Posttranslational modification and regulation of glutamate-cysteine ligase by the α,β-unsaturated aldehyde 4-hydroxy-2-nonenal

Free Radical Biology and Medicine

Volumn 50, Issue 1, 2011, Pages 14-26

  Backos, Donald S ^a   Fritz, Kristofer S ^a   Roede, James R ^b   Petersen, Dennis R ^a   Franklin, Christopher C ^a,c  

^a UNIVERSITY OF COLORADO   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

4 Hydroxynonenal; Antioxidants; Free radicals; Glutamate cysteine ligase; Glutathione; Oxidative stress

Indexed keywords

4 HYDROXYNONENAL; CYSTEINE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; HOLOENZYME; LYSINE;

ARTICLE; BINDING AFFINITY; BIOSYNTHESIS; CATALYSIS; ENZYME ACTIVITY; HOMEOSTASIS; PRIORITY JOURNAL; PROTEIN PROCESSING;

ALDEHYDES; ANIMALS; CYSTEINE; CYSTEINE PROTEINASE INHIBITORS; GLUTAMATE-CYSTEINE LIGASE; HUMANS; LIPID PEROXIDATION; LYSINE; MASS SPECTROMETRY; METABOLIC DETOXICATION, PHASE I; MICE; OXIDATIVE STRESS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; STEREOISOMERISM; TUMOR CELLS, CULTURED;

EID: 78650692177     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.10.694     Document Type: Article

References (65)

