The effects of insecticides on two splice variants of the glutamate‐gated chloride channel receptor of the major malaria vector, Anopheles gambiae
Background and Purpose Between half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately, resistance has emerged to the agents currently used to control A. gambiae, creating a demand for novel control measures. The pentameric glutamate‐...
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Published in | British journal of pharmacology Vol. 177; no. 1; pp. 175 - 187 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
Published |
England
Blackwell Publishing Ltd
01.01.2020
John Wiley and Sons Inc |
Subjects | |
Online Access | Get full text |
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Abstract | Background and Purpose
Between half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately, resistance has emerged to the agents currently used to control A. gambiae, creating a demand for novel control measures. The pentameric glutamate‐gated chloride channel (GluCl) expressed in the muscle and nerve cells of these organisms are a potentially important biological target for malaria control. The pharmacological properties of Anophiline GluCl receptors are, however, largely unknown. Accordingly, we compared the efficacy of four insecticides (lindane, fipronil, picrotoxin, and ivermectin) on two A. gambiae GluCl receptor splice variants with the aim of providing a molecular basis for designing novel anti‐malaria treatments.
Experimental Approach
The A. gambiae GluCl receptor b1 and c splice variants were expressed homomerically in Xenopus laevis oocytes and studied with electrophysiological techniques, using two‐electrode voltage‐clamp.
Key Results
The b1 and c GluCl receptors were activated with similar potencies by glutamate and ivermectin. Fipronil was more potent than picrotoxin and lindane at inhibiting glutamate‐ and ivermectin‐gated currents. Importantly, b1 GluCl receptors exhibited reduced sensitivity to picrotoxin and lindane. They also recovered from these effects to a greater extent than c GluCl receptors
Conclusions and Implications
The two splice variant subunits exhibited differential sensitivities to multiple, structurally divergent insecticides, without accompanying changes in the sensitivity to the endogenous neurotransmitter, glutamate, implying that drug resistance may be caused by alterations in relative subunit expression levels, without affecting physiological function. Our results strongly suggest that it should be feasible to develop novel subunit‐specific pharmacological agents. |
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AbstractList | Background and PurposeBetween half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately, resistance has emerged to the agents currently used to control A. gambiae, creating a demand for novel control measures. The pentameric glutamate‐gated chloride channel (GluCl) expressed in the muscle and nerve cells of these organisms are a potentially important biological target for malaria control. The pharmacological properties of Anophiline GluCl receptors are, however, largely unknown. Accordingly, we compared the efficacy of four insecticides (lindane, fipronil, picrotoxin, and ivermectin) on two A. gambiae GluCl receptor splice variants with the aim of providing a molecular basis for designing novel anti‐malaria treatments.Experimental ApproachThe A. gambiae GluCl receptor b1 and c splice variants were expressed homomerically in Xenopus laevis oocytes and studied with electrophysiological techniques, using two‐electrode voltage‐clamp.Key ResultsThe b1 and c GluCl receptors were activated with similar potencies by glutamate and ivermectin. Fipronil was more potent than picrotoxin and lindane at inhibiting glutamate‐ and ivermectin‐gated currents. Importantly, b1 GluCl receptors exhibited reduced sensitivity to picrotoxin and lindane. They also recovered from these effects to a greater extent than c GluCl receptorsConclusions and ImplicationsThe two splice variant subunits exhibited differential sensitivities to multiple, structurally divergent insecticides, without accompanying changes in the sensitivity to the endogenous neurotransmitter, glutamate, implying that drug resistance may be caused by alterations in relative subunit expression levels, without affecting physiological function. Our results strongly suggest that it should be feasible to develop novel subunit‐specific pharmacological agents. Background and Purpose Between half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately, resistance has emerged to the agents currently used to control A. gambiae , creating a demand for novel control measures. The pentameric glutamate‐gated chloride channel (GluCl) expressed in the muscle and nerve cells of these organisms are a potentially important biological target for malaria control. The pharmacological properties of Anophiline GluCl receptors are, however, largely unknown. Accordingly, we compared the efficacy of four insecticides (lindane, fipronil, picrotoxin, and ivermectin) on two A. gambiae GluCl receptor splice variants with the aim of providing a molecular basis for designing novel anti‐malaria treatments. Experimental Approach The A. gambiae GluCl receptor b1 and c splice variants were expressed homomerically in Xenopus laevis oocytes and studied with electrophysiological techniques, using two‐electrode voltage‐clamp. Key Results The b1 and c GluCl receptors were activated with similar potencies by glutamate and ivermectin. Fipronil was more potent than picrotoxin and lindane at inhibiting glutamate‐ and ivermectin‐gated currents. Importantly, b1 GluCl receptors exhibited reduced sensitivity to picrotoxin and lindane. They also recovered from these effects to a greater extent than c GluCl receptors Conclusions and Implications The two splice variant subunits exhibited differential sensitivities to multiple, structurally divergent insecticides, without accompanying changes in the sensitivity to the endogenous neurotransmitter, glutamate, implying that drug resistance may be caused by alterations in relative subunit expression levels, without affecting physiological function. Our results strongly suggest that it should be feasible to develop novel subunit‐specific pharmacological agents. Background and Purpose Between half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately, resistance