Relationship between Knockdown Resistance, Metabolic Detoxification and Organismal Resistance to Pyrethroids in Anopheles sinensis

Daibin Zhong, Xuelian Chang, Guofa Zhou, Zhengbo He, Fengyang Fu, Zhentian Yan, Guoding Zhu, Tielong Xu, Mariangela Bonizzoni, Mei Hui Wang, Liwang Cui, Bin Zheng, Bin Chen, Guiyun Yan

Research output: Contribution to journalArticle

49 Citations (Scopus)

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.

Original languageEnglish (US)
Article numbere55475
JournalPloS one
Volume8
Issue number2
DOIs
StatePublished - Feb 6 2013

Fingerprint

Anopheles sinensis
metabolic detoxification
pesticide resistance
Pyrethrins
Detoxification
Anopheles
Insecticides
pyrethrins
China
Mixed Function Oxygenases
insecticides
Culicidae
Population
deltamethrin
resistance mechanisms
mutation
malaria
Mutation
Genes
Malaria

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

Cite this

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. / Relationship between Knockdown Resistance, Metabolic Detoxification and Organismal Resistance to Pyrethroids in Anopheles sinensis. In: PloS one. 2013 ; Vol. 8, No. 2.
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title = "Relationship between Knockdown Resistance, Metabolic Detoxification and Organismal Resistance to Pyrethroids in Anopheles sinensis",
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.",
author = "Daibin Zhong and Xuelian Chang and Guofa Zhou and Zhengbo He and Fengyang Fu and Zhentian Yan and Guoding Zhu and Tielong Xu and Mariangela Bonizzoni and Wang, {Mei Hui} and Liwang Cui and Bin Zheng and Bin Chen and Guiyun Yan",
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Zhong, D, Chang, X, Zhou, G, He, Z, Fu, F, Yan, Z, Zhu, G, Xu, T, Bonizzoni, M, Wang, MH, Cui, L, Zheng, B, Chen, B & Yan, G 2013, 'Relationship between Knockdown Resistance, Metabolic Detoxification and Organismal Resistance to Pyrethroids in Anopheles sinensis', PloS one, vol. 8, no. 2, e55475. https://doi.org/10.1371/journal.pone.0055475

Relationship between Knockdown Resistance, Metabolic Detoxification and Organismal Resistance to Pyrethroids in Anopheles sinensis. / 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.

In: PloS one, Vol. 8, No. 2, e55475, 06.02.2013.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Relationship between Knockdown Resistance, Metabolic Detoxification and Organismal Resistance to Pyrethroids in Anopheles sinensis

AU - Zhong, Daibin

AU - Chang, Xuelian

AU - Zhou, Guofa

AU - He, Zhengbo

AU - Fu, Fengyang

AU - Yan, Zhentian

AU - Zhu, Guoding

AU - Xu, Tielong

AU - Bonizzoni, Mariangela

AU - Wang, Mei Hui

AU - Cui, Liwang

AU - Zheng, Bin

AU - Chen, Bin

AU - Yan, Guiyun

PY - 2013/2/6

Y1 - 2013/2/6

N2 - 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.

AB - 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.

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