Particle and Fibre Toxicology | |
ABC transporters are involved in defense against permethrin insecticide in the malaria vector Anopheles stephensi | |
Sandra Urbanelli2  Claudio Bandi5  Claudio Genchi5  Guido Favia1  Domenico Otranto3  Claudia Cafarchia3  Paolo Rossi1  Davide Sassera4  Francesco Comandatore4  Valentina Mastrantonio2  Daniele Porretta2  Sara Epis5  | |
[1] School of Bioscience and Veterinary Medicine, University of Camerino, Camerino, Italy;Department of Environmental Biology, University “La Sapienza” of Rome, Rome, Italy;Department of Veterinary Medicine, University of Bari, Bari, Italy;Department of Biology and Biotechnology, University of Pavia, Pavia, Italy;Department of Veterinary Science and Public Health, University of Milan, Milan, Italy | |
关键词: ABC transporters; Vector control; Culicidae; Insecticide resistance; Bioassays; Mosquitoes; | |
Others : 1181887 DOI : 10.1186/1756-3305-7-349 |
|
received in 2014-06-05, accepted in 2014-07-15, 发布年份 2014 | |
【 摘 要 】
Background
Proteins from the ABC family (ATP-binding cassette) represent the largest known group of efflux pumps, responsible for transporting specific molecules across lipid membranes in both prokaryotic and eukaryotic organisms. In arthropods they have been shown to play a role in insecticide defense/resistance. The presence of ABC transporters and their possible association with insecticide transport have not yet been investigated in the mosquito Anopheles stephensi, the major vector of human malaria in the Middle East and South Asian regions. Here we investigated the presence and role of ABCs in transport of permethrin insecticide in a susceptible strain of this mosquito species.
Methods
To identify ABC transporter genes we obtained a transcriptome from untreated larvae of An. stephensi and then compared it with the annotated transcriptome of Anopheles gambiae. To analyse the association between ABC transporters and permethrin we conducted bioassays with permethrin alone and in combination with an ABC inhibitor, and then we investigated expression profiles of the identified genes in larvae exposed to permethrin.
Results
Bioassays showed an increased mortality of mosquitoes when permethrin was used in combination with the ABC-transporter inhibitor. Genes for ABC transporters were detected in the transcriptome, and five were selected (AnstABCB2, AnstABCB3, AnstABCB4, AnstABCmember6 and AnstABCG4). An increased expression in one of them (AnstABCG4) was observed in larvae exposed to the LD50 dose of permethrin. Contrary to what was found in other insect species, no up-regulation was observed in the AnstABCB genes.
Conclusions
Our results show for the first time the involvement of ABC transporters in larval defense against permethrin in An. stephensi and, more in general, confirm the role of ABC transporters in insecticide defense. The differences observed with previous studies highlight the need of further research as, despite the growing number of studies on ABC transporters in insects, the heterogeneity of the results available at present does not allow us to infer general trends in ABC transporter-insecticide interactions.
【 授权许可】
2014 Epis et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150515085118938.pdf | 240KB | download | |
Figure 1. | 28KB | Image | download |
【 图 表 】
Figure 1.
【 参考文献 】
- [1]Hay SI, Guerra CA, Tatem AJ, Noor AM, Snow RW: The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis 2004, 4:327-336. 1
- [2]World Health Organization: World malaria report 2012. http://www.who.int/malaria/publications/world_malaria_report_2012/report/en/ webcite
- [3]Alonso PL, Tanner M: Public health challenges and prospects for malaria control and elimination. Nat Med 2013, 19(2):150-155.
- [4]Karunamoorthi K: Vector control: a cornerstone in the malaria elimination campaign. Clin Microbiol Infect 2011, 17:1608-1616.
- [5]Tikar SN, Mendki MJ, Sharma AK, Sukumaran D, Veer V, Prakash S, Parashar BD: Resistance status of the malaria vector mosquitoes, Anopheles stephensi and Anopheles subpictus towards adulticides and larvicides in arid and semi-arid areas of India. J Insect Sci 2011, 11:85.
- [6]Perry T, Batterham P, Daborn PJ: The biology of insecticidal activity and resistance. Insect Biochem Mol Biol 2011, 41:411-422.
