Cloning and characterization of two glutathione S-transferases from pyrethroid-resistant Culex pipiens

Pest Management Science

Volumn 68, Issue 5, 2012, Pages 764-772

  Samra, Aman I ^a   Kamita, Shizuo G ^a   Yao, Hong Wei ^a,b   Cornel, Anthony J ^a   Hammock, Bruce D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Culex pipiens; Glutathione S transferase; GST; Insecticide; Mosquito

Indexed keywords

GLUTATHIONE TRANSFERASE; INSECT PROTEIN; PYRETHROID;

AMINO ACID; BIOCHEMISTRY; CLONAL GROWTH; DDT; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; METABOLISM; MOSQUITO; PERMETHRIN; PESTICIDE RESISTANCE; PYRETHROID; SUBSTRATE;

ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; CULEX; DRUG EFFECT; ENZYMOLOGY; GENETICS; INSECTICIDE RESISTANCE; KINETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY;

ANIMALS; CLONING, MOLECULAR; CULEX; GLUTATHIONE TRANSFERASE; INSECT PROTEINS; INSECTICIDE RESISTANCE; KINETICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PYRETHRINS;

CALIFORNIA; MARIN COUNTY; UNITED STATES;

CULEX PIPIENS; ESCHERICHIA COLI; HEXAPODA;

EID: 84859435247     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.2324     Document Type: Article

References (50)

