Indoleamine 2,3-dioxygenase overexpression causes kynurenine-modification of proteins, fiber cell apoptosis and cataract formation in the mouse lens

Laboratory Investigation

Volumn 89, Issue 5, 2009, Pages 498-512

  Mailankot, Maneesh ^a   Staniszewska, Magdalena M ^a   Butler, Heather ^b   Caprara, Moonkyung H ^b   Howell, Scott ^b   Wang, Benlian ^b   Doller, Catherine ^b   Reneker, Lixing W ^c   Nagaraj, Ram H ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c University of Missouri   (United States)

Author keywords

Cataract; Crystallin; Indoleamine 2,3 dioxygenase; Kynurenine

Indexed keywords

CASPASE 3; CASPASE 9; GLUTATHIONE; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; TRYPTOPHAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CATARACT; CATARACTOGENESIS; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE OVEREXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; ANIMAL; GROWTH, DEVELOPMENT AND AGING; LENS; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; CATARACT; GLUTATHIONE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KYNURENINE; LENS, CRYSTALLINE; MICE; MICE, TRANSGENIC; TRYPTOPHAN;

EID: 65649150722     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2009.22     Document Type: Article

References (61)

1. King NJ, Thomas SR. Molecules in focus: indoleamine 2,3-dioxygenase. Int J Biochem Cell Biol 2007;39:2167-2172.
2. Takikawa O. Biochemical and medical aspects of the indoleamine 2,3-dioxygenase-initiated L-tryptophan metabolism. Biochem Biophys Res Commun 2005;338:12-19.
3. MacKenzie CR, Heseler K, Muller A, et al. Role of indoleamine 2,3-dioxygenase in antimicrobial defence and immuno-regulation: tryptophan depletion versus production of toxic kynurenines. Curr Drug Metab 2007;8:237-244.
4. Fallarino F, Gizzi S, Mosci P, et al. Tryptophan catabolism in IDO+ plasmacytoid dendritic cells. Curr Drug Metab 2007;8:209-216.
5. Mellor AL, Munn D, Chandler P, et al. Tryptophan catabolism and T cell responses. Adv Exp Med Biol 2003;527:27-35.
6. Li Y, Tredget EE, Ghaffari A, et al. Local expression of indoleamine 2,3-dioxygenase protects engraftment of xenogeneic skin substitute. J Invest Dermatol 2006;126:128-136.
7. Brandacher G, Cakar F, Winkler C, et al. Non-invasive monitoring of kidney allograft rejection through IDO metabolism evaluation. Kidney Int 2007;71:60-67.
8. Zamanakou M, Germenis AE, Karanikas V. Tumor immune escape mediated by indoleamine 2,3-dioxygenase. Immunol Lett 2007;111:69-75.
9. Muller AJ, DuHadaway JB, Donover PS, et al. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat Med 2005;11:312-319.
10. Okuda S, Nishiyama N, Saito H, et al. 3-Hydroxykynurenine, an endogenous oxidative stress generator, causes neuronal cell death with apoptotic features and region selectivity. J Neurochem 1998;70:299-307.
11. Morita T, Saito K, Takemura M, et al. 3-Hydroxyanthranilic acid, an L-tryptophan metabolite, induces apoptosis in monocyte-derived cells stimulated by interferon-gamma. Ann Clin Biochem 2001;38:242-251.
12. Wirleitner B, Rudzite V, Neurauter G, et al. Immune activation and degradation of tryptophan in coronary heart disease. Eur J Clin Invest 2003;33:550-554.
13. Tankiewicz A, Pawlak D, Topczewska-Bruns J, et al. Kidney and liver kynurenine pathway enzymes in chronic renal failure. Adv Exp Med Biol 2003;527:409-414.
14. Sala A, Campagnoli M, Perani E, et al. Human alpha-1-microglobulin is covalently bound to kynurenine-derived chromophores. J Biol Chem 2004;279:51033-51041.
15. Mohib K, Guan Q, Diao H, et al. Proapoptotic activity of indoleamine 2,3-dioxygenase expressed in renal tubular epithelial cells. Am J Physiol Renal Physiol 2007;293:F801-F812.
