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The silkworm GSTe4 is sensitive to phoxim and protects HEK293 cells against UV-induced cell apoptosis

Published online by Cambridge University Press:  08 April 2015

X.Y. Chen ,
J. Liu ,
C.D. Zhang ,
Y.F. Li ,
T.H. Liu ,
L. Wang ,
Q.Y. Yu ,
Y.H. Zhang ,
C. Lu  and
M.H. Pan
X.Y. Chen
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
J. Liu
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China The management of experimental teaching center, ChongQing Medical University, Chongqing 400016, China
C.D. Zhang
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China Department of Biochemistry and Molecular Biology, ChongQing Medical University, Chongqing 400016, China
Y.F. Li
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
T.H. Liu
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
L. Wang
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China
Q.Y. Yu
Affiliation:
The Institute of Agricultural and Life Sciences, Chongqing University, Chongqing 400044, China
Y.H. Zhang
Affiliation:
The Sericultural Research Institute, Sichuan Academy of Agricultural Science, Sichuan 637000, China
C. Lu
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China Key Laboratory for Sericulture Functional Genomics and Biotechnology of Agricultural Ministry, Southwest University, Chongqing 400716, China
M.H. Pan*
Affiliation:
State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, China Key Laboratory for Sericulture Functional Genomics and Biotechnology of Agricultural Ministry, Southwest University, Chongqing 400716, China
*
*Author for correspondence Phone: +86 23 68250793 Fax: +86 23 68251128 E-mail: [email protected]
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Abstract

Glutathione S-transferases (GSTs, EC 2.5.1.18) are a family of super enzymes with multiple functions that play a major role in the detoxification of endogenous and xenobiotic compounds. In our previous study, we have predicted 23 putative cytosolic GSTs in the silkworm genome using bioinformatic methods. In this study, we cloned and studied the insect-specific epsilon-class GST gene GSTe4 from the silkworm, Bombyx mori. The recombinant BmGSTe4 (Bac-BmGSTe4) was overexpressed in SF-9 cell lines, and it was found to have effective GST activity. We also found that the expression of BmGSTe4 was especially down-regulated after the silkworms were fumigated with or ingested phoxim. Moreover, BmGSTe4 protected HEK293 cells against UV-induced cell apoptosis. These results demonstrated that BmGSTe4 has GST activity, is sensitive to phoxim, and plays a role in inhibition of UV-induced cell apoptosis.

Keywords

glutathione S-transferasefunctionsensitive to phoximcell apoptosis
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 4 , August 2015 , pp. 399 - 407
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Copyright
Copyright © Cambridge University Press 2015 

