Constitutive activation of the Nrf2/Keap1 pathway in insecticide-resistant strains of Drosophila

Insect Biochemistry and Molecular Biology

Volumn 43, Issue 12, 2013, Pages 1116-1124

  Misra, Jyoti R ^a   Lam, Geanette ^a   Thummel, Carl S ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Gene regulation; Insecticide resistance; Nrf2; Transcriptional control

Indexed keywords

DROSOPHILA PROTEIN; INSECTICIDE; KEAP1 PROTEIN, DROSOPHILA; SIGNAL PEPTIDE;

ANIMAL; ARTICLE; BINDING SITE; DROSOPHILA MELANOGASTER; DRUG DETOXIFICATION; DRUG EFFECT; GENE CONTROL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INSECTICIDE RESISTANCE; METABOLISM; NRF2; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL CONTROL;

GENE REGULATION; INSECTICIDE RESISTANCE; NRF2; TRANSCRIPTIONAL CONTROL;

ANIMALS; BINDING SITES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; HUMANS; INSECTICIDE RESISTANCE; INSECTICIDES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; METABOLIC DETOXICATION, DRUG; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 84885990241     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2013.09.005     Document Type: Article

References (44)

1. Amichot M., Tarès S., Brun-Barale A., Arthaud L., Bride J.M., Berge J.B. Point mutations associated with insecticide resistance in the Drosophila cytochrome P450 Cyp6a2 enable DDT metabolism. Eur. J. Biochem. 2004, 271:1250-1257.
2. Bogwitz M.R., Chung H., Magoc L., Rigby S., Wong W., O'Keefe M., McKenzie J.A., Batterham P., Daborn P.J. Cyp12a4 confers lufenuron resistance in a natural population of Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12807-12812.
3. Bowerman B., Eaton B.A., Priess J.R. skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C.elegans embryo. Cell 1992, 20:1061-1075.
4. Choe K.P., Leung C.K., Miyamoto M.M. Unique structure and regulation of the nematode detoxification gene regulator, SKN-1: implications to understanding and controlling drug resistance. Drug Metab. Rev. 2012, 44:209-223.
5. Chung H., Sztal T., Pasricha S., Sridhar M., Batterham P., Daborn P.J. Characterization of Drosophila melanogaster cytochrome P450 genes. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:5731-5736.
6. Cùany A., Pralavorio M., Pauron D., Berge J.B., Fournier D., Blais C., Lafont R., Salaun J.P., Weissbart D., Larroque C. Characterization of microsomal oxidative activities in a wild-type and in a DDT resistant strain of Drosophila melanogaster. Pest Biochem. Phys. 1990, 37:293-302.
7. Daborn P.J., Yen J.L., Bogwitz M.R., Le Goff G., Feil E., Jeffers S., Tijet N., Perry T., Heckel D., Batterham P. Asingle P450 allele associated with insecticide resistance in Drosophila. Science 2002, 297:2253-2256.
8. Daborn P.J., Lumb C., Boey A., Wong W., Ffrench-Constant R.H., Batterham P. Evaluating the insecticide resistance potential of eight Drosophila melanogaster cytochrome P450 genes by transgenic over-expression. Insect Biochem. Mol. Biol. 2007, 37:512-519.
9. Dapkus D., Merrell D.J. Chromosomal analysis of DDT-resistance in a long-term selected population of Drosophila melanogaster. Genetics 1977, 87:685-697.
10. Duda D.M., Scott D.C., Calabrese M.F., Zimmerman E.S., Zheng N., Schulman B.A. Structural regulation of cullin-RING ubiquitin ligase complexes. Curr. Opin. Struct. Biol. 2011, 21:257-264.
11. Ffrench-Constant R.H., Mortlock D.P., Shaffer C.D., MacIntyre R.J., Roush R.T. Molecular cloning and transformation of cyclodiene resistance in Drosophila: an invertebrate gamma-aminobutyric acid subtype A receptor locus. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:7209-7213.
12. Ffrench-Constant R.H., Rocheleau T.A., Steichen J.C., Chalmers A.E. Apoint mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 1993, 363:449-451.
13. Ffrench-Constant R.H., Anthony N., Aronstein K., Rocheleau T., Stilwell G. Cyclodiene insecticide resistance: from molecular to population genetics. Annu. Rev. Entomol. 2000, 45:449-466.
14. Ffrench-Constant R.H., Daborn P.J., Goff G.L. The genetics and genomics of insecticide resistance. Trends Genet. 2004, 20:163-170.
15. Heckel D.G. Insecticide resistance after silent spring. Science 2012, 337:1612-1614.
16. Houpt D.R., Pursey J.C., Morton R.A. Genes controlling malathion resistance in a laboratory-selected population of Drosophila melanogaster. Genome 1988, 30:844-853.
17. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharm. Tox. 2007, 47:89-116.
18. Keum Y.S. Regulation of the Keap1/Nrf2 system by chemopreventive sulforaphane: implications of posttranslational modifications. Ann. N. Y. Acad. Sci. 2011, 1229:184-189.
19. Kinch L., Grishin N.V., Brugarolas J. Succination of Keap1 and activation of Nrf2-dependent antioxidant pathways in FH-deficient papillary renal cell carcinoma type 2. Cancer Cell 2011, 20:418-420.
