Skip to main content

Advertisement

SpringerLink
Log in

Structure, function and disease relevance of Omega-class glutathione transferases

  • Review Article
  • Published:
Archives of Toxicology Aims and scope Submit manuscript

Abstract

The Omega-class cytosolic glutathione transferases (GSTs) have distinct structural and functional attributes that allow them to perform novel roles unrelated to the functions of other GSTs. Mammalian GSTO1-1 has been found to play a previously unappreciated role in the glutathionylation cycle that is emerging as significant mechanism regulating protein function. GSTO1-1-catalyzed glutathionylation or deglutathionylation of a key signaling protein may explain the requirement for catalytically active GSTO1-1 in LPS-stimulated pro-inflammatory signaling through the TLR4 receptor. The observation that ML175 a specific GSTO1-1 inhibitor can block LPS-stimulated inflammatory signaling has opened a new avenue for the development of novel anti-inflammatory drugs that could be useful in the treatment of toxic shock and other inflammatory disorders. The role of GSTO2-2 remains unclear. As a dehydroascorbate reductase, it could contribute to the maintenance of cellular redox balance and it is interesting to note that the GSTO2 N142D polymorphism has been associated with multiple diseases including Alzheimer’s disease, Parkinson’s disease, familial amyotrophic lateral sclerosis, chronic obstructive pulmonary disease, age-related cataract and breast cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adam GC, Sorensen EJ, Cravatt BF (2002) Proteomic profiling of mechanistically distinct enzyme classes using a common chemotype. Nat Biotechnol 20(8):805–809

    Article  CAS  PubMed  Google Scholar 

  • Agrawal SA, Anand D, Siddam AD et al (2015) Compound mouse mutants of bZIP transcription factors Mafg and Mafk reveal a regulatory network of non-crystallin genes associated with cataract. Hum Genet 134(7):717–735

    Article  CAS  PubMed  Google Scholar 

  • Agusa T, Iwata H, Fujihara J et al (2010) Genetic polymorphisms in glutathione S-transferase (GST) superfamily and arsenic metabolism in residents of the Red River Delta, Vietnam. Toxicol Appl Pharmacol 242(3):352–362

    Article  CAS  PubMed  Google Scholar 

  • Akhtar MH (1979) Sequential participation of glutathione and sulph-hydryl(s) in reductive dechlorination of 2,4-di-, and 2,4,5-trichloro phenacyl chlorides by soluble fraction (105,000×g) of chicken liver homogenate. J Environ Sci Health Part B 14(1):53–71

    Article  CAS  Google Scholar 

  • Allen EM, Mieyal JJ (2012) Protein-thiol oxidation and cell death: regulatory role of glutaredoxins. Antioxid Redox Signal 17(12):1748–1763. doi:10.1089/ars.2012.4644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen M, Zou F, Chai HS et al (2012) Glutathione S-transferase omega genes in Alzheimer and Parkinson disease risk, age-at-diagnosis and brain gene expression: an association study with mechanistic implications. Mol Neurodegener 7:13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anathy V, Roberson EC, Guala AS, Godburn KE, Budd RC, Janssen-Heininger YMW (2012) Redox based regulation of apoptosis: S-glutathionylation as a regulatory mechanism to control cell death. Antioxid Redox Signal 16(6):496–505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antonelli R, Shao K, Thomas DJ, Sams R 2nd, Cowden J (2014) AS3MT, GSTO, and PNP polymorphisms: impact on arsenic methylation and implications for disease susceptibility. Environ Res 132:156–167

    Article  CAS  PubMed  Google Scholar 

  • Aposhian HV, Zakharyan RA, Avram MD, Sampayo-Reyes A, Wollenberg ML (2004) A review of the enzymology of arsenic metabolism and a new potential role of hydrogen peroxide in the detoxication of the trivalent arsenic species. Toxicol Appl Pharmacol 198(3):327–335

    Article  PubMed  CAS  Google Scholar 

  • Armstrong RN (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem Res Toxicol 10(1):2–18

    Article  CAS  PubMed  Google Scholar 

  • Arning L, Jagiello P, Wieczorek S, Saft C, Andrich J, Epplen JT (2004) Glutathione S-transferase omega 1 variation does not influence age at onset of Huntington’s disease. BMC Med Genet 5:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Bachovchin DA, Brown SJ, Rosen H, Cravatt BF (2009) Identification of selective inhibitors of uncharacterized enzymes by high-throughput screening with fluorescent activity-based probes. Nat Biotechnol 27(4):387–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ballantyne B, Swanston DW (1978) The comparative acute mammalian toxicity of 1-chloroacetophenone (CN) and 2-chlorobenzylidene malononitrile (CS). Arch Toxicol 40(2):75–95

    Article  CAS  PubMed  Google Scholar 

  • Bedhomme M, Adamo M, Marchand CH et al (2012) Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem J 445(3):337–347

    Article  CAS  PubMed  Google Scholar 

  • Beebe-Dimmer JL, Iyer PT, Nriagu JO et al (2012) Genetic variation in glutathione S-transferase omega-1, arsenic methyltransferase and methylene-tetrahydrofolate reductase, arsenic exposure and bladder cancer: a case–control study. Environ Health 11:43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berenson JR, Yeh HS (2006) Arsenic compounds in the treatment of multiple myeloma: a new role for a historical remedy. Clin Lymphoma Myeloma 7(3):192–198

    Article  CAS  PubMed  Google Scholar 

  • Board PG (2011) The omega-class glutathione transferases: structure, function, and genetics. Drug Metab Rev 43(2):226–235

    Article  CAS  PubMed  Google Scholar 

  • Board PG, Anders MW (2007) Glutathione transferase omega 1 catalyzes the reduction of S-(phenacyl)glutathiones to acetophenones. Chem Res Toxicol 20(1):149–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Board PG, Menon D (2013) Glutathione transferases, regulators of cellular metabolism and physiology. Biochim Biophys Acta 1830(5):3267–3288

