Functional characterization of an arrestin gene on insecticide resistance of Culex pipiens pallens

Particle and Fibre Toxicology

Chang-Liang Zhu¹  Lei Ma¹  Dong-Hui Zhang¹  Bo Shen¹  Wei-Jie Wang¹  Xue-Lian Chang¹  Dan Zhou¹  Shan-Chao Hong¹  Lin-Na Shi¹  Jing Yu¹  Chen Chen¹  Xin-You Yu¹  Ping Zou¹  Yan Sun¹ 

[1] Department of Pathogen Biology, Nanjing Medical University, 140 Hanzhong Road,, Nanjing, 210029, Jiang Su Province, People’s Republic of China

关键词: Cell viability;    SiRNA;    Transfection;    Gene cloning;    Arrestin;    Insecticide resistance;   

Others  :  1231763
DOI  :  10.1186/1756-3305-5-134

 received in 2012-03-14, accepted in 2012-06-29,  发布年份 2012

【 摘 要 】

Background

Continuous and excessive application of insecticides has resulted in the rapid development of insecticide resistance in several mosquito species, including Culex pipiens pallens. Previous studies in our laboratory found that arrestin gene expression was higher in the deltamethrin-resistant (DR) strain than in the deltamethrin-susceptible (DS) strain of Cx. pipiens pallens. Similarly, other studies reported that arrestin was highly expressed in permethrin-resistant Cx. quinquefasciatus and in dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila melanogaster.

Methods

Full-length cDNAs of an arrestin gene were cloned from Cx. pipiens pallens via polymerase chain reaction (PCR) and rapid amplification of cDNA end (RACE). The mRNA levels of the arrestin gene in the whole life cycle of DR and DS strains of Cx. pipiens pallens were investigated via quantitative real-time PCR. In addition, the relationship between arrestin and deltamethrin (DM) resistance were identified using genetic overexpression strategies and arrestin RNAi in mosquito cells. Cell viability was analyzed with cholecystokinin octapeptide after DM treatment. Moreover, the mRNA levels of cytochrome P450 6A1 (CYP6A1) and opsin in the transfected cells and controls were analyzed.

Results

Complete arrestin gene sequence was cloned and expressed throughout the life cycle of Cx. pipiens pallens. Moreover, arrestin was significantly upregulated in the DR strain, compared with that in the DS strain at the egg, pupae, and adult stages. Arrestin overexpression comparably increased the mosquito cell viability, whereas arrestin knockdown by siRNA decreased mosquito cell viability with deltamethrin (DM) treatment. Meanwhile, the mRNA levels of CYP6A1 and opsin were upregulated in mosquito cells transfected with arrestin and downregulated in mosquito cells with arrestin knockdown.

Conclusion

This study presented the first evidence that arrestin might be associated with insecticide resistance in Cx. pipiens pallens.