1. Salinas AE and Wong MG, Glutathione S-transferases-a review. Curr Med Chem 6: 279-309 (1999).
2. Hayes JD, Flanagan JU and Jowsey IR, Glutathione transferases. Ann Rev Pharmacol Toxicol 45: 51-88 (2005).
3. Cnubben NHP, Rietjens IMCM, Wortelboer H, van Zanden J and van Bladeren PJ, The interplay of glutathione-related processes in antioxidant defense. Environ Toxicol Pharmacol 10: 141-152 (2001).
4. Ranson H and Hemingway J, Mosquito glutathione transferase, in Glutathione Transferases and gamma-Glutamyl Transpeptidases, ed. by Sies H and Packer L. Academic Press, New York, NY, pp. 226-239 (2005).
5. Chiang FM and Sun CN, Glutathione transferase isozymes of diamondback moth larvae and their role in the degradation of some organophosphorus insecticides. Pestic Biochem Physiol 45: 7-14 (1993).
6. Enayati AA, Ranson H and Hemingway J, Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14: 3-8 (2005).
7. Prapanthadara LA, Hemingway J and Ketterman AJ, Partial purification and characterization of glutathione S-transferases involved in DDT resistance from the mosquito Anopheles gambiae. Pestic Biochem Physiol 47: 119-133 (1993).
8. Lumjuan N, McCarroll L, Prapanthadara LA, Hemingway J and Ranson H, Elevated activity of an Epsilon class glutathione transferase confers DDT resistance in the dengue vector, Aedes aegypti. Insect Biochem Mol Biol 35: 861-871 (2005).
9. Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P, Prapanthadara L, et al., The role of the Aedes aegypti Epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochem Mol Biol 41: 203-209 (2011).
10. David JP, Strode C, Vontas J, Nikou D, Vaughan A, Pignatelli PM, et al., The Anopheles gambiae detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. PNAS 102: 4080-4084 (2005).
11. Qin G, Jia M, Liu T, Xuan T, Zhu KY, Guo Y, et al., Identification and characterisation of ten glutathione S-transferase genes from oriental migratory locust, Locusta migratoria manilensis (Meyen). Pest Manag Sci 67: 697-704 (2011).
12. Vontas JG, Small GJ and Hemingway J, Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J 357: 65-72 (2001).
13. Kostaropoulos I, Papadopoulos AI, Metaxakis A, Boukouvala E and Papadopoulou-Mourkidou E, Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochem Mol Biol 31: 313-319 (2001).
14. Jirajaroenrat K, Pongjaroenkit S, Krittanai C, Prapanthadara LA and Ketterman AJ, Heterologous expression and characterization of alternatively spliced glutathione S-transferases from a single Anopheles gene. Insect Biochem Mol Biol 31: 867-875 (2001).
15. Sardelis MR, Turell MJ, Dohm DJ and O'Guinn ML, Vector competence of selected North American Culex and Coquillettidia mosquitoes for West Nile virus. Emerg Infect Dis 7: 1018-1022 (2001).
16. Tsai TF, Smith GC, Happ CM, Kirk LJ, Jakob WL, Bolin RA, et al., Surveillance of St Louis encephalitis virus vectors in Grand Junction, Colorado, in 1987. J Am Mosq Control Assoc 5: 161-165 (1989).
17. Meegan JM, The Rift Valley fever epizootic in Egypt 1977-1978. 1. Description of the epizootic and virological studies. Trans R Soc Trop Med Hyg 73: 618-623 (1979).
18. Farid HA, Hammad RE, Hassan MM, Morsy ZS, Kamal IH, Weil GJ, et al., Detection of Wuchereria bancrofti in mosquitoes by the polymerase chain reaction: a potentially useful tool for large-scale control programmes. Trans R Soc Trop Med Hyg 95: 29-32 (2001).
19. Lai CH, Tung KC, Ooi HK and Wang JS, Competence of Aedes albopictus and Culex quinquefasciatus as a vector of Dirofilaria immitis after blood meal with different microfilarial density. Vet Parasitol 90: 231-237 (2000).
20. Atkinson CT, Dusek RJ, Woods KL and Iko WM, Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. J Wildlife Dis 36: 197-204 (2000).
21. Curtis CF, Pesticides and their application for the control of vectors and pests of public health importance. World Health Organization, Report No. WHO/CDS/NTD/WHOPES/GCDPP/2006.1 (2006).
22. Amin AM and Hemingway J, Preliminary investigation of the mechanisms of DDT and pyrethroid resistance in Culex quinquefasciatus Say (Diptera, Culicidae) from Saudi Arabia. Bull Entomol Res 79: 361-366 (1989).
23. Curtis CF and Pasteur N, Organophosphate resistance in vector populations of the complex of Culex pipiens L (Diptera, Culicidae). Bull Entomol Res 71: 153-161 (1981).
24. Wirth MC, Marquine M, Georghiou GP and Pasteur N, Esterase A2 and esterase B2 in Culex quinquefasciatus (Diptera, Culicidae)-role in organophosphate resistance and linkage. J Med Entomol 27: 202-206 (1990).
25. Hemingway J and Ranson H, Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45: 371-391 (2000).