    Article  CAS  PubMed  Google Scholar 

  • Board PG, Coggan M, Chelvanayagam G et al (2000) Identification, characterization and crystal structure of the omega class glutathione transferases. J Biol Chem 275(32):24798–24806

    Article  CAS  PubMed  Google Scholar 

  • Board PG, Coggan M, Cappello J, Zhou H, Oakley AJ, Anders MW (2008) S-(4-nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1. Anal Biochem 374:25–30

    Article  CAS  PubMed  Google Scholar 

  • Brock J, Board PG, Oakley AJ (2013) Structural insights into omega-class glutathione transferases: a snapshot of enzyme reduction and identification of a non-catalytic ligandin site. PLoS One 8(4):e60324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brundin A, Ratnayake JH, Sunram JM, Anders MW (1982) Glutathione-dependent reductive dehalogenation of 2,2′,4′-trichloroacetophenone–2′,4′-dichloroacetophenone. Biochem Pharmacol 31(23):3885–3890

    Article  CAS  PubMed  Google Scholar 

  • Burmeister C, Luersen K, Heinick A et al (2008) Oxidative stress in Caenorhabditis elegans: protective effects of the Omega class glutathione transferase (GSTO-1). FASEB J 22(2):343–354

    Article  CAS  PubMed  Google Scholar 

  • Capurso C, Panza F, Seripa D et al (2010) Polymorphisms in glutathione s-transferase omega-1 gene and increased risk of sporadic Alzheimer disease. Rejuvenation Res 13(6):645–652

    Article  CAS  PubMed  Google Scholar 

  • Casula M, Iyer AM, Spliet WG et al (2011) Toll-like receptor signaling in amyotrophic lateral sclerosis spinal cord tissue. Neuroscience 179:233–243

    Article  CAS  PubMed  Google Scholar 

  • Chantzoura E, Prinarakis E, Panagopoulos D, Mosialos G, Spyrou G (2010) Glutaredoxin-1 regulates TRAF6 activation and the IL-1 receptor/TLR4 signalling. Biochem Biophys Res Commun 403(3–4):335–339

    Article  CAS  PubMed  Google Scholar 

  • Chen JH, Ni RZ, Xiao MB, Guo JG, Zhou JW (2009) Comparative proteomic analysis of differentially expressed proteins in human pancreatic cancer tissue. Hepatobiliary Pancreatc Dis Int 8(2):193–200

    CAS  Google Scholar 

  • Chuang JJ, Dai YC, Lin YL et al (2014) Downregulation of glutathione S-transferase M1 protein in N-butyl-N-(4-hydroxybutyl)nitrosamine-induced mouse bladder carcinogenesis. Toxicol Appl Pharmacol 279(3):322–330

    Article  CAS  PubMed  Google Scholar 

  • Chung S, Sundar IK, Yao H, Ho Y-S, Rahman I (2010) Glutaredoxin 1 regulates cigarette smoke-mediated lung inflammation through differential modulation of IκB kinases in mice: impact on histone acetylation. Am J Physiol Lung Cell Mol Physiol 299(2):L192–L203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coll RC, O’Neill LA (2010) New insights into the regulation of signalling by toll-like receptors and nod-like receptors. J Innate Immun 2(5):406–421

    Article  CAS  PubMed  Google Scholar 

  • Cooper AJ, Pinto JT, Callery PS (2011) Reversible and irreversible protein glutathionylation: biological and clinical aspects. Expert Opin Drug Metab Toxicol 7(7):891–910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crawford MJ, Hutson DH, King PA (1976) Metabolic demethylation of the insecticide dimethylvinphos in rats, in dogs, and in vitro. Xenobiotica 6(12):745–762

    Article  CAS  PubMed  Google Scholar 

  • Cromer BA, Morton CJ, Board PG, Parker MW (2002) From glutathione transferase to pore in a CLIC. Eur Biophys J 31(5):356–364

    Article  CAS  PubMed  Google Scholar 

  • Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43(2):266–280

    Article  CAS  PubMed  Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radic Med 43:883–898

    Article  CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Colombo G, Giustarini D, Milzani A (2009) Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem Sci 34(2):85–96

    Article  CAS  PubMed  Google Scholar 

  • de Jong K, Boezen HM, Hacken NH, Postma DS, Vonk JM, LifeLines Cohort Study (2013) GST-omega genes interact with environmental tobacco smoke on adult level of lung function. Respir Res 14:83

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Demas GE, Chefer V, Talan MI, Nelson RJ (1997) Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice. Am J Physiol 273(5):1631–1637

    Google Scholar 

  • Deroy A, Saiag F, Kebbi-Benkeder Z et al (2015) The GSTome reflects the chemical environment of white-rot fungi. PLoS One 10(10):e0137083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dittrich AM, Meyer HA, Krokowski M et al (2010) Glutathione peroxidase-2 protects from allergen-induced airway inflammation in mice. Eur Respir J 35(5):1148–1154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dowling JK, O’Neill LA (2012) Biochemical regulation of the inflammasome. Crit Rev Biochem Mol Biol 47(5):424–443

    Article  CAS  PubMed  Google Scholar 

  • Doyle SL, O’Neill LA (2006) Toll-like receptors: from the discovery of NFκB to new insights into transcriptional regulations in innate immunity. Biochem Pharmacol 72(9):1102–1113

    Article  CAS  PubMed  Google Scholar 

  • Dulhunty A, Gage P, Curtis S, Chelvanayagam G, Board P (2001) The glutathione transferase structural family includes a nuclear chloride channel and a ryanodine receptor calcium release channel modulator. J Biol Chem 276(5):3319–3323

    Article  CAS  PubMed  Google Scholar 

  • Dulhunty AF, Hewawasam R, Liu D, Casarotto MG, Board PG (2011) Regulation of the cardiac muscle ryanodine receptor by glutathione transferases. Drug Metab Rev 43(2):236–252

