BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Oxidative modification of ferritin induced by methylglyoxal

  • An, Sung-Ho (Department of Genetic Engineering, Cheongju University) ;
  • Lee, Myeong-Seon (Department of Genetic Engineering, Cheongju University) ;
  • Kang, Jung-Hoon (Department of Genetic Engineering, Cheongju University)
  • Received : 2011.12.27
  • Accepted : 2011.12.30
  • Published : 2012.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Methylglyoxal (MG) was identified as an intermediate in non-enzymatic glycation and increased levels were reported in patients with diabetes. In this study, we evaluated the effects of MG on the modification of ferritin. When ferritin was incubated with MG, covalent crosslinking of the protein increased in a time- and MG dose-dependent manner. Reactive oxygen species (ROS) scavengers, $N-acetyl-_L-cysteine$ and thiourea suppressed the MG-mediated ferritin modification. The formation of dityrosine was observed in MG-mediated ferritin aggregates and ROS scavengers inhibited the formation of dityrosine. During the reaction between ferritin and MG, the generation of ROS was increased as a function of incubation time. These results suggest that ROS may play a role in the modification of ferritin by MG. The reaction between ferritin and MG led to the release of iron ions from the protein. Ferritin exposure to MG resulted in a loss of arginine, histidine and lysine residues. It was assumed that oxidative damage to ferritin caused by MG may induce an increase in the iron content in cells, which is deleterious to cells. This mechanism, in part, may provide an explanation or the deterioration of organs under diabetic conditions.

Keywords

References

  1. Thornalley, P. J., Langborg, A. and Minhas, H. S. (1999) Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem. J. 344, 109-116. https://doi.org/10.1042/0264-6021:3440109
  2. Brownlee, M., Cerami, A. and Vlassara, H. (1988) Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N. Eng. J. Med. 318, 1315-1321. https://doi.org/10.1056/NEJM198805193182007
  3. Nagaraj, R., Shipanova, I. N. and Faust, F. (1996) Protein cross-linking by the Maillard reaction. Isolation, characterization, and in vivo detection of a lysine-lysine cross-link derived from methylglyoxal. J. Biol. Chem. 271, 19338-19345. https://doi.org/10.1074/jbc.271.32.19338
  4. Monnier, V. M., Vishwanath, V., Frank, K. E, Elmets, C. A., Dauchot, P. and Kohn, R. R. (1986) Relation between complications of type I diabetes mellitus and collagen-linked fluorescence. N. Engl. J. Med. 314, 403-408. https://doi.org/10.1056/NEJM198602133140702
  5. Monnier, V. M. and Cerami, A. (1981) Nonenzymatic browning in vivo: possible process for aging of long-lived proteins. Science 214, 491-493.
  6. Vlassara, H., Brownlee, M. and Cerami, A. (1981) Nonenzymatic glycosylation of peripheral nerve protein in diabetes mellitus. Proc. Natl. Acad. Sci. U.S.A. 78, 5190-5192. https://doi.org/10.1073/pnas.78.8.5190
  7. Aisen, P. and Listowsky, I. (1980) Iron transport and storage proteins. Annu. Rev. Biochem. 49, 357-393. https://doi.org/10.1146/annurev.bi.49.070180.002041
  8. Santambrogio, P., Levi, S., Cozzi, A., Rovida, E., Albertini, A. and Arosio, P. (1993) Production and characterization of recombinant heteropolymers of human ferritin H and L chains. J. Biol. Chem. 268, 12744-12748.
  9. Welch, K. D., Davis, T. Z., Van Eden, M. E. and Aust, S. D. (2002) Deleterious iron-mediated oxidation of biomolecules. Free Radic. Biol. Med. 32, 577-583. https://doi.org/10.1016/S0891-5849(02)00760-8
  10. Haap, M., Fritsche, A., Mensing, H. J., Haring, H. U. and Stumvoll, M. (2003) Association of high serum ferritin concentration with glucose intolerance and insulin resistance in healthy people. Ann. Intern. Med. 139, 869-871.