16. Cerstiaens A, Huybrechts J, Kotanen S, et al. Neurotoxic and neurobehavioral effects of kynurenines in adult insects. Biochem Biophys Res Commun 2003;312:1171-1177.
17. Pearson SJ, Meldrum A, Reynolds GP. An investigation of the activities of 3-hydroxykynureninase and kynurenine aminotransferase in the brain in Huntington's disease. J Neural Transm Gen Sect 1995;102:67-73.
18. Ogawa T, Matson WR, Beal MF, et al. Kynurenine pathway abnormalities in Parkinson's disease. Neurology 1992;42:1702-1706.
19. Sas K, Robotka H, Toldi J, et al. Mitochondria, metabolic disturbances, oxidative stress and the kynurenine system, with focus on neurodegenerative disorders. J Neurol Sci 2007;257:221-239.
20. Schrocksnadel K, Wirleitner B, Winkler C, et al. Monitoring tryptophan metabolism in chronic immune activation. Clin Chim Acta 2006;364:82-90.
21. Szanto S, Koreny T, Mikecz K, et al. Inhibition of indoleamine 2,3-dioxygenase-mediated tryptophan catabolism accelerates collageninduced arthritis in mice. Arthritis Res Ther 2007;9:R50.
22. Takikawa O, Littlejohn T, Jamie JF, et al. Regulation of indoleamine 2,3-dioxygenase, the first enzyme in UV filter biosynthesis in the human lens. Relevance for senile nuclear cataract. Adv Exp Med Biol 1999;467:241-245.
23. Bova LM, Sweeney MH, Jamie JF, et al. Major changes in human ocular UV protection with age. Invest Ophthalmol Vis Sci 2001;42: 200-205.
24. Taylor LM, Andrew Aquilina J, Jamie JF, et al. UV filter instability: consequences for the human lens. Exp Eye Res 2002;75:165-175.
25. Vazquez S, Aquilina JA, Jamie JF, et al. Novel protein modification by kynurenine in human lenses. J Biol Chem 2002;277: 4867-4873.
26. Korlimbinis A, Aquilina JA, Truscott RJ. Protein-bound UV filters in normal human lenses: the concentration of bound UV filters equals that of free UV filters in the center of older lenses. Invest Ophthalmol Vis Sci 2007;48:1718-1723.
27. Vazquez S, Parker NR, Sheil M, et al. Protein-bound kynurenine decreases with the progression of age-related nuclear cataract. Invest Ophthalmol Vis Sci 2004;45:879-883.
28. Staniszewska MM, Nagaraj RH. 3-Hydroxykynurenine-mediated modification of human lens proteins: structure determination of a major modification using a monoclonal antibody. J Biol Chem 2005;280:22154-22164.
29. Staniszewska M, Nagaraj RH. Detection of kynurenine modifications in proteins using a monoclonal antibody. J Immunol Methods 2007;324:63-73.
30. Bhattacharyya J, Padmanabha Udupa EG, Wang J, et al. Mini-alphaBcrystallin: a functional element of alphaB-crystallin with chaperone-like activity. Biochemistry 2006;45:3069-3076.
31. Cui XL, Lou MF. The effect and recovery of long-term H2O2 exposure on lens morphology and biochemistry. Exp Eye Res 1993;57: 157-167.
32. Giblin FJ. Glutathione: a vital lens antioxidant. J Ocul Pharmacol Ther 2000;16:121-135.
33. Kamei A. Glutathione levels of the human crystalline lens in aging and its antioxidant effect against the oxidation of lens proteins. Biol Pharm Bull 1993;16:870-875.
34. Reddy VN, Giblin FJ. Metabolism and function of glutathione in the lens. Ciba Found Symp 1984;106:65-87.
35. Hwu P, Du MX, Lapointe R, et al. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J Immunol 2000;164:3596-3599.
36. Hains PG, Simpanya MF, Giblin F, et al. UV filters in the lens of the thirteen lined ground squirrel (Spermophilus tridecemlineatus). Exp Eye Res 2006;82:730-737.
37. Piatigorsky J. Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation 1981;19: 134-153.
38. Bassnett S, McNulty R. The effect of elevated intraocular oxygen on organelle degradation in the embryonic chicken lens. J Exp Biol 2003;206:4353-4361.
39. Beebe DC, Silver MH, Belcher KS, et al. Lentropin, a protein that controls lens fiber formation, is related functionally and immunologically to the insulin-like growth factors. Proc Natl Acad Sci USA 1987;84:2327-2330.