    Article  CAS  PubMed  Google Scholar 

  • Emery M, Schorderet DF, Roduit R (2011) Acute hypoglycemia induces retinal cell death in mouse. PLoS One 6(6):e21586. doi:10.1371/journal.pone.0021586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erian AW, Sherif SM, Gaber HM (2003) The chemistry of alpha-haloketones and their utility in heterocyclic synthesis. Molecules 8(11):793–865

    Article  CAS  Google Scholar 

  • Escobar-Garcia DM, Del Razo LM, Sanchez-Pena LC, Mandeville PB, Lopez-Campos C, Escudero-Lourdes C (2012) Association of glutathione S-transferase omega 1-1 polymorphisms (A140D and E208K) with the expression of interleukin-8 (IL-8), transforming growth factor beta (TGF-beta), and apoptotic protease-activating factor 1 (Apaf-1) in humans chronically exposed to arsenic in drinking water. Arch Toxicol 86(6):857–868

    Article  CAS  PubMed  Google Scholar 

  • Feingold KR, Wang Y, Moser A, Shigenaga JK, Grunfeld C (2008) LPS decreases fatty acid oxidation and nuclear hormone receptors in the kidney. J Lipid Res 49(10):2179–2187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Findlay VJ, Townsend DM, Morris TE, Fraser JP, He L, Tew KD (2006) A novel role for human sulfiredoxin in the reversal of glutathionylation. Cancer Res 66(13):6800–6804

    Article  CAS  PubMed  Google Scholar 

  • Fornai F, Saviozzi M, Piaggi S et al (1999) Localization of a glutathione-dependent dehydroascorbate reductase within the central nervous system of the rat. Neuroscience 94(3):937–948

    Article  CAS  PubMed  Google Scholar 

  • Fornai F, Piaggi S, Gesi M et al (2001) Subcellular localization of a glutathione-dependent dehydroascorbate reductase within specific rat brain regions. Neuroscience 104(1):15–31

    Article  CAS  PubMed  Google Scholar 

  • Freemerman AJ, Johnson AR, Sacks GN et al (2014) Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J Biol Chem 289(11):7884–7896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallogly MM, Starke DW, Mieyal JJ (2009) Mechanistic and kinetic details of catalysis of thiol-disulphide exchange by glutaredoxins and potential mechanisms of regulation. Antioxid Redox Signal 11(5):1059–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill R, Tsung A, Billiar T (2010) Linking oxidative stress to inflammation: toll-like receptors. Free Radic Biol Med 48(9):1121–1132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Girardini J, Amirante A, Zemzoumi K, Serra E (2002) Characterization of an omega-class glutathione S-transferase from Schistosoma mansoni with glutaredoxin-like dehydroascorbate reductase and thiol transferase activities. Eur J Biochem 269(22):5512–5521

    Article  CAS  PubMed  Google Scholar 

  • Giri U, Terry NH, Kala SV, Lieberman MW, Story MD (2005) Elimination of the differential chemoresistance between the murine B-cell lymphoma LY-ar and LY-as cell lines after arsenic (As2O3) exposure via the overexpression of gsto1 (p28). Cancer Chemother Pharmacol 55(6):511–521

    Article  CAS  PubMed  Google Scholar 

  • Giustarini D, Milzani A, Aldini G, Carini M, Rossi R, Dalle-Donne I (2005) S-nitrosation versus S-glutathionylation of protein sulfhydryl groups by S-nitrosoglutathione. Antioxid Redox Signal 7(7–8):930–939

    Article  CAS  PubMed  Google Scholar 

  • Hanna ME, Bednarova A, Rakshit K, Chaudhuri A, O’Donnell JM, Krishnan N (2015) Perturbations in dopamine synthesis lead to discrete physiological effects and impact oxidative stress response in Drosophila. J Insect Physiol 73:11–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harju TH, Peltoniemi MJ, Rytila PH et al (2007) Glutathione S-transferase omega in the lung and sputum supernatants of COPD patients. Respir Res 8:48

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haschemi A, Kosma P, Gille L et al (2012) The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism. Cell Metab 15(6):813–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayes JD, Pulford DJ (1995) The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 30(6):445–600

    Article  CAS  PubMed  Google Scholar 

  • Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88

    Article  CAS  PubMed  Google Scholar 

  • Hsieh YC, Lien LM, Chung WT et al (2011) Significantly increased risk of carotid atherosclerosis with arsenic exposure and polymorphisms in arsenic metabolism genes. Environ Res 111(6):804–810

    Article  CAS  PubMed  Google Scholar 

  • Hundhausen C, Boesch-Saadatmandi C, Matzner N et al (2008) Ochratoxin a lowers mRNA levels of genes encoding for key proteins of liver cell metabolism. Cancer Genomics Proteomics 5(6):319–332

    CAS  PubMed  Google Scholar 

  • Ishikawa T, Casini AF, Nishikimi M (1998) Molecular cloning and functional expression of rat liver glutathione-dependent dehydroascorbate reductase. J Biol Chem 273(44):28708–28712

    Article  CAS  PubMed  Google Scholar 

  • Jakobsson PJ, Morgenstern R, Mancini J, Ford-Hutchinson A, Persson B (1999) Common structural features of MAPEG—a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism. Protein Sci 8(3):689–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jalilian C, Gallant EM, Board PG, Dulhunty AF (2008) Redox potential and the response of cardiac ryanodine receptors to CLIC-2, a member of the glutathione transferase structural family. Antioxid Redox Signal 10(10):1675–1686

    Article  CAS  PubMed  Google Scholar 

  • Kim K, Yim J (2014) Structural modelling and molecular characterization of omega-class glutathione S-transferase 2 from Drosophila melanogaster. Insect Mol Biol 23(3):357–366