  11. Gonzalez, A. S., Guerrero, D. B., Soto, M. B., Diaz, S. P., Martinez-Olmos, M. and Vidal, O. (2006) Metabolic syndrome, insulin resistance and the inflammation markers C-reactive protein and ferritin. Eur. J. Clin. Nutr. 60, 802-809. https://doi.org/10.1038/sj.ejcn.1602384
  12. Gastaldelli, A., Perego, L., Paganelli, M., Sesti, G., Hribal, M., Chavez, A. O., Defronzo, R. A., Pontiroli, A. and Folli, F. (2009) Elevated concentrations of liver enzymes and ferritin identify a new phenotype of insulin resistance: effect of weight loss after gastric banding. Obes. Surg. 19, 80-86. https://doi.org/10.1007/s11695-008-9690-9
  13. Salonen, J. T., Tuomainen, T. P., Nyyssonen, K., Lakka, H. M. and Punnonen, K. (1998) Relation between iron stores and non-insulin dependent diabetes in men: case-control study. BMJ 317:727. https://doi.org/10.1136/bmj.317.7160.727
  14. Ford, E. S., Cogswell, M. E. and Diabetes. (1999) Diabetes and serum ferritin concentration among U.S. adults. Diabetes Care 22, 1978-1983. https://doi.org/10.2337/diacare.22.12.1978
  15. Babusikova, E. M., Kaplan, P., Lehotsky, J. M., Jesenak, M. and Dobrota, D. (2004) Oxidative modification of rat cardiac mitochondrial membranes and myofibrils by hydroxyl radicals. Gen. Physiol. Biophys. 23, 327-335.
  16. Schuessler, H. and Davies, J. V. (1983) Radiation-induced reduction reactions with bovine serum albumin. Int. J. Radiat. Biol. Relay. Stud. Phys. Chem. Med. 43, 291-301. https://doi.org/10.1080/09553008314550331
  17. Garner, W. H., Garner, M. H. and Spector, A. (1983) $H_{2}O_{2}$-induced uncoupling of bovine lens $Na^{+}$,$K^{+}$-ATPase. Proc. Natl. Acad. Sci. U.S.A. 80, 2044-2048. https://doi.org/10.1073/pnas.80.7.2044
  18. Prtiz de Montellano, P. R. and Kerr, D. E. (1983) Inactivation of catalase by phenylhydrazine. Formation of a stable aryl-iron heme complex. J. Biol. Chem. 258, 10558-10563.
  19. Shinar, E., Navok, T. and Chevion, M. (1983) The analogous mechanisms of enzymatic inactivation induced by ascorbate and superoxide in the presence of copper. J. Biol. Chem. 258, 14778-14782.
  20. Halliwell, B. and Gutteridge, J. M. (1981) Formation of thiobarbituric- acid-reactive substance from deoxyribose in the presence of iron salts: the role of superoxide and hydroxyl radicals. FEBS Lett. 128, 347-352. https://doi.org/10.1016/0014-5793(81)80114-7
  21. Halliwell, B. and Gutteridge, J. M. (2007) pp. 484, Oxford University Press, Oxford, UK
  22. Kim, K. S., Choi, S. Y., Kwon, H. Y., Won, M. H., Kang, T. C. and Kang, J. H. (2002) Aggregation of alpha-synuclein induced by the Cu,Zn-superoxide dismutase and hydrogen peroxide system. Free Radic. Biol. Med. 32, 544-550. https://doi.org/10.1016/S0891-5849(02)00741-4
  23. Kang, J. H. (2009) Ferritin enhances salsolinol-mediated DNA strand breakage: protection by carnosine and related compounds. Toxicol. Lett. 188, 20-25. https://doi.org/10.1016/j.toxlet.2009.02.011
  24. Knovich, M. A., Storey, J. A., Coffman, L. G., Torti, S. V. and Torti, F. M. (2009) Ferritin for the clinician. Blood Rev. 23, 95-104. https://doi.org/10.1016/j.blre.2008.08.001
  25. Chang, Y. C. and Chuang, L. M. (2010) The role of oxidative stress in the pathogenesis of type 2 diabetes: from molecular mechanism to clinical implication. Am. J. Transl. Res. 2, 316-331.