26. McAbee RD, Kang KD, Stanich MA, Christiansen JA, Wheelock CE, Inman AD, et al., Pyrethroid tolerance in Culex pipiens pipiens var molestus from Marin County, California. Pest Manag Sci 60: 359-368 (2004).
27. Liu HQ, Cupp EW, Micher KM, Guo AG and Liu NN, Insecticide resistance and cross-resistance in Alabama and Florida strains of Culex quinquefaciatus. J Med Entomol 41: 408-413 (2004).
28. Hemingway J, Hawkes NJ, McCarroll L and Ranson H, The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34: 653-665 (2004).
29. Liu N, Xu Q, Zhu F and Zhang L, Pyrethroid resistance in mosquitoes. Insect Sci 13: 159-166 (2006).
30. Maeda DY, Mahajan SS, Atkins WM and Zebala JA, Bivalent inhibitors of glutathione S-transferase: the effect of spacer length on isozyme selectivity. Bioorg Med Chem Lett 16: 3780-3783 (2006).
31. Thompson JD, Higgins DG and Gibson TJ and Clustal-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680 (1994).
32. Ding YC, Ortelli F, Rossiter LC, Hemingway J and Ranson H, The Anopheles gambiae glutathione transferase supergene family: annotation, phylogeny and expression profiles. BMC Genomics 4: 35 (2003).
33. Tu CPD and Akgul B, Drosophila glutathione S-transferases, in Glutathione Transferases and gamma-Glutamyl Transpeptidases, ed. by Sies H and Packer L. Academic Press, New York, NY, pp. 204-226 (2005).
34. Altschul SF, Gish W, Miller W, Myers EW and Lipman DJ, Basic local alignment search tool. J Mol Biol 215: 403-410 (1990).
35. Tamura K, Dudley J, Nei M and Kumar S, MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599 (2007).
36. Ranson H, Prapanthadara LA and Hemingway J, Cloning and characterization of two glutathione S-transferases from a DDT-resistant strain of Anopheles gambiae. Biochem J 324: 97-102 (1997).
37. Sawicki R, Singh SP, Mondal AK, Benes H and Zimniak P, Cloning, expression and biochemical characterization of one Epsilon class (GST-3) and ten Delta class (GST-1) glutathione S-transferases from Drosophila melanogaster, and identification of additional nine members of the Epsilon class. Biochem J 370: 661-669 (2003).
38. Grant DF, Dietze EC and Hammock BD, Glutathione S-transferase isozymes in Aedes aegypti-purification, characterization, and isozyme-specific regulation. Insect Biochem 21: 421-433 (1991).
39. Abernathy CO and Casida JE, Pyrethroid insecticides: esterase cleavage in relation to selective toxicity. Science 179: 1235-1236 (1973).
40. Nakamura Y, Sugihara K, Sone T, Isobe M, Ohta S and Kitamura S, The in vitro metabolism of a pyrethroid insecticide, permethrin, and its hydrolysis products in rats. Toxicol 235: 176-184 (2007).
41. Chen LQ, Hall PR, Zhou XYE, Ranson H, Hemingway J and Meehan EJ, Structure of an insect Delta class glutathione S-transferase from a DDT-resistant strain of the malaria vector Anopheles gambiae. Acta Crystallogr, Sect D: Biol Crystallogr 59: 2211-2217 (2003).
42. Kasai S, Komagata O, Okamura Y and Tomita T, Alternative splicing and developmental regulation of glutathione transferases in Culex quinquefasciatus Say. Pestic Biochem Physiol 94: 21-29 (2009).
43. Cornel AJ, McAbee RD, Rasgon J, Stanich MA, Scott TW and Coetzee M, Differences in extent of genetic introgression between sympatric Culex pipiens and Culex quinquefasciatus (Diptera: Culicidae) in California and South Africa. J Med Entomol 40: 36-51 (2003).
44. Parkes TL, Hilliker AJ and Phillips JP, Genetic and biochemical analysis of glutathione S-transferase in the oxygen defense system of Drosophila melanogaster. Genome 36: 1007-1014 (1993).
45. Tang AH and Tu CPD, Biochemical characterization of Drosophila glutathione S-transferases D1 and D21. J Biol Chem 269: 27 876-27 884 (1994).
46. Ortelli F, Rossiter LC, Vontas J, Ranson H and Hemingway J, 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 (2003).
47. Awasthi S, Srivastava SK, Ahmad F, Ahmad H and Ansari GAS, Interactions of glutathione S-transferase pi with ethacrynic acid and its glutathione conjugate. Biochim Biophys Acta 1164: 173-178 (1993).
48. Miyamoto T, Silva M and Hammock BD, Inhibition of epoxide hydrolases and glutathione S-transferases by 2-substituted, 3-substituted, and 4-substituted derivatives of 4′-phenylchalcone and its oxide. Arch Biochem Biophys 254: 203-213 (1987).
49. Miyamoto T and Yamamoto I, Glutathione conjugates as the activated form of chalcones for glutathione S-transferase inhibition. J Pestic Sci 19: 53-58 (1994).
50. Lyon RP, Hill JJ and Atkins WM, Novel class of bivalent glutathione S-transferase inhibitors. Biochemistry 42: 10 418-10 428 (2003).