A novel Omega-class glutathione S-transferase gene in Apis cerana cerana: Molecular characterisation of GSTO2 and its protective effects in oxidative stress

Cell Stress and Chaperones

Volumn 18, Issue 4, 2013, Pages 503-516

  Zhang, Yuanying ^a,b   Yan, Huiru ^a   Lu, Wenjing ^a   Li, Yuzhen ^a   Guo, Xingqi ^a   Xu, Baohua ^a  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

^b TAISHAN MEDICAL UNIVERSITY   (China)

Author keywords

Apis cerana cerana; Biochemical properties; Gene expression pattern; GSTO2; Oxidative stress

Indexed keywords

DEHYDROASCORBIC ACID REDUCTASE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; PEROXIDASE; TRANSCRIPTION FACTOR;

ABIOTIC STRESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; APIS; APIS CERANA CERANA; ARTICLE; BINDING SITE; BRAIN TISSUE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENETIC TRANSCRIPTION; GSTO2 GENE; LARVA; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BEES; CLONING, MOLECULAR; DNA DAMAGE; ESCHERICHIA COLI; GLUTATHIONE TRANSFERASE; HYDROGEN-ION CONCENTRATION; LARVA; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; SEQUENCE ALIGNMENT; TEMPERATURE;

APIS CERANA CERANA; ESCHERICHIA COLI; HEXAPODA;

EID: 84879504491     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-013-0406-2     Document Type: Article

References (59)

1. Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybee immunocompetence. Biol Lett 6:562-565
2. Ament SA, Corona M, Pollock HS, Robinson GE (2008) Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc Natl Acad Sci USA 105:4226-4231
3. Board PG, Coggan M, Chelvanayagam G, Easteal S, Jermiin LS, Schulte GK, Danley DE, Hoth LR, Griffor MC, Kamath AV, Rosner MH, Chrunyk BA, Perregaux DE, Gabel CA, Geoghegan KF, Pandit J (2000) Identification, characterization, and crystal structure of the Omega class glutathione transferases. J Biol Chem 275:24798-24806
4. Board PG (2011) The omega-class glutathione transferases: structure, function, and genetics. Drug Metab Rev 43:226-235
5. Boldyrev AA, Yuneva MO, Sorokina EV, Kramarenko GG, Fedorova TN, Konovalova GG, Lankin VZ (2001) Antioxidant systems in tissues of senescence accelerated mice. Biochemistry (Mosc) 66:1157-1163
6. Burmeister C, Luersen K, Heinick A, Hussein A, Domagalski M, Walter RD, Liebau E (2008) Oxidative stress in Caenorhabditis elegans: protective effects of the Omega class glutathione transferase (GSTO-1). FASEB J 22:343-354
7. Carlezon WA Jr, Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28:436-445
8. Chowdhury UK, Zakharyan RA, Hernandez A, Avram MD, Kopplin MJ, Aposhian HV (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
9. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, Berenbaum MR, Feyereisen R, Oakeshott JG (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honey bee. Insect Mol Biol 15:615-636
10. Cnubben NH, Rietjens IM, Wortelboer H, van Zanden J, van Bladeren PJ (2001) The interplay of glutathione-related processes in antioxidant defense. Environ Toxicol Pharmacol 10:141-152
11. Corona M, Robinson GE (2006) Genes of the antioxidant system of the honey bee: annotation and phylogeny. Insect Mol Biol 15:687-701
12. Ding YC, Hawkes N, Meredith J, Eggleston P, Hemingway J, Ranson H (2005) Characterization of the promoters of Epsilon glutathione transferases in the mosquito Anopheles gambiae and their response to oxidative stress. Biochem J 387:879-888
13. Dixon DP, Davis BG, 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
14. 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
15. Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14:3-8
16. Ericsson A, Kotarsky K, Svensson M, Sigvardsson M, Agace W (2006) Functional characterization of the CCL25 promoter in small intestinal epithelial cells suggests a regulatory role for Caudal-Related Homeobox (Cdx) transcription factors. J Immunol 176:3642-3651
17. Frei B, England L, Ames BN (1989) Ascorbate is an outstanding antioxidant in human blood plasma. Proc Natl Acad Sci USA 86:6377-6381
18. 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
19. Gilbert MD, Wilkinson CF (1975) An inhibitor of microsomal oxidation from gut tissues of the honey bee (Apis mellifera). Comp Biochem Physiol B 50:613-619
20. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130-7139
21. Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Ann Rev Pharmacol Toxicol 45:51-88
22. Huang YF, Xu ZB, Lin XY, Feng QL, Zheng SC (2011) Structure and expression of glutathione S-transferase genes from the midgut of the Common cutworm, Spodoptera litura (Noctuidae) and their response to xenobiotic compounds and bacteria. J Insect Physiol 57:1033-1044
23. Ishida M, Mitsui T, Yamakawa K, Sugiyama N, Takahashi W, Shimura H, Endo T, Kobayashi T, Arita J (2007) Involvement of cAMP response element-binding protein in the regulation of cell proliferation and the prolactin promoter of lactotrophs in primary culture. Am J Physiol Endocrinol Metab 293:E1529-E1537
24. Kampkötter A, Volkmann TE, de Castro SH, Leiers B, Klotz LO, Johnson TE, Link CD, Henkle-Duhrsen K (2003) Functional analysis of the glutathione S-transferase 3 from Onchocerca volvulus (Ov-GST-3): a parasite GST confers increased resistance to oxidative stress in Caenorhabditis elegans. J Mol Biol 325:25-37
25. Ketterman AJ, Saisawang C, Wongsantichon J (2011) Insect glutathione transferases. Drug Metab Rev 43:253-265
26. Kim K, Kim SH, Kim J, Kim H, Yim J (2012) Glutathione S-transferase Omega 1 activity is sufficient to suppress neurodegeneration in a Drosophila model of Parkinson disease. J Biol Chem 287:6628-6641
27. Krishnan N, Sehnal F (2006) Compartmentalization of oxidative stress and antioxidant defense in the larval gut of Spodoptera littoralis. Arch Insect Biochem Physiol 63:1-10
28. Kottuparambil S, Shinb W, Brownc MT, Han T (2012) UV-B affects photosynthesis, ROS production and motility of the freshwater flagellate, Euglena agilis Carter. Aquat Toxicol 122-123:206-213
29. Laliberte RE, Perregaux DG, Hoth LR, Rosner PJ, Jordan CK, Peese KM, Eggler JF, Dombroski MA, Geoghegan KF, Gabel CA (2003) Glutathione S-transferase Omega 1-1 is a target of cytokine release inhibitory drugs and may be responsible for their effect on interleukin-1β posttranslational processing. J Biol Chem 278:16567-16578
30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-(Delta Delta C(T)) method. Methods 25:402-408
