Cargando…

The G119S Acetylcholinesterase (Ace-1) Target Site Mutation Confers Carbamate Resistance in the Major Malaria Vector Anopheles gambiae from Cameroon: A Challenge for the Coming IRS Implementation

Growing resistance is reported to carbamate insecticides in malaria vectors in Cameroon. However, the contribution of acetylcholinesterase (Ace-1) to this resistance remains uncharacterised. Here, we established that the G119S mutation is driving resistance to carbamates in Anopheles gambiae populat...

Descripción completa

Detalles Bibliográficos
Autores principales: Elanga-Ndille, Emmanuel, Nouage, Lynda, Ndo, Cyrille, Binyang, Achille, Assatse, Tatiane, Nguiffo-Nguete, Daniel, Djonabaye, Doumani, Irving, Helen, Tene-Fossog, Billy, Wondji, Charles S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6826778/
https://www.ncbi.nlm.nih.gov/pubmed/31614683
http://dx.doi.org/10.3390/genes10100790
_version_ 1783465171238256640
author Elanga-Ndille, Emmanuel
Nouage, Lynda
Ndo, Cyrille
Binyang, Achille
Assatse, Tatiane
Nguiffo-Nguete, Daniel
Djonabaye, Doumani
Irving, Helen
Tene-Fossog, Billy
Wondji, Charles S.
author_facet Elanga-Ndille, Emmanuel
Nouage, Lynda
Ndo, Cyrille
Binyang, Achille
Assatse, Tatiane
Nguiffo-Nguete, Daniel
Djonabaye, Doumani
Irving, Helen
Tene-Fossog, Billy
Wondji, Charles S.
author_sort Elanga-Ndille, Emmanuel
collection PubMed
description Growing resistance is reported to carbamate insecticides in malaria vectors in Cameroon. However, the contribution of acetylcholinesterase (Ace-1) to this resistance remains uncharacterised. Here, we established that the G119S mutation is driving resistance to carbamates in Anopheles gambiae populations from Cameroon. Insecticide bioassay on field-collected mosquitoes from Bankeng, a locality in southern Cameroon, showed high resistance to the carbamates bendiocarb (64.8% ± 3.5% mortality) and propoxur (55.71% ± 2.9%) but a full susceptibility to the organophosphate fenitrothion. The TaqMan genotyping of the G119S mutation in field-collected adults revealed the presence of this resistance allele (39%). A significant correlation was observed between the Ace-1(R) and carbamate resistance at allelic ((bendiocarb; odds ratio (OR) = 75.9; p < 0.0001) and (propoxur; OR = 1514; p < 0.0001)) and genotypic (homozygote resistant vs. homozygote susceptible (bendiocarb; OR = 120.8; p < 0.0001) and (propoxur; OR = 3277; p < 0.0001)) levels. Furthermore, the presence of the mutation was confirmed by sequencing an Ace-1 portion flanking codon 119. The cloning of this fragment revealed a likely duplication of Ace-1 in Cameroon as mosquitoes exhibited at least three distinct haplotypes. Phylogenetic analyses showed that the predominant Ace-1(R) allele is identical to that from West Africa suggesting a recent introduction of this allele in Central Africa from the West. The spread of this Ace-1(R) represents a serious challenge to future implementation of indoor residual spraying (IRS)-based interventions using carbamates or organophosphates in Cameroon.
format Online
Article
Text
id pubmed-6826778
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-68267782019-11-18 The G119S Acetylcholinesterase (Ace-1) Target Site Mutation Confers Carbamate Resistance in the Major Malaria Vector Anopheles gambiae from Cameroon: A Challenge for the Coming IRS Implementation Elanga-Ndille, Emmanuel Nouage, Lynda Ndo, Cyrille Binyang, Achille Assatse, Tatiane Nguiffo-Nguete, Daniel Djonabaye, Doumani Irving, Helen Tene-Fossog, Billy Wondji, Charles S. Genes (Basel) Article Growing resistance is reported to carbamate insecticides in malaria vectors in Cameroon. However, the contribution of acetylcholinesterase (Ace-1) to this resistance remains uncharacterised. Here, we established that the G119S mutation is driving resistance to carbamates in Anopheles gambiae populations from Cameroon. Insecticide bioassay on field-collected mosquitoes from Bankeng, a locality in southern Cameroon, showed high resistance to the carbamates bendiocarb (64.8% ± 3.5% mortality) and propoxur (55.71% ± 2.9%) but a full susceptibility to the organophosphate fenitrothion. The TaqMan genotyping of the G119S mutation in field-collected adults revealed the presence of this resistance allele (39%). A significant correlation was observed between the Ace-1(R) and carbamate resistance at allelic ((bendiocarb; odds ratio (OR) = 75.9; p < 0.0001) and (propoxur; OR = 1514; p < 0.0001)) and genotypic (homozygote resistant vs. homozygote susceptible (bendiocarb; OR = 120.8; p < 0.0001) and (propoxur; OR = 3277; p < 0.0001)) levels. Furthermore, the presence of the mutation was confirmed by sequencing an Ace-1 portion flanking codon 119. The cloning of this fragment revealed a likely duplication of Ace-1 in Cameroon as mosquitoes exhibited at least three distinct haplotypes. Phylogenetic analyses showed that the predominant Ace-1(R) allele is identical to that from West Africa suggesting a recent introduction of this allele in Central Africa from the West. The spread of this Ace-1(R) represents a serious challenge to future implementation of indoor residual spraying (IRS)-based interventions using carbamates or organophosphates in Cameroon. MDPI 2019-10-11 /pmc/articles/PMC6826778/ /pubmed/31614683 http://dx.doi.org/10.3390/genes10100790 Text en © 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Elanga-Ndille, Emmanuel
Nouage, Lynda
Ndo, Cyrille
Binyang, Achille
Assatse, Tatiane
Nguiffo-Nguete, Daniel
Djonabaye, Doumani
Irving, Helen
Tene-Fossog, Billy
Wondji, Charles S.
The G119S Acetylcholinesterase (Ace-1) Target Site Mutation Confers Carbamate Resistance in the Major Malaria Vector Anopheles gambiae from Cameroon: A Challenge for the Coming IRS Implementation
title The G119S Acetylcholinesterase (Ace-1) Target Site Mutation Confers Carbamate Resistance in the Major Malaria Vector Anopheles gambiae from Cameroon: A Challenge for the Coming IRS Implementation
title_full The G119S Acetylcholinesterase (Ace-1) Target Site Mutation Confers Carbamate Resistance in the Major Malaria Vector Anopheles gambiae from Cameroon: A Challenge for the Coming IRS Implementation
title_fullStr The G119S Acetylcholinesterase (Ace-1) Target Site Mutation Confers Carbamate Resistance in the Major Malaria Vector Anopheles gambiae from Cameroon: A Challenge for the Coming IRS Implementation
title_full_unstemmed The G119S Acetylcholinesterase (Ace-1) Target Site Mutation Confers Carbamate Resistance in the Major Malaria Vector Anopheles gambiae from Cameroon: A Challenge for the Coming IRS Implementation
title_short The G119S Acetylcholinesterase (Ace-1) Target Site Mutation Confers Carbamate Resistance in the Major Malaria Vector Anopheles gambiae from Cameroon: A Challenge for the Coming IRS Implementation
title_sort g119s acetylcholinesterase (ace-1) target site mutation confers carbamate resistance in the major malaria vector anopheles gambiae from cameroon: a challenge for the coming irs implementation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6826778/
https://www.ncbi.nlm.nih.gov/pubmed/31614683
http://dx.doi.org/10.3390/genes10100790
work_keys_str_mv AT elangandilleemmanuel theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT nouagelynda theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT ndocyrille theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT binyangachille theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT assatsetatiane theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT nguiffonguetedaniel theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT djonabayedoumani theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT irvinghelen theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT tenefossogbilly theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT wondjicharless theg119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT elangandilleemmanuel g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT nouagelynda g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT ndocyrille g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT binyangachille g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT assatsetatiane g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT nguiffonguetedaniel g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT djonabayedoumani g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT irvinghelen g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT tenefossogbilly g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation
AT wondjicharless g119sacetylcholinesteraseace1targetsitemutationconferscarbamateresistanceinthemajormalariavectoranophelesgambiaefromcameroonachallengeforthecomingirsimplementation