1. Y. Ando, T. Brannstrom, K. Uchida, N. Nyhlin, B. Nasman, O. Suhr, T. Yamashita, T. Olsson, M. El Salhy, M. Uchino, and M. Ando Histochemical detection of 4-hydroxynonenal protein in Alzheimer amyloid J. Neurol. Sci. 156 1998 172 176
2. D.L. Carbone, J.A. Doorn, Z. Kiebler, B.R. Ickes, and D.R. Petersen Modification of heat shock protein 90 by 4-hydroxynonenal in a rat model of chronic alcoholic liver disease J. Pharmacol. Exp. Ther. 315 2005 8 15
3. I. Rahman, A.A. van Schadewijk, A.J. Crowther, P.S. Hiemstra, J. Stolk, W. MacNee, and W.I. De Boer 4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease Am. J. Respir. Crit. Care Med. 166 2002 490 495
4. H. Esterbauer, R.J. Schaur, and H. Zollner Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radic. Biol. Med. 11 1991 81 128
5. L.M. Sayre, D. Lin, Q. Yuan, X. Zhu, and X. Tang Protein adducts generated from products of lipid oxidation: focus on HNE and ONE Drug Metab. Rev. 38 2006 651 675
6. A.J. Kurtz, and R.S. Lloyd 1, N2-deoxyguanosine adducts of acrolein, crotonaldehyde, and trans-4-hydroxynonenal cross-link to peptides via Schiff base linkage J. Biol. Chem. 278 2003 5970 5976
7. R.M. LoPachin, T. Gavin, D.R. Petersen, and D.S. Barber Molecular mechanisms of 4-hydroxy-2-nonenal and acrolein toxicity: nucleophilic targets and adduct formation Chem. Res. Toxicol. 22 2009 1499 1508
8. J.A. Doorn, and D.R. Petersen Covalent modification of amino acid nucleophiles by the lipid peroxidation products 4-hydroxy-2-nonenal and 4-oxo-2-nonenal Chem. Res. Toxicol. 15 2002 1445 1450
9. D.R. Petersen, and J.A. Doorn Reactions of 4-hydroxynonenal with proteins and cellular targets Free Radic. Biol. Med. 37 2004 937 945
10. K. Uchida, and E.R. Stadtman Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase: a possible involvement of intra- and intermolecular cross-linking reaction J. Biol. Chem. 268 1993 6388 6393
11. B. Friguet, E.R. Stadtman, and L.I. Szweda Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal: formation of cross-linked protein that inhibits the multicatalytic protease J. Biol. Chem. 269 1994 21639 21643
12. B.J. Stewart, J.A. Doorn, and D.R. Petersen Residue-specific adduction of tubulin by 4-hydroxynonenal and 4-oxononenal causes cross-linking and inhibits polymerization Chem. Res. Toxicol. 20 2007 1111 1119
13. D.L. Carbone, J.A. Doorn, Z. Kiebler, and D.R. Petersen Cysteine modification by lipid peroxidation products inhibits protein disulfide isomerase Chem. Res. Toxicol. 18 2005 1324 1331
14. D.L. Vander Jagt, L.A. Hunsaker, T.J. Vander Jagt, M.S. Gomez, D.M. Gonzales, L.M. Deck, and R.E. Royer Inactivation of glutathione reductase by 4-hydroxynonenal and other endogenous aldehydes Biochem. Pharmacol. 53 1997 1133 1140
15. A.E. Mitchell, D. Morin, M.W. Lame, and A.D. Jones Purification, mass spectrometric characterization, and covalent modification of murine glutathione S-transferases Chem. Res. Toxicol. 8 1995 1054 1062
16. T. Ishii, E. Tatsuda, S. Kumazawa, T. Nakayama, and K. Uchida Molecular basis of enzyme inactivation by an endogenous electrophile 4-hydroxy-2-nonenal: identification of modification sites in glyceraldehyde-3-phosphate dehydrogenase Biochemistry 42 2003 3474 3480
17. B.P. Sampey, D.L. Carbone, J.A. Doorn, D.A. Drechsel, and D.R. Petersen 4-Hydroxy-2-nonenal adduction of extracellular signal-regulated kinase (Erk) and the inhibition of hepatocyte Erk-Est-like protein-1-activating protein-1 signal transduction Mol. Pharmacol. 71 2007 871 883
18. J.R. Roede, D.L. Carbone, J.A. Doorn, O.V. Kirichenko, P. Reigan, and D.R. Petersen In vitro and in silico characterization of peroxiredoxin 6 modified by 4-hydroxynonenal and 4-oxononenal Chem. Res. Toxicol. 21 2008 2289 2299
19. B.J. Stewart, J.R. Roede, J.A. Doorn, and D.R. Petersen Lipid aldehyde-mediated cross-linking of apolipoprotein B-100 inhibits secretion from HepG2 cells Biochim. Biophys. Acta 1791 2009 772 780
20. W. Liu, M. Kato, A.A. Akhand, A. Hayakawa, H. Suzuki, T. Miyata, K. Kurokawa, Y. Hotta, N. Ishikawa, and I. Nakashima 4-Hydroxynonenal induces a cellular redox status-related activation of the caspase cascade for apoptotic cell death J. Cell Sci. 113 2000 635 641
21. H. Raza, A. John, E.M. Brown, S. Benedict, and A. Kambal Alterations in mitochondrial respiratory functions, redox metabolism and apoptosis by oxidant 4-hydroxynonenal and antioxidants curcumin and melatonin in PC12 cells Toxicol. Appl. Pharmacol. 226 2008 161 168