- [7]Buss DS, Callaghan A: Interaction of pesticides with p-glycoprotein and other ABC proteins: a survey of the possible importance to insecticide, herbicide and fungicide resistance. Pestic Biochem Physiol 2008, 90:141-153.
- [8]Dermauw W, Van Leeuwen T: The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Bio 2014, 45:89-110.
- [9]Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap C, Patil AP, Temperley WH, Gething PW, Elyazar IRF, Kabaria CW, Harbach RE, Hay SI: The dominant anopheles vectors of human malaria in Asia-Pacific: occurrence data, distribution maps and bionomic précis. Parasit Vectors 2011, 4:89.
- [10]Soderlund DM: Pyrethroids, knockdown resistance and sodium channels. Pest Manag Sci 2008, 64:610-616.
- [11]Schleier JJ III, Peterson RKD: Pyrethrins and Pyrethroid Insecticides. In Green Trends in Insect Control. Edited by Lopez O, Fernandez-Bolanos JG. London, UK: Royal Society of Chemistry; 2011:94-131.
- [12]Mayer F, Mayer N, Chinn L, Pinsonneault RL, Kroetz D, Bainton RJ: Evolutionary conservation of vertebrate blood–brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 2009, 29:3538-3550.
- [13]Andersson O, Badisco L, Hakans Son Hansen A, Hansen SH, Hellman K, Nielsen PA, Olsen LR, Verdonck R, Abbott NJ, Vanden Broeck J, Andersson G: Characterization of a novel brain barrier ex vivo insect-based P-glycoprotein screening model. Pharma Res Per 2014, 2(4):e00050.
- [14]Srinivas R, Shamsundar GS, Jayalakshmi SK, Sreermalu K: Effect of insecticides and inhibitors on P-glycoprotein ATPase (M-type) activity of resistant pest Helicoverpa armigera. Curr Sci 2005, 88:1449-1452.
- [15]Aurade R, Jayalaksh mi SK, Sreeramulu K: Stimulatory effect of insecticides on partially purified P-glycoprotein ATPase from the resistant pest Helicoverpa armigera. Biochem Cell Biol 2006, 84:1045-1050.
- [16]Aurade RM, Jayalak shmi SK, Sreeramulu K: P-glycoprotein ATPase from the resistan pest, Helicoverpa armigera: purification, characterization and effect of various insecticides on its transport function. Biochim Biophys Acta 2010, 1798:1135-1143.
- [17]Hawthorne DJ, Dively GP: Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honey bees. PLoS One 2011, 6:e26796.
- [18]Buss DS, McCaffery AR, Callaghan A: Evidence for p-glycoprotein modification of insecticide toxicity in mosquitoes of the Culex pipiens complex. Med Vet Entomol 2002, 16(2):218-222.
- [19]Zhu F, Gujar H, Gordon JR, Haynes KF, Potter MF, Palli SR: Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Sci Rep 2013, 3:1456.
- [20]Bonizzoni M, Afrane Y, Dunn WA, Atieli FK, Zhou G, Zhong D, Li J, Githeko A, Yan G: Comparative transcriptome analyses of deltamethrin-resistant and -susceptible Anopheles gambiae mosquitoes from Kenya by RNA-Seq. PLoS One 2012, 7:e44607.
- [21]Bariami V, Jones CM, Poupardin R, Vontas J, Ranson H: Gene amplification, ABC transporters and cytochrome P450s: unraveling the molecular basis of pyrethroid resistance in the dengue vector, Aedes aegypti. PLoS Negl Trop Dis 2012, 6:e1692.
- [22]Thomas H, Coley HM: Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting P-glycoprotein. Cancer Control 2003, 10(02):159-165.
- [23]World Health Organization: Guidelines for Laboratory and Field Testing of Mosquito Larvicides. Communicable Disease Control, Prevention and Eradication. Geneva: WHO; 2005. [WHO Pesticide Evaluation Scheme] WHO/CDS/WHOPES/GCDPP/2005.13
- [24]Finney DJ: Probit Analysis. Cambridge: Cambridge University Press; 1971.
- [25]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A: Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652.
