Interactions of glutathione transferases with 4-hydroxynonenal

References

• Adman, E. T., Le Trong, I., Stenkamp, R. E., Nieslanik, B. S., Dietze, E. C., Tai, G., et al. (2001). Localization of the C-terminus of rat glutathione S-transferase A1-1: crystal structure of mutants W21F and W21F/F220Y. Proteins 42:192–200.
   PubMed Web of Science ®Google Scholar
• Alary, J., Debrauwer, L., Fernandez, Y., Cravedi, J. P., Rao, D., Bories, G. (1998). 1,4-dihydroxynonene mercapturic acid, the major end metabolite of exogenous 4-hydroxy-2-nonenal, is a physiological component of rat and human urine. Chem Res Toxicol 11:130–135.
   PubMed Web of Science ®Google Scholar
• Alary, J., Gueraud, F., Cravedi, J. P. (2003). Fate of 4-hydroxynonenal in vivo: disposition and metabolic pathways. Mol Aspects Med, 24:177–187.
   PubMedGoogle Scholar
• Aldini, G., Gamberoni, L., Orioli, M., Beretta, G., Regazzoni, L., Maffei Facino, R., et al. (2006). Mass spectrometric characterization of covalent modification of human serum albumin by 4-hydroxy-trans-2-nonenal. J Mass Spectrom, 41:1149–1161.
   PubMed Web of Science ®Google Scholar
• Alin, P., Danielson, U. H., Mannervik, B. (1985). 4-hydroxyalk-2-enals are substrates for glutathione transferase. FEBS Lett 179:267–270.
   PubMed Web of Science ®Google Scholar
• Amunom, I., Stephens, L. J., Tamasi, V., Cai, J., Pierce, W. M., Jr., Conklin, D. J., et al. (2007). Cytochromes P450 catalyze oxidation of alpha,beta-unsaturated aldehydes. Arch Biochem Biophys, 464:187–196.
   PubMed Web of Science ®Google Scholar
• Armstrong, R. N. (1997). Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem Res Toxicol 10:2–18.
   PubMed Web of Science ®Google Scholar
• Awasthi, S., Singhal, S. S., Yadav, S., Singhal, J., Drake, K., Nadkar, A., et al. (2005a). RLIP76 is a major determinant of radiation sensitivity. Cancer Res, 65:6022–6028.
   PubMed Web of Science ®Google Scholar
• Awasthi, Y. C., Yang, Y., Tiwari, N. K., Patrick, B., Sharma, A., Li, J., et al. (2004). Regulation of 4-hydroxynonenal-mediated signaling by glutathione S-transferases. Free Radic Biol Med, 37:607–619.
   PubMed Web of Science ®Google Scholar
• Ayyadevara, S., Dandapat, A., Singh, S. P., Benes, H., Zimniak, L., Shmookler Reis, R. J., et al. (2005a). Lifespan extension in hypomorphic daf-2 mutants of Caenorhabditis elegans is partially mediated by glutathione transferase CeGSTP2-2. Aging Cell, 4:299–307.
   PubMed Web of Science ®Google Scholar
• Ayyadevara, S., Dandapat, A., Singh, S. P., Siegel, E. R., Shmookler Reis, R. J., Zimniak, L., et al. (2007). Life span and stress resistance of Caenorhabditis elegans are differentially affected by glutathione transferases metabolizing 4-hydroxynon-2- enal. Mech Ageing Dev, 128:196–205.
   PubMed Web of Science ®Google Scholar
• Ayyadevara, S., Engle, M. R., Singh, S. P., Dandapat, A., Lichti, C. F., Benes, H., et al. (2005b). Lifespan and stress resistance of Caenorhabditis elegans are increased by expression of glutathione transferases capable of metabolizing the lipid peroxidation product 4- hydroxynonenal. Aging Cell, 4:257–271.
   PubMed Web of Science ®Google Scholar
• Babbitt, P. C. (2000). Reengineering the glutathione S-transferase scaffold: a rational design strategy pays off. Proc Natl Acad Sci U S A, 97:10298–10300.
   PubMed Web of Science ®Google Scholar
• Awasthi, Y. C., Ansari, G. A., Awasthi, S. (2005). Regulation of 4-hydroxynonenal mediated signaling by glutathione S-transferases. Meth Enzymol 401:379–407.
   PubMed Web of Science ®Google Scholar
• Balchin, D., Fanucchi, S., Achilonu, I., Adamson, R. J., Burke, J., Fernandes, M., et al. (2010). Stability of the domain interface contributes towards the catalytic function at the H-site of class alpha glutathione transferase A1-1. Biochim Biophys Acta 1804:2228–2233.
   Google Scholar
• Balogh, L. M., Le Trong, I., Kripps, K. A., Shireman, L. M., Stenkamp, R. E., Zhang, W., et al. (2010). Substrate specificity combined with stereopromiscuity in glutathione transferase A4-4-dependent metabolism of 4-hydroxynonenal. Biochemistry 49:1541–1548.