22. K. Berhane, M. Widersten, A. Engstrom, J.W. Kozarich, and B. Mannervik Detoxication of base propenals and other alpha, beta-unsaturated aldehyde products of radical reactions and lipid peroxidation by human glutathione transferases Proc. Natl Acad. Sci. USA 91 1994 1480 1484
23. A. Fukuda, T. Osawa, K. Hitomi, and K. Uchida 4-Hydroxy-2-nonenal cytotoxicity in renal proximal tubular cells: protein modification and redox alteration Arch. Biochem. Biophys. 333 1996 419 426
24. R. Sekura, and A. Meister γ-Glutamylcysteine synthetase J. Biol. Chem. 252 1977 2599 2605
25. O.W. Griffith, and R.T. Mulcahy The enzymes of glutathione synthesis: gamma-glutamylcysteine synthetase Adv. Enzymol. Relat. Areas Mol. Biol. 73 1999 209 267
26. Y. Chen, H.G. Shertzer, S.N. Schneider, D.W. Nebert, and T.P. Dalton Glutamate cysteine ligase catalysis: dependence on ATP and modifier subunit for regulation of tissue glutathione levels J. Biol. Chem. 280 2005 33766 33774
27. Z. Tu, and M.W. Anders Expression and characterization of human glutamate-cysteine ligase Arch. Biochem. Biophys. 354 1998 247 254
28. Y. Yang, Y. Chen, E. Johansson, S.N. Schneider, H.G. Shertzer, D.W. Nebert, and T.P. Dalton Interaction between the catalytic and modifier subunits of glutamate-cysteine ligase Biochem. Pharmacol. 74 2007 372 381
29. D.A. Dickinson, A.L. Levonen, D.R. Moellering, E.K. Arnold, H. Zhang, V.M. Darley-Usmar, and H.J. Forman Human glutamate cysteine ligase gene regulation through the electrophile response element Free Radic. Biol. Med. 37 2004 1152 1159
30. S.C. Lu Regulation of glutathione synthesis Mol. Aspects Med. 30 2009 42 59
31. H.J. Forman, D.A. Dickinson, and K.E. Iles HNE-signaling pathways leading to its elimination Mol. Aspects Med. 24 2003 189 194
32. R.M. Liu, L. Gao, J. Choi, and H.J. Forman gamma-Glutamylcysteine synthetase: mRNA stabilization and independent subunit transcription by 4-hydroxy-2-nonenal Am. J. Physiol. 275 1998 L861 L869
33. R.M. Liu, Z. Borok, and H.J. Forman 4-Hydroxy-2-nonenal increases gamma-glutamylcysteine synthetase gene expression in alveolar epithelial cells Am. J. Respir. Cell Mol. Biol. 24 2001 499 505
34. D.A. Dickinson, K.E. Iles, N. Watanabe, T. Iwamoto, H. Zhang, D.M. Krzywanski, and H.J. Forman 4-Hydroxynonenal induces glutamate cysteine ligase through JNK in HBE1 cells Free Radic. Biol. Med. 33 2002 974
35. D.M. Krzywanski, D.A. Dickinson, K.E. Iles, A.F. Wigley, C.C. Franklin, R.M. Liu, T.J. Kavanagh, and H.J. Forman Variable regulation of glutamate cysteine ligase subunit proteins affects glutathione biosynthesis in response to oxidative stress Arch. Biochem. Biophys. 423 2004 116 125
36. K.E. Iles, and R.M. Liu Mechanisms of glutamate cysteine ligase (GCL) induction by 4-hydroxynonenal Free Radic. Biol. Med. 38 2005 547 556
37. C.C. Franklin, D.S. Backos, I. Mohar, C.C. White, H.J. Forman, and T.J. Kavanagh Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase Mol. Aspects Med. 30 2009 86 98
38. T. Ochi Hydrogen peroxide increases the activity of gamma- glutamylcysteine synthetase in cultured Chinese hamster V79 cells Arch. Toxicol. 70 1995 96 103
39. T. Ochi Menadione causes increases in the level of glutathione and in the activity of gamma-glutamylcysteine synthetase in cultured Chinese hamster V79 cells Toxicology 112 1996 45 55
40. D. Toroser, C.S. Yarian, W.C. Orr, and R.S. Sohal Mechanisms of gamma-glutamylcysteine ligase regulation Biochim. Biophys. Acta 1760 2006 233 244
41. Z. Tu, and M.W. Anders Identification of an important cysteine residue in human glutamate-cysteine ligase catalytic subunit by site-directed mutagenesis Biochem. J. 336 1998 675 680
42. L.S. Chang The functional involvement of Lys-38 in the heavy subunit of rat kidney gamma-glutamylcysteine synthetase: chemical modification and mutagenesis studies J. Protein Chem. 15 1996 321 326
43. G.F. Seelig, R.P. Simondsen, and A. Meister Reversible dissociation of γ-glutamylcysteine synthetase into two subunits J. Biol. Chem. 259 1984 9345 9347
44. C.M. Krejsa, C.C. Franklin, C.C. White, J.A. Ledbetter, G.L. Schieven, and T.J. Kavanagh Rapid activation of glutamate cysteine ligase following oxidative stress J. Biol. Chem. 285 2010 16116 16124