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References

Adler, V., Yin, Z., Fuchs, S.Y., Benezra, M., Rosario, L., Tew, K.D. & Ronai, Z.E. (1999) Regulation of JNK signaling by GSTp. EMBO journal 18, 1321–1334.Google Scholar
Armstrong, R.N. (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. Chemical Research in Toxicology 10, 2–18.Google Scholar
Board, P., Russell, R.J., Marano, R.J. & Oakeshott, J.G. (1994) Purification, molecular cloning and heterologous expression of a glutathione S-transferase from the Australian sheep blowfly (Lucilia cuprina). Biochemical Journal 299, 425–430.CrossRefGoogle ScholarPubMed
Board, P.G., Coggan, M., Wilce, M.C. & Parker, M.W. (1995) Evidence for an essential serine residue in the active site of the Theta class glutathione transferases. Biochemical Journal 311, 247–250.Google Scholar
Board, P.G., Baker, R.T., Chelvanayagam, G. & Jermiin, L. (1997) Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochemical Journal 328, 929–935.Google Scholar
Cho, S.G., Lee, Y.H., Park, H.S., Ryoo, K., Kang, K.W., Park, J. & Choi, E.J. (2001) Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. Journal of Biological Chemistry 276, 12749–12755.Google Scholar
Claudianos, C., Ranson, H., Johnson, R.M., Biswas, S., Schuler, M.A., Berenbaum, M.R., Feyereisen, R. & Oakeshott, J.G. (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Molecular Biology 15, 615–636.Google Scholar
Enayati, A.A., Ranson, H. & Hemingway, J. (2005) Insect glutathione transferases and insecticide resistance. Insect Molecular Biology 14, 3–8.CrossRefGoogle ScholarPubMed
Fan, Y., Wu, D., Jin, L. & Yin, Z. (2005) Human glutamylcysteine synthetase protects HEK293 cells against UV-induced cell death through inhibition of c-Jun NH2-terminal kinase. Cell Biology International 29, 695–702.Google Scholar
Feng, Q.L., Davey, K.G., Pang, A.S.D., Primavera, M., Ladd, T.R., Zheng, S.C., Sohi, S.S., Retnakaran, A & Palli, S.R. (1999) Glutathione S-transferase from the spruce budworm, Choristoneura fumiferana: identification, characterization, localization, cDNA cloning, and expression. Insect Biochemistry and Molecular Biology 29, 779–793.Google Scholar
Fournier, D., Bride, J.M., Poirie, M., Berge, J.B. & Plapp, F.W. (1992) Insect glutathione S-transferases. Biochemical characteristics of the major forms from houseflies susceptible and resistant to insecticides. Journal of Biological Chemistry 267, 1840–1845.Google Scholar
Goldsmith, M.R., Shimada, T. & Abe, H. (2005) The genetics and genomics of the silkworm, Bombyx mori . Annual Review of Entomology 50, 71–100.Google Scholar
Gui, Z., Hou, C., Liu, T., Qin, G., Li, M. & Jin, B. (2009) Effects of insect viruses and pesticides on glutathione S-transferase activity and gene expression in Bombyx mori. Journal of Economic Entomology 102, 1591–1598.Google Scholar
Habig, W.H., Pabst, M.J. & Jakoby, W.B. (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 7130–7139.Google Scholar
Hayes, J.D., Flanagan, J.U. & Jowsey, I.R. (2005) Glutathione transferases. Annual Review of Pharmacology and Toxicology 45, 51–88.Google Scholar
Huang, H.S., Hu, N.T., Yao, Y.E., Wu, C.Y., Chiang, S.W. & Sun, C.N. (1998) Molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the diamondback moth, Plutella xylostella . Insect Biochemistry and Molecular Biology 28, 651–658.Google Scholar
International Silkworm Genome Consortium (2008) The genome of a lepidopteran model insect, the silkworm Bombyx mori . Insect Biochemistry and Molecular Biology 38, 1036–1045.Google Scholar
Ishisaki, A., Hayashi, H., Suzuki, S., Ozawa, K., Mizukoshi, E., Miyakawa, K., Suzuki, M. & Imamura, T. (2001) Glutathione S-transferase Pi is a dopamine-inducible suppressor of dopamine-induced apoptosis in PC12 cells. Journal of Neurochemistry 77, 1362–1371.CrossRefGoogle ScholarPubMed
Li, X., Schuler, M.A. & Berenbaum, M.R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231–253.Google Scholar
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25, 402–408.Google Scholar
Lumjuan, N., Stevenson, B.J., Prapanthadara, L., Somboon, P., Brophy, P.M., Loftus, B.J., Severson, D.W. & Ranson, H. (2007) The Aedes aegypti glutathione transferase family. Insect Biochemistry and Molecular Biology 37, 1026–1035.Google Scholar
Martin, S.A. & Ouchi, T. (2005) BRCA1 phosphorylation regulates caspase-3 activation in UV-induced apoptosis. Cancer Research 65, 10657–10662.CrossRefGoogle ScholarPubMed
Matsuoka, T. & Fujiwara, H. (2000) Expression of ecdysteroid-regulated genes is reduced specifically in the wing discs of the wing-deficient mutant (fl) of Bombyx mori . Development Genes and Evolution 210, 120–128.Google Scholar
Oakley, A. (2011) Glutathione transferases: a structural perspective. Drug Metabolism Review 43, 138–151.Google Scholar
Piaggi, S., Raggi, C., Corti, A., Pitzalis, E., Mascherpa, M.C., Saviozzi, M., Pompella, A. & Casini, A.F. (2010) Glutathione transferase omega 1–1 (GSTO1–1) plays an anti-apoptotic role in cell resistance to cisplatin toxicity. Carcinogenesis 31, 804–811.Google Scholar
