? Trends Cardiovasc. Med. 11 (2001) 93-102.
48. Traverso, N. Oxidative elements in the pathogenesis of atherosclerosis. Ital. Heart J. 2 (2001) 37S-39S.
49. Kovacic, P. and Jacintho, J.D. Mechanisms of carcinogenesis: focus on oxidative stress and electron transfer. Curr. Med. Chem. 8 (2001) 773-796.
50. Kawanishi, S., Hiraku, Y. and Oikawa, S. Mechanism of guanine-specific DNA damage by oxidative stress and its role in carcinogenesis and aging, Mutat. Res. 488 (2001) 65-76.
51. Lipinski, B. Pathophysiology of oxidative stress in diabetes mellitus. J. Diabetes Complicat. 15 (2001) 203-210.
52. Odeh, M. New insights into the pathogenesis and treatment of rheumatoid arthritis. Clin. Immunol. Immunopathol. 83 (1997) 103-116.
53. Stangel, M., Mix, E., Zettl, U.K. and Gold, R. Oxides and apoptosis in inflammatory myopathies. Microsc. Res. Tech. 55 (2001) 249-258.
54. Smith, K.J., Kapoor, R. and Felts, P.A. Demyelination: the role of reactive oxygen and nitrogen species. Brain Pathol. 9 (1999) 69-92.
55. Mantle, D. and Preedy, V.R. Free radicals as mediators of alcohol toxicity. Adverse Drug React. Toxicol. Rev. 18 (1999) 235-252.
56. Bailey, S.M. and Cunningham, C.C. Contribution of mitochondria to oxidative stress associated with alcoholic liver disease. Free Radic. Biol. Med. 32 (2002) 11-16.
57. Milhavet, O. and Lehmann, S. Oxidative stress and the prion protein in transmissible spongiform encephalopathies. Brain Res. Rev. 38 (2002) 328-339.
58. Contestabile, A. Oxidative stress in neurodegeneration: mechanisms and therapeutic perspectives. Curr. Top Med. Chem. 1 (2001) 553-568.
59. Sayre, L.M., Smith, M.A. and Perry, G. Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr. Med. Chem. 8 (2001) 721-738.
60. Marshall, B., Keskin, D.B. and Mellor, A.L. Regulation of prostaglandin synthesis and cell adhesion by a tryptophan catabolizing enzyme. BMC Biochem. 2 (2001) 5.
61. Hayaishi, O. Utilization of superoxide anion by indoleamine oxygenase-catalyzed tryptophan and indoleamine oxidation. Adv. Exp. Med. Biol. 398 (1996) 285-289.
62. Quick, K.L., Hardt, J.I. and Dugan, L.L. Rapid microplate assay for superoxide scavenging efficiency. J. Neurosci. Methods 97 (2000) 139-144.
63. Lowenstein, C.J., Alley, E.W., Raval, P., Snowman, A.M., Snyder, S.H., Russell, S.W. and Murphy, W.J. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 9730-9734.
64. Ducrocq, C., Blanchard, B., Pignatelli, B. and Ohshima, H. Peroxynitrite: an endogenous oxidizing and nitrating agent. Cell Mol. Life Sci. 55 (1999) 1068-1077.
65. Hornbeck, P., Winston, S. and Fuller, S.A. in: Current Protocols in Molecular Biology (Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K., Eds.), John Wiley & Sons, New York.1991, Vol. 2, pp. 11.2.
66. Levine, R.L., Williams, J.A., Stadtman, E.R. and Shacter, E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 233 (1994) 346-363.
67. Buss, H., Chan, T.P., Sluis, K.B., Domigan, N.M. and Winterbourn, C.C. Protein carbonyl measurement by a sensitive ELISA method. Free Radic. Biol. Med. 23 (1997) 361-366.
68. Wood, J.M., Ehrke, C. and Schallreuter, K.U. Tryptophan protects human melanoma cells against gamma-interferon and tumour necrosis factor-alpha: a unifying mechanism of action. Melanoma Res. 1 (1991) 177-185.
69. Daley-Yates, P.T., Powell, A.P. and Smith, L.L. Pulmonary indoleamine 2,3-dioxygenase activity and its significance in the response of rats, mice, and rabbits to oxidative stress. Toxicol. Appl. Pharmacol. 96 (1988) 222-232.
70. Goda, K., Hamane, Y., Kishimoto, R. and Ogishi, Y. Radical scavenging properties of tryptophan metabolites. Estimation of their radical reactivity. Adv. Exp. Med. Biol. 467 (1999) 397-402.
71. Thomas, S.R. and Stocker, R. Antioxidant activities and redox regulation of interferon-gamma-induced tryptophan metabolism in human monocytes and macrophages. Adv. Exp. Med. Biol. 467 (1999) 541-552.
