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Annual Review of Entomology

Volume 67, 2022

The Molecular Physiology and Toxicology of Inward Rectifier Potassium Channels in Insects

Abstract

Inward rectifier K+ (Kir) channels have been studied extensively in mammals, where they play critical roles in health and disease. In insects, Kir channels have recently been found to be key regulators of diverse physiological processes in several tissues. The importance of Kir channels in insects has positioned them to serve as emerging targets for the development of insecticides with novel modes of action. In this article, we provide the first comprehensive review of insect Kir channels, highlighting the rapid progress made in understanding their molecular biology, physiological roles, pharmacology, and toxicology. In addition, we highlight key gaps in our knowledge and suggest directions for future research to advance our understanding of Kir channels and their roles in insect physiology. Further knowledge of their functional roles will also facilitate their exploitation as targets for controlling arthropod pests and vectors of economic, medical, and/or veterinary relevance.

Keyword(s): ion transport, K+ channels, molecular biology, pesticides, pharmacology
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2022-01-07
2024-05-10
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Literature Cited

  1. 1. 
    Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185–95
     [Google Scholar]
  2. 2. 
    Aretz C, Kharade SV, Chronister K, Trigueros RR, Rodriguez EM et al. 2020. Further SAR on the (phenylsulfonyl)piperazine scaffold as inhibitors of the Aedes aegypti Kir1 (AeKir) channel and larvicides. ChemMedChem 16:319–27
     [Google Scholar]
  3. 3. 
    Aretz C, Morwitzer MJ, Sanford A, Hogan AM, Portillo M et al. 2019. Discovery and characterization of 2-nitro-5-(4-(phenylsulfonyl)piperazin-1-yl)-N-(pyridin-4-ylmethyl)anilines as novel inhibitors of the Aedes aegypti Kir1 (AeKir1) channel. ACS Infect. Dis. 14:917–31
     [Google Scholar]
  4. 4. 
    Ausborn J, Wolf H, Mader W, Kayser H. 2005. The insecticide pymetrozine selectively affects chordotonal mechanoreceptors. J. Exp. Biol. 208:4451–66
     [Google Scholar]
  5. 5. 
    Baker DA, Nolan T, Fischer B, Pinder A, Crisanti A, Russell S 2011. A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae. BMC Genom. 12:296
     [Google Scholar]
  6. 6. 
    Beyenbach KW, Masia R. 2002. Membrane conductances of principal cells in Malpighian tubules of Aedes aegypti. J. Insect Physiol. 48:375–86
     [Google Scholar]
  7. 7. 
    Beyenbach KW, Yu Y, Piermarini PM, Denton J. 2015. Targeting renal epithelial channels for the control of insect vectors. Tissue Barriers 3:e1081861
     [Google Scholar]
  8. 8. 
    Chen R, Swale DR. 2018. Inwardly rectifying potassium (Kir) channels represent a critical ion conductance pathway in the nervous systems of insects. Sci. Rep 8:1617Showed that Kir channel inhibition disrupts K+ conductances in the central nervous system of D. melanogaster.
     [Google Scholar]
  9. 9. 
    Cheng WW, Enkvetchakul D, Nichols CG 2009. KirBac1.1: It's an inward rectifying potassium channel. J. Gen. Physiol. 133:295–305
     [Google Scholar]
  10. 10. 
    Chintapalli V, Wang J, Herzyk P, Davies S, Dow J. 2013. Data-mining the FlyAtlas online resource to identify core functional motifs across transporting epithelia. BMC Genom 14:518
     [Google Scholar]
  11. 11. 
    Coles JA, Tsacopoulos M. 1979. Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J. Physiol. 290:525–49
     [Google Scholar]
  12. 12. 
    Croker B, Crozat K, Berger M, Xia Y, Sovath S et al. 2007. ATP-sensitive potassium channels mediate survival during infection in mammals and insects. Nat. Genet. 39:1453–60
     [Google Scholar]
  13. 13. 