31. Li HM, Buczkowski G, Mittapalli O, Xie J, Wu J, Westerman R, Schemerhorn BJ, Murdock LL, Pittendrigh BR (2008) Transcriptomic profiles of Drosophila melanogaster third instar larval midgut and responses to oxidative stress. Insect Mol Biol 17:325-339
32. Li X, Zhang X, Zhang J, Zhang X, Starkey SR, Zhu KY (2009) Identification and characterization of eleven glutathione S-transferase genes from the aquatic midge Chironomus tentans (Diptera: Chironomidae). Insect Biochem Mol Biol 39:745-754
33. Li YJ, Oliveira SA, Xu P, Martin ER, Stenger JE, Scherzer CR, Hauser MA, Scott WK, Small GW, Nance MA, Watts RL, Hubble JP, Koller WC, Pahwa R, Stern MB, Hiner BC, Jankovic J, Goetz CG, Mastaglia F, Middleton LT, Roses AD, Saunders AM, Schmechel DE, Gullans SR, Haines JL, Gilbert JR, Vance JM, Pericak-Vance MA, Hulette C, Welsh-Bohmer KA (2003) Glutathione S-transferase Omega-1 modifies age-at-onset of Alzheimer disease and Parkinson disease. Hum Mol Genet 12:3259-3267
34. Lourenco AP, Mackert A, Cristino AS, Simoes ZLP (2008) Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39:372-385
35. Lumjuan N, McCarroll L, Prapanthadara L, Hemingway J, Ranson H (2005) Elevated activity of an Epsilon class glutathione transferase confers DDT resistance in the dengue vector, Aedes aegypti. Insect Biochem Mol Biol 35:861-871
36. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13-30
37. Mahmoud KZ, Edens FW (2003) Influence of selenium sources on age-related and mild heat stress-related changes of blood and liver glutathione redox cycle in broiler chicken (Gallus domesticus). Comp Biochem Physiol B Biochem Mol Biol 136:921-934
38. Meng F, Kang M, Liu L, Luo L, Xu B, Guo X (2011) Characterization of the TAK1 gene in Apis cerana cerana (AccTAK1) and its involvement in the regulation of tissue-specific development. BMB Rep 44:187-192
39. Meng F, Zhang L, Kang M, Guo X, Xu B (2010) Molecular characterization, immunohistochemical localization and expression of a ribosomal protein L17 gene from Apis cerana cerana. Arch Insect Biochem Physiol 75:121-138
40. Michelette ERF, Soares AEE (1993) Characterization of preimaginal developmental stages in Africanized honey bee workers (Apis mellifera L). Apidologie 24:431-440
41. Ortelli F, Rossiter LC, Vontas J, Ranson H, Hemingway J (2003) Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. Biochem J 373:957-963
42. Poli G, Leonarduzzi G, Biasi F, Chiarpotto E (2004) Oxidative stress and cell signaling. Curr Med Chem 11:1163-1182
43. Rice ME (2000) Ascorbate regulation and its neuroprotective role in the brain. Trends Neurosci 23:209-216
44. Rival T, Soustelle L, Strambi C, Besson MT, Iche M, Birman S (2004) Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in Drosophila brain. Curr Biol 14:599-605
45. Rørth P (1994) Specification of C/EBP function during Drosophila development by the bZIP basic region. Science 266:1878-1881
46. 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
47. Scharlaken B, de Graaf DC, Goossens K, Brunain M, Peelman LJ, Jacobs FJ (2008) Reference gene selection for insect expression studies using quantitative real-time PCR: The honeybee, Apis mellifera, head after a bacterial challenge. J Insect Sci 8:1-10
48. Singh SP, Coronella JA, Benes H, Cochrane BJ, Zimniak P (2001) Catalytic function of Drosophila melanogaster glutathione S-transferase DmGSTS1-1 (GST-2) in conjugation of lipid peroxidation end products. Eur J Biochem 268:2912-2923
49. Stanojević D, Hoey T, Levine M (1989) Sequence specific DNA-binding activities of the gap proteins encoded by hunchback and Krüppel in Drosophila. Nature 341:331-335
50. Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266:37-56
51. Walters KB, Grant P, Johnson DL (2009) Evolution of the GST Omega gene family in 12 Drosophila species. J Hered 100:742-753
52. Wan Q, Whang I, Lee JS, Lee J (2009) Novel Omega glutathione S-transferases in disk abalone: characterization and protective roles against environmental stress. Comp Biochem Physiol C Toxicol Pharmacol 150:558-568
53. Wells WW, Xu DP, Washburn MP (1995) Glutathione: dehydroascorbate oxidoreductases. Methods Enzymol 252:30-38
54. Xun L, Belchik SM, Xun R, Huang Y, Zhou H, Sanchez E, Kang C, Board PG (2010) S-glutathionyl-(chloro)hydroquinone reductases: a novel class of glutathione transferases. Biochem J 428:419-427
55. Yamamoto K, Zhang P, Miake F, Kashige N, Aso Y, Banno Y, Fujii H (2005) Cloning, expression and characterization of theta-class glutathione S-transferase from the silkworm, Bombyx mori. Comp Biochem Physiol B Biochem Mol Biol 141:340-346
56. Yamamoto K, Teshiba S, Shigeoka Y, Aso Y, Banno Y, Fujiki T, Katakura Y (2011) Characterization of an Omega-class glutathione S-transferase in the stress response of the silkmoth. Insect Mol Biol 20:379-386
57. Yin S, Li X, Meng Y, Finley RL Jr, Sakr W, Yang H, Reddy N, Sheng S (2005) Tumor-suppressive maspin regulates cell response to oxidative stress by direct interaction with glutathione S-transferase. J Biol Chem 280:34985-34996
58. Yu F, Kang M, Meng F, Guo X, Xu B (2011) Molecular cloning and characterization of a thioredoxin peroxidase gene from Apis cerana cerana. Insect Mol Biol 20:367-378
59. 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 420:190-203