    CAS  PubMed  Google Scholar 

  • Kim J, Suh H, Kim S, Kim K, Ahn C, Yim J (2006) Identification and characteristics of the structural gene for the Drosophila eye colour mutant sepia, encoding PDA synthase, a member of the omega class glutathione S-transferases. Biochem J 398(3):451–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JH, Dahms HU, Rhee JS et al (2010) Expression profiles of seven glutathione S-transferase (GST) genes in cadmium-exposed river pufferfish (Takifugu obscurus). Comp Biochem Physiol Toxicol Pharmacol 151(1):99–106

    Article  CAS  Google Scholar 

  • Kim HS, Ullevig SL, Zamora D, Lee CF, Asmis R (2012a) Redox regulation of MAPK phosphatase 1 controls monocyte migration and macrophage recruitment. Proc Natl Acad Sci USA 109(41):E2803–E2812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim K, Kim SH, Kim J, Kim H, Yim J (2012b) Glutathione s-transferase omega 1 activity is sufficient to suppress neurodegeneration in a Drosophila model of Parkinson disease. J Biol Chem 287(9):6628–6641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitada M, McLenithan JC, Anders MW (1985) Purification and characterization of S-phenacylglutathione reductase from rat liver. J Biol Chem 260(21):11749–11754

    CAS  PubMed  Google Scholar 

  • Kodym R, Calkins P, Story M (1999) The cloning and characterization of a new stress response protein. A mammalian member of a family of theta class glutathione S-transferase-like proteins. J Biol Chem 274(8):5131–5137

    Article  CAS  PubMed  Google Scholar 

  • Kodym R, Calkins PR, Story MD (2001) Anthracycline-induced erythroid differentiation of K562 cells is inhibited by p28, a novel mammalian glutathione-binding stress protein. Leuk Res 25(2):151–156

    Article  CAS  PubMed  Google Scholar 

  • Kolsch H, Linnebank M, Lutjohann D et al (2004) Polymorphisms in glutathione S-transferase omega-1 and AD, vascular dementia, and stroke. Neurology 63(12):2255–2260

    Article  CAS  PubMed  Google Scholar 

  • Kuroda N, Inoue K, Ikeda T, Hara Y, Wake K, Sato T (2014) Apoptotic response through a high mobility box 1 protein-dependent mechanism in LPS/GalN-induced mouse liver failure and glycyrrhizin-mediated inhibition. PLoS One 9(4):e92884

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Laliberte RE, Peeregaux DG, Hoth LR et al (2003) Glutathione S-transferase omega 1-1 is a target of cytokine release inhibitory drugs and may be responsible for their effect on interleukin-1beta posttranslational processing. J Biol Chem 278(19):16567–16578

    Article  CAS  PubMed  Google Scholar 

  • Lallement PA, Brouwer B, Keech O, Hecker A, Rouhier N (2014) The still mysterious roles of cysteine-containing glutathione transferases in plants. Front Pharmacol 5:192

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Langen RC, Korn SH, Wouters EF (2003) ROS in the local and systemic pathogenesis of COPD. Free Radic Biol Med 35(3):226–235

    Article  CAS  PubMed  Google Scholar 

  • Lantz RC, Lynch BJ, Boitano S et al (2007) Pulmonary biomarkers based on alterations in protein expression after exposure to arsenic. Environ Health Perspect 115(4):586–591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JJ, Son J, Ha HH, Chang YT (2011) Fluorescent labeling of membrane proteins on the surface of living cells by a self-catalytic glutathione S-transferase omega 1 tag. Mol BioSyst 7(4):1270–1276

    Article  CAS  PubMed  Google Scholar 

  • Li YJ, Scott WK, Hedges DJ et al (2002) Age at onset in two common neurodegenerative diseases is genetically controlled. Am J Hum Genet 70(4):985–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YJ, Oliveira SA, Xu P et al (2003) Glutathione S-transferase omega-1 modifies age-at-onset of Alzheimer disease and Parkinson disease. Hum Mol Genet 12(24):3259–3267

    Article  CAS  PubMed  Google Scholar 

  • Li YJ, Scott WK, Zhang L et al (2006) Revealing the role of glutathione S-transferase omega in age-at-onset of Alzheimer and Parkinson diseases. Neurobiol Aging 27(8):1087–1093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Zhang Q, Peng B, Shao Q, Qian W, Zhang JY (2014) Identification of glutathione S-transferase omega 1 (GSTO1) protein as a novel tumor-associated antigen and its autoantibody in human esophageal squamous cell carcinoma. Tumour Biol 35(11):10871–10877

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Jiang X, Tang N, Yang L, Chen H, Wang Q (2015) Quantification and visualization of glutathione S-transferase omega 1 in cells using inductively coupled plasma mass spectrometry (ICP-MS) and fluorescence microscopy. Anal Bioanal Chem 407(9):2373–2381

    Article  CAS  PubMed  Google Scholar 

  • Liao YT, Li WF, Chen CJ et al (2009) Synergistic effect of polymorphisms of paraoxonase gene cluster and arsenic exposure on electrocardiogram abnormality. Toxicol Appl Pharmacol 239(2):178–183

    Article  CAS  PubMed  Google Scholar 

  • Liao BC, Hsieh CW, Lin YC, Wung BS (2010) The glutaredoxin/glutathione system modulates NF-kappaB activity by glutathionylation of p65 in cinnamaldehyde-treated endothelial cells. Toxicol Sci 116(1):151–163

    Article  CAS  PubMed  Google Scholar 

  • Lindahl M, Mata-Cabana A, Kieselbach T (2011) The disulphide proteome and other reactive cysteine proteomes: analysis and functional significance. Antioxid Redox Signal 14(12):2581–2642

    Article  CAS  PubMed  Google Scholar 

  • Litwack G, Ketterer B, Arias IM (1971) Ligandin: a hepatic protein which binds steroids, bilirubin, carcinogens and a number of exogenous organic anions. Nature 234(5330):466–467

