1,014
Views
74
CrossRef citations to date
0
Altmetric
Review Article

The omega-class glutathione transferases: structure, function, and genetics

Pages 226-235 | Received 23 Jan 2011, Accepted 04 Feb 2011, Published online: 15 Apr 2011

References

  • Adam, G. C., Sorensen, E. J., Cravatt, B. F. (2002). Proteomic profiling of mechanistically distinct enzyme classes using a common chemotype. Nat Biotechnol 20:805–809.
  • Andonova, I. E., Justenhoven, C., Winter, S., Hamann, U., Baisch, C., Rabstein, S., et al. (2010). No evidence for glutathione S-transferases GSTA2, GSTM2, GSTO1, GSTO2, and GSTZ1 in breast cancer risk. Breast Cancer Res Treat 121:497–502.
  • Armstrong, R. N. (1997). Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem Res Toxicol 10:2–18.
  • Bachovchin, D. A., Brown, S. J., Rosen, H., Cravatt, B. F. (2009). Identification of selective inhibitors of uncharacterized enzymes by high-throughput screening with fluorescent activity-based probes. Nat Biotechnol 27:387–394.
  • Ball, L. J., Kuhne, R., Schneider-Mergener, J., Oschkinat, H. (2005). Recognition of proline-rich motifs by protein-protein-interaction domains. Angew Chem Int Ed Engl 44:2852–2869.
  • Berenson, J. R., Yeh, H. S. (2006). Arsenic compounds in the treatment of multiple myeloma: a new role for a historical remedy. Clin Lymphoma Myeloma 7:192–198.
  • Board, P. G., Anders, M. W. (2007). Glutathione transferase omega 1 catalyzes the reduction of S-(phenacyl)glutathiones to acetophenones. Chem Res Toxicol 20:149–154.
  • Board, P. G., Coggan, M., Cappello, J., Zhou, H., Oakley, A. J., Anders, M. W. (2008). S-(4-Nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1. Anal Biochem 374:25–30.
  • Board, P. G., Coggan, M., Chelvanayagam, G., Easteal, S., Jermiin, L. S., Schulte, G. K., et al. (2000). Identification, characterization, and crystal structure of the omega class glutathione transferases. J Biol Chem 275:24798–24806.
  • Burmeister, C., Luersen, K., Heinick, A., Hussein, A., Domagalski, M., Walter, R. D., et al. (2008). Oxidative stress in Caenorhabditis elegans: protective effects of the omega class glutathione transferase (GSTO-1). FASEB J 22:343–354.
  • Capurso, C., Panza, F., Seripa, D., Frisardi, V., Imbimbo, B. P., Verdile, G., et al. (2010). Polymorphisms in glutathione S-transferase omega-1 gene and increased risk of sporadic Alzheimer’s disease. Rejuvenation Res 13:645–652.
  • Chariyalertsak, S., Purisa, W., Sangrajrang, S. (2009). Role of glutathione S-transferase omega gene polymorphisms in breast-cancer risk. Tumori 95:739–743.
  • Chowdhury, U. K., Zakharyan, R. A., Hernandez, A., Avram, M. D., Kopplin, M. J., Aposhian, H. V. (2006). Glutathione-S-transferase-omega [MMA(V) reductase] knockout mice: enzyme and arsenic species concentrations in tissues after arsenate administration. Toxicol Appl Pharmacol 216:446–457.
  • Cromer, B. A., Gorman, M. A., Hansen, G., Adams, J. J., Coggan, M., Littler, D. R., et al. (2007). Structure of the Janus protein human CLIC2. J Mol Biol 374:719–731.
  • Dixon, D. P., Davis, B. G., Edwards, R. (2002). Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869.
  • 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 276:3319–3323.
  • Fahn, S., Cohen, G. (1992). The oxidant stress hypothesis in Parkinson’s disease: evidence supporting it. Ann Neurol 32:804–812.
  • Fornai, F., Gesi, M., Saviozzi, M., Lenzi, P., Piaggi, S., Ferrucci, M., et al. (2001a). Immunohistochemical evidence and ultrastructural compartmentalization of a new antioxidant enzyme in the rat substantia nigra. J Neurocytol 30:97–105.
  • Fornai, F., Piaggi, S., Gesi, M., Saviozzi, M., Lenzi, P., Paparelli, A., et al. (2001b). Subcellular localization of a glutathione-dependent dehydroascorbate reductase within specific rat brain regions. Neuroscience 104:15–31.