    Dahal GR, Pradhan SJ, Bates EA. 2017. Inwardly rectifying potassium channels influence Drosophila wing morphogenesis by regulating Dpp release. Development 144:2771–83
     [Google Scholar]
  14. 14. 
    Dahal GR, Rawson J, Gassaway B, Kwok B, Tong Y et al. 2012. An inwardly rectifying K+ channel is required for patterning. Development 139:3653–64Showed that embryonic Kir gene silencing or ablation disrupts survival and/or development in D. melanogaster.
     [Google Scholar]
  15. 15. 
    Dale RP, Jones AK, Tamborindeguy C, Davies TG, Amey JS et al. 2010. Identification of ion channel genes in the Acyrthosiphon pisum genome. Insect Mol. Biol. 19:Suppl. 2141–53
     [Google Scholar]
  16. 16. 
    Dassau L, Conti LR, Radeke CM, Ptacek LJ, Vandenberg CA. 2011. Kir2.6 regulates the surface expression of Kir2.x inward rectifier potassium channels. J. Biol. Chem. 286:9526–41
     [Google Scholar]
  17. 17. 
    Dissanayake SN, Marinotti O, Ribeiro JMC, James AA. 2006. angaGEDUCI: Anopheles gambiae gene expression database with integrated comparative algorithms for identifying conserved DNA motifs in promoter sequences. BMC Genom. 7:116
     [Google Scholar]
  18. 18. 
    Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD 2007. Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J. Neurosci. 27:11354–65
     [Google Scholar]
  19. 19. 
    Doring F, Wischmeyer E, Kuhnlein RP, Jackle H, Karschin A. 2002. Inwardly rectifying K+ (Kir) channels in Drosophila: a crucial role of cellular milieu factors Kir channel function. J. Biol. Chem. 277:25554–61First study to clone insect Kir cDNAs and characterize their molecular expression and functional properties.
     [Google Scholar]
  20. 20. 
    Eleftherianos I, Won S, Chtarbanova S, Squiban B, Ocorr K et al. 2011. ATP-sensitive potassium channel (KATP)-dependent regulation of cardiotropic viral infections. PNAS 108:12024–29Showed that Kir1 and Kir2 form putative KATP channels contributing to antiviral immunity in the D. melanogaster heart.
     [Google Scholar]
  21. 21. 
    Esquivel CJ, Cassone BJ, Piermarini PM. 2014. Transcriptomic evidence for a dramatic functional transition of the Malpighian tubules after a blood meal in the Asian tiger mosquito Aedes albopictus. PLOS Negl. Trop. Dis. 8:e2929
     [Google Scholar]
  22. 22. 
    Esquivel CJ, Cassone BJ, Piermarini PM. 2016. A de novo transcriptome of the Malpighian tubules in non-blood-fed and blood-fed Asian tiger mosquitoes Aedes albopictus: insights into diuresis, detoxification, and blood meal processing. PeerJ 4:e1784
     [Google Scholar]
  23. 23. 
    Estep AS, Sanscrainte ND, Waits CM, Louton JE, Becnel JJ. 2017. Resistance status and resistance mechanisms in a strain of Aedes aegypti (Diptera: Culicidae) from Puerto Rico. J. Med. Entomol. 54:1643–48
     [Google Scholar]
  24. 24. 
    Evans JM, Allan AK, Davies SA, Dow JA. 2005. Sulphonylurea sensitivity and enriched expression implicate inward rectifier K+ channels in Drosophila melanogaster renal function. J. Exp. Biol. 208:3771–83
     [Google Scholar]
  25. 25. 
    Fridell Y-WC, Hoh M, Kréneisz O, Hosier S, Chang C et al. 2009. Increased uncoupling protein (UCP) activity in Drosophila insulin-producing neurons attenuates insulin signaling and extends lifespan. Aging 1:699–713
     [Google Scholar]
  26. 26. 
    Haley C, Donnell M. 1997. K+ reabsorption by the lower Malpighian tubule of Rhodnius prolixus: inhibition by Ba2+ and blockers of H+/K+-ATPases. J. Exp. Biol. 200:139–47
     [Google Scholar]
  27. 27. 
    Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y. 2010. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol. Rev. 90:291–366
     [Google Scholar]
  28. 28. 
    Hyde D, Baldrick P, Marshall SL, Anstee JH 2001. Rubidium reduces potassium permeability and fluid secretion in Malpighian tubules of Locusta migratoria, L. J. Insect Physiol. 47:629–37
     [Google Scholar]
  29. 29. 
    Kandasamy R, London D, Stam L, von Deyn W, Zhao X et al. 2017. Afidopyropen: new and potent modulator of insect transient receptor potential channels. Insect Biochem. Mol. Biol. 84:32–39
     [Google Scholar]
  30. 30. 
    Kocmarek AL, O'Donnell MJ. 2011. Potassium fluxes across the blood brain barrier of the cockroach, Periplaneta americana. J. Insect Physiol. 57:127–35
     [Google Scholar]
  31. 31. 
    Kofuji P, Connors NC. 2003. Molecular substrates of potassium spatial buffering in glial cells. Mol. Neurobiol. 28:195–208
     [Google Scholar]
  32. 32. 
    Kofuji P, Newman EA. 2004. Potassium buffering in the central nervous system. Neuroscience 129:1045–56
     [Google Scholar]
  33. 33. 
    Kolosov D, Donly C, MacMillan H, O'Donnell MJ. 2019. Transcriptomic analysis of the Malpighian tubules of Trichoplusia ni: clues to mechanisms for switching from ion secretion to ion reabsorption in the distal ileac plexus. J. Insect Physiol. 112:73–89
     [Google Scholar]
  34. 34. 
    Kolosov D, O'Donnell MJ. 2019. Malpighian tubules of caterpillars: blending RNAseq and physiology to reveal regional functional diversity and novel epithelial ion transport control mechanisms. J. Exp. Biol. 222:jeb211623
     [Google Scholar]
  35. 35. 
    Kolosov D, Tauqir M, Rajaruban S, Piermarini PM, Donini A, O'Donnell MJ. 2018. Molecular mechanisms of bi-directional ion transport in the Malpighian tubules of a lepidopteran crop pest, Trichoplusia ni. J. Insect Physiol. 109:55–68
     [Google Scholar]
  36. 36. 
    Lai X, Xu J, Ma H, Liu Z, Zheng W et al. 2020. Identification and expression of inward-rectifying potassium channel subunits in Plutella xylostella. Insects 11:461
     [Google Scholar]
  37. 37. 
    Leader DP, Krause SA, Pandit A, Davies SA, Dow JAT. 2017. FlyAtlas 2: a new version of the Drosophila melanogaster expression atlas with RNA-Seq, miRNA-Seq and sex-specific data. Nucleic Acids Res 46:D809–15
     [Google Scholar]
  38. 38. 
    Leyssens A, Dijkstra S, Van Kerkhove E, Steels P. 1994. Mechanisms of K+ uptake across the basal membrane of Malpighian tubules of Formica polyctena: the effect of ions and inhibitors. J. Exp. Biol. 195:123–45
     [Google Scholar]
  39. 39. 
    Li W, Zhu Y-C, Li F, He Y. 2020. In silico discovery of genes encoding insecticide targets and detoxifying enzymes in Brevicoryne brassicae and Lipaphis erysimi. J. Asia-Pac. Entomol. 23:159–66
     [Google Scholar]
  40. 40. 
    Li Z, Davis JA, Swale DR. 2019. Chemical inhibition of Kir channels reduces salivary secretions and phloem feeding of the cotton aphid, Aphis gossypii (Glover). Pest Manag. Sci. 75:2725–34
     [Google Scholar]
  41. 41. 
    Li Z, Guerrero F, Pérez de León AA, Foil LD, Swale DR 2020. Small-molecule inhibitors of inward rectifier potassium (Kir) channels reduce bloodmeal feeding and have insecticidal activity against the horn fly (Diptera: Muscidae). J. Med. Entomol. 57:1131–40
     [Google Scholar]
  42. 42. 