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Chan C (2014) The role of inflammasome in Alzheimer’s disease. Ageing Res Rev 15:6–15

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Zhao L, Zhang Y, Zhang Q, Ding Y (2007) Proteomic analysis of Tiam1-mediated metastasis in colorectal cancer. Cell Biol Int 31(8):805–814

    Article  CAS  PubMed  Google Scholar 

  • Lock JT, Sinkins WG, Schilling WP (2011) Effect of protein S-glutathionylation on Ca2+ homeostasis in cultured aortic endothelial cells. Am J Physiol Heart Circ Physiol 300:493–506

    Article  CAS  Google Scholar 

  • Lombardi S, Fuoco I, di Fluri G et al (2015) Genomic instability and cellular stress in organ biopsies and peripheral blood lymphocytes from patients with colorectal cancer and predisposing pathologies. Oncotarget 6(17):14852–14864

    Article  PubMed  PubMed Central  Google Scholar 

  • Maellaro E, Del Bello B, Sugherini L, Santucci A, Comporti M, Casini AF (1994) Purification and characterization of glutathione-dependent dehydroascorbate reductase from rat liver. Biochem J 301(Pt 2):471–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mailloux RJ, Xuan JY, McBride S et al (2014) Glutaredoxin-2 is required to control oxidative phosphorylation in cardiac muscle by mediating deglutathionylation reactions. J Biol Chem 289(21):14812–14828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mannervik B, Axelsson K (1980) Role of cytoplasmic thioltransferase in cellular regulation by thiol–disulphide interchange. Biochem J 190(1):125–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mannervik B, Danielson UH (1988) Glutathione transferases—structure and catalytic activity. CRC Crit Rev Biochem 23(3):283–337

    Article  CAS  PubMed  Google Scholar 

  • Mannervik B, Widersten M (1995) Human glutathione transferases: classification, tissue distribution, structure and functional properties. In: Pacifici GM, Fracchia GN (eds) Advances in Drug Metabolism in Man. The European Commission, Brussels, pp 407–460

    Google Scholar 

  • Marnell LL, Garcia-Vargas GG, Chowdhury UK et al (2003) Polymorphisms in the human monomethylarsonic acid (MMA V) reductase/hGSTO1 gene and changes in urinary arsenic profiles. Chem Res Toxicol 16(12):1507–1513

    Article  CAS  PubMed  Google Scholar 

  • Mashiyama ST, Malabanan MM, Akiva E et al (2014) Large-scale determination of sequence, structure, and function relationships in cytosolic glutathione transferases across the biosphere. PLoS Biol 12(4):e1001843

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McCaulley ME, Grush KA (2015) Alzheimer’s disease: exploring the role of inflammation and implications for treatment. Int J Alzheimer’s Dis 2015:515248

    Google Scholar 

  • McCray JW, Weil R (1982) Inactivation of interferons: halomethyl ketone derivatives of phenylalanine as affinity labels. Proc Natl Acad Sci USA 79(16):4829–4833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menon D, Board PG (2013) A role for glutathione transferase omega 1 (GSTO1-1) in the glutathionylation cycle. J Biol Chem 288(36):25769–25779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menon D, Coll R, O’Neill LA, Board PG (2014) Glutathione transferase omega 1 is required for the lipopolysaccharide-stimulated induction of NADPH oxidase 1 and the production of reactive oxygen species in macrophages. Free Radic Biol Med 73:318–327

    Article  CAS  PubMed  Google Scholar 

  • Menon D, Coll R, O’Neill LA, Board PG (2015) GSTO1-1 modulates metabolism in macrophages activated through the LPS and TLR4 pathway. J Cell Sci 128(10):1982–1990

    Article  CAS  PubMed  Google Scholar 

  • Meux E, Morel M, Lamant T et al (2013) New substrates and activity of Phanerochaete chrysosporium omega glutathione transferases. Biochimie 95(2):336–346

    Article  CAS  PubMed  Google Scholar 

  • Meza MM, Yu L, Rodriguez YY et al (2005) Developmentally restricted genetic determinants of human arsenic metabolism: association between urinary methylated arsenic and CYT19 polymorphisms in children. Environ Health Perspect 113(6):775–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirkovic N, Voehringer DW, Story MD, McConkey DJ, McDonnell TJ, Meyn RE (1997) Resistance to radiation-induced apoptosis in Bcl-2-expressing cells is reversed by depleting cellular thiols. Oncogene 15(12):1461–1470

    Article  CAS  PubMed  Google Scholar 

  • Mo C, Wang L, Zhang J et al (2013) The crosstalk between Nrf2 and AMPK signal pathways is important for the anti-inflammatory effect of berberine in LPS-stimulated macrophages and endotoxin-shocked mice. Antioxid Redox Signal 20(4):574–588

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee B, Salavaggione OE, Pelleymounter LL et al (2006) Glutathione S-transferase omega 1 and omega 2 pharmacogenomics. Drug Metab Dispos 34(7):1237–1246

    Article  CAS  PubMed  Google Scholar 

  • Navarro J, Abdel Ghany M, Racker E (1982) Inhibition of tyrosine protein kinases by halomethyl ketones. Biochemistry 21(24):6138–6144

    Article  CAS  PubMed  Google Scholar 

  • Nemeti B, Gregus Z (2013) Reduction of dimethylarsinic acid to the highly toxic dimethylarsinous acid by rats and rat liver cytosol. Chem Res Toxicol 26(3):432–443

    Article  CAS  PubMed  Google Scholar 

  • Nemeti B, Poor M, Gregus Z (2015a) A high-performance liquid chromatography-based assay of glutathione transferase omega 1 supported by glutathione or non-physiological reductants. Anal Biochem 469:12–18

