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ARS Home » Plains Area » Kerrville, Texas » Knipling-Bushland U.S. Livestock Insects Research Laboratory » LAPRU » Research » Publications at this Location » Publication #336026
Title: Role of inward rectifier potassium channels in salivary gland function and sugar feeding of the fruit fly, Drosophila melanogaster

Author
item SWALE, DANIEL - Louisiana State University Agcenter
item LI, ZHILIN - Louisiana State University Agcenter
item Guerrero, Felicito
item Perez De Leon, Adalberto - Beto
item FOIL, LANE - Louisiana State University Agcenter

Submitted to: Pesticide Biochemistry and Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/26/2016
Publication Date: 9/1/2017
Citation: Swale, D., Li, Z., Guerrero, F., Perez De Leon, A.A., Foil, L. 2017. Role of inward rectifier potassium channels in salivary gland function and sugar feeding of the fruit fly, Drosophila melanogaster. Pesticide Biochemistry and Physiology. 141:41-49.

Interpretive Summary: The arthropod salivary gland is of critical importance for horizontal transmission of pathogens, yet a detailed understanding of the ion conductance pathways responsible for saliva production and excretion in the salivary gland is lacking. A superfamily of potassium ion channels, known as inward rectifying potassium (Kir) channels, has been shown to play key roles in the Malpighian tubules, a tissue that is functionally related to salivary glands. Furthermore, the RNA that codes for the Kir potassium channel is overexpressed in the salivary gland of the fruit fly, Drosophila melanogaster, by 32-fold compared to other tissues in that fly. Therefore, we aimed to test the hypothesis that depletion of salivary gland specific Kir channels alters the efficiency of the gland and reduce the insect's feeding capabilities. We chose to do these studies in Drosophila melanogaster because of the extensive number of genetic tools and genomic sequence information that is available for this species. D. melanogaster serves as an excellent model for other flies. Exposure to a selective Kir channel blocker known as VU041 reduced the volume of sucrose consumption by up to 3.2-fold compared to flies not exposed to VU041. Next, we used the genetic tools available to D. melanogaster to specifically inhibit the expression of the Kir potassium channel gene in the salivary glands to assess the role of these channels specifically in the salivary gland and in fly feeding. The Kir-depleted fliles had a reduction in total volume ingested and they displayed an increase in the time spent feeding, both suggestive of a reduction in salivary gland function. These findings suggest that Kir channels likely provide a principal potassium conductance pathway in the Drosophila salivary gland and may provide a target for inducing salivary gland failure in arthropod disease vectors.

Technical Abstract: The arthropod salivary gland is of critical importance for horizontal transmission of pathogens, yet a detailed understanding of the ion conductance pathways responsible for saliva production and excretion is lacking. A superfamily of potassium ion channels, known as inward rectifying potassium (Kir) channels, has been shown to play key roles in the Malpighian tubules, a functionally related tissue when compared to salivary glands. Furthermore, Kir1 is overexpressed in the Drosophila salivary gland by 32-fold. Therefore, we aimed to test the hypothesis that pharmacological and genetic depletion of salivary gland specific Kir channels alters the efficiency of the gland and reduced feeding capabilities. Exposure to VU041, a selective Kir channel blocker, reduced the volume of sucrose consumption by up to 3.2-fold and was found to be concentration-dependent with an EC50 of 68 µM. Importantly, the inactive analog, VU937, was shown to not influence feeding, suggesting the reduction in feeding observed with VU041 is due to Kir channel inhibition. Next, we performed a salivary gland specific knockdown of Kir1 to assess the role of these channels specifically in the salivary gland. The genetically depleted animals had a reduction in total volume ingested and was observed and they displayed an increased in the time spent feeding, both suggestive of a reduction in salivary gland function. Furthermore, a compensatory mechanism appears to be present at day 1 of RNAi-treated animals and is likely to be the Na+-K+-2Cl- cotransporter and/or Na+-K+-ATPase pumps that serve to supplement the inward flow of K+ ions, which highlights the functional redundancy of these glands. These findings suggest that Kir channels likely provide, at least in part, a principal potassium conductance pathway in the Drosophila salivary gland and may provide a target for inducing salivary gland failure in arthropod disease vectors.