  26. Park, J. G. and Oh, G. T. (2011) The role of peroxidases in the pathogenesis of atherosclerosis. BMB Rep. 44, 497-505. https://doi.org/10.5483/BMBRep.2011.44.8.497
  27. Bartzokis, G., Tishler, T. A., Shin, I. S., Lu, P. H. and Cummings, J. L. (2004) Brain ferritin iron as a risk factor for age at onset in neurodegenerative diseases. Ann. N. Y. Acad. Sci. 1012, 224-236. https://doi.org/10.1196/annals.1306.019
  28. Koziorowski, D., Friedman, A., Arosio, P., Santambrogio, P. and Dziewulska, D. (2007) ELISA reveals a difference in the structure of substantia nigra ferritin in Parkinson's disease and incidental Lewy body compared to control. Parkinsonism Relat Disord 13, 214-218. https://doi.org/10.1016/j.parkreldis.2006.10.002
  29. Schuessler, H. and Schilling, K. (1984) Oxygen effect in the radiolysis of proteins. Part 2. Bovine serum albumin. Int. J. Radiat. Biol. 45, 267-281. https://doi.org/10.1080/09553008414550381
  30. Hunt, J. V. and Dean, R. T. (1989) Free radical-mediated degradation of proteins: the protective and deleterious effects of membranes. Biochem. Biophys. Res. Commun 162, 1073-1084.
  31. Stadtman, E. R. and Berlett, B. S. (1997) Reactive oxygen- mediated protein oxidation in aging and disease. Chem. Res. Toxicol. 10, 485-494. https://doi.org/10.1021/tx960133r
  32. McLellan, A. C., Thornallet, P. J., Benn, J. and Sonksen, P. H. (1994) Glyoxalase system in clinical diabetes mellitus and correlation with diabetic complications. Clin. Sci. (London) 87, 21-29.
  33. Phillips, S. A., Mirrlees, D. and Thornalley, P. J. (1993) Modification of the glyoxalase system in streptozotocin induced diabetic rats. Effect of the aldose reductasebinhibitor Statil. Biochem. Pharmacol. 46, 805-811. https://doi.org/10.1016/0006-2952(93)90488-I
  34. Stadtman, E. R. (1993) Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem. 62, 797-821. https://doi.org/10.1146/annurev.bi.62.070193.004053
  35. Davies, K. J. (1986) Intracellular proteolytic systems may function as secondary antioxidant defenses: an hypothesis. J. Free. Radic. Biol. Med. 2, 155-173. https://doi.org/10.1016/S0748-5514(86)80066-6
  36. Oliver, C. N., Levine, R. L. and Stadtman, E. R. (1987) A role of mixed-function oxidation reactions in the accumulation of altered enzyme forms during aging. J. Am. Geriatr. Soc. 35, 947-956. https://doi.org/10.1111/j.1532-5415.1987.tb02297.x
  37. Ciudin, A., Hernandez, C. and Simo, R. (2010) Iron overload in diabetic retinopathy: a cause or a consequence of impaired mechanisms? Exp. Diabetes. Res. 2010, 1-8.
  38. Eshed, I., Elis, A. and Lishner, M. (2001) Plasma ferritin and type 2 diabetes mellitus: a critical review. Endocr. Res. 27, 91-97. https://doi.org/10.1081/ERC-100107172
  39. Fernandez-Real, J. M., Ricart-Engel, W., Arroyo, E., Balanca, R., Casamitjana-Abella, R., Cabrero, D., Fernandez-Castaner, M. and Soler, J. (1998) Serum ferritin as a component of the insulin resistance syndrome. Diabetes Care 21, 62-68. https://doi.org/10.2337/diacare.21.1.62
  40. Jehn, M., Clark, J. M. and Guallar, E. (2004) Serum ferritin and risk of the metabolic syndrome in U.S. adults. Diabetes Care 27, 2422-2428. https://doi.org/10.2337/diacare.27.10.2422
  41. Chen, J., Wildman, R. P., Hamm, L. L., Muntner, P., Revnolds, K., Whelton, P. K. and He, J. (2004) Association between inflammation and insulin resistance in U.S. nondiabetic adults: results from the Third National Health and Nutrition Examination Survey. Diabetes Care 27, 2960-2965. https://doi.org/10.2337/diacare.27.12.2960
  42. Tuomainen, T. P., Nyyssonen, K., Salonen, R., Tervahauta, A., Korpela, H., Lakka, T., Kaplan, G. A. and Salonen, J. T. (1997) Body iron stores are associated with serum insulin and blood glucose concentrations. Population study in 1,013 eastern Finnish men. Diabetes Care 20, 426-428. https://doi.org/10.2337/diacare.20.3.426
  43. Phillips, S. A. and Thornalley, P. J. (1993) The formation of methylglyoxal from triose phosphates. Investigation using a specific assay for methylglyoxal. Eur. J. Biochem 212, 101-105. https://doi.org/10.1111/j.1432-1033.1993.tb17638.x
  44. Lee, C., Yim, M. B., Chock, P. B., Yim, H. S. and Kang, S. O. (1998) Oxidation-reduction properties of methylglyoxal- modified protein in relation to free radical generation. J. Biol. Chem 273, 25272-25278. https://doi.org/10.1074/jbc.273.39.25272
  45. Davies, K. J., Delsignore, M. E. and Lin, S. W. (1987) Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J. Biol. Chem. 262, 9902-9907.