    Article  CAS  PubMed  Google Scholar 

  • Nemeti B, Poor M, Gregus Z (2015b) Reduction of the pentavalent arsenical dimethylarsinic acid and the GSTO1 substrate S-(4-nitrophenacyl)glutathione by rat liver cytosol: analyzing the role of GSTO1 in arsenic reduction. Chem Res Toxicol 28(11):2199–2209

    Article  CAS  PubMed  Google Scholar 

  • Nishimura M, Sakamoto T, Kaji R, Kawakami H (2004) Influence of polymorphisms in the genes for cytokines and glutathione S-transferase omega on sporadic Alzheimer’s disease. Neurosci Lett 368(2):140–143

    Article  CAS  PubMed  Google Scholar 

  • Nishimura M, Kuno S, Kaji R, Yasuno K, Kawakami H (2005) Glutathione-S-transferase-1 and interleukin-1beta gene polymorphisms in Japanese patients with Parkinson’s disease. Mov Disord 20(7):901–902

    Article  PubMed  Google Scholar 

  • O’Neill LA, Hardie DG (2013) Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 493(7432):346–355

    Article  PubMed  CAS  Google Scholar 

  • Ozinsky A, Underhill DM, Fontenot JD et al (2000) The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci 97(25):13766–13771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozturk A, Desai PP, Minster RL, Dekosky ST, Kamboh MI (2005) Three SNPs in the GSTO1, GSTO2 and PRSS11 genes on chromosome 10 are not associated with age-at-onset of Alzheimer’s disease. Neurobiol Aging 26(8):1161–1165

    Article  CAS  PubMed  Google Scholar 

  • Pace NJ, Pimental DR, Weerapana E (2012) An inhibitor of glutathione S-transferase omega 1 that selectively targets apoptotic cells. Angew Chem Int Ed Engl 51(33):8365–8368

    Article  CAS  PubMed  Google Scholar 

  • Paiva L, Marcos R, Creus A, Coggan M, Oakley AJ, Board PG (2008) Polymorphism of glutathione transferase Omega 1 in a population exposed to a high environmental arsenic burden. Pharmacogenet Genomics 18:1–10

    Article  CAS  PubMed  Google Scholar 

  • Paiva L, Hernandez A, Martinez V, Creus A, Quinteros D, Marcos R (2010) Association between GSTO2 polymorphism and the urinary arsenic profile in copper industry workers. Environ Res 110(5):463–468

    Article  CAS  PubMed  Google Scholar 

  • Park MY, Mun ST (2014) Carnosic acid inhibits TLR4-MyD88 signaling pathway in LPS-stimulated 3T3-L1 adipocytes. Nutr Res Pract 8(5):516–520

    Article  PubMed  PubMed Central  Google Scholar 

  • Park EY, Cho IJ, Kim SG (2004) Transactivation of the PPAR-responsive enhancer module in chemopreventive glutathione S-transferase gene by the peroxisome proliferator-activated receptor-γ and retinoid X receptor heterodimer. Cancer Res 64(10):3701–3713

    Article  CAS  PubMed  Google Scholar 

  • Pastore A, Piemonte F (2012) S-glutathionylation signaling in cell biology: progress and prospects. Eur J Pharm Sci 46(5):279–292

    Article  CAS  PubMed  Google Scholar 

  • Pearson WR (2005) Phylogenies of glutathione transferase families. Methods Enzymol 401:186–204

    Article  CAS  PubMed  Google Scholar 

  • Piacentini S, Polimanti R, Squitti R et al (2012) GSTO1*E155del polymorphism associated with increased risk for late-onset Alzheimer’s disease: association hypothesis for an uncommon genetic variant. Neurosci Lett 506(2):203–207

    Article  CAS  PubMed  Google Scholar 

  • Piaggi S, Marchi S, Ciancia E et al (2009) Nuclear translocation of glutathione transferase omega is a progression marker in Barrett’s esophagus. Oncol Rep 21(2):283–287

    CAS  PubMed  Google Scholar 

  • Piaggi S, Raggi C, Corti A et al (2010) Glutathione transferase omega 1-1 (GSTO1-1) plays an anti-apoptotic role in cell resistance to cisplatin toxicity. Carcinogenesis 31(5):804–811

    Article  CAS  PubMed  Google Scholar 

  • Porter KE, Basu A, Hubbard AE et al (2010) Association of genetic variation in cystathionine-beta-synthase and arsenic metabolism. Environ Res 110(6):580–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman I, MacNee W (1996) Role of oxidants/antioxidants in smoking-induced lung diseases. Free Radic Biol Med 21(5):669–681

    Article  CAS  PubMed  Google Scholar 

  • Raso GM, Meli R, Di CarloG, Pacilio M, Di CarloR (2001) Inhibition of inducible nitric oxide synthase and cyclooxygenase-2 expression by flavonoids in macrophage J774A.1. Life Sci 68(8):921–931

    Article  CAS  PubMed  Google Scholar 

  • Ratnaike RN (2003) Acute and chronic arsenic toxicity. Postgrad Med J 79(933):391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynaert NL, van der Vliet A, Guala AS et al (2006) Dynamic redox control of NF-κB through glutaredoxin-regulated S-glutathionylation of inhibitory κB kinase β. Proc Natl Acad Sci 103(35):13086–13091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rigsby RE, Fillgrove KL, Beihoffer LA, Armstrong RN (2005) Fosfomycin resistance proteins: a nexus of glutathione transferases and epoxide hydrolases in a metalloenzyme superfamily. Methods Enzymol 401:367–379

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues EG, Kile M, Hoffman E et al (2012) GSTO and AS3MT genetic polymorphisms and differences in urinary arsenic concentrations among residents in Bangladesh. Biomarkers 17(3):240–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roh T, Kwak MY, Kwak EH et al (2012) Chemopreventive mechanisms of methionine on inhibition of benzo(a)pyrene-DNA adducts formation in human hepatocellular carcinoma HepG2 cells. Toxicol Lett 208(3):232–238. doi:10.1016/j.toxlet.2011.11.013

