Relationship between knockdown resistance, metabolic detoxification and organismal resistance to pyrethroids in Anopheles sinensis
Anopheles sinensis is the most important vector of malaria in Southeast Asia, including China. Currently, the most effective measure to prevent malaria transmission relies on vector control through the use of insecticides, primarily pyrethroids. Extensive use of insecticides poses strong selection p...
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| Veröffentlicht in: | PloS one 2013-02, Vol.8 (2), p.e55475 |
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| creator | Zhong, Daibin Chang, Xuelian Zhou, Guofa He, Zhengbo Fu, Fengyang Yan, Zhentian Zhu, Guoding Xu, Tielong Bonizzoni, Mariangela Wang, Mei-Hui Cui, Liwang Zheng, Bin Chen, Bin Yan, Guiyun |
| description | Anopheles sinensis is the most important vector of malaria in Southeast Asia, including China. Currently, the most effective measure to prevent malaria transmission relies on vector control through the use of insecticides, primarily pyrethroids. Extensive use of insecticides poses strong selection pressure on mosquito populations for resistance. Resistance to insecticides can arise due to mutations in the insecticide target site (target site resistance), which in the case of pyrethroids is the para-type sodium channel gene, and/or the catabolism of the insecticide by detoxification enzymes before it reaches its target (metabolic detoxification resistance). In this study, we examined deltamethrin resistance in An. sinensis from China and investigated the relative importance of target site versus metabolic detoxification mechanisms in resistance. A high frequency (>85%) of nonsynonymous mutations in the para gene was found in populations from central China, but not in populations from southern China. Metabolic detoxification as measured by the activity of monooxygenases and glutathione S-transferases (GSTs) was detected in populations from both central and southern China. Monooxygenase activity levels were significantly higher in the resistant than the susceptible mosquitoes, independently of their geographic origin. Stepwise multiple regression analyses in mosquito populations from central China found that both knockdown resistance (kdr) mutations and monooxygenase activity were significantly associated with deltamethrin resistance, with monooxygenase activity playing a stronger role. These results demonstrate the importance of metabolic detoxification in pyrethroid resistance in An. sinensis, and suggest that different mechanisms of resistance could evolve in geographically different populations. |
| doi_str_mv | 10.1371/journal.pone.0055475 |
| format | Article |
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Currently, the most effective measure to prevent malaria transmission relies on vector control through the use of insecticides, primarily pyrethroids. Extensive use of insecticides poses strong selection pressure on mosquito populations for resistance. Resistance to insecticides can arise due to mutations in the insecticide target site (target site resistance), which in the case of pyrethroids is the para-type sodium channel gene, and/or the catabolism of the insecticide by detoxification enzymes before it reaches its target (metabolic detoxification resistance). In this study, we examined deltamethrin resistance in An. sinensis from China and investigated the relative importance of target site versus metabolic detoxification mechanisms in resistance. A high frequency (>85%) of nonsynonymous mutations in the para gene was found in populations from central China, but not in populations from southern China. Metabolic detoxification as measured by the activity of monooxygenases and glutathione S-transferases (GSTs) was detected in populations from both central and southern China. Monooxygenase activity levels were significantly higher in the resistant than the susceptible mosquitoes, independently of their geographic origin. Stepwise multiple regression analyses in mosquito populations from central China found that both knockdown resistance (kdr) mutations and monooxygenase activity were significantly associated with deltamethrin resistance, with monooxygenase activity playing a stronger role. These results demonstrate the importance of metabolic detoxification in pyrethroid resistance in An. sinensis, and suggest that different mechanisms of resistance could evolve in geographically different populations.