  • Fornai, F., Saviozzi, M., Piaggi, S., Gesi, M., Corsini, G. U., Malvaldi, G., et al. (1999). Localization of a glutathione-dependent dehydroascorbate reductase within the central nervous system of the rat. Neuroscience 94:937–948.
  • Garcera, A., Barreto, L., Piedrafita, L., Tamarit, J., Herrero, E. (2006). Saccharomyces cerevisiae cells have three omega class glutathione S-transferases acting as 1-Cys thiol transferases. Biochem J 398:187–196.
  • Granja, F., Morari, E. C., Assumpcao, L. V., Ward, L. S. (2005). GSTO polymorphism analysis in thyroid nodules suggest that GSTO1 variants do not influence the risk for malignancy. Eur J Cancer Prev 14:277–280.
  • Harrop, S. J., DeMaere, M. Z., Fairlie, W. D., Reztsova, T., Valenzuela, S. M., Mazzanti, M., et al. (2001). Crystal structure of a soluble form of the intracellular chloride ion channel CLIC1 (NCC27) at 1.4-A resolution. J Biol Chem 276:44993–45000.
  • Hayes, J. D., Flanagan, J. U., Jowsey, I. R. (2005). Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88.
  • Ishikawa, T., Casini, A. F., Nishikimi, M. (1998). Molecular cloning and functional expression of rat liver glutathione-dependent dehydroascorbate reductase. J Biol Chem 273:28708–28712.
  • 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 274:5131–5137.
  • Kolsch, H., Linnebank, M., Lutjohann, D., Jessen, F., Wullner, U., Harbrecht, U., et al. (2004). Polymorphisms in glutathione S-transferase omega-1 and AD, vascular dementia, and stroke. Neurology 63:2255–2260.
  • Kuwano, R., Miyashita, A., Arai, H., Asada, T., Imagawa, M., Shoji, M., et al. (2006). Dynamin-binding protein gene on chromosome 10q is associated with late-onset Alzheimer’s disease. Hum Mol Genet 15:2170–2182.
  • Laliberte, R. E., Perregaux, D. G., Hoth, L. R., Rosner, P. J., Jordan, C. K., Peese, K. M., 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 278:16567–16578.
  • Li, Y. J., Oliveira, S. A., Xu, P., Martin, E. R., Stenger, J. E., Scherzer, C. R., et al. (2003). Glutathione S-transferase omega-1 modifiesage-at-onset of Alzheimer’s disease and Parkinson’s disease. Hum Mol Genet 12:3259–3267.
  • Li, Y. J., Scott, W. K., Hedges, D. J., Zhang, F., Gaskell, P. C., Nance, M. A., et al. (2002). Age at onset in two common neurodegenerative diseases is genetically controlled. Am J Hum Genet 70:985–993.
  • Li, Y. J., Scott, W. K., Zhang, L., Lin, P. I., Oliveira, S. A., Skelly, T., et al. (2006). Revealing the role of glutathione S-transferase omega in age-at-onset of Alzheimer’s and Parkinson’s diseases. Neurobiol Aging 27:1087–1093.
  • Mannervik, B., Board, P. G., Hayes, J. D., Listowsky, I., Pearson, W. R. (2005). Nomenclature for mammalian soluble glutathione transferases. Meth Enzymol 401:1–8.
  • Mannervik, B., Danielson, U. H. (1988). Glutathione transferases—structure and catalytic activity. CRC Crit Rev Biochem 23:283–337.
  • Marnell, L. L., Garcia-Vargas, G. G., Chowdhury, U. K., Zakharyan, R. A., Walsh, B., Avram, M. D., et al. (2003). Polymorphisms in the human monomethylarsonic acid (MMA V) reductase/hGSTO1 gene and changes in urinary arsenic profiles. Chem Res Toxicol 16:1507–1513.
  • Masoudi, M., Saadat, I., Omidvari, S., Saadat, M. (2009). Genetic polymorphisms of GSTO2, GSTM1, and GSTT1 and risk of gastric cancer. Mol Biol Rep 36:781–784.
  • Mattson, M. P. (2004). Pathways towards and away from Alzheimer’s disease. Nature 430:631–639.