    Article  CAS  PubMed  Google Scholar 

  • Rouimi P, Anglade P, Benzekri A et al (2001) Purification and characterization of a glutathione S-transferase omega in pig: evidence for two distinct organ-specific transcripts. Biochem J 358(Pt 1):257–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samarasinghe K, Liu D, Tummala P et al (2015) Glutathione transferase M2 variants inhibit ryanodine receptor function in adult mouse cardiomyocytes. Biochem Pharmacol 97(3):269–280. doi:10.1016/j.bcp.2015.08.004

    Article  CAS  PubMed  Google Scholar 

  • Sampayo-Reyes A, Zakharyan RA (2006) Inhibition of human glutathione S-transferase omega by tocopherol succinate. Biomed Pharmacother 60(5):238–244

    Article  CAS  PubMed  Google Scholar 

  • Schieber M, Chandel NS (2014) TOR signaling couples oxygen sensing to lifespan in C. elegans. Cell Rep 9(1):9–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt M, Raghavan B, Muller V et al (2010) Crucial role for human Toll-like receptor 4 in the development of contact allergy to nickel. Nat Immunol 11(9):814–819

    Article  CAS  PubMed  Google Scholar 

  • Schmuck EM, Board PG, Whitbread AK et al (2005) Characterization of the monomethylarsonate reductase and dehydroascorbate reductase activities of omega class glutathione transferase variants: implications for arsenic metabolism and the age-at-onset of Alzheimer’s and Parkinson’s diseases. Pharmacogenet Genomics 15(7):493–501

    Article  CAS  PubMed  Google Scholar 

  • Schmuck E, Cappello J, Coggan M et al (2008) Deletion of Glu155 causes a deficiency of glutathione transferase omega 1-1 but does not alter sensitivity to arsenic trioxide and other cytotoxic drugs. Int J Biochem Cell Biol 40(11):2553–2559

    Article  CAS  PubMed  Google Scholar 

  • Shelton MD, Chock PB, Mieyal JJ (2005) Glutaredoxin: role in reversible protein S-glutathionylation and regulation of redox signal transduction and protein translocation. Antioxid Redox Signal 7:348–366

    Article  CAS  PubMed  Google Scholar 

  • Shield AJ, Murray TP, Board PG (2006) Functional characterisation of ganglioside-induced differentiation-associated protein 1 as a glutathione transferase. Biochem Biophys Res Commun 347(4):859–866

    Article  CAS  PubMed  Google Scholar 

  • Son J, Lee JJ, Lee JS, Schuller A, Chang YT (2010) Isozyme-specific fluorescent inhibitor of glutathione s-transferase omega 1. ACS Chem Biol 5(5):449–453

    Article  CAS  PubMed  Google Scholar 

  • Stamenkovic M, Radic T, Stefanovic I et al (2014) Glutathione S-transferase omega-2 polymorphism Asn142Asp modifies the risk of age-related cataract in smokers and subjects exposed to ultraviolet irradiation. Clin Exp Ophthalmol 42(3):277–283. doi:10.1111/ceo.12180

    Article  Google Scholar 

  • Stoll LL, Denning GM, Weintraub NL (2006) Endotoxin, TLR4 signaling and vascular inflammation: potential therapeutic targets in cardiovascular disease. Curr Pharm Des 12(32):4229–4245

    Article  CAS  PubMed  Google Scholar 

  • Summer KH, Klein D, Lichtmannegger J, Wolff T (1996) 2-Chloroacetophenone is an effective glutathione depletor in isolated rat hepatocytes. Arch Toxicol 71(1–2):127–129

    CAS  PubMed  Google Scholar 

  • Tallman MS (2007) Treatment of relapsed or refractory acute promyelocytic leukemia. Best Pract Res Clin Haematol 20(1):57–65

    Article  PubMed  Google Scholar 

  • Tannahill GM, Curtis AM, Adamik J et al (2013) Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature 496(7444):238–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terentyev D, Györke I, Belevych AE et al (2008) Redox modification of ryanodine receptors contributes to sarcoplasmic reticulum Ca2+ leak in chronic heart failure. Circ Res 103(12):1466–1472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thimmulappa RK, Scollick C, Traore K et al (2006) Nrf2-dependent protection from LPS induced inflammatory response and mortality by CDDO-imidazolide. Biochem Biophys Res Commun 351(4):883–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Townsend DM, Manevich Y, He L, Hutchens S, Pazoles CJ, Tew KD (2009) Novel role for glutathione S-transferase pi. Regulator of protein S-glutathionylation following oxidative and nitrosative stress. J Biol Chem 284(1):436–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsou PS, Addanki V, Haas JA, Page NA, Fung H-L (2009) Role of glutaredoxin-mediated protein S-glutathionylation in cellular nitroglycerin tolerance. J Pharmacol Exp Ther 329(2):649–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuboi K, Bachovchin DA, Speers AE et al (2010) Optimization and characterization of an inhibitor for glutathione S-transferase omega 1 (GSTO1). Probe Reports from the NIH Molecular Libraries Program, Bethesda

    Google Scholar 

  • Tsuboi K, Bachovchin DA, Speers AE et al (2011) Potent and selective inhibitors of glutathione S-transferase omega 1 that impair cancer drug resistance. J Am Chem Soc 133(41):16605–16616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urzua U, Roby KF, Gangi LM, Cherry JM, Powell JI, Munroe DJ (2006) Transcriptomic analysis of an in vitro murine model of ovarian carcinoma: functional similarity to the human disease and identification of prospective tumoral markers and targets. J Cell Physiol 206(3):594–602

    Article  CAS  PubMed  Google Scholar 

  • Vahter M (2000) Genetic polymorphism in the biotransformation of inorganic arsenic and its role in toxicity. Toxicol Lett 112–113:209–217