   PubMed Web of Science ®Google Scholar
• Balogh, L. M., Le Trong, I., Kripps, K. A., Tars, K., Stenkamp, R. E., Mannervik, B., et al. (2009). Structural analysis of a glutathione transferase A1-1 mutant tailored for high catalytic efficiency with toxic alkenals. Biochemistry, 48:7698–7704.
   PubMed Web of Science ®Google Scholar
• Balogh, L. M., Roberts, A. G., Shireman, L. M., Greene, R. J., Atkins, W. M. (2008). The stereochemical course of 4-hydroxy-2-nonenal metabolism by glutathione S-transferases. J Biol Chem 283:16702–16710.
   PubMed Web of Science ®Google Scholar
• Benedetti, A., Comporti, M., Esterbauer, H. (1980). Identification of 4-hydroxynonenal as a cytotoxic product originating from the peroxidation of liver microsomal lipids. Biochim Biophys Acta 620:281–296.
   PubMed Web of Science ®Google Scholar
• Bjornestedt, R., Stenberg, G., Widersten, M., Board, P. G., Sinning, I., Jones, T. A., et al. (1995). Functional significance of arginine 15 in the active site of human class alpha glutathione transferase A1-1. J Mol Biol 247:765–773.
   PubMed Web of Science ®Google Scholar
• Bjornestedt, R., Tardioli, S., Mannervik, B. (1995b). The high activity of rat glutathione transferase 8-8 with alkene substrates is dependent on a glycine residue in the active site. J Biol Chem, 270:29705–29709.
   PubMed Web of Science ®Google Scholar
• Blikstad, C., Shokeer, A., Kurtovic, S., Mannervik, B. (2008). Emergence of a novel highly specific and catalytically efficient enzyme from a naturally promiscuous glutathione transferase. Biochim Biophys Acta, 1780:1458–1463.
   PubMed Web of Science ®Google Scholar
• Board, P. G. (1998). Identification of cDNAs encoding two human alpha class glutathione transferases (GSTA3 and GSTA4) and the heterologous expression of GSTA4-4. Biochem J 330:827–831.
   PubMed Web of Science ®Google Scholar
• Bogaards, J. J., Venekamp, J. C., van Bladeren, P. J. (1997). Stereoselective conjugation of prostaglandin A2 and prostaglandin J2 with glutathione, catalyzed by the human glutathione S-transferases A1-1, A2-2, M1a-1a, and P1-1. Chem Res Toxicol 10:310–317.
   PubMed Web of Science ®Google Scholar
• Bolgar, M. S., Yang, C. Y., Gaskell, S. J. (1996). First direct evidence for lipid/protein conjugation in oxidized human low density lipoprotein. J Biol Chem 271:27999–28001.
   PubMed Web of Science ®Google Scholar
• Boon, P. J., Marinho, H. S., Oosting, R., Mulder, G. J. (1999). Glutathione conjugation of 4-hydroxy-trans-2,3-nonenal in the rat in vivo, the isolated perfused liver, and erythrocytes. Toxicol Appl Pharmacol 159:214–223.
   PubMed Web of Science ®Google Scholar
• Bull, A. W., Seeley, S. K., Geno, J., Mannervik, B. (2002). Conjugation of the linoleic acid oxidation product, 13-oxooctadeca-9,11-dienoic acid, a bioactive endogenous substrate for mammalian glutathione transferase. Biochim Biophys Acta 1571:77–82.
   PubMed Web of Science ®Google Scholar
• Butterfield, D. A., Bader Lange, M. L., Sultana, R. (2010a). Involvements of the lipid peroxidation product, HNE, in the pathogenesis and progression of Alzheimer’s disease. Biochim Biophys Acta, 1801:924–929.
   PubMed Web of Science ®Google Scholar
• Butterfield, D. A., Hardas, S. S., Lange, M. L. (2010). Oxidatively modified glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and Alzheimer’s disease: many pathways to neurodegeneration. J Alzheimers Dis 20:369–393.
   PubMed Web of Science ®Google Scholar
• Butterfield, D. A., Reed, T., Perluigi, M., De Marco, C., Coccia, R., Cini, C., et al. (2006). Elevated protein-bound levels of the lipid peroxidation product, 4-hydroxy-2-nonenal, in brain from persons with mild cognitive impairment. Neurosci Lett, 397:170–173.
   PubMed Web of Science ®Google Scholar
• Cameron, A. D., Sinning, I., L’Hermite, G., Olin, B., Board, P. G., Mannervik, B., et al. (1995). Structural analysis of human alpha-class glutathione transferase A1-1 in the apo-form and in complexes with ethacrynic acid and its glutathione conjugate. Structure 3:717–727.
   PubMed Web of Science ®Google Scholar
• Carini, M., Aldini, G., Facino, R. M. (2004). Mass spectrometry for detection of 4-hydroxy-trans- 2-nonenal (HNE) adducts with peptides and proteins. Mass Spectrom Rev, 23:281–305.
