ABC transporters are involved in defense against permethrin insecticide in the malaria vector Anopheles stephensi

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• 作者：Sara Epis (1)
  Daniele Porretta (2)
  Valentina Mastrantonio (2)
  Francesco Comandatore (1) (3)
  Davide Sassera (3)
  Paolo Rossi (4)
  Claudia Cafarchia (5)
  Domenico Otranto (5)
  Guido Favia (4)
  Claudio Genchi (1)
  Claudio Bandi (1)
  Sandra Urbanelli (2)
  
  1. Department of Veterinary Science and Public Health ; University of Milan ; Milan ; Italy
  2. Department of Environmental Biology ; University 鈥淟a Sapienza鈥?of Rome ; Rome ; Italy
  3. Department of Biology and Biotechnology ; University of Pavia ; Pavia ; Italy
  4. School of Bioscience and Veterinary Medicine ; University of Camerino ; Camerino ; Italy
  5. Department of Veterinary Medicine ; University of Bari ; Bari ; Italy
  
• 关键词：Mosquitoes ; Bioassays ; Insecticide resistance ; Culicidae ; Vector control ; ABC transporters
• 刊名：Parasites & Vectors
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：7
• 期：1
• 全文大小：325 KB
• 参考文献：1. Hay, SI, Guerra, CA, Tatem, AJ, Noor, AM, Snow, RW (2004) The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis 4: pp. 327-336 CrossRef
  2. World Health Organization: World malaria report 2012. http://www.who.int/malaria/publications/world_malaria_report_2012/report/en/
  3. Alonso, PL, Tanner, M (2013) Public health challenges and prospects for malaria control and elimination. Nat Med 19: pp. 150-155 CrossRef
  4. Karunamoorthi, K (2011) Vector control: a cornerstone in the malaria elimination campaign. Clin Microbiol Infect 17: pp. 1608-1616 CrossRef
  5. Tikar, SN, Mendki, MJ, Sharma, AK, Sukumaran, D, Veer, V, Prakash, S, Parashar, BD (2011) 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 11: pp. 85 CrossRef
  6. Perry, T, Batterham, P, Daborn, PJ (2011) The biology of insecticidal activity and resistance. Insect Biochem Mol Biol 41: pp. 411-422 CrossRef
  7. Buss, DS, Callaghan, A (2008) 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 90: pp. 141-153 CrossRef
  8. Dermauw, W, Van Leeuwen, T (2014) The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Bio 45: pp. 89-110 CrossRef
  9. Sinka, ME, Bangs, MJ, Manguin, S, Chareonviriyaphap, C, Patil, AP, Temperley, WH, Gething, PW, Elyazar, IRF, Kabaria, CW, Harbach, RE, Hay, SI (2011) The dominant anopheles vectors of human malaria in Asia-Pacific: occurrence data, distribution maps and bionomic pr茅cis. Parasit Vectors 4: pp. 89 CrossRef
  10. Soderlund, DM (2008) Pyrethroids, knockdown resistance and sodium channels. Pest Manag Sci 64: pp. 610-616 CrossRef
  11. Schleier, JJ, Peterson, RKD Pyrethrins and Pyrethroid Insecticides. In: Lopez, O, Fernandez-Bolanos, JG eds. (2011) Green Trends in Insect Control. Royal Society of Chemistry, London, UK, pp. 94-131 CrossRef
  12. Mayer, F, Mayer, N, Chinn, L, Pinsonneault, RL, Kroetz, D, Bainton, RJ (2009) Evolutionary conservation of vertebrate blood鈥揵rain barrier chemoprotective mechanisms in Drosophila. J Neurosci 29: pp. 3538-3550 CrossRef
  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 (2014) Characterization of a novel brain barrier ex vivo insect-based P-glycoprotein screening model. Pharma Res Per 2: pp. e00050
  14. Srinivas, R, Shamsundar, GS, Jayalakshmi, SK, Sreermalu, K (2005) Effect of insecticides and inhibitors on P-glycoprotein ATPase (M-type) activity of resistant pest Helicoverpa armigera. Curr Sci 88: pp. 1449-1452
  15. Aurade, R, Jayalaksh mi, SK, Sreeramulu, K (2006) Stimulatory effect of insecticides on partially purified P-glycoprotein ATPase from the resistant pest Helicoverpa armigera. Biochem Cell Biol 84: pp. 1045-1050 CrossRef
  16. Aurade, RM, Jayalak shmi, SK, Sreeramulu, K (2010) P-glycoprotein ATPase from the resistan pest, Helicoverpa armigera: purification, characterization and effect of various insecticides on its transport function. Biochim Biophys Acta 1798: pp. 1135-1143 CrossRef
  17. Hawthorne, DJ, Dively, GP (2011) Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honey bees. PLoS One 6: pp. e26796 CrossRef