45. C.S. Huang, W.R. Moore, and A. Meister On the active site thiol of gamma-glutamylcysteine synthetase: relationships to catalysis, inhibition, and regulation Proc. Natl Acad. Sci. USA 85 1988 2464 2468
46. W.-M. Sun, Z.-Z. Huang, and S.C. Lu Regulation of γ- glutamylcysteine synthetase by protein phosphorylation Biochem. J. 320 1996 321 328
47. C.C. Franklin, C.M. Krejsa, R.H. Pierce, C.C. White, N. Fausto, and T.J. Kavanagh Caspase-3-dependent cleavage of the glutamate-l-cysteine ligase catalytic subunit during apoptotic cell death Am. J. Pathol. 160 2002 1887 1894
48. D.P. Hartley, D.J. Kroll, and D.R. Petersen Prooxidant-initiated lipid peroxidation in isolated rat hepatocytes: detection of 4-hydroxynonenal- and malondialdehyde-protein adducts Chem. Res. Toxicol. 10 1997 895 905
49. D.S. Backos, C.N. Brocker, and C.C. Franklin Manipulation of cellular GSH biosynthetic capacity via TAT-mediated protein transduction of wild-type or a dominant-negative mutant of glutamate cysteine ligase alters cell sensitivity to oxidant-induced cytotoxicity Toxicol. Appl. Pharmacol. 243 2010 35 45
50. C.C. White, H. Viernes, C.M. Krejsa, D. Botta, and T.J. Kavanagh Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity Anal. Biochem. 318 2003 175 180
51. U. Pieper, N. Eswar, H. Braberg, M.S. Madhusudhan, F.P. Davis, A.C. Stuart, N. Mirkovic, A. Rossi, M.A. Marti-Renom, A. Fiser, B. Webb, D. Greenblatt, C.C. Huang, T.E. Ferrin, and A. Sali MODBASE, a database of annotated comparative protein structure models, and associated resources Nucleic Acids Res. 32 2004 D217 D222
52. A. Pedretti, L. Villa, and G. Vistoli VEGA-an open platform to develop chemo-bio-informatics applications, using plug-in architecture and script programming J. Comput.-Aided Mol. Des. 18 2004 167 173
53. H. Li, A.D. Robertson, and J.H. Jensen Very fast empirical prediction and rationalization of protein pKa values Proteins 61 2005 704 721 (Pubitemid 41753142)
54. G. Ausiello, G. Cesareni, and M. Helmer-Citterich ESCHER: a new docking procedure applied to the reconstruction of protein tertiary structure Proteins 28 1997 556 567
55. S. Ray, N.L. Misso, J.C. Lenzo, C. Robinson, and P.J. Thompson γ-Glutamylcysteine synthetase activity in human lung epithelial (A549) cells: factors influencing its measurement Free Radic. Biol. Med. 27 1999 1346 1356
56. G. Poli, R.J. Schaur, W.G. Siems, and G. Leonarduzzi 4-Hydroxynonenal: a membrane lipid oxidation product of medicinal interest Med. Res. Rev. 28 2008 569 631
57. D.V. Nadkarni, and L.M. Sayre Structural definition of early lysine and histidine adduction chemistry of 4-hydroxynonenal Chem. Res. Toxicol. 8 1995 284 291
58. E.I. Biterova, and J.J. Barycki Mechanistic details of glutathione biosynthesis revealed by crystal structures of Saccharomyces cerevisiae glutamate cysteine ligase J. Biol. Chem. 284 2009 32700 32708
59. J.A. Fraser, R.D. Saunders, and L.I. McLellan Drosophila melanogaster glutamate-cysteine ligase activity is regulated by a modifier subunit with a mechanism of action similar to that of the mammalian form J. Biol. Chem. 277 2002 1158 1165
60. W.A. Solis, T.P. Dalton, M.Z. Dieter, S. Freshwater, J.M. Harrer, L. He, H.G. Shertzer, and D.W. Nebert Glutamate-cysteine ligase modifier subunit: mouse Gclm gene structure and regulation by agents that cause oxidative stress Biochem. Pharmacol. 63 2002 1739 1754
61. M.M. Shi, T. Iwamoto, and H.J. Forman gamma-Glutamylcysteine synthetase and GSH increase in quinone-induced oxidative stress in BPAEC Am. J. Physiol. 267 1994 L414 L421
62. R.M. Liu, L. Gao, J. Choi, and H.J. Forman γ-Glutamylcysteine synthetase: mRNA stabilization and independent subunit transcription by 4-hydroxy-2-nonenal Am. J. Physiol. 275 1998 L861 L869
63. D.L. Carbone, J.A. Doorn, Z. Kiebler, B.P. Sampey, and D.R. Petersen Inhibition of Hsp72-mediated protein refolding by 4-hydroxy-2-nonenal Chem. Res. Toxicol. 17 2004 1459 1467
64. C.S. Huang, L.S. Chang, M.E. Anderson, and A. Meister Catalytic and regulatory properties of the heavy subunit of rat kidney gamma-glutamylcysteine synthetase J. Biol. Chem. 268 1993 19675 19680
65. J.I. Lee, J. Kang, and M.H. Stipanuk Differential regulation of glutamate-cysteine ligase subunit expression and increased holoenzyme formation in response to cysteine deprivation Biochem. J. 393 2006 181 190