   PubMed Web of Science ®Google Scholar
• Cenini, G., Sultana, R., Memo, M., Butterfield, D. A. (2008). Elevated levels of pro-apoptotic p53 and its oxidative modification by the lipid peroxidation product, HNE, in brain from subjects with amnestic mild cognitive impairment and Alzheimer’s disease. J Cell Mol Med, 12:987–994.
   PubMed Web of Science ®Google Scholar
• Cheng, J. Z., Sharma, R., Yang, Y., Singhal, S. S., Sharma, A., Saini, M. K., et al. (2001). Accelerated metabolism and exclusion of 4-hydroxynonenal through induction of RLIP76 and hGST5.8 is an early adaptive response of cells to heat and oxidative stress. J Biol Chem 276:41213–41223.
   PubMed Web of Science ®Google Scholar
• Cheng, J. Z., Yang, Y., Singh, S. P., Singhal, S. S., Awasthi, S., Pan, S. S., et al. (2001b). Two distinct 4-hydroxynonenal metabolizing glutathione S-transferase isozymes are differentially expressed in human tissues. Biochem Biophys Res Commun, 282:1268- 1274.
   PubMed Web of Science ®Google Scholar
• Codreanu, S. G., Zhang, B., Sobecki, S. M., Billheimer, D. D., Liebler, D. C. (2009). Global analysis of protein damage by the lipid electrophile 4-hydroxy-2-nonenal. Mol Cell Proteomics 8:670–680.
   PubMed Web of Science ®Google Scholar
• Coles, B. F., Kadlubar, F. F. (2005). Human alpha class glutathione S-transferases: genetic polymorphism, expression, and susceptibility to disease. Methods Enzymol, 401:9–42.
   PubMed Web of Science ®Google Scholar
• Curtis, J. M., Grimsrud, P. A., Wright, W. S., Xu, X., Foncea, R. E., Graham, D. W., et al. (2010). Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress, and mitochondrial dysfunction. Diabetes, 59:1132–1142.
   PubMed Web of Science ®Google Scholar
• Danielson, U. H., Esterbauer, H., Mannervik, B. (1987). Structure-activity relationships of 4-hydroxyalkenals in the conjugation catalysed by mammalian glutathione transferases. Biochem J 247:707–713.
   PubMed Web of Science ®Google Scholar
• Dirr, H., Reinemer, P., Huber, R. (1994). X-ray crystal structures of cytosolic glutathione S-transferases. Implications for protein architecture, substrate recognition, and catalytic function. Eur J Biochem 220:645–661.
   PubMedGoogle Scholar
• Dirr, H. W., Little, T., Kuhnert, D. C., Sayed, Y. (2005). A conserved N-capping motif contributes significantly to the stabilization and dynamics of the C-terminal region of class alpha glutathione S-transferases. J Biol Chem 280:19480–19487.
   PubMed Web of Science ®Google Scholar
• Dirr, H. W., Wallace, L. A. (1999). Role of the C-terminal helix 9 in the stability and ligandin function of class alpha glutathione transferase A1-1. Biochemistry 38:15631–15640.
   PubMed Web of Science ®Google Scholar
• Dourado, D. F., Fernandes, P. A., Mannervik, B., Ramos, M. J. (2010). Glutathione transferase A1-1: catalytic importance of arginine 15. J Phys Chem B 114:1690–1697.
   PubMed Web of Science ®Google Scholar
• Dourado, D. F., Fernandes, P. A., Ramos, M. J. (2008). Mammalian cytosolic glutathione transferases. Curr Prot Pept Sci 9:325–337.
   PubMed Web of Science ®Google Scholar
• Eaton, D. L., Bammler, T. K. (1999). Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol Sci 49;156–164.
   PubMed Web of Science ®Google Scholar
• Engle, M. R., Singh, S. P., Czernik, P. J., Gaddy, D., Montague, D. C., Ceci, J. D., et al. (2004). Physiological role of mGSTA4-4, a glutathione S-transferase metabolizing 4- hydroxynonenal: generation and analysis of mGsta4 null mouse. Toxicol Appl Pharmacol, 194:296–308.
   PubMed Web of Science ®Google Scholar
• Esterbauer, H., Schaur, R. J., Zollner, H. (1991). Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde, and related aldehydes. Free Radic Biol Med 11:81–128.
   PubMed Web of Science ®Google Scholar
• Esterbauer, H., Zollner, H., Scholz, N. (1975). Reaction of glutathione with conjugated carbonyls. Z Naturforsch [C] 30:466–473.
   PubMed Web of Science ®Google Scholar
• Gallagher, E. P., Huisden, C. M., Gardner, J. L. (2007). Transfection of HepG2 cells with hGSTA4 provides protection against 4-hydroxynonenal-mediated oxidative injury. Toxicol In Vitro, 21:1365–1372.