  18. Buss, DS, McCaffery, AR, Callaghan, A (2002) Evidence for p-glycoprotein modification of insecticide toxicity in mosquitoes of the Culex pipiens complex. Med Vet Entomol 16: pp. 218-222 CrossRef
  19. Zhu, F, Gujar, H, Gordon, JR, Haynes, KF, Potter, MF, Palli, SR (2013) Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Sci Rep 3: pp. 1456
  20. Bonizzoni, M, Afrane, Y, Dunn, WA, Atieli, FK, Zhou, G, Zhong, D, Li, J, Githeko, A, Yan, G (2012) Comparative transcriptome analyses of deltamethrin-resistant and -susceptible Anopheles gambiae mosquitoes from Kenya by RNA-Seq. PLoS One 7: pp. e44607 CrossRef
  21. Bariami, V, Jones, CM, Poupardin, R, Vontas, J, Ranson, H (2012) Gene amplification, ABC transporters and cytochrome P450s: unraveling the molecular basis of pyrethroid resistance in the dengue vector, Aedes aegypti. PLoS Negl Trop Dis 6: pp. e1692 CrossRef
  22. Thomas, H, Coley, HM (2003) Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting P-glycoprotein. Cancer Control 10: pp. 159-165
  WHO Pesticide Evaluation Scheme. Guidelines for Laboratory and Field Testing of Mosquito Larvicides. Communicable Disease Control, Prevention and Eradication. WHO, Geneva
  23. Finney, DJ (1971) Probit Analysis. Cambridge University Press, Cambridge
  24. 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 (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: pp. 644-652 CrossRef
  25. Uniprot_Consortium: activities at the Universal Protein Resource (UniProt) / Nucleic Acids Res 2014, 42:D191-D198.
  26. Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F, Higgins, DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: pp. 4876-4882 CrossRef
  27. Felsenstein, J (1989) PHYLIP -- phylogeny inference package (version 3.2). Cladistics 5: pp. 164-166
  28. Figueira-Mansur, J, Ferreira-Pereira, A, Mansur, JF, Franco, TA, Alvarenga, ES, Sorgine, MH, Neves, BC, Melo, AC, Leal, WS, Masuda, H, Moreira, MF (2013) Silencing of P-glycoprotein increases mortality in temephos-treated Aedes aegypti larvae. Insect Mol Biol 22: pp. 648-658 CrossRef
  29. Lee, EJ, Schmittgen, TD (2006) Comparison of RNA assay methods used to normalize cDNA for quantitative real-time PCR. Anal Biochem 357: pp. 299-301 CrossRef
  30. 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 (2013) Interactions between Asaia, Plasmodium and Anopheles: new insights into mosquito symbiosis and implications in malaria symbiotic control. Parasit Vectors 6: pp. 182 CrossRef
  31. Tarr, PT, Tarling, EJ, Bojanic, DD, Edwards, PA, Baldan, A (2009) Emerging new paradigms for ABCG transporters. Biochim Biophys Acta 1791: pp. 584-593 CrossRef
  32. Jones, CM, To茅, HK, Sanou, A, Namountougou, M, Hughes, A, Diabat茅, A, Dabir茅, R, Simard, F, Ranson, H (2012) Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS One 7: pp. e45995 CrossRef
  33. Pedra, JHF, McIntyre, LM, Scharf, ME, Pittendrigh, BR (2004) Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltri-chloroethane (DDT) resistant Drosophila. Proc Natl Acad Sci U S A 101: pp. 7034-7039 CrossRef
  34. 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 (2013) A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 45: pp. 220-225 CrossRef
  35. 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 (2013) Transcriptomic and proteomic responses of sweetpotato whitefly, Bemisia tabaci, to thiamethoxam. PLoS One 8: pp. e61820 CrossRef
  36. Fossog Tene, B, Poupardin, R, Costantini, C, Awono-Ambene, P, Wondji, CS, Ranson, H, Antonio-Nkondjio, C (2013) Resistance to DDT in an urban setting: common mechanisms implicated in both M and S forms of Anopheles gambiae in the city of Yaound茅 Cameroon. PLoS One 8: pp. e61408 CrossRef
  37. Hayashi, K, Schoonbeek, H, Sugiura, H, De Waard, MA (2001) 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 70: pp. 168-179 CrossRef
  38. Urbanelli, S, Della Rosa, V, Punelli, F, Porretta, D, Reverberi, M, Fabbri, AA, Fanelli, C (2007) DNA-fingerprinting (AFLP and RFLP) for genotypic identification in species of the Pleurotus eryngii complex. Appl Microbiol Biotechnol 74: pp. 592-600 CrossRef
