Molecular adaptations of Helicoverpa armigera midgut tissue under pyrethroid insecticide stress characterized by differential proteome analysis and enzyme activity assays

Achaleke, 2009, Esterase-mediated resistance to pyrethroids in field populations of Helicoverpa armigera (Lepidoptera: Noctuidae) from Central Africa, Pest. Manag. Sci., 65, 1147, 10.1002/ps.1807 Ai, 2009, HPLC assay for characterizing a-cyano-3-phenoxybenzyl pyrethroids hydrolytic metabolism by Helicoverpa armigera (Hübner) based on the quantitative analysis of 3-phenoxybenzoic acid, J. Agric. Food Chem., 58, 694, 10.1021/jf9030376 Anon, 1986, Worldwide resistance to synthetic pyrethroids Bloomquist, 1996, Ion channels as targets for insecticides, Annu. Rev. Entomol., 41, 163, 10.1146/annurev.en.41.010196.001115 Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3 Byrne, 2000, The role of B-type esterases in conferring insecticide resistance in the tobacco whitefly, Bemisia tabaci (Genn), Pest. Manag. Sci., 56, 867, 10.1002/1526-4998(200010)56:10<867::AID-PS218>3.0.CO;2-P Campbell, 2008, Proteomic analysis of the peritrophic matrix from the gut of the caterpillar. Helicoverpa armigera, Insect. Biochem. Mol. Biol., 38, 950, 10.1016/j.ibmb.2008.07.009 Dawkar, 2011, Assimilatory potential of Helicoverpa armigera reared on host (Chickpea) and nonhost (Cassia tora) diets, J. Proteome. Res., 10, 5128, 10.1021/pr200591m Djihinto, 2009, Variation in resistance to pyrethroids in Helicoverpa armigera from Benin Republic, West Africa, J. Econ. Entomol., 102, 1928, 10.1603/029.102.0525 Ernst, 1992, Comparative measurements of resistance to insecticides in three closely-related old and new world bollworm species, Pestic. Sci., 34, 147, 10.1002/ps.2780340209 Grajeda-Cota, 2004, Vitamin C protects against in vitro cytotoxicity of cypermethrin in rat hepatocytes, Toxicol. In Vitro, 18, 13, 10.1016/S0887-2333(03)00077-8 Grant, 1989, Quantitative kinetic assays for glutathione S-transferase and general esterase in individual mosquitoes using an EIA reader, Insect. Biochem., 19, 741, 10.1016/0020-1790(89)90055-3 Grubor, 2007, Evaluation of the role of CYP6B cytochrome P450s in pyrethroid resistant Australian Helicoverpa armigera, Insect. Mol. Biol., 16, 15, 10.1111/j.1365-2583.2006.00697.x Gunning, 1996, Esterases and esfenvalerate resistance in AustralianHelicoverpa armigera(Hübner) Lepidoptera: Noctuidae, Pestic. Biochem. Physiol., 54, 12, 10.1006/pest.1996.0004 Gunning, 1999, Esterase inhibitors synergise the toxicity of pyrethroids in Australian Helicoverpa armigera(Hübner) (Lepidoptera: Noctuidae), Pestic. Biochem. Physiol., 63, 50, 10.1006/pest.1998.2388 Gunning, 2007, Use of pyrethroid analogues to identify key structural features for enhanced-esterase resistance in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), Pest. Manag. Sci., 63, 569, 10.1002/ps.1377 Habig, 1974, Glutathione S-transferases, J. Biol. Chem., 249, 7130, 10.1016/S0021-9258(19)42083-8 Heidari, 2005, Hydrolysis of pyrethroids by carboxylesterases from Lucilia cuprina and Drosophila melanogaster with active sites modified by in vitro mutagenesis, Insect. Biochem. Mol. Biol., 35, 597, 10.1016/j.ibmb.2005.02.018 Heitner, 2006, Differentiation of HELLP patients from healthy pregnant women by proteome analysis, J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 840, 10, 10.1016/j.jchromb.2006.06.002 Horváth, 2004, Damage of sunflower caused by the cotton bollworm (Helicoverpa armigera, Hübner) in the region of Kecskemét and Bácsalmás in 2003, Helia, 27, 173, 10.2298/HEL0441173H Huang, 2004, Development of pyrethroid substrates for esterases associated with pyrethroid resistance in the tobacco budworm, Heliothis virescens (F.). J. Agric, Food Chem., 52, 6539, 10.1021/jf0493472 Just, 2006, Differential proteome analysis of tonsils from children with chronic tonsillitis or with hyperplasia reveals disease-associated protein expression differences, Anal. Bioanal. Chem., 384, 1134, 10.1007/s00216-005-0288-y Kozaki, 2008, The Bombyx mori P450s, 43 Kranthi, 2001, Pyrethroid resistance and mechanisms of resistance in field strains of Helicoverpa armigera (Lepidoptera: Noctuidae), J. Econ. Entomol., 94, 253, 10.1603/0022-0493-94.1.253 Lowry, 1951, Protein measurement with the Folin phenol reagent, J. Biol. Chem., 193, 265, 10.1016/S0021-9258(19)52451-6 Lu, 2010, Proteomic and phosphoproteomic analysis at diapause initiation in the cotton bollworm. Helicoverpa armigera, J. Proteome Res., 9, 5053, 10.1021/pr100356t Mádi, 2003, Profiling stage-dependent changes of protein expression in Caenorhabditis elegans by mass spectrometric proteome analysis leads to the identification of stage-specific marker proteins, Electrophoresis, 24, 1809, 10.1002/elps.200305390 Mádi, 2003, Mass spectrometric proteome analysis for profiling