has emerged to the agents currently used to control A. gambiae, creating a demand for novel control measures. The pentameric glutamate‐gated chloride channel (GluCl) expressed in the muscle and nerve cells of these organisms are a potentially important biological target for malaria control. The pharmacological properties of Anophiline GluCl receptors are, however, largely unknown. Accordingly, we compared the efficacy of four insecticides (lindane, fipronil, picrotoxin, and ivermectin) on two A. gambiae GluCl receptor splice variants with the aim of providing a molecular basis for designing novel anti‐malaria treatments. Experimental Approach The A. gambiae GluCl receptor b1 and c splice variants were expressed homomerically in Xenopus laevis oocytes and studied with electrophysiological techniques, using two‐electrode voltage‐clamp. Key Results The b1 and c GluCl receptors were activated with similar potencies by glutamate and ivermectin. Fipronil was more potent than picrotoxin and lindane at inhibiting glutamate‐ and ivermectin‐gated currents. Importantly, b1 GluCl receptors exhibited reduced sensitivity to picrotoxin and lindane. They also recovered from these effects to a greater extent than c GluCl receptors Conclusions and Implications The two splice variant subunits exhibited differential sensitivities to multiple, structurally divergent insecticides, without accompanying changes in the sensitivity to the endogenous neurotransmitter, glutamate, implying that drug resistance may be caused by alterations in relative subunit expression levels, without affecting physiological function. Our results strongly suggest that it should be feasible to develop novel subunit‐specific pharmacological agents. Between half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately, resistance has emerged to the agents currently used to control A. gambiae, creating a demand for novel control measures. The pentameric glutamate-gated chloride channel (GluCl) expressed in the muscle and nerve cells of these organisms are a potentially important biological target for malaria control. The pharmacological properties of Anophiline GluCl receptors are, however, largely unknown. Accordingly, we compared the efficacy of four insecticides (lindane, fipronil, picrotoxin, and ivermectin) on two A. gambiae GluCl receptor splice variants with the aim of providing a molecular basis for designing novel anti-malaria treatments. The A. gambiae GluCl receptor b1 and c splice variants were expressed homomerically in Xenopus laevis oocytes and studied with electrophysiological techniques, using two-electrode voltage-clamp. The b1 and c GluCl receptors were activated with similar potencies by glutamate and ivermectin. Fipronil was more potent than picrotoxin and lindane at inhibiting glutamate- and ivermectin-gated currents. Importantly, b1 GluCl receptors exhibited reduced sensitivity to picrotoxin and lindane. They also recovered from these effects to a greater extent than c GluCl receptors CONCLUSIONS AND IMPLICATIONS: The two splice variant subunits exhibited differential sensitivities to multiple, structurally divergent insecticides, without accompanying changes in the sensitivity to the endogenous neurotransmitter, glutamate, implying that drug resistance may be caused by alterations in relative subunit expression levels, without affecting physiological function. Our results strongly suggest that it should be feasible to develop novel subunit-specific pharmacological agents. |
Author | Keramidas, Angelo Atif, Mohammed Lynch, Joseph W. |
AuthorAffiliation | 1 Queensland Brain Institute The University of Queensland Brisbane QLD Australia |
AuthorAffiliation_xml | – name: 1 Queensland Brain Institute The University of Queensland Brisbane QLD Australia |
Author_xml | – sequence: 1 givenname: Mohammed surname: Atif fullname: Atif, Mohammed organization: The University of Queensland – sequence: 2 givenname: Joseph W. surname: Lynch fullname: Lynch, Joseph W. email: j.lynch@uq.edu.au organization: The University of Queensland – sequence: 3 givenname: Angelo surname: Keramidas fullname: Keramidas, Angelo email: a.keramidas@uq.edu.au organization: The University of Queensland |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31479507$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_pestbp_2020_104743 crossref_primary_10_1371_journal_ppat_1008863 crossref_primary_10_1002_ejoc_202101531 crossref_primary_10_1128_mSphere_00218_21 crossref_primary_10_3389_fnins_2020_00879 crossref_primary_10_1038_s42003_023_04907_x |
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Notes | Present Address: Angelo Keramidas, Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia. |
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mutations in the M2 region of the alpha, beta, or gamma subunit of the GABAA channel that abolish block by picrotoxin publication-title: Receptors & Channels contributor: fullname: Gurley D. |
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Between half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately,... Between half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately, resistance has emerged to... Background and Purpose Between half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately,... Background and PurposeBetween half to 1 million people die annually from malaria. Anopheles gambiae mosquitoes are major malaria vectors. Unfortunately,... |
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SubjectTerms | Alternative splicing Amino Acid Sequence Animals Anopheles - genetics Anopheles - metabolism Anopheles gambiae Chloride Channels - genetics Chloride Channels - metabolism Chlorides Dose-Response Relationship, Drug Drug resistance Female Fipronil Gametocytes Glutamic Acid - pharmacology Insecticide resistance Insecticides Insecticides - pharmacology Ivermectin Ivermectin - pharmacology Lindane Malaria Mosquito Vectors - genetics Mosquito Vectors - metabolism Muscles Oocytes Oocytes - drug effects Oocytes - metabolism Picrotoxin Protein Isoforms - genetics Protein Isoforms - metabolism Receptor mechanisms Research Paper Research Papers Vector-borne diseases Vectors Xenopus laevis |
Title | The effects of insecticides on two splice variants of the glutamate‐gated chloride channel receptor of the major malaria vector, Anopheles gambiae |
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