    Li Z, Macaluso KR, Foil LD, Swale DR. 2019. Inward rectifier potassium (Kir) channels mediate salivary gland function and blood feeding in the lone star tick, Amblyomma americanum. PLOS Negl. Trop. Dis. 13:e0007153
     [Google Scholar]
  43. 43. 
    Luan Z, Li HS. 2012. Inwardly rectifying potassium channels in Drosophila. Acta Physiol. Sinica 64:515–19
     [Google Scholar]
  44. 44. 
    MacLean SJ, Andrews BC, Verheyen EM. 2002. Characterization of Dir: a putative potassium inward rectifying channel in Drosophila. Mech. Dev. 116:193–97
     [Google Scholar]
  45. 45. 
    Mamidala P, Mittapelly P, Jones SC, Piermarini PM, Mittapalli O. 2013. Molecular characterization of genes encoding inward rectifier potassium (Kir) channels in the bed bug (Cimex lectularius). Comp. Biochem. Physiol. B 164:275–79
     [Google Scholar]
  46. 46. 
    Marshall AT, Clode PL. 2009. X-ray microanalysis of Rb+ entry into cricket Malpighian tubule cells via putative K+ channels. J. Exp. Biol. 212:2977–82
     [Google Scholar]
  47. 47. 
    McCormack TJ. 2003. Comparison of K+-channel genes within the genomes of Anopheles gambiae and Drosophila melanogaster. Genome Biol 4:R58
     [Google Scholar]
  48. 48. 
    Meng X, Wu Z, Yang X, Qian K, Zhang N et al. 2021. Flonicamid and knockdown of inward rectifier potassium channel gene CsKir2B adversely affect the feeding and development of Chilo suppressalis. Pest Manag. Sci. 77:2045–53
     [Google Scholar]
  49. 49. 
    Miller C. 2000. An overview of the potassium channel family. Genome Biol 1:reviews0004
     [Google Scholar]
  50. 50. 
    Morishige K, Inanobe A, Yoshimoto Y, Kurachi H, Murata Y et al. 1999. Secretagogue-induced exocytosis recruits G protein-gated K+ channels to plasma membrane in endocrine cells. J. Biol. Chem. 274:7969–74
     [Google Scholar]
  51. 51. 
    Mutunga JM, Anderson TD, Craft DT, Gross AD, Swale DR et al. 2015. Carbamate and pyrethroid resistance in the Akron strain of Anopheles gambiae. Pestic. Biochem. Physiol. 121:116–21
     [Google Scholar]
  52. 52. 
    Nesterov A, Spalthoff C, Kandasamy R, Katana R, Rankl NB et al. 2015. TRP channels in insect stretch receptors as insecticide targets. Neuron 86:665–71
     [Google Scholar]
  53. 53. 
    O'Donnell MJ, Dow JA, Huesmann GR, Tublitz NJ, Maddrell SH. 1996. Separate control of anion and cation transport in Malpighian tubules of Drosophila melanogaster. J. Exp. Biol. 199:1163–75
     [Google Scholar]
  54. 54. 
    O'Neal ST, Swale DR, Anderson TD. 2017. ATP-sensitive inwardly rectifying potassium channel regulation of viral infections in honey bees. Sci. Rep. 7:8668
     [Google Scholar]
  55. 55. 
    O'Neal ST, Swale DR, Bloomquist JR, Anderson TD. 2017. ATP-sensitive inwardly rectifying potassium channel modulators alter cardiac function in honey bees. J. Insect Physiol. 99:95–100
     [Google Scholar]
  56. 56. 
    Overend G, Cabrero P, Halberg KA, Ranford-Cartwright LC, Woods DJ et al. 2015. A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae. Insect Biochem. Mol. Biol. 67:47–58
     [Google Scholar]
  57. 57. 