  • McGeer, P. L., McGeer, E. G. (2001). Polymorphisms in inflammatory genes and the risk of Alzheimer’s disease. Arch Neurol 58:1790–1792.
  • Mukherjee, B., Salavaggione, O. E., Pelleymounter, L. L., Moon, I., Eckloff, B. W., Schaid, D. J., et al. (2006). Glutathione S-transferase omega 1 and omega 2 pharmacogenomics. Drug Metab Dispos 34:1237–1246.
  • 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 20:901–902.
  • Nishimura, M., Mizuta, I., Mizuta, E., Yamasaki, S., Ohta, M., Kuno, S. (2000). Influence of interleukin-1beta gene polymorphisms on age-at-onset of sporadic Parkinson’s disease. Neurosci Lett 284:73–76.
  • 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 368:140–143.
  • Ozturk, A., Desai, P. P., Minster, R. L., Dekosky, S. T., Kamboh, M. I. (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 26:1161–1165.
  • 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 110:463–468.
  • Paiva, L., Marcos, R., Creus, A., Coggan, M., Oakley, A. J., Board, P. G. (2008). Polymorphism of glutathione transferase omega 1 in a population exposed to a high environmental arsenic burden. Pharmacogenet Genomics 18:1–10.
  • Paolicchi, A., Pezzini, A., Saviozzi, M., Piaggi, S., Andreuccetti, M., Chieli, E., et al. (1996). Localization of a GSH-dependent dehydroascorbate reductase in rat tissues and subcellular fractions. Arch Biochem Biophys 333:489–495.
  • Papassotiropoulos, A., Lambert, J. C., Wavrant-De Vrieze, F., Wollmer, M. A., von der Kammer, H., Streffer, J. R., Maddalena, A., et al. (2005). Cholesterol 25-hydroxylase on chromosome 10q is a susceptibility gene for sporadic Alzheimer’s disease. Neurodegener Dis 2:233–241.
  • Pearson, W. R. (2005). Phylogenies of glutathione transferase families. Meth Enzymol 401:186–204.
  • Peddareddygari, L. R., Dutra, A. V., Levenstien, M. A., Sen, S., Grewal, R. P. (2009). An analysis of methylenetetrahydrofolate reductase and glutathione S-transferase omega-1 genes as modifiers of the cerebral response to ischemia. BMC Neurol 9:37.
  • Pongstaporn, W., Pakakasama, S., Sanguansin, S., Hongeng, S., Petmitr, S. (2009). Polymorphism of glutathione S-transferase omega gene: association with risk of childhood acute lymphoblastic leukemia. J Cancer Res Clin Oncol 135:673–678.
  • Pongstaporn, W., Rochanawutanon, M., Wilailak, S., Linasamita, V., Weerakiat, S., Petmitr, S. (2006). Genetic alterations in chromosome 10q24.3 and glutathione S-transferase omega 2 gene polymorphism in ovarian cancer. J Exp Clin Cancer Res 25:107–114.
  • Rice, M. E. (2000). Ascorbate regulation and its neuroprotective role in the brain. Trends Neurosci 23:209–216.
  • Rouimi, P., Anglade, P., Benzekri, A., Costet, P., Debrauwer, L., Pineau, T., Tulliez, J. (2001). Purification and characterization of a glutathione S-transferase omega in pig: evidence for two distinct organ-specific transcripts. Biochem J 358:257–262.
  • Sampayo-Reyes, A., Zakharyan, R. A. (2006). Inhibition of human glutathione S-transferase omega by tocopherol succinate. Biomed Pharmacother 60:238–244.
  • Schmuck, E., Cappello, J., Coggan, M., Brew, J., Cavanaugh, J. A., Blackburn, A. C., 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 40:2553–2559.
  • Schmuck, E. M., Board, P. G., Whitbread, A. K., Tetlow, N., Cavanaugh, J. A., Blackburn, A. C., 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 15:493–501.
  • Simonian, N. A., Coyle, J. T. (1996). Oxidative stress in neurodegenerative diseases. Annu Rev Pharmacol Toxicol 36:83–106.
  • Son, J., Lee, J. J., Lee, J. S., Schuller, A., Chang, Y. T. (2010). Isozyme-specific fluorescent inhibitor of glutathione S-transferase omega 1. ACS Chem Biol 5:449–453.