  46. Levine, R. L., Oliver, C. N., Fulks, R. M. and Stadtman, E. R. (1981) Turnover of bacterial glutamine synthetase: oxidative inactivation precedes proteolysis. Proc. Natl. Acad. Sci. U.S.A. 78, 2120-2124. https://doi.org/10.1073/pnas.78.4.2120
  47. Cervera, J. and Levine, R. L. (1988) Modulation of the hydrophobicity of glutamine synthetase by mixed-function oxidation. FASEB J. 2, 2591-2595. https://doi.org/10.1096/fasebj.2.10.2898411
  48. Refsgaardm, H. H., Tsai, L. and Stadman, E. R. (2000) Modifications of proteins by polyunsaturated fatty acid peroxidation products. Proc. Natl. Acad. Sci. U.S.A. 97, 611-616. https://doi.org/10.1073/pnas.97.2.611
  49. Granier, T., Langlois d'Estaintot, B., Gallios, B., Chevalier, J. M., Precigoux, G., Santambrogio, P. and Arosio, P. (2003) Modifications of proteins by polyunsaturated fatty acid peroxidation products. J. Biol. Inorg. Chem. 8, 105-111. https://doi.org/10.1007/s00775-002-0389-4
  50. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, M. N., Olson, B. J. and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85. https://doi.org/10.1016/0003-2697(85)90442-7
  51. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685. https://doi.org/10.1038/227680a0
  52. Kim, N. H. and Kang, J. H. (2006) Oxidative damage of DNA induced by the cytochrome C and hydrogen peroxide system. J. Biochem. Mol. Biol. 39, 452-456. https://doi.org/10.5483/BMBRep.2006.39.4.452
  53. Pieroni, L., Khalil, L., Charlotte, F., Poynard, T., Piton, A., Hainque, B. and Imbert-Bismut, F. (2001) Comparison of bathophenanthroline sulfonate and ferene as chromogens in colorimetric measurement of low hepatic iron concentration. Clin. Chem. 47, 2059-2061.
  54. Hugli, T. E. and Moore, S. (1972) Determination of the tryptophan content of proteins by ion exchange chromatography of alkaline hydrolysates. J. Biol. Chem. 247, 2828-2834.

Cited by

  1. Modification and inactivation of Cu,Zn-superoxide dismutase by the lipid peroxidation product, acrolein vol.46, pp.11, 2013, https://doi.org/10.5483/BMBRep.2013.46.11.138
  2. Pathophysiological Insights of Methylglyoxal Induced Type-2 Diabetes vol.28, pp.9, 2015, https://doi.org/10.1021/acs.chemrestox.5b00171
  3. 2-Cyclopropylimino-3-methyl-1,3-thiazoline Hydrochloride Protects Against Beta-amyloid-induced Activation of the Apoptotic Cascade in Cultured Cortical Neurons vol.34, pp.7, 2014, https://doi.org/10.1007/s10571-014-0080-7
  4. Anti-inflammatory mechanisms of N-adamantyl-4-methylthiazol-2-amine in lipopolysaccharide-stimulated BV-2 microglial cells vol.22, pp.1, 2014, https://doi.org/10.1016/j.intimp.2014.06.022
  5. Can the beneficial effects of methionine restriction in rats be explained in part by decreased methylglyoxal generation resulting from suppressed carbohydrate metabolism? vol.13, pp.6, 2012, https://doi.org/10.1007/s10522-012-9401-8
  6. Salsolinol, a catechol neurotoxin, induces oxidative modification of cytochrome c vol.46, pp.2, 2013, https://doi.org/10.5483/BMBRep.2013.46.2.220
  7. 2-Cyclopropylimino-3-Methyl-1,3-Thiazoline Hydrochloride Inhibits Microglial Activation by Suppression of Nuclear Factor-Kappa B and Mitogen-Activated Protein Kinase Signaling vol.9, pp.4, 2014, https://doi.org/10.1007/s11481-014-9542-4
  8. Iron reduction response and demographic differences between diabetics and non-diabetics with cardiovascular disease entered into a controlled clinical trial vol.10, pp.2, 2018, https://doi.org/10.1039/C7MT00282C