Ranson, H. & Hemingway, J. (2005) Mosquito glutathione transferases. Methods in Enzymology 401, 226–241.CrossRefGoogle ScholarPubMed
Ranson, H., Rossiter, L., Ortelli, F., Jensen, B., Wang, X., Roth, C., Collins, F.H. & Hemingway, J. (2001) Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae . Biochemical Journal 359, 295–304.CrossRefGoogle ScholarPubMed
Ranson, H., Claudianos, C., Ortelli, F., Abgrall, C., Hemingway, J., Sharakhova, M.V., Unger, M.F., Collins, F.H. & Feyereisen, R. (2002) Evolution of supergene families associated with insecticide resistance. Science 298, 179–181.Google Scholar
Reinemer, P., Prade, L., Hof, P., Neuefeind, T., Huber, R., Zettl, R., Palme, K., Schell, J., Koelln, I., Bartunik, H.D. & Bieseler, B. (1996) Three-dimensional structure of glutathione S-transferase from Arabidopsis thaliana at 2.2 Å resolution: structural characterization of herbicide-conjugating plant glutathione S-transferases and a novel active site architecture. Journal of Molecular Biology 255, 289–309.Google Scholar
Rossjohn, J., McKinstry, W.J., Oakley, A.J., Verger, D., Flanagan, J., Chelvanayagam, G., Tan, K.L., Board, P.G. & Parker, M.W. (1998) Human theta class glutathione transferase: the crystal structure reveals a sulfate-binding pocket within a buried active site. Structure 6, 309–322.Google Scholar
Ryoo, K., Huh, S.H., Lee, Y.H., Yoon, K.W., Cho, S.G. & Choi, E.J. (2004) Negative regulation of MEKK1-induced signaling by glutathione S-transferase Mu. Journal of Biological Chemistry 279, 43589–43594.Google Scholar
Sheehan, D., Meade, G., Foley, V. & Dowd, C. (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochemical Journal 360, 1–16.Google Scholar
Singh, S.P., Coronella, J.A., Beneš, H., Cochrane, B.J. & Zimniak, P. (2001) Catalytic function of Drosophila melanogaster glutathione S transferase DmGSTS1–1 (GST-2) in conjugation of lipid peroxidation end products. European Journal of Biochemistry 268, 2912–2923.CrossRefGoogle ScholarPubMed
Snyder, M.J., Walding, J.K. & Feyereisen, R. (1995) Glutathione S-transferases from larval Manduca sexta midgut: sequence of two cDNAs and enzyme induction. Insect Biochemistry and Molecular Biology 25, 455–465.Google Scholar
Tjalkens, R.B., Valerio, L.G. Jr., Awasthi, Y.C. & Petersen, D.R. (1998) Association of glutathione S-transferase isozyme-specific induction and lipid peroxidation in two inbred strains of mice subjected to chronic dietary iron overload. Toxicology and Applied Pharmacology 151, 174–181.Google Scholar
Tu, C.P. & Akgul, B. (2005) Drosophila glutathione S-transferases. Methods in Enzymology 401, 204–226.Google Scholar
Vararattanavech, A., Prommeenate, P. & Ketterman, A. (2006) The structural roles of a conserved small hydrophobic core in the active site and an ionic bridge in domain I of Delta class glutathione S-transferase. Biochemical Journal 393, 89–95.Google Scholar
Vontas, J., Small, G. & Hemingway, J. (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens . Biochemical Journal 357, 65–72.Google Scholar
Vontas, J., Small, G., Nikou, D., Ranson, H. & Hemingway, J. (2002) Purification, molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the rice brown planthopper, Nilaparvata lugens . Biochemical Journal 362, 329–337.Google Scholar
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 . Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 141, 340–346.CrossRefGoogle ScholarPubMed
Yamamoto, K., Zhang, P.B., Banno, Y. & Fujii, H. (2006) Identification of a sigma-class glutathione-S-transferase from the silkworm, Bombyx mori . Journal of Applied Entomology 130, 515–522.CrossRefGoogle Scholar
Yamamoto, K., Nagaoka, S., Banno, Y. & Aso, Y. (2009 a) Biochemical properties of an omega-class glutathione S-transferase of the silkmoth, Bombyx mori . Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 149, 461–467.Google ScholarPubMed
Yamamoto, K., Shigeoka, Y., Aso, Y., Banno, Y., Kimura, M. & Nakashima, T. (2009 b) Molecular and biochemical characterization of a Zeta-class glutathione S-transferase of the silkmoth. Pesticide Biochemistry and Physiology 94, 30–35.Google Scholar
Yamamoto, K., Aso, Y. & Yamada, N. (2013) Catalytic function of an Epsilon – class glutathione S-transferase of the silkworm. Insect Molecular Biology 22, 523–531.Google Scholar
Yu, Q., Lu, C., Li, B., Fang, S., Zuo, W., Dai, F., Zhang, Z. & Xiang, Z. (2008) Identification, genomic organization and expression pattern of glutathione S-transferase in the silkworm, Bombyx mori . Insect Biochemistry and Molecular Biology 38, 1158–1164.Google Scholar
Yu, Q.Y., Fang, S.M., Zuo, W.D., Dai, F.Y., Zhang, Z. & Lu, C. (2011) Effect of organophosphate phoxim exposure on certain oxidative stress biomarkers in the silkworm. Journal of Economic Entomology 104, 101–106.Google Scholar
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