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0055475</identifier><identifier>PMID: 23405157</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agriculture ; Agrochemicals ; Analysis ; Animals ; Anopheles ; Anopheles - drug effects ; Anopheles - genetics ; Anopheles - metabolism ; Anopheles gambiae ; Anopheles sinensis ; Aquatic insects ; Binding sites ; Biology ; Catabolism ; China ; Culicidae ; Culicidae - drug effects ; Deltamethrin ; Detoxification ; Disease control ; Disease transmission ; Enzymes ; Gene Knockdown Techniques ; Genotype ; Glutathione ; Glutathione Transferase - genetics ; Glutathione Transferase - metabolism ; Health sciences ; Inactivation, Metabolic - genetics ; Insect Vectors - genetics ; Insecticide resistance ; Insecticide Resistance - drug effects ; Insecticide Resistance - genetics ; Insecticides ; Insecticides - pharmacology ; Life sciences ; Malaria ; Metabolism ; Mixed Function Oxygenases - genetics ; Mixed Function Oxygenases - metabolism ; Molecular biology ; Monooxygenase ; Mosquito Control - methods ; Mosquitoes ; Mutation ; Mutation - drug effects ; Mutation - genetics ; Nitriles - pharmacology ; Oryza ; ParA gene ; Parasitic diseases ; Pathogens ; Pest control ; Populations ; Public health ; Pyrethrins - pharmacology ; Pyrethroids ; Regression analysis ; Rice ; Sodium ; Sodium channels ; Transferases ; Vector-borne diseases</subject><ispartof>PloS one, 2013-02, Vol.8 (2), p.e55475</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Zhong et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Zhong et al 2013 Zhong et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-b79baf9e2be08818ceb0396f810320a17578728392859fff98debf8a52b977b33</citedby><cites>FETCH-LOGICAL-c692t-b79baf9e2be08818ceb0396f810320a17578728392859fff98debf8a52b977b33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3566193/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3566193/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23405157$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Terenius, Olle</contributor><creatorcontrib>Zhong, Daibin</creatorcontrib><creatorcontrib>Chang, Xuelian</creatorcontrib><creatorcontrib>Zhou, Guofa</creatorcontrib><creatorcontrib>He, Zhengbo</creatorcontrib><creatorcontrib>Fu, Fengyang</creatorcontrib><creatorcontrib>Yan, Zhentian</creatorcontrib><creatorcontrib>Zhu, Guoding</creatorcontrib><creatorcontrib>Xu, Tielong</creatorcontrib><creatorcontrib>Bonizzoni, Mariangela</creatorcontrib><creatorcontrib>Wang, Mei-Hui</creatorcontrib><creatorcontrib>Cui, Liwang</creatorcontrib><creatorcontrib>Zheng, Bin</creatorcontrib><creatorcontrib>Chen, Bin</creatorcontrib><creatorcontrib>Yan, Guiyun</creatorcontrib><title>Relationship between knockdown resistance, metabolic detoxification and organismal resistance to pyrethroids in Anopheles sinensis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Anopheles sinensis is the most important vector of malaria in Southeast Asia, including China. Currently, the most effective measure to prevent malaria transmission relies on vector control through the use of insecticides, primarily pyrethroids. Extensive use of insecticides poses strong selection pressure on mosquito populations for resistance. Resistance to insecticides can arise due to mutations in the insecticide target site (target site resistance), which in the case of pyrethroids is the para-type sodium channel gene, and/or the catabolism of the insecticide by detoxification enzymes before it reaches its target (metabolic detoxification resistance). In this study, we examined deltamethrin resistance in An. sinensis from China and investigated the relative importance of target site versus metabolic detoxification mechanisms in resistance. A high frequency (>85%) of nonsynonymous mutations in the para gene was found in populations from central China, but not in populations from southern China. Metabolic detoxification as measured by the activity of monooxygenases and glutathione S-transferases (GSTs) was detected in populations from both central and southern China. Monooxygenase activity levels were significantly higher in the resistant than the susceptible mosquitoes, independently of their geographic origin. Stepwise multiple regression analyses in mosquito populations from central China found that both knockdown resistance (kdr) mutations and monooxygenase activity were significantly associated with deltamethrin resistance, with monooxygenase activity playing a stronger role. These results demonstrate the importance of metabolic detoxification in pyrethroid resistance in An. sinensis, and suggest that different mechanisms of resistance could evolve in geographically different populations.</description><subject>Agriculture</subject><subject>Agrochemicals</subject><subject>Analysis</subject><subject>Animals</subject><subject>Anopheles</subject><subject>Anopheles - drug effects</subject><subject>Anopheles - genetics</subject><subject>Anopheles - metabolism</subject><subject>Anopheles gambiae</subject><subject>Anopheles sinensis</subject><subject>Aquatic insects</subject><subject>Binding sites</subject><subject>Biology</subject><subject>Catabolism</subject><subject>China</subject><subject>Culicidae</subject><subject>Culicidae - drug effects</subject><subject>Deltamethrin</subject><subject>Detoxification</subject><subject>Disease control</subject><subject>Disease transmission</subject><subject>Enzymes</subject><subject>Gene Knockdown Techniques</subject><subject>Genotype</subject><subject>Glutathione</subject><subject>Glutathione Transferase - genetics</subject><subject>Glutathione Transferase - metabolism</subject><subject>Health sciences</subject><subject>Inactivation, Metabolic - genetics</subject><subject>Insect Vectors - genetics</subject><subject>Insecticide