20. Komatsu M., Kurokawa H., Waguri S., Taguchi K., Kobayashi A., Ichimura Y., Sou Y.-S., Ueno I., Sakamoto A., Tong K.I., Kim M., Nishito Y., Iemura S., Natsume T., Ueno T., Kominami E., Motohashi H., Tanaka K., Yamamoto M. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 2010, 12:213-223.
21. Kuruganti S., Lam V., Zhou X., Bennett G., Pittendrigh B.R., Ganguly R. High expression of Cyp6g1, a cytochrome P450 gene, does not necessarily confer DDT resistance in Drosophila melanogaster. Gene 2007, 388:43-53.
22. Li X., Schuler M.A., Berenbaum M.R. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 2007, 52:231-253.
23. Lo S.C., Hannink M. CAND1-mediated substrate adaptor recycling is required for efficient repression of Nrf2 by Keap1. Mol. Cell Biol. 2006, 26:1235-1244.
24. Maitra S., Dombrowski S.M., Basu M., Raustol O., Waters L.C., Ganguly R. Factors on the third chromosome affect the level of Cyp6a2 and Cyp6a8 expression in Drosophila melanogaster. Gene 2000, 248:147-156.
25. McGinnis N., Ragnhildstveit E., Veraksa A., McGinnis W. Acap "n" collar protein isoform contains a selective Hox repressor function. Development 1998, 125:4553-4564.
26. Merrell D.J., Underhill J.C. Selection for DDT resistance in inbred, laboratory, and wild stocks of Drosophila melanogaster. J.Econ. Entomol. 1956, 49:300-306.
27. Misra J.R., Horner M.A., Lam G., Thummel C.S. Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev. 2011, 25:1796-1806.
28. Oron E., Tuller T., Li L., Rozovsky N., Yekutieli D., Rencus-Lazar S., Segal D., Chor B., Edgar B.A., Chamovitz D.A. Genomic analysis of COP9 signalosome function in Drosophila melanogaster reveals a role in temporal regulation of gene expression. Mol. Syst. Biol. 2007, 3:108.
29. Park S.K., Tedesco P.M., Johnson T.E. Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 2009, 8:258-269.
30. Pedra J.H., McIntyre L.M., Scharf M.E., Pittendrigh B.R. Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7034-7039.
31. Perry T., Batterham P., Daborn P.J. The biology of insecticidal activity and resistance. Insect Biochem. Mol. Biol. 2011, 41:411-422.
32. Qiu X., Sun W., McDonnell C.M., Li-Byarlay H., Steele L.D., Wu J., Xie J., Muir W.M., Pittendrigh B.R. Genome-wide analysis of genes associated with moderate and high DDT resistance in Drosophila melanogaster. Pest. Manag. Sci. 2013, 69:930-937.
33. Rajasekaran N.S., Connell P., Christians E.S., Yan L.-J., Taylor R.P., Orosz A., Zhang X.Q., Stevenson T.J., Peshock R.M., Leopold J.A., Barry W.H., Loscalzo J., Odelberg S.J., Benjamin I.J. Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 2007, 130:427-439.
34. Schlipalius D.I., Chen W., Collins P.J., Nguyen T., Reilly P.E.B., Ebert P.R. Gene interactions constrain the course of evolution of phosphine resistance in the lesser grain borer, Rhyzopertha dominica. Heredity 2008, 100:506-516.
35. Shibata T., Kokubu A., Gotoh M., Ojima H., Ohta T., Yamamoto M., Hirohashi S. Genetic alteration of Keap1 confers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer. Gastroenterology 2008, 135:1358-1368.
36. Shim G.S., Manandhar S., Shin D.H., Kim T.H., Kwak M.K. Acquisition of doxorubicin resistance in ovarian carcinoma cells accompanies activation of the NRF2 pathway. Free Radic. Biol. Med. 2009, 47:1619-1631.
37. Singh A., Misra V., Thimmulappa R.K., Lee H., Ames S., Hoque M.O., Herman J.G., Baylin S.B., Sidransky D., Gabrielson E., Brock M.V., Biswal S. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med. 2006, 3:e420.
38. Sykiotis G.P., Bohmann D. Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev. Cell 2008, 14:76-85.
39. Tarès S., Arthaud L., Brun-Barale A., Crochard D., Bride J.M., Amichot M. Very high conservation between Cyp6a2 from Drosophila melanogaster and its ortholog Cyp6a26 from D.simulans. Insect Sci. 2007, 14:15-27.
40. Veraksa A., McGinnis N., Li X., Mohler J., McGinnis W. Cap "n" collar B cooperates with a small Maf subunit to specify pharyngeal development and suppress deformed homeotic function in the Drosophila head. Development 2000, 127:4023-4037.
41. Waters L.C., Nix C.E. Regulation of insecticide resistance-related cytochrome P-450 expression in Drosophila melanogaster. Pest Biochem. Phys. 1988, 30:214-227.
42. Wei N., Deng X.W. The COP9 signalosome. Ann. Rev. Cell Dev. Biol. 2003, 19:261-286.
43. Zhang P., Singh A., Yegnasubramanian S., Esopi D., Kombairaju P., Bodas M., Wu H., Bova S.G., Biswal S. Loss of Kelch-Like ECH-associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol. Cancer Ther. 2010, 9:336-346.
44. Zhu F., Parthasarathy R., Bai H., Woithe K., Kaussmann M., Nauen R., Harrison D.A., Palli S.R. Abrain-specific cytochrome P450 responsible for the majority of deltamethrin resistance in the QTC279 strain of Tribolium castaneum. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:8557-8562.