【 授权许可】

   
2012 Sun et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】

• [1]White MT, Griffin JT, Churcher TS, Ferguson NM, Basáñez MG, Ghani AC: Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit Vectors 2011, 4:153. BioMed Central Full Text
• [2]Gubler D, Jeffery JAL, Thi Yen N, Nam VS, Nghia LT, Hoffmann AA, Kay BH, Ryan PA: Characterizing the Aedes aegypti Population in a Vietnamese Village in Preparation for a Wolbachia-Based Mosquito Control Strategy to Eliminate Dengue. PLoS Negl Trop Dis 2009, 3(11):e552.
• [3]Peng R, Maklokova VI, Chandrashekhar JH, Lan Q: In vivo functional genomic studies of sterol carrier protein-2 gene in the yellow fever mosquito. PLoS One 2011, 6(3):e18030.
• [4]Koelle K, Gambhir M, Michael E: Complex Ecological Dynamics and Eradicability of the Vector Borne Macroparasitic Disease, Lymphatic Filariasis. PLoS One 2008, 3(8):e2874.
• [5]Smith DR, Adams AP, Kenney JL, Wang E, Weaver SC: Venezuelan equine encephalitis virus in the mosquito vector Aedes taeniorhynchus: infection initiated by a small number of susceptible epithelial cells and a population bottleneck. Virology 2008, 372(1):176-186.
• [6]Styer LM, Lim PY, Louie KL, Albright RG, Kramer LD, Bernard KA: Mosquito Saliva Causes Enhancement of West Nile Virus Infection in Mice. J Virol 2010, 85(4):1517-1527.
• [7]Powers AM, Soumahoro M-K, Boelle P-Y, Gaüzere B-A, Atsou K, Pelat C, Lambert B, La Ruche G, Gastellu-Etchegorry M, Renault P: The Chikungunya Epidemic on La Réunion Island in 2005–2006: a cost-of-illness study. PLoS Negl Trop Dis 2011, 5(6):e1197.
• [8]World Health Organisation: Pesticides and their application for the control of vectors and pests of public health importance. WHO/CDS/NTD/WHOPES/GCDPP/2006.1, ; 2006:-.
• [9]Molyneux DH, Malecela MN: Neglected tropical diseases and the millennium development goals: why the "other diseases" matter: reality versus rhetoric. Parasit Vectors 2011, 4:234. BioMed Central Full Text
• [10]Hemingway J, Beaty BJ, Rowland M, Scott TW, Sharp BL: The Innovative Vector Control Consortium: improved control of mosquito-borne diseases. Trends Parasitol 2006, 22(7):308-312.
• [11]Katsuda Y, Leemingsawat S, Thongrungkiat S, Prummonkol S, Samung Y, Kanzaki T, Watanabe T, Kahara T: Control of mosquito vectors of tropical infectious diseases: (2) pyrethroid susceptibility of Aedes aegypti (l) collected from different sites in Thailand. Southeast Asian J Trop Med Public Health 2008, 39(2):229-234.
• [12]Tungu P, Magesa S, Maxwell C, Malima R, Masue D, Sudi W, Myamba J, Pigeon O, Rowland M: Evaluation of PermaNet 3.0 a deltamethrin-PBO combination net against Anopheles gambiae and pyrethroid resistant Culex quinquefasciatus mosquitoes: an experimental hut trial in Tanzania. Malaria J 2010, 9(1):21. BioMed Central Full Text
• [13]Rivero A, Vezilier J, Weill M, Read AF, Gandon S: Insecticide control of vector-borne diseases: when is insecticide resistance a problem? PLoS Pathog 2010, 6(8):e1001000.
• [14]Hansen IA, Marcombe S, Mathieu RB, Pocquet N, Riaz M-A, Poupardin R, Sélior S, Darriet F, Reynaud S, Yébakima A, et al.: Insecticide resistance in the dengue vector Aedes aegypti from Martinique: distribution, mechanisms and relations with environmental factors. PLoS One 2012, 7(2):e30989.
• [15]Nardini L, Christian RN, Coetzer N, Ranson H, Coetzee M, Koekemoer LL: Detoxification enzymes associated with insecticide resistance in laboratory strains of Anopheles arabiensis of different geographic origin. Parasit Vectors 2012, 5(1):113. BioMed Central Full Text