    Article  PubMed  Google Scholar 

  • Vahter M (2002) Mechanisms of arsenic biotransformation. Toxicology 181–182:211–217

    Article  PubMed  Google Scholar 

  • van de Giessen E, Fogh I, Gopinath S et al (2008) Association study on glutathione S-transferase omega 1 and 2 and familial ALS. Amyotroph Lateral Scler 9(2):81–84

    Article  PubMed  CAS  Google Scholar 

  • Veitinger M, Oehler R, Umlauf E et al (2014) A platelet protein biochip rapidly detects an Alzheimer’s disease-specific phenotype. Acta Neuropathol 128(5):665–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang T (2015) Glutathione S-transferases variants as risk factors in Alzheimer’s disease. Neurol Sci 36(10):1785–1792

    Article  PubMed  Google Scholar 

  • Wang J, Boja ES, Tan W et al (2001) Reversible glutathionylation regulates actin polymerization in A431 cells. J Biol Chem 276(51):47763–47766

    CAS  PubMed  Google Scholar 

  • Wang Q, Liu Y, Zhou J (2015) Neuroinflammation in Parkinson’s disease and its potential as therapeutic target. Transl Neurodegener 4:19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West AP, Brodsky IE, Rahner C et al (2011) TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472(7344):476–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitbread AK, Tetlow N, Eyre HJ, Sutherland GR, Board PG (2003) Characterization of the human omega class glutathione transferase genes and associated polymorphisms. Pharmacogenetics 13(3):131–144

    Article  CAS  PubMed  Google Scholar 

  • Whitbread AK, Masoumi A, Tetlow N, Schmuck E, Coggan M, Board PG (2005) Characterization of the omega class of glutathione transferases. Methods Enzymol 401:78–99

    Article  CAS  PubMed  Google Scholar 

  • Wilk JB, Walter RE, Laramie JM, Gottlieb DJ, O’Connor GT (2007) Framingham Heart Study genome-wide association: results for pulmonary function measures. BMC Med Genet 8(Suppl. 1):S8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu Y, Li X, Zheng Q, Wang H, Wang Y, Sun G (2009) Lack of association of glutathione-S-transferase omega 1(A140D) and omega 2 (N142D) gene polymorphisms with urinary arsenic profile and oxidative stress status in arsenic-exposed population. Mutat Res 679(1–2):44–49

    Article  CAS  PubMed  Google Scholar 

  • Xu YT, Wang J, Yin R et al (2014) Genetic polymorphisms in glutathione S-transferase omega (GSTO) and cancer risk: a meta-analysis of 20 studies. Sci Rep 4:6578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto K, Suzuki M, Higashiura A, Nakagawa A (2013) Three-dimensional structure of a Bombyx mori omega-class glutathione transferase. Biochem Biophys Res Commun 438(4):588–593

    Article  CAS  PubMed  Google Scholar 

  • Yan XD, Pan LY, Yuan Y, Lang JH, Mao N (2007) Identification of platinum-resistance associated proteins through proteomic analysis of human ovarian cancer cells and their platinum-resistant sublines. J Proteome Res 6(2):772–780

    Article  CAS  PubMed  Google Scholar 

  • Yanbaeva DG, Wouters EF, Dentener MA, Spruit MA, Reynaert NL (2009) Association of glutathione-S-transferase omega haplotypes with susceptibility to chronic obstructive pulmonary disease. Free Radic Res 43(8):738–743

    Article  CAS  PubMed  Google Scholar 

  • Yin ZL, Dahlstrom JE, Le Couteur DG, Board PG (2001) Immunohistochemistry of omega class glutathione S-transferase in human tissues. J Histochem Cytochem 49(8):983–987

    Article  CAS  PubMed  Google Scholar 

  • Yu L, Kalla K, Guthrie E, Vidrine A, Klimecki WT (2003) Genetic variation in genes associated with arsenic metabolism: glutathione S-transferase omega 1-1 and purine nucleoside phosphorylase polymorphisms in European and indigenous Americans. Environ Health Perspect 111(11):1421–1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zakharyan RA, Aposhian HV (1999) Enzymatic reduction of arsenic compounds in mammalian systems: the rate- limiting enzyme of rabbit liver arsenic biotransformation is MMA(V) reductase. Chem Res Toxicol 12(12):1278–1283

    Article  CAS  PubMed  Google Scholar 

  • Zakharyan RA, Sampayo-Reyes A, Healy SM et al (2001) Human monomethylarsonic acid (MMA(V)) reductase is a member of the glutathione-S-transferase superfamily. Chem Res Toxicol 14(8):1051–1057

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Ghosh S (2001) Toll-like receptor-mediated NF-κB activation: a phylogenetically conserved paradigm in innate immunity. J Clin Investig 107(1):13–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J (2009) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11(2):136–140

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, Brock J, Casarotto MG, Oakley AJ, Board PG (2011) Novel folding and stability defects cause a deficiency of human glutathione transferase omega 1. J Biol Chem 286(6):4271–4279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou H, Brock J, Liu D, Board PG, Oakley AJ (2012) Structural insights into the dehydroascorbate reductase activity of human omega-class glutathione transferases. J Mol Biol 420(3):190–203

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Fotinos A, Mao LL et al (2015) Neuroprotective agents target molecular mechanisms of disease in ALS. Drug Discov Today 20(1):65–75

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant from the Gordon and Gretel Bootes Medical Research Foundation.

Author information

Authors and Affiliations

  1. John Curtin School of Medical Research, Australian National University, PO Box 334, Canberra, ACT, 2601, Australia

    Philip G. Board & Deepthi Menon

Authors
  1. Philip G. Board
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Deepthi Menon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philip G. Board.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Board, P.G., Menon, D. Structure, function and disease relevance of Omega-class glutathione transferases. Arch Toxicol 90, 1049–1067 (2016). https://doi.org/10.1007/s00204-016-1691-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00204-016-1691-1

Keywords

Search

Navigation