  • Story, M. D., Meyn, R. E. (1999). Modulation of apoptosis and enhancement of chemosensitivity by decreasing cellular thiols in a mouse B-cell lymphoma cell line that overexpresses bcl-2. Cancer Chemother Pharmacol 44:362–366.
  • Tallman, M. S. (2007). Treatment of relapsed or refractory acute promyelocytic leukemia. Best Pract Res Clin Haematol 20:57–65.
  • Tanaka-Kagawa, T., Jinno, H., Hasegawa, T., Makino, Y., Seko, Y., Hanioka, N., et al. (2003). Functional characterization of two variant human GSTO 1-1s (Ala140Asp and Thr217Asn). Biochem Biophys Res Commun 301:516–520.
  • van de Giessen, E., Fogh, I., Gopinath, S., Smith, B., Hu, X., Powell, J., et al. (2008). Association study on glutathione S-transferase omega 1 and 2 and familial ALS. Amyotroph Lateral Scler 9:81–84.
  • Walters, K. B., Grant, P., Johnson, D. L. (2009). Evolution of the GST omega gene family in 12 Drosophila species. J Hered 100:742–753.
  • Wang, L., Xu, J., Ji, C., Gu, S., Lv, Y., Li, S., et al. (2005). Cloning, expression, and characterization of human glutathione S-transferase omega 2. Int J Mol Med 16:19–27.
  • Wang, Y. H., Yeh, S. D., Shen, K. H., Shen, C. H., Juang, G. D., Hsu, L. I., et al. (2009). A significantly joint effect between arsenic and occupational exposures and risk genotypes/diplotypes of CYP2E1, GSTO1, and GSTO2 on risk of urothelial carcinoma. Toxicol Appl Pharmacol 241:111–118.
  • Whitbread, A. K., Masoumi, A., Tetlow, N., Schmuck, E., Coggan, M., Board, P. G. (2005). Characterization of the omega class of glutathione transferases. Meth Enzymol 401:78–99.
  • Whitbread, A. K., Mellick, G. D., Silburn, P. A., Le Couteur, D. G., Board, P. G. (2004). Glutathione transferase omega class polymorphisms in Parkinson’s disease. Neurology 62:1910–1911.
  • Whitbread, A. K., Tetlow, N., Eyre, H. J., Sutherland, G. R., Board, P. G. (2003). Characterization of the human omega class glutathione transferase genes and associated polymorphisms. Pharmacogenetics 13:131–144.
  • Wilk, J. B., Walter, R. E., Laramie, J. M., Gottlieb, D. J., and O’Connor, G. T. (2007). Framingham Heart Study genome-wide association: results for pulmonary function measures. BMC Med Genet 8(Suppl 1):S8.
  • Wilson, R., Ainscough, R., Anderson, K., Baynes, C., Berks, M., Bonfield, J., et al. (1994). 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368:32–38.
  • Xun, L., Belchik, S. M., Xun, R., Huang, Y., Zhou, H., Sanchez, E., et al. (2010). S-glutathionyl-(chloro)hydroquinone reductases: a novel class of glutathione transferases. Biochem J 428:419–427.
  • Yan, X. D., Pan, L. Y., Yuan, Y., Lang, J. H., 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 6:772–780.
  • Yanbaeva, D. G., Wouters, E. F., Dentener, M. A., Spruit, M. A., Reynaert, N. L. (2009). Association of glutathione-S-transferase omega haplotypes with susceptibility to chronic obstructive pulmonary disease. Free Radic Res 43:738–743.
  • Yin, Z. L., Dahlstrom, J. E., Le Couteur, D. G., Board, P. G. (2001). Immunohistochemistry of omega class glutathione S-transferase in human tissues. J Histochem Cytochem 49:983–987.
  • Yu, L., Kalla, K., Guthrie, E., Vidrine, A., Klimecki, W. T. (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 111:1421–1427.
  • Zakharyan, R. A., Sampayo-Reyes, A., Healy, S. M., Tsaprailis, G., Board, P. G., Liebler, D. C., et al. (2001). Human monomethylarsonic acid (MMA(V)) reductase is a member of the glutathione-S-transferase superfamily. Chem Res Toxicol 14:1051–1057.
  • Zhou, H., Brock, J., Casarotto, M. G., Oakley, A. J., Board, P. G. (2011). Novel folding and stability defects cause a deficiency of human glutathione transferase omega 1. J Biol Chem 286:4271–4279.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.