• [16]Hu Z, Du Y, Nomura Y, Dong K: A sodium channel mutation identified in Aedes aegypti selectively reduces cockroach sodium channel sensitivity to type I, but not type II pyrethroids. Insect Biochem Mol Biol 2011, 41(1):9-13.
• [17]Xu Y, Yang M, Sun J, Qian J, Zhang D, Sun Y, Ma L, Zhu C: Glycogen branching enzyme: a novel deltamethrin resistance-associated gene from Culex pipiens pallens. Parasitol Res 2008, 103(2):449-458.
• [18]Yang M, Qian J, Sun J, Xu Y, Zhang D, Ma L, Sun Y, Zhu C: Cloning and characterization of myosin regulatory light chain (MRLC) gene from Culex pipiens pallens. Comp Biochem Physiol B Biochem Mol Biol 2008, 151(2):230-235.
• [19]Zhang J, Yang M, Wang W, Sun H, Xu Y, Ma L, Sun Y, Zhu C: prag01, a novel deltamethrin-resistance-associated gene from Culex pipiens pallens. Parasitol Res 2010, 108(2):417-423.
• [20]Hu XB, Sun Y, Wang WJ, Yang MX, Sun LX, Tan WB, Sun J, Qian J, Ma L, Zhang DH, Zhu CL: Cloning and characterization of NYD-OP7, a novel deltamethrin resistance associated gene from Culex pipiens pallens. Pestic Biochem Phys 2007, 88(1):82-91.
• [21]Liu N, Liu H, Zhu F, Zhang L: Differential expression of genes in pyrethroid resistant and susceptible mosquitoes, Culex quinquefasciatus (S.). Gene 2007, 394(1–2):61-68.
• [22]Palczewski K: Structure and functions of arrestins. Protein Sci 1994, 3(9):1355-1361.
• [23]Fong AM, Premont RT, Richardson RM, Yu YR, Lefkowitz RJ, Patel DD: Defective lymphocyte chemotaxis in beta-arrestin2- and GRK6-deficient mice. Proc Natl Acad Sci U S A 2002, 99(11):7478-7483.
• [24]Li TT, Alemayehu M, Aziziyeh AI, Pape C, Pampillo M, Postovit LM, Mills GB, Babwah AV, Bhattacharya M: Beta-arrestin/Ral signaling regulates lysophosphatidic acid-mediated migration and invasion of human breast tumor cells. Mol Cancer Res 2009, 7(7):1064-1077.
• [25]Sonoda N, Imamura T, Yoshizaki T, Babendure JL, Lu JC, Olefsky JM: Beta-Arrestin-1 mediates glucagon-like peptide-1 signaling to insulin secretion in cultured pancreatic beta cells. Proc Natl Acad Sci U S A 2008, 105(18):6614-6619.
• [26]Luan B, Zhao J, Wu H, Duan B, Shu G, Wang X, Li D, Jia W, Kang J, Pei G: Deficiency of a beta-arrestin-2 signal complex contributes to insulin resistance. Nature 2009, 457(7233):1146-1149.
• [27]Kemena C, Notredame C: Upcoming challenges for multiple sequence alignment methods in the high-throughput era. Bioinformatics 2009, 25(19):2455-2465.
• [28]Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30(9):e36.
• [29]Kozak M: Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 1986, 44(2):283-292.
• [30]Sano K, Maeda K, Oki M, Maeda Y: Enhancement of protein expression in insect cells by a lobster tropomyosin cDNA leader sequence. FEBS Lett 2002, 532(1–2):143-146.
• [31]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 2001, 25(4):402-408.
• [32]Brooke BD, Koekemoer LL: Major effect genes or loose confederations? The development of insecticide resistance in the malaria vector Anopheles gambiae. Parasit Vectors 2010, 3:74. BioMed Central Full Text
• [33]Kendall RT, Luttrell LM: Diversity in arrestin function. Cell Mol Life Sci 2009, 66(18):2953-2973.
• [34]Aubry L, Guetta D, Klein G: The arrestin fold: variations on a theme. Curr Genomics 2009, 10(2):133-142.
• [35]Mounsey KE, Pasay CJ, Arlian LG, Morgan MS, Holt DC, Currie BJ, Walton SF, McCarthy JS: Increased transcription of Glutathione S-transferases in acaricide exposed scabies mites. Parasit Vectors 2010, 3:43. BioMed Central Full Text