resistance</subject><subject>Insecticide Resistance - drug effects</subject><subject>Insecticide Resistance - genetics</subject><subject>Insecticides</subject><subject>Insecticides - pharmacology</subject><subject>Life sciences</subject><subject>Malaria</subject><subject>Metabolism</subject><subject>Mixed Function Oxygenases - genetics</subject><subject>Mixed Function Oxygenases - metabolism</subject><subject>Molecular biology</subject><subject>Monooxygenase</subject><subject>Mosquito Control - methods</subject><subject>Mosquitoes</subject><subject>Mutation</subject><subject>Mutation - drug effects</subject><subject>Mutation - genetics</subject><subject>Nitriles - pharmacology</subject><subject>Oryza</subject><subject>ParA gene</subject><subject>Parasitic diseases</subject><subject>Pathogens</subject><subject>Pest control</subject><subject>Populations</subject><subject>Public health</subject><subject>Pyrethrins - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhong, Daibin</au><au>Chang, Xuelian</au><au>Zhou, Guofa</au><au>He, Zhengbo</au><au>Fu, Fengyang</au><au>Yan, Zhentian</au><au>Zhu, Guoding</au><au>Xu, Tielong</au><au>Bonizzoni, Mariangela</au><au>Wang, Mei-Hui</au><au>Cui, Liwang</au><au>Zheng, Bin</au><au>Chen, Bin</au><au>Yan, Guiyun</au><au>Terenius, Olle</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Relationship between knockdown resistance, metabolic detoxification and organismal resistance to pyrethroids in Anopheles sinensis</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-02-06</date><risdate>2013</risdate><volume>8</volume><issue>2</issue><spage>e55475</spage><pages>e55475-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Anopheles sinensis is the most important vector of malaria in Southeast Asia, including China. Currently, the most effective measure to prevent malaria transmission relies on vector control through the use of insecticides, primarily pyrethroids. Extensive use of insecticides poses strong selection pressure on mosquito populations for resistance. Resistance to insecticides can arise due to mutations in the insecticide target site (target site resistance), which in the case of pyrethroids is the para-type sodium channel gene, and/or the catabolism of the insecticide by detoxification enzymes before it reaches its target (metabolic detoxification resistance). In this study, we examined deltamethrin resistance in An. sinensis from China and investigated the relative importance of target site versus metabolic detoxification mechanisms in resistance. A high frequency (>85%) of nonsynonymous mutations in the para gene was found in populations from central China, but not in populations from southern China. Metabolic detoxification as measured by the activity of monooxygenases and glutathione S-transferases (GSTs) was detected in populations from both central and southern China. Monooxygenase activity levels were significantly higher in the resistant than the susceptible mosquitoes, independently of their geographic origin. Stepwise multiple regression analyses in mosquito populations from central China found that both knockdown resistance (kdr) mutations and monooxygenase activity were significantly associated with deltamethrin resistance, with monooxygenase activity playing a stronger role. These results demonstrate the importance of metabolic detoxification in pyrethroid resistance in An. sinensis, and suggest that different mechanisms of resistance could evolve in geographically different populations.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23405157</pmid><doi>10.1371/journal.pone.0055475</doi><tpages>e55475</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-02, Vol.8 (2), p.e55475 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1330878088 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Agriculture Agrochemicals Analysis Animals Anopheles Anopheles - drug effects Anopheles - genetics Anopheles - metabolism Anopheles gambiae Anopheles sinensis Aquatic insects Binding sites Biology Catabolism China Culicidae Culicidae - drug effects Deltamethrin Detoxification Disease control Disease transmission Enzymes Gene Knockdown Techniques Genotype Glutathione Glutathione Transferase - genetics Glutathione Transferase - metabolism Health sciences Inactivation, Metabolic - genetics Insect Vectors - genetics Insecticide resistance Insecticide Resistance - drug effects Insecticide Resistance - genetics Insecticides Insecticides - pharmacology Life sciences Malaria Metabolism Mixed Function Oxygenases - genetics Mixed Function Oxygenases - metabolism Molecular biology Monooxygenase Mosquito Control - methods Mosquitoes Mutation Mutation - drug effects Mutation - genetics Nitriles - pharmacology Oryza ParA gene Parasitic diseases Pathogens Pest control Populations Public health Pyrethrins - pharmacology Pyrethroids Regression analysis Rice Sodium Sodium channels Transferases Vector-borne diseases |
| title | Relationship between knockdown resistance, metabolic detoxification and organismal resistance to pyrethroids in Anopheles sinensis |
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