- [26]Uniprot_Consortium: activities at the Universal Protein Resource (UniProt) Nucleic Acids Res 2014, 42:D191-D198.
- [27]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25(24):4876-4882.
- [28]Felsenstein J: PHYLIP -- phylogeny inference package (version 3.2). Cladistics 1989, 5:164-166.
- [29]Figueira-Mansur J, Ferreira-Pereira A, Mansur JF, Franco TA, Alvarenga ES, Sorgine MH, Neves BC, Melo AC, Leal WS, Masuda H, Moreira MF: Silencing of P-glycoprotein increases mortality in temephos-treated Aedes aegypti larvae. Insect Mol Biol 2013, 22(6):648-658.
- [30]Lee EJ, Schmittgen TD: Comparison of RNA assay methods used to normalize cDNA for quantitative real-time PCR. Anal Biochem 2006, 357(2):299-301.
- [31]Capone A, Ricci I, Damiani C, Mosca M, Rossi P, Scuppa P, Crotti E, Epis S, Angeletti M, Valzano M, Sacchi L, Bandi C, Daffonchio D, Mandrioli M, Favia G: Interactions between Asaia, Plasmodium and Anopheles: new insights into mosquito symbiosis and implications in malaria symbiotic control. Parasit Vectors 2013, 6:182.
- [32]Tarr PT, Tarling EJ, Bojanic DD, Edwards PA, Baldan A: Emerging new paradigms for ABCG transporters. Biochim Biophys Acta 2009, 1791(7):584-593.
- [33]Jones CM, Toé HK, Sanou A, Namountougou M, Hughes A, Diabaté A, Dabiré R, Simard F, Ranson H: Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS One 2012, 7(9):e45995.
- [34]Pedra JHF, McIntyre LM, Scharf ME, Pittendrigh BR: Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltri-chloroethane (DDT) resistant Drosophila. Proc Natl Acad Sci U S A 2004, 101:7034-7039.
- [35]You M, Yue Z, He W, Yang X, Yang G, Xie M, Zhan D, Baxter SW, Vasseur L, Gurr GM, Douglas CJ, Bai J, Wang P, Cui K, Huang S, Li X, Zhou Q, Wu Z, Chen Q, Liu C, Wang B, Li X, Xu X, Lu C, Hu M, Davey JW, Smith SM, Chen M, Xia X, Tang W, et al.: A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 2013, 45(2):220-225.
- [36]Yang N, Xie W, Yang X, Wang S, Wu Q, Li R, Pan H, Liu B, Shi X, Fang Y, Xu B, Zhou X, Zhang Y: Transcriptomic and proteomic responses of sweetpotato whitefly, Bemisia tabaci, to thiamethoxam. PLoS One 2013, 8(5):e61820.
- [37]Fossog Tene B, Poupardin R, Costantini C, Awono-Ambene P, Wondji CS, Ranson H, Antonio-Nkondjio C: Resistance to DDT in an urban setting: common mechanisms implicated in both M and S forms of Anopheles gambiae in the city of Yaoundé Cameroon. PLoS One 2013, 8(4):e61408.
- [38]Hayashi K, Schoonbeek H, Sugiura H, De Waard MA: Multidrug resistance in Botrytis cinerea associated with decreased accumulation of the azole fungicide oxpoconazole and increased transcription of the ABC transporter gene BcatrD. Pestic Biochem Physiol 2001, 70:168-179.
- [39]Urbanelli S, Della Rosa V, Punelli F, Porretta D, Reverberi M, Fabbri AA, Fanelli C: DNA-fingerprinting (AFLP and RFLP) for genotypic identification in species of the Pleurotus eryngii complex. Appl Microbiol Biotechnol 2007, 74(3):592-600.
- [40]Punelli F, Reverberi M, Porretta D, Nogarotto S, Fabbri A, Fanelli C, Urbanelli S: Molecular characterization and enzymatic activity of laccases in two Pleurotus spp. with different pathogenic behavior. Mycol Res 2009, 113:381-387.
- [41]Dantas-Torres F, Figueredo LA, Otranto D: Seasonal variation in the effect of climate on the biology of Rhipicephalus sanguineus in southern Europe. Parasitology 2011, 138:527-536.