temperature-dependent changes of protein expression in wild-type Caenorhabditis elegans, Proteomics, 3, 1526, 10.1002/pmic.200300490 Martin, 2002, Pyrethroid resistance mechanisms in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) from West Africa, Pestic. Biochem. Physiol., 74, 17, 10.1016/S0048-3575(02)00117-7 McCaffery, 1998, Resistance to insecticides in Heliothine Lepidoptera: a global view, Phil. Trans. R. Soc. Lond., B Biol. Sci., 353, 1735, 10.1098/rstb.1998.0326 Mikkat, 2010, MS characterization of qualitative protein polymorphisms in the spinal cords of inbred mouse strains, Proteomics, 10, 1050 Nakamura, 2007, The in vitro metabolism of a pyrethroid insecticide, permethrin, and its hydrolysis products in rats, Toxicology, 235, 176, 10.1016/j.tox.2007.03.016 Neuhoff, 1988, Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250, Electrophoresis, 9, 255, 10.1002/elps.1150090603 Pauchet, 2008, Mapping the larval midgut lumen proteome of Helicoverpa armigera, a generalist herbivorous insect, J. Proteome Res., 7, 1629, 10.1021/pr7006208 Petrak, 2008, Déjà vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins, Proteomics, 8, 1744, 10.1002/pmic.200700919 Qiu, 2000, The tissue distribution of monooxygenase activities of the cotton bollworm, Helicoverpa armigera, Acta Ecol. Sin., 20, 299 Röwer, 2011, Mass spectrometric characterization of protein structure details refines the proteome signature for invasive ductal breast carcinoma, J. Am. Soc. Mass Spectrom., 22, 440, 10.1007/s13361-010-0031-6 Scollon, 2009, In vitro metabolism of pyrethroid pesticides by rat and human hepatic microsomes and cytochrome P450 isoforms, Drug Metab. Dispos., 37, 221, 10.1124/dmd.108.022343 Sekulic, 2004, Incidence and damage of cotton bollworm (Helicoverpa armigera Hbn.) in Vojvodina Province in 2003, Biljni Lekar Plant Doctor, 32, 113 Sequeira, 2001, Abundance of Helicoverpa (Lepidoptera: Noctuidae) pupae under cotton and other crops in central Queensland: implications for resistance management, Aust. J. Entomol., 40, 264, 10.1046/j.1440-6055.2001.00234.x Soderlund, 2002, Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment, Toxicology, 171, 3, 10.1016/S0300-483X(01)00569-8 Strode, 2008, Genomic analysis of detoxification genes in the mosquito Aedes aegypti, Insect. Biochem. Mol. Biol., 38, 113, 10.1016/j.ibmb.2007.09.007 Ugurlu, 2007, Pyrethroid resistance and possible involvement of glutathione S-transferases in Helicoverpa armigera from Turkey, Phytoparasitica, 35, 23, 10.1007/BF02981058 Ugurlu, 2013, Determination of susceptibility levels of Helicoverpa armigera (Hübner) (Noctuidae: Lepidoptera) strains collected from different regions to some insecticides in Turkey, J. Entomol. Res. Soc., 15, 37 van Asperen, 1962, A study of housefly esterases by means of a sensitive colorimetric method, J. Insect. Physiol., 8, 401, 10.1016/0022-1910(62)90074-4 Vontas, 2001, Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens, Biochem. J., 357, 65, 10.1042/0264-6021:3570065 Vontas, 2002, Purification, molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the rice brown planthopper, Nilaparvata lugens, Biochem. J., 362, 329, 10.1042/0264-6021:3620329 Wang, 2009, Generally detected proteins in comparative proteomics — a matter of cellular stress response?, Proteomics, 9, 2955, 10.1002/pmic.200800826 Way, 1984, Cyanide intoxication and its mechanism of antagonism, Annu. Rev. Pharmacol. Toxicol., 24, 451, 10.1146/annurev.pa.24.040184.002315 Werr, 2009, Identification and characterization of two arginine kinases from the parasitic insect Ctenocephalides felis, Insect. Biochem. Mol. Biol., 39, 634, 10.1016/j.ibmb.2009.07.001 Wieczorek, 1999, The plasma membrane H+-V-ATPase from tobacco hornworm midgut, J. Bioenerg. Biomembr., 31, 67, 10.1023/A:1005448614450 Wieczorek, 2000, Structure and regulation of insect plasma membrane H(+)V-ATPase, J. Exp. Biol., 203, 127, 10.1242/jeb.203.1.127 Yang, 2004, The involvement of microsomal oxidases in pyrethroid resistance in Helicoverpa armigera from Asia, Insect. Biochem. Mol. Biol., 34, 763, 10.1016/j.ibmb.2004.04.001 Yang, 2005, Relative contribution of detoxifying enzymes to pyrethroid resistance in a resistant strain of Helicoverpa armigera”, J. Appl. Entomol., 129, 521, 10.1111/j.1439-0418.2005.00999.x Yu, 1995, Tissue-specific expression of glutathione transferase isozymes in fall armyworm larvae, Pestic. Biochem. Physiol., 53, 164, 10.1006/pest.1995.1064 Zhang, 2011, Integrated proteomic and metabolomic analysis of larval brain associated with diapause induction and preparation in the cotton bollworm. Helicoverpa armigera, J. Proteome Res., 11, 1042, 10.1021/pr200796a Zhao, 2005, Identification of differentially expressed proteins during larval molting of Helicoverpa armigera, J. Proteome Res., 5, 164, 10.1021/pr0502424