40. Lovicu FJ, McAvoy JW. Growth factor regulation of lens development. Dev Biol 2005;280:1-14.
41. Belecky-Adams TL, Adler R, Beebe DC. Bone morphogenetic protein signaling and the initiation of lens fiber cell differentiation. Development 2002;129:3795-3802.
42. Peek R, McAvoy JW, Lubsen NH, et al. Rise and fall of crystallin gene messenger levels during fibroblast growth factor induced terminal differentiation of lens cells. Dev Biol 1992;152:152-160.
43. Weber GF, Menko AS. Phosphatidylinositol 3-kinase is necessary for lens fiber cell differentiation and survival. Invest Ophthalmol Vis Sci 2006;47:4490-4499.
44. Ring BZ, Cordes SP, Overbeek PA, et al. Regulation of mouse lens fiber cell development and differentiation by the Maf gene. Development 2000;127:307-317.
45. Nishiguchi S, Wood H, Kondoh H, et al. Sox1 directly regulates the gamma-crystallin genes and is essential for lens development in mice. Genes Dev 1998;12:776-781.
46. Wigle JT, Chowdhury K, Gruss P, et al. Prox1 function is crucial for mouse lens-fibre elongation. Nat Genet 1999;21:318-322.
47. Fallarino F, Grohmann U, Vacca C, et al. T cell apoptosis by kynurenines. Adv Exp Med Biol 2003;527:183-190.
48. Morita T, Saito K, Takemura M, et al. L-tryptophan-kynurenine pathway metabolite 3-hydroxyanthranilic acid induces apoptosis in macrophage-derived cells under pathophysiological conditions. Adv Exp Med Biol 1999;467:559-563.
49. Wei H, Leeds P, Chen RW, et al. Neuronal apoptosis induced by pharmacological concentrations of 3-hydroxykynurenine: characterization and protection by dantrolene and Bcl-2 overexpression. J Neurochem 2000;75:81-90.
50. Morozov V, Wawrousek EF. Caspase-dependent secondary lens fiber cell disintegration in alphaA-/alphaB-crystallin double-knockout mice. Development 2006;133:813-821.
51. Aquilina JA, Truscott RJ. Kynurenine binds to the peptide binding region of the chaperone alphaB-crystallin. Biochem Biophys Res Commun 2001;285:1107-1113.
52. Stolen CM, Griep AE. Disruption of lens fiber cell differentiation and survival at multiple stages by region-specific expression of truncated FGF receptors. Dev Biol 2000;217:205-220.
53. Fromm L, Shawlot W, Gunning K, et al. The retinoblastoma proteinbinding region of simian virus 40 large T antigen alters cell cycle regulation in lenses of transgenic mice. Mol Cell Biol 1994;14: 6743-6754.
54. Lovicu FJ, Overbeek PA. Overlapping effects of different members of the FGF family on lens fiber differentiation in transgenic mice. Development 1998;125:3365-3377.
55. Rao V, Wawrousek E, Tamm ER, et al. Rho GTPase inactivation impairs lens growth and integrity. Lab Invest 2002;82:231-239.
56. Breitman ML, Rombola H, Maxwell IH, et al. Genetic ablation in transgenic mice with an attenuated diphtheria toxin A gene. Mol Cell Biol 1990;10:474-479.
57. Thomas SR, Mohr D, Stocker R. Nitric oxide inhibits indoleamine 2,3-dioxygenase activity in interferon-gamma primed mononuclear phagocytes. J Biol Chem 1994;269:14457-14464.
58. Poljak A, Grant R, Austin CJ, et al. Inhibition of indoleamine 2,3 dioxygenase activity by H2O2. Arch Biochem Biophys 2006;450: 9-19.
59. Lacomba MS, Martin CM, Chamond RR, et al. Aqueous and serum interferon gamma, interleukin (IL) 2, IL-4, and IL-10 in patients with uveitis. Arch Ophthalmol 2000;118:768-772.
60. Awasthi N, Wagner BJ. Interferon-gamma induces apoptosis of lens alphaTN4-1 cells and proteasome inhibition has an antiapoptotic effect. Invest Ophthalmol Vis Sci 2004;45:222-229.
61. Geiger K, Howes E, Gallina M, et al. Transgenic mice expressing IFNgamma in the retina develop inflammation of the eye and photoreceptor loss. Invest Ophthalmol Vis Sci 1994;35:2667-2681.