- [42]Porretta D, Mastrantonio V, Bellini R, Somboon P, Urbanelli S: Glacial history of a modern invader: phylogeography and species distribution modelling of the asian tiger mosquito Aedes albopictus. Plos One 2012, 7(9):e44515.
- [43]Porretta D, Mastrantonio V, Amendolia S, Gaiarsa S, Epis S, Genchi C, Bandi C, Otranto D, Urbanelli S: Effects of global changes on the climatic niche of the tick Ixodes ricinus inferred by species distribution modelling. Parasit Vectors 2013, 6:271.
- [44]Steele J, Orsel K, Cuyler C, Hoberg EP, Schmidt NM, Kutz SJ: Divergent parasite faunas in adjacent populations of west Greenland caribou: natural and anthropogenic influences on diversity. Int J Parasitol Parasites Wildl 2013, 2:197-202.
- [45]Porretta D, Canestrelli D, Bellini R, Celli G, Urbanelli S: Improving insect pest management through population genetic data: a case study of the mosquito Ochlerotatus caspius (Pallas). J Appl Ecol 2007, 44:682-691.
- [46]Otranto D, Wall R: New strategies for the control of arthropod vectors of disease in dogs and cats. Med Vet Entomol 2008, 22:291-302.
- [47]Calvitti M, Moretti R, Porretta D, Bellini R, Urbanelli S: Effects on male fitness of removing wolbachia infections from the mosquito aedes albopictus. Med Vet Entomol 2009, 23(2):132-140.
- [48]Bouyer F, Hamadou S, Adakal H, Lancelot R, Stachurski F, Belem AM, Bouyer J: Restricted application of insecticides: a promising tsetse control technique, but what do the farmers think of it? PLoS Negl Trop Dis 2011, 5(8):e1276.
- [49]Marcombe S, Poupardin R, Darriet F, Reynaud S, Bonnet J, Strode C, Brengues C, Yébakima A, Ranson H, Corbel V, David JP: Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: a case study in Martinique Island (French West Indies). BMC Genomics 2009, 10:494.
- [50]Bellini R, Albieri A, Balestrino F, Carrieri M, Porretta D, Urbanelli S, Calvitti M, Moretti R, Maini S: Dispersal and survival of Aedes albopictus (Diptera: Culicidae) males in Italian urban areas and significance for sterile insect technique application. J Med Entomol 2010, 47(6):1082-1091.
- [51]Porretta D, Canestrelli D, Urbanelli S, Bellini R, Schaffner F, Petric D, Nascetti G: Southern crossroads of the Western Palaearctic during the late pleistocene and their imprints on current patterns of genetic diversity: insights from the mosquito Aedes caspius. J Biogeogr 2011, 38:20-30.
- [52]Kennedy C, Tierney K: Xenobiotic Protection/Resistance Mechanisms in Organisms. New York: E.A Laws, Environ Toxicol: Springer; 2013.
- [53]Porretta D, Mastrantonio V, Mona S, Epis S, Montagna M, Sassera D, Bandi C, Urbanelli S: The integration of multiple independent data reveals an unusual response to pleistocene climatic changes in the hard tick Ixodes ricinus. Mol Eco 2013, 22(6):1666-1682.
- [54]Jones CM, Haji KA, Khatib BO, Bagi J, Mcha J, Devine GJ, Daley M, Kabula B, Ali AS, Majambere S, Ranson H: The dynamics of pyrethroid resistance in Anopheles arabiensis from Zanzibar and an assessment of the underlying genetic basis. Parasit Vectors 2013, 6:343.
- [55]Porretta D, Gargani M, Bellini R, Medici A, Punelli F, Urbanelli S: Defence mechanism against insecticides temephos and diflubenzuron in the mosquito Aedes caspius: the P-glycoprotein efflux pumps. Med Vet Entomol 2008, 22:48-54.
- [56]Pohl PC, Klafke GM, Carvalho DD, Martins JR, Daffre S, da Silva Vaz I Jr, Masuda A: ABC transporter efflux pumps: a defence mechanism against ivermectin in Rhipicephalus (Boophilus) microplus. Int J Parasitol 2011, 41:1323-1333.