   PubMed Web of Science ®Google Scholar
• Gildenhuys, S., Dobreva, M., Kinsley, N., Sayed, Y., Burke, J., Pelly, S., et al. (2010). Arginine 15 stabilizes an S(N)Ar reaction transition state and the binding of anionic ligands at the active site of human glutathione transferase A1-1. Biophys Chem 146:118–125.
   PubMed Web of Science ®Google Scholar
• Grahn, E., Novotny, M., Jakobsson, E., Gustafsson, A., Grehn, L., Olin, B., et al. (2006). New crystal structures of human glutathione transferase A1-1 shed light on glutathione binding and the conformation of the C-terminal helix. Acta Crystallogr D Biol Crystallogr 62:197–207.
   PubMed Web of Science ®Google Scholar
• Grimsrud, P. A., Picklo, M. J., Sr., Griffin, T. J., Bernlohr, D. A. (2007). Carbonylation of adipose proteins in obesity and insulin resistance: identification of adipocyte fatty acid-binding protein as a cellular target of 4-hydroxynonenal. Mol Cell Proteomics 6:624–637.
   PubMed Web of Science ®Google Scholar
• Gustafsson, A., Etahadieh, M., Jemth, P., Mannervik, B. (1999). The C-terminal region of human glutathione transferase A1-1 affects the rate of glutathione binding and the ionization of the active-site Tyr9. Biochemistry 38:16268–16275.
   PubMed Web of Science ®Google Scholar
• Hardwick, R. N., Fisher, C. D., Canet, M. J., Lake, A. D., Cherrington, N. J. (2010). Diversity in antioxidant response enzymes in progressive stages of human non-alcoholic fatty liver disease. Drug Metab Dispos 38:2293–2301.
   PubMed Web of Science ®Google Scholar
• Hashimoto, M., Sibata, T., Wasada, H., Toyokuni, S., Uchida, K. (2003). Structural basis of protein-bound endogenous aldehydes. Chemical and immunochemical characterizations of configurational isomers of a 4-hydroxy-2-nonenal-histidine adduct. J Biol Chem 278:5044–5051.
   PubMed Web of Science ®Google Scholar
• Hayes, J. D., Flanagan, J. U., Jowsey, I. R. (2005). Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88.
   PubMed Web of Science ®Google Scholar
• Hayes, J. D., McLellan, L. I. (1999). Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res 31:273–300.
   PubMed Web of Science ®Google Scholar
• Hiratsuka, A., Hirose, K., Saito, H., Watabe, T. (2000). 4-hydroxy-2(E)-nonenal enantiomers: (S)-selective inactivation of glyceraldehyde-3-phosphate dehydrogenase and detoxification by rat glutathione S-transferase A4-4. Biochem J 349:729–735.
   PubMed Web of Science ®Google Scholar
• Hou, L., Honaker, M. T., Shireman, L. M., Balogh, L. M., Roberts, A. G., Ng, K. C., et al. (2007). Functional promiscuity correlates with conformational heterogeneity in A-class glutathione S-transferases. J Biol Chem 282:23264–23274.
   PubMed Web of Science ®Google Scholar
• Hu, W., Feng, Z., Eveleigh, J., Iyer, G., Pan, J., Amin, S., et al. (2002). The major lipid peroxidation product, trans-4-hydroxy-2-nonenal, preferentially forms DNA adducts at codon 249 of human p53 gene, a unique mutational hotspot in hepatocellular carcinoma. Carcinogenesis, 23:1781–1789.
   PubMed Web of Science ®Google Scholar
• Huang, H., Wang, H., Qi, N., Lloyd, R. S., Rizzo, C. J., Stone, M. P. (2008). The stereochemistry of trans-4-hydroxynonenal-derived exocyclic 1,N2-2’-deoxyguanosine adducts modulates formation of interstrand cross-links in the 5′-CpG-3′ sequence. Biochemistry 47:11457–11472.
   PubMed Web of Science ®Google Scholar
• Hubatsch, I., Mannervik, B. (2001). A highly acidic tyrosine 9 and a normally titrating tyrosine 212 contribute to the catalytic mechanism of human glutathione transferase A4-4. Biochem Biophys Res Commun 280:878–882.
   PubMed Web of Science ®Google Scholar
• Hubatsch, I., Ridderstrom, M., Mannervik, B. (1998). Human glutathione transferase A4-4: an alpha class enzyme with high catalytic efficiency in the conjugation of 4-hydroxynonenal and other genotoxic products of lipid peroxidation. Biochem J 330:175–179.
   PubMed Web of Science ®Google Scholar
• Ibarra, C., Nieslanik, B. S., Atkins, W. M. (2001). Contribution of aromatic-aromatic interactions to the anomalous pK(a) of tyrosine-9 and the C-terminal dynamics of glutathione S-transferase A1-1. Biochemistry 40:10614–10624.