72. Grant, R.S., Naif, H., Espinosa, M. and Kapoor, V. IDO induction in IFN-gamma activated astroglia: a role in improving cell viability during oxidative stress. Redox Rep. 5 (2000) 101-104.
73. Grant, R.S., Passey, R., Matanovic, G., Smythe, G. and Kapoor, V., Evidence for increased de novo synthesis of NAD in immune-activated RAW264.7 macrophages: a self-protective mechanism? Arch. Biochem. Biophys. 372 (1999) 1-7.
74. Alberati-Giani, D., Ricciardi-Castagnoli, P., Köhler, C. and Cesura, A.M. Regulation of the kynurenine metabolic pathway by interferon-gamma in murine cloned macrophages and microglial cells. J. Neurochem. 66 (1996) 996-1004.
75. Knight, J.A. Review: Free radicals, antioxidants, and the immune system. Ann. Clin. Lab. Sci. 30 (2000) 145-158.
76. Klebanoff, S.J., Locksley, R.M., Jong, E.C. and Rosen, H. Oxidative response of phagocytes to parasite invasion. Ciba Found. Symp. 99 (1983) 92-112.
77. Fridovich, I. Biological effects of the superoxide radical. Arch. Biochem. Biophys. 247 (1986) 1-11.
78. Schisler, N.J. and Singh, S.M. Tissue-specific developmental regulation of superoxide dismutase (SOD-1 and SOD-2) activities in genetic strains of mice. Biochem. Genet. 23 (1985) 291-308.
79. Zelko, I.N., Mariani, T.J. and Folz, R.J. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic. Biol. Med. 33 (2002) 337-349.
80. Grankvist, K., Marklund, S.L. and Taljedal, I.B. CuZn-superoxide dismutase, Mn-superoxide dismutase, catalase and glutathione peroxidase in pancreatic islets and other tissues in the mouse. Biochem. J. 199 (1981) 393-398.
81. Halliwell, B. Biochemical mechanisms accounting for the toxic action of oxygen on living organisms: the key role of superoxide dismutase. Cell Biol. Int. Rep. 2 (1978) 113-128.
82. Hayaishi, O. and Yoshida, R. Specific induction of pulmonary indoleamine 2,3-dioxygenase by bacterial lipopolysaccharide. Ciba Found. Symp. (1978) 199-203.
83. Kamimura, S., Eguchi, K., Yonezawa, M. and Sekiba, K. Localization and developmental change of indoleamine 2,3-dioxygenase activity in the human placenta. Acta Med. Okayama 45 (1991) 135-139.
84. Cook, J.S., Pogson, C.I. and Smith, S.A. Indoleamine 2,3-dioxygenase. A new, rapid, sensitive radiometric assay and its application to the study of the enzyme in rat tissues. Biochem. J. 189 (1980) 461-466.
85. Takikawa, O., Yoshida, R., Kido, R. and Hayaishi, O. Tryptophan degradation in mice initiated by indoleamine 2,3-dioxygenase. J. Biol. Chem. 261 (1986) 3648-3653.
86. Fujiwara, M., Shibata, M., Watanabe, Y., Nukiwa, T., Hirata, F., Mizuno, N. and Hayaishi, O. Indoleamine 2,3-dioxygenase. Formation of L-kynurenine from L-tryptophan in cultured rabbit pineal gland. J. Biol. Chem. 253 (1978) 6081-6085.
87. Gál, E.M. and Sherman, A.D. L-kynurenine: its synthesis and possible regulatory function in brain. Neurochem. Res. 5 (1980) 223-239.
88. Takikawa, O., Littlejohn, T.K. and Truscott, R.J. Indoleamine 2,3-dioxygenase in the human lens, the first enzyme in the synthesis of UV filters. Exp. Eye Res. 72 (2001) 271-277.
89. Taylor, M.W. and Feng, G. Relationship between interferon-g, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 5 (1991) 2516-2522.
90. Heyes, M.P., Achim, C.L., Wiley, C.A., Major, E.O., Saito, K. and Markey, S.P. Human microglia convert L-tryptophan into the neurotoxin quinolinic acid. Biochem. J. 320 (1996) 595-597.
91. Heyes, M.P., Chen, C.Y., Major, E.O. and Saito, K. Different kynurenine pathway enzymes limit quinolinic acid formation by various human cell types. Biochem. J. 326 (1997) 351-356.
92. Santoso, D.I., Rogers, P., Wallace, E.M., Manuelpillai, U., Walker, D. and Subakir, S.B. Localization of indoleamine 2,3-dioxygenase and 4-hydroxynonenal in normal and pre-eclamptic placentae. Placenta 23 (2002) 373-379.