• [36]Hemingway J, Hawkes NJ, McCarroll L, Ranson H: The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 2004, 34(7):653-665.
• [37]Vontas J, Blass C, Koutsos AC, David JP, Kafatos FC, Louis C, Hemingway J, Christophides GK, Ranson H: Gene expression in insecticide resistant and susceptible Anopheles gambiae strains constitutively or after insecticide exposure. Insect Mol Biol 2005, 14(5):509-521.
• [38]Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, Jeffers S, Tijet N, Perry T, Heckel D, Batterham P, Feyereisen R, Wilson TG: ffrench-Constant RH: A single p450 allele associated with insecticide resistance in Drosophila. Science 2002, 297(5590):2253-2256.
• [39]Daborn PJ, Boundy S, Yen J, Pittendrigh B, ffrench-Constant R: DDT resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid. Mol Genet Genomics 2001, 266(4):556-563.
• [40]Carino FA, Koener JF, Plapp FW, Feyereisen R: Constitutive overexpression of the cytochrome P450 gene CYP6A1 in a house fly strain with metabolic resistance to insecticides. Insect Biochem Mol Biol 1994, 24(4):411-418.
• [41]Weill M, Berthomieu A, Berticat C, Lutfalla G, Nègre V, Pasteur N, Philips A, Leonetti JP, Fort P, Raymond M: Insecticide resistance: a silent base prediction. Curr Biol 2004, 14(14):552-553.
• [42]David JP, Strode C, Vontas J, Nikou D, Vaughan A, Pignatelli PM, Louis C, Hemingway J, Ranson H: The Anopheles gambiae detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. Proc Natl Acad Sci U S A 2005, 102(11):4080-4084.
• [43]DeWire SM, Ahn S, Lefkowitz RJ, Shenoy SK: β-Arrestins and Cell Signaling. Annu Rev Physiol 2007, 69(1):483-510.
• [44]Feyereisen R, Koener JF, Farnsworth DE, Nebert DW: Isolation and sequence of cDNA encoding a cytochrome P450 from an insecticide-resistant strain of the house fly, Musca domestica. Proc Natl Acad Sci U S A 1989, 86(5):1465-1469.
• [45]He J, Sun H, Zhang D, Sun Y, Ma L, Chen L, Liu Z, Xiong C, Yan G, Zhu C: Cloning and characterization of 60 S ribosomal protein L22 (RPL22) from Culex pipiens pallens. Comp Biochem Physiol B Biochem Mol Biol 2009, 153(2):216-222.
• [46]Yang CH, Huang HW, Chen KH, Chen YS, Sheen-Chen SM, Lin CR: Antinociceptive potentiation and attenuation of tolerance by intrathecal -arrestin 2 small interfering RNA in rats. Br J Anaesth 2011, 107(5):774-781.
• [47]Dang VC, Chieng B, Azriel Y, Christie MJ: Cellular Morphine Tolerance Produced by Arrestin-2-Dependent Impairment of Opioid Receptor Resensitization. J Neurosci 2011, 31(19):7122-7130.
• [48]Bohn LM, Gainetdinov RR, Sotnikova TD, Medvedev IO, Lefkowitz RJ, Dykstra LA, Caron MG: Enhanced rewarding properties of morphine, but not cocaine, in beta(arrestin)-2 knock-out mice. J Neurosci 2003, 23(32):10265-10273.
• [49]Raehal KM, Walker JK, Bohn LM: Morphine side effects in beta-arrestin 2 knockout mice. J Pharmacol Exp Ther 2005, 314(3):1195-1201.
• [50]Pedra JH, McIntyre LM, Scharf ME, Pittendrigh BR: Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila. Proc Natl Acad Sci U S A 2004, 101(18):7034-7039.
• [51]Summers RJ: Molecular pharmacology of G protein-coupled receptors. Br J Pharmacol 2010, 159(5):983-985.
• [52]Vishnivetskiy SA, Raman D, Wei J, Kennedy MJ, Hurley JB, Gurevich VV: Regulation of arrestin binding by rhodopsin phosphorylation level. J Biol Chem 2007, 282(44):32075-32083.
• [53]Merrill CE, Pitts RJ, Zwiebel LJ: Molecular characterization of arrestin family members in the malaria vector mosquito, Anopheles gambiae. Insect Mol Biol 2003, 12(6):641-650.