   PubMed Web of Science ®Google Scholar
• Jacobs, A. T., Marnett, L. J. (2010). Systems analysis of protein modification and cellular responses induced by electrophile stress. Acc Chem Res, 43:673–683.
   PubMed Web of Science ®Google Scholar
• Ji, B., Ito, K., Suzuki, H., Sugiyama, Y., Horie, T. (2002). Multidrug resistance-associated protein2 (MRP2) plays an important role in the biliary excretion of glutathione conjugates of 4-hydroxynonenal. Free Radic Biol Med 33:370–378.
   PubMed Web of Science ®Google Scholar
• Kuhnert, D. C., Sayed, Y., Mosebi, S., Sayed, M., Sewell, T., Dirr, H. W. (2005). Tertiary interactions stabilise the C-terminal region of human glutathione transferase A1-1: a crystallographic and calorimetric study. J Mol Biol 349:825–838.
   PubMed Web of Science ®Google Scholar
• Le Trong, I., Stenkamp, R. E., Ibarra, C., Atkins, W. M., Adman, E. T. (2002). 1.3-A resolution structure of human glutathione S-transferase with S-hexyl glutathione bound reveals possible extended ligandin binding site. Proteins 48:618–627.
   PubMed Web of Science ®Google Scholar
• Leitinger, N. (2003). Cholesteryl ester oxidation products in atherosclerosis. Mol Aspects Med, 24:239–250.
   PubMedGoogle Scholar
• Levonen, A. L., Landar, A., Ramachandran, A., Ceaser, E. K., Dickinson, D. A., Zanoni, G., et al. (2004). Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem J, 378:373–382.
   PubMed Web of Science ®Google Scholar
• Liu, L., Komatsu, H., Murray, I. V., Axelsen, P. H. (2008). Promotion of amyloid beta protein misfolding and fibrillogenesis by a lipid oxidation product. J Mol Biol, 377:1236–1250.
   PubMed Web of Science ®Google Scholar
• Liu, S., Stoesz, S. P., Pickett, C. B. (1998). Identification of a novel human glutathione S-transferase using bioinformatics. Arch Biochem Biophys 352:306–313.
   PubMed Web of Science ®Google Scholar
• Lopachin, R. M., Barber, D. S.Gavin, T. (2008). Molecular mechanisms of the conjugated alpha,beta-unsaturated carbonyl derivatives: relevance to neurotoxicity and neurodegenerative diseases. Toxicol Sci, 104:235–249.
   PubMed Web of Science ®Google Scholar
• Lovell, M. A., Xie, C., Markesbery, W. R. (1998). Decreased glutathione transferase activity in brain and ventricular fluid in Alzheimer’s disease. Neurology 51:1562–1566.
   PubMed Web of Science ®Google Scholar
• McElwee, J. J., Schuster, E., Blanc, E., Piper, M. D., Thomas, J. H., Patel, D. S., et al. (2007). Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biol, 8:R132.
   PubMed Web of Science ®Google Scholar
• McElwee, J. J., Schuster, E., Blanc, E., Thomas, J. H., Gems, D. (2004). Shared transcriptional signature in Caenorhabditis elegans Dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance. J Biol Chem, 279:44533–44543.
   PubMed Web of Science ®Google Scholar
• Miller, B. G., Wolfenden, R. (2002). Catalytic proficiency: the unusual case of OMP decarboxylase. Annu Rev Biochem 71:847–885.
   PubMed Web of Science ®Google Scholar
• Mitchell, A. E., Morin, D., Lame, M. W., Jones, A. D. (1995). Purification, mass spectrometric characterization, and covalent modification of murine glutathione S-transferases. Chem Res Toxicol, 8:1054–1062.
   PubMed Web of Science ®Google Scholar
• Morel, F., Rauch, C., Coles, B., Le Ferrec, E., Guillouzo, A. (2002). The human glutathione transferase alpha locus: genomic organization of the gene cluster and functional characterization of the genetic polymorphism in the hGSTA1 promoter. Pharmacogenetics, 12:277–286.
   PubMedGoogle Scholar
• Mosebi, S., Sayed, Y., Burke, J., Dirr, H. W. (2003). Residue 219 impacts on the dynamics of the C-terminal region in glutathione transferase A1-1: implications for stability and catalytic and ligandin functions. Biochemistry 42:15326–15332.
   PubMed Web of Science ®Google Scholar
• Nair, U., Bartsch, H., Nair, J. (2007). Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans. Free Radic Biol Med, 43:1109–1120.
   PubMed Web of Science ®Google Scholar
• Nieslanik, B. S., Atkins, W. M. (2000). The catalytic Tyr-9 of glutathione S-transferase A1-1 controls the dynamics of the C terminus. J Biol Chem 275:17447–17451.
   PubMed Web of Science ®Google Scholar
• Nieslanik, B. S., Dabrowski, M. J., Lyon, R. P., Atkins, W. M. (1999). Stopped-flow kinetic analysis of the ligand-induced coil-helix transition in glutathione S-transferase A1-1: evidence for a persistent denatured state. Biochemistry 38:6971–6980.