  39. Punelli, F, Reverberi, M, Porretta, D, Nogarotto, S, Fabbri, A, Fanelli, C, Urbanelli, S (2009) Molecular characterization and enzymatic activity of laccases in two Pleurotus spp. with different pathogenic behavior. Mycol Res 113: pp. 381-387 CrossRef
  40. Dantas-Torres, F, Figueredo, LA, Otranto, D (2011) Seasonal variation in the effect of climate on the biology of Rhipicephalus sanguineus in southern Europe. Parasitology 138: pp. 527-536 CrossRef
  41. Porretta, D, Mastrantonio, V, Bellini, R, Somboon, P, Urbanelli, S (2012) Glacial history of a modern invader: phylogeography and species distribution modelling of the asian tiger mosquito Aedes albopictus. Plos One 7: pp. e44515 CrossRef
  42. Porretta, D, Mastrantonio, V, Amendolia, S, Gaiarsa, S, Epis, S, Genchi, C, Bandi, C, Otranto, D, Urbanelli, S (2013) Effects of global changes on the climatic niche of the tick Ixodes ricinus inferred by species distribution modelling. Parasit Vectors 6: pp. 271 CrossRef
  43. Steele, J, Orsel, K, Cuyler, C, Hoberg, EP, Schmidt, NM, Kutz, SJ (2013) Divergent parasite faunas in adjacent populations of west Greenland caribou: natural and anthropogenic influences on diversity. Int J Parasitol Parasites Wildl 2: pp. 197-202 CrossRef
  44. Porretta, D, Canestrelli, D, Bellini, R, Celli, G, Urbanelli, S (2007) Improving insect pest management through population genetic data: a case study of the mosquito Ochlerotatus caspius (Pallas). J Appl Ecol 44: pp. 682-691 CrossRef
  45. Otranto, D, Wall, R (2008) New strategies for the control of arthropod vectors of disease in dogs and cats. Med Vet Entomol 22: pp. 291-302 CrossRef
  46. Calvitti, M, Moretti, R, Porretta, D, Bellini, R, Urbanelli, S (2009) Effects on male fitness of removing wolbachia infections from the mosquito aedes albopictus. Med Vet Entomol 23: pp. 132-140 CrossRef
  47. Bouyer, F, Hamadou, S, Adakal, H, Lancelot, R, Stachurski, F, Belem, AM, Bouyer, J (2011) Restricted application of insecticides: a promising tsetse control technique, but what do the farmers think of it?. PLoS Negl Trop Dis 5: pp. e1276 CrossRef
  48. Marcombe, S, Poupardin, R, Darriet, F, Reynaud, S, Bonnet, J, Strode, C, Brengues, C, Y茅bakima, A, Ranson, H, Corbel, V, David, JP (2009) Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: a case study in Martinique Island (French West Indies). BMC Genomics 10: pp. 494 CrossRef
  49. Bellini, R, Albieri, A, Balestrino, F, Carrieri, M, Porretta, D, Urbanelli, S, Calvitti, M, Moretti, R, Maini, S (2010) Dispersal and survival of Aedes albopictus (Diptera: Culicidae) males in Italian urban areas and significance for sterile insect technique application. J Med Entomol 47: pp. 1082-1091 CrossRef
  50. Porretta, D, Canestrelli, D, Urbanelli, S, Bellini, R, Schaffner, F, Petric, D, Nascetti, G (2011) 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 38: pp. 20-30 CrossRef
  51. Kennedy, C, Tierney, K (2013) Xenobiotic Protection/Resistance Mechanisms in Organisms. E.A Laws, Environ Toxicol: Springer, New York
  52. Porretta, D, Mastrantonio, V, Mona, S, Epis, S, Montagna, M, Sassera, D, Bandi, C, Urbanelli, S (2013) The integration of multiple independent data reveals an unusual response to pleistocene climatic changes in the hard tick Ixodes ricinus. Mol Eco 22: pp. 1666-1682 CrossRef
  53. Jones, CM, Haji, KA, Khatib, BO, Bagi, J, Mcha, J, Devine, GJ, Daley, M, Kabula, B, Ali, AS, Majambere, S, Ranson, H (2013) The dynamics of pyrethroid resistance in Anopheles arabiensis from Zanzibar and an assessment of the underlying genetic basis. Parasit Vectors 6: pp. 343 CrossRef
  54. Porretta, D, Gargani, M, Bellini, R, Medici, A, Punelli, F, Urbanelli, S (2008) Defence mechanism against insecticides temephos and diflubenzuron in the mosquito Aedes caspius: the P-glycoprotein efflux pumps. Med Vet Entomol 22: pp. 48-54 CrossRef
  55. Pohl, PC, Klafke, GM, Carvalho, DD, Martins, JR, Daffre, S, da Silva Vaz, I, Masuda, A (2011) ABC transporter efflux pumps: a defence mechanism against ivermectin in Rhipicephalus (Boophilus) microplus. Int J Parasitol 41: pp. 1323-1333 CrossRef
  
• 刊物主题：Parasitology; Infectious Diseases; Tropical Medicine; Entomology;
• 出版者：BioMed Central
• ISSN：1756-3305

文摘

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.