   PubMed Web of Science ®Google Scholar
• Nieslanik, B. S., Ibarra, C., Atkins, W. M. (2001). The C-terminus of glutathione S-transferase A1-1 is required for entropically-driven ligand binding. Biochemistry 40:3536–3543.
   PubMed Web of Science ®Google Scholar
• Nilsson, L. O., Edalat, M., Pettersson, P. L., Mannervik, B. (2002). Aromatic residues in the C-terminal region of glutathione transferase A1-1 influence rate-determining steps in the catalytic mechanism. Biochim Biophys Acta 1598:199–205.
   PubMed Web of Science ®Google Scholar
• Nilsson, L. O., Gustafsson, A., Mannervik, B. (2000). Redesign of substrate-selectivity determining modules of glutathione transferase A1-1 installs high catalytic efficiency with toxic alkenal products of lipid peroxidation. Proc Natl Acad Sci U S A 97:9408–9412.
   PubMed Web of Science ®Google Scholar
• Oakley, A. J., Rossjohn, J., Lo Bello, M., Caccuri, A. M., Federici, G., Parker, M. W. (1997). The three-dimensional structure of the human pi class glutathione transferase P1-1 in complex with the inhibitor ethacrynic acid and its glutathione conjugate. Biochemistry 36:576–585.
   PubMed Web of Science ®Google Scholar
• Petersen, D. R., Doorn, J. A. (2004). Reactions of 4-hydroxynonenal with proteins and cellular targets. Free Radic Biol Med 37:937–945.
   PubMed Web of Science ®Google Scholar
• Qin, Z., Hu, D., Han, S., Reaney, S. H., Di Monte, D. A., Fink, A. L. (2007). Effect of 4-hydroxy-2-nonenal modification on alpha-synuclein aggregation. J Biol Chem 282:5862–5870.
   PubMed Web of Science ®Google Scholar
• Ramana, K. V., Bhatnagar, A., Srivastava, S., Yadav, U. C., Awasthi, S., Awasthi, Y. C., et al. (2006). Mitogenic responses of vascular smooth muscle cells to lipid peroxidationderived aldehyde 4-hydroxy-trans-2-nonenal (HNE): role of aldose reductase-catalyzed reduction of the HNE-glutathione conjugates in regulating cell growth. J Biol Chem, 281:17652–17660.
   PubMed Web of Science ®Google Scholar
• Raza, H., John, A. (2006). 4-hydroxynonenal induces mitochondrial oxidative stress, apoptosis and expression of glutathione S-transferase A4-4 and cytochrome P450 2E1 in PC12 cells. Toxicol Appl Pharmacol, 216:309–318.
   PubMed Web of Science ®Google Scholar
• Reed, T. T., Pierce, W. M., Markesbery, W. R., Butterfield, D. A. (2009). Proteomic identification of HNE-bound proteins in early Alzheimer disease: Insights into the role of lipid peroxidation in the progression of AD. Brain Res, 1274:66–76.
   PubMed Web of Science ®Google Scholar
• Renes, J., De Vries, E. E., Hooiveld, G. J., Krikken, I., Jansen, P. L., Muller, M. (2000). Multidrug resistance protein MRP1 protects against the toxicity of the major lipid peroxidation product 4-hydroxynonenal. Biochem J, 350 Pt 2:555–561.
   PubMed Web of Science ®Google Scholar
• Selley, M. L. (1998). (E)-4-hydroxy-2-nonenal may be involved in the pathogenesis of Parkinson’s disease. Free Radic Biol Med, 25:169–174.
   PubMed Web of Science ®Google Scholar
• Sharma, R., Awasthi, S., Zimniak, P., Awasthi, Y. C. (2000). Transport of glutathione-conjugates in human erythrocytes. Acta Biochim Pol, 47:751–762.
   PubMed Web of Science ®Google Scholar
• Sharma, R., Yang, Y., Sharma, A., Awasthi, S., Awasthi, Y. C. (2004). Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stressmediated apoptosis. Antioxid Redox Signal, 6:289–300.
   PubMed Web of Science ®Google Scholar
• Sheehan, D., Meade, G., Foley, V. M., Dowd, C. A. (2001). Structure, function, and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16.
   PubMed Web of Science ®Google Scholar
• Shireman, L. M., Kripps, K. A., Balogh, L. M., Conner, K. P., Whittington, D., Atkins, W. M. (2010). Glutathione transferase A4-4 resists adduction by 4-hydroxynonenal. Arch Biochem Biophys 504:182–189.
   PubMed Web of Science ®Google Scholar
• Siegel, S. J., Bieschke, J., Powers, E. T., Kelly, J. W. (2007). The oxidative stress metabolite 4- hydroxynonenal promotes Alzheimer protofibril formation. Biochemistry, 46:1503–1510.
   PubMed Web of Science ®Google Scholar
• Singh, S. P., Niemczyk, M., Saini, D., Awasthi, Y. C., Zimniak, L., Zimniak, P. (2008). Role of the electrophilic lipid peroxidation product 4-hydroxynonenal in the development and maintenance of obesity in mice. Biochemistry, 47:3900–3911.
   PubMed Web of Science ®Google Scholar
• Singh, S. P., Niemczyk, M., Saini, D., Sadovov, V., Zimniak, L., Zimniak, P. (2010). Disruption of the mGsta4 gene increases life span of C57BL mice. J Gerontol A Biol Sci Med Sci 65:14–23.
   Google Scholar
• Singhal, J., Singhal, S. S., Yadav, S., Suzuki, S., Warnke, M. M., Yacoub, A., et al. (2008). RLIP76 in defense of radiation poisoning. Int J Radiat Oncol Biol Phys, 72:553–561.
   PubMed Web of Science ®Google Scholar
• Singhal, S. S., Zimniak, P., Awasthi, S., Piper, J. T., He, N. G., Teng, J. I., et al. (1994). Several closely related glutathione S-transferase isozymes catalyzing conjugation of 4- hydroxynonenal are differentially expressed in human tissues. Arch Biochem Biophys, 311:242–250.
   PubMed Web of Science ®Google Scholar
• Sinning, I., Kleywegt, G. J., Cowan, S. W., Reinemer, P., Dirr, H. W., Huber, R., et al. (1993). Structure determination and refinement of human alpha class glutathione transferase A1-1, and a comparison with the mu and pi class enzymes. J Mol Biol 232:192–212.
   PubMed Web of Science ®Google Scholar
• Stenberg, G., Ridderstrom, M., Engstrom, A., Pemble, S. E., Mannervik, B. (1992). Cloning and heterologous expression of cDNA encoding class alpha rat glutathione transferase 8-8, an enzyme with high catalytic activity towards genotoxic alpha,beta-unsaturated carbonyl compounds. Biochem J 284(Pt 2):313–319.
   PubMed Web of Science ®Google Scholar
• Straus, D. S., Glass, C. K. (2001). Cyclopentenone prostaglandins: new insights on biological activities and cellular targets. Med Res Rev 21:185–210.
   PubMed Web of Science ®Google Scholar
• Sultana, R., Butterfield, D. A. (2004). Oxidatively modified GST and MRP1 in Alzheimer’s disease brain: implications for accumulation of reactive lipid peroxidation products. Neurochem Res 29:2215–2220.
   PubMed Web of Science ®Google Scholar
• Szapacs, M. E., Riggins, J. N., Zimmerman, L. J., Liebler, D. C. (2006). Covalent adduction of human serum albumin by 4-hydroxy-2-nonenal: kinetic analysis of competing alkylation reactions. Biochemistry, 45:10521–10528.
   PubMed Web of Science ®Google Scholar
• Uchida, K. (2003). 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res, 42:318–343.
   PubMed Web of Science ®Google Scholar
• Uchida, K. (2007). Future of toxicology—lipid peroxidation in the future: from biomarker to etiology. Chem Res Toxicol 20:3–5.
   PubMed Web of Science ®Google Scholar
• Vaillancourt, F., Fahmi, H., Shi, Q., Lavigne, P., Ranger, P., Fernandes, J. C., et al. (2008). 4-hydroxynonenal induces apoptosis in human osteoarthritic chondrocytes: the protective role of glutathione-S-transferase. Arthritis Res Ther 10:R107.
   PubMed Web of Science ®Google Scholar
• van Iersel, M. L., Ploemen, J. P., Lo Bello, M., Federici, G., Van Bladeren, P. J. (1997). Interactions of alpha, beta-unsaturated aldehydes and ketones with human glutathione Stransferase P1-1. Chem Biol Interact, 108:67–78.
   PubMed Web of Science ®Google Scholar
• Volkel, W., Alvarez-Sanchez, R., Weick, I., Mally, A., Dekant, W., Pahler, A. (2005). Glutathione conjugates of 4-hydroxy-2(E)-nonenal as biomarkers of hepatic oxidative stress-induced lipid peroxidation in rats. Free Radic Biol Med 38:1526–1536.
   PubMed Web of Science ®Google Scholar
• Volkel, W., Sicilia, T., Pahler, A., Gsell, W., Tatschner, T., Jellinger, K., et al. (2006). Increased brain levels of 4-hydroxy-2-nonenal glutathione conjugates in severe Alzheimer’s disease. Neurochem Int, 48:679–686.
   Web of Science ®Google Scholar
• West, J. D., Ji, C., Duncan, S. T., Amarnath, V., Schneider, C., Rizzo, C. J., et al. (2004). Induction of apoptosis in colorectal carcinoma cells treated with 4-hydroxy-2-nonenal and structurally related aldehydic products of lipid peroxidation. Chem Res Toxicol 17:453–462.
   PubMed Web of Science ®Google Scholar
• West, J. D., Marnett, L. J. (2005). Alterations in gene expression induced by the lipid peroxidation product, 4-hydroxy-2-nonenal. Chem Res Toxicol, 18:1642–1653.
   PubMed Web of Science ®Google Scholar
• Williams, T. I., Lynn, B. C., Markesbery, W. R., Lovell, M. A. (2006). Increased levels of 4- hydroxynonenal and acrolein, neurotoxic markers of lipid peroxidation, in the brain in Mild Cognitive Impairment and early Alzheimer’s disease. Neurobiol Aging, 27:1094- 1099.
   PubMed Web of Science ®Google Scholar
• Xiao, B., Singh, S. P., Nanduri, B., Awasthi, Y. C., Zimniak, P., Ji, X. (1999). Crystal structure of a murine glutathione S-transferase in complex with a glutathione conjugate of 4-hydroxynon-2-enal in one subunit and glutathione in the other: evidence of signaling across the dimer interface. Biochemistry 38:11887–11894.
   PubMed Web of Science ®Google Scholar
• Xie, C., Lovell, M. A., Markesbery, W. R. (1998). Glutathione transferase protects neuronal cultures against four hydroxynonenal toxicity. Free Radic Biol Med, 25:979–988.
   PubMed Web of Science ®Google Scholar
• Yang, Y., Cheng, J. Z., Singhal, S. S., Saini, M., Pandya, U., Awasthi, S., et al. (2001). Role of glutathione S-transferases in protection against lipid peroxidation. Overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation. J Biol Chem, 276:19220–19230.
   PubMed Web of Science ®Google Scholar
• Yang, Y., Sharma, R., Sharma, A., Awasthi, S.Awasthi, Y. C. (2003). Lipid peroxidation and cell cycle signaling: 4-hydroxynonenal, a key molecule in stress mediated signaling. Acta Biochim Pol, 50:319–336.
   PubMed Web of Science ®Google Scholar
• Yang, Y., Trent, M. B., He, N., Lick, S. D., Zimniak, P., Awasthi, Y. C., et al. (2004). Glutathione-S-transferase A4-4 modulates oxidative stress in endothelium: possible role in human atherosclerosis. Atherosclerosis 173:211–221.
   PubMed Web of Science ®Google Scholar
• Yang, Y., Xu, Y., Lick, S. D., Awasthi, Y. C., Boor, P. J. (2008). Endothelial glutathione-S-transferase A4-4 protects against oxidative stress and modulates iNOS expression through NF-kappaB translocation. Toxicol Appl Pharmacol 230:187–196.
   PubMed Web of Science ®Google Scholar
• Yoshihara, D., Fujiwara, N., Ookawara, T., Kato, S., Sakiyama, H., Yokoe, S., et al. (2009). Protective role of glutathione S-transferase A4 induced in copper/zinc-superoxide dismutase knockout mice. Free Radic Biol Med 47:559–567.
   PubMed Web of Science ®Google Scholar
• Zarkovic, K. (2003a). 4-hydroxynonenal and neurodegenerative diseases. Mol Aspects Med, 24:293–303.
   PubMedGoogle Scholar
• Zarkovic, N. (2003b). 4-hydroxynonenal as a bioactive marker of pathophysiological processes. Mol Aspects Med 24:281–291.
   PubMedGoogle Scholar
• Zhan, Y., Rule, G. S. (2004). Glutathione induces helical formation in the carboxy terminus of human glutathione transferase A1-1. Biochemistry 43:7244–7254.
   PubMed Web of Science ®Google Scholar
• Zhang, H., Forman, H. J. (2009). Signaling pathways involved in phase II gene induction by alpha, beta-unsaturated aldehydes. Toxicol Ind Health, 25:269–278.
   PubMed Web of Science ®Google Scholar
• Zhao, T., Singhal, S. S., Piper, J. T., Cheng, J., Pandya, U., Clark-Wronski, J., et al. (1999). The role of human glutathione S-transferases hGSTA1-1 and hGSTA2-2 in protection against oxidative stress. Arch Biochem Biophys, 367:216–224.
   PubMed Web of Science ®Google Scholar
• Zhou, C., Huang, Y., Przedborski, S. (2008). Oxidative stress in Parkinson’s disease: a mechanism of pathogenic and therapeutic significance. Ann N Y Acad Sci, 1147:93–104.
   PubMed Web of Science ®Google Scholar
• Zimniak, P. (2008). Detoxification reactions: relevance to aging. Ageing Res Rev, 7:281–300.
   PubMed Web of Science ®Google Scholar
• Zimniak, P., Eckles, M. A., Saxena, M., Awasthi, Y. C. (1992). A subgroup of class alpha glutathione S-transferases. Cloning of cDNA for mouse lung glutathione S-transferase GST 5.7. FEBS Lett 313:173–176.
   PubMed Web of Science ®Google Scholar