    Pacey EK, O'Donnell MJ. 2014. Transport of H+, Na+ and K+ across the posterior midgut of blood-fed mosquitoes (Aedes aegypti). J. Insect Physiol. 61:42–50
     [Google Scholar]
  58. 58. 
    Piermarini PM, Dunemann SM, Rouhier MF, Calkins TL, Raphemot R et al. 2015. Localization and role of inward rectifier K+ channels in Malpighian tubules of the yellow fever mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 67:59–73
     [Google Scholar]
  59. 59. 
    Piermarini PM, Esquivel CJ, Denton JS. 2017. Malpighian tubules as novel targets for mosquito control. Int. J. Environ. Res. Public Health 14:111
     [Google Scholar]
  60. 60. 
    Piermarini PM, Inocente EA, Acosta N, Hopkins CR, Denton JS, Michel AP. 2018. Inward rectifier potassium (Kir) channels in the soybean aphid Aphis glycines: functional characterization, pharmacology, and toxicology. J. Insect Physiol. 110:57–65
     [Google Scholar]
  61. 61. 
    Piermarini PM, Rouhier MF, Schepel M, Kosse C, Beyenbach KW 2013. Cloning and functional characterization of inward-rectifying potassium (Kir) channels from Malpighian tubules of the mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 43:75–90
     [Google Scholar]
  62. 62. 
    Prole DL, Marrion NV. 2012. Identification of putative potassium channel homologues in pathogenic protozoa. PLOS ONE 7:e32264
     [Google Scholar]
  63. 63. 
    Raphemot R, Estevez-Lao TY, Rouhier MF, Piermarini PM, Denton JS, Hillyer JF. 2014. Molecular and functional characterization of Anopheles gambiae inward rectifier potassium (Kir1) channels: a novel role in egg production. Insect Biochem. Mol. Biol. 51C:10–19
     [Google Scholar]
  64. 64. 
    Raphemot R, Rouhier MF, Hopkins CR, Gogliotti RD, Lovell KM et al. 2013. Eliciting renal failure in mosquitoes with a small-molecule inhibitor of inward-rectifying potassium channels. PLOS ONE 8:e64905Showed that inhibition of Kir1 in mosquitoes induces toxicity via renal failure.
     [Google Scholar]
  65. 65. 
    Raphemot R, Rouhier MF, Swale DR, Days E, Weaver CD et al. 2014. Discovery and characterization of a potent and selective inhibitor of Aedes aegypti inward rectifier potassium channels. PLOS ONE 9:e110772
     [Google Scholar]
  66. 66. 
    Ren M, Niu J, Hu B, Wei Q, Zheng C et al. 2018. Block of Kir channels by flonicamid disrupts salivary and renal excretion of insect pests. Insect Biochem. Mol. Biol. 99:17–26Showed that flonicamid inhibits Kir1, disrupts feeding, and reduces renal excretion in N. lugens.
     [Google Scholar]
  67. 67. 
    Rouhier MF, Hine RM, Park ST, Raphemot R, Denton JS et al. 2014. The excretion of NaCl and KCl loads in mosquitoes: 2. Effects of the small molecule Kir channel modulator VU573 and its inactive analog VU342. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307:R850–61
     [Google Scholar]
  68. 68. 
    Rouhier MF, Piermarini PM. 2014. Identification of life-stage and tissue-specific splice variants of an inward rectifying potassium (Kir) channel in the yellow fever mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 48:91–99
     [Google Scholar]
  69. 69. 
    Rouhier MF, Raphemot R, Denton JS, Piermarini PM. 2014. Pharmacological validation of an inward-rectifier potassium (Kir) channel as an insecticide target in the yellow fever mosquito Aedes aegypti. PLOS ONE 9:e100700
     [Google Scholar]
  70. 70. 
    Rusconi Trigueros R, Hopkins CR, Denton JS, Piermarini PM. 2018. Pharmacological inhibition of inward rectifier potassium channels induces lethality in larval Aedes aegypti. Insects 9:163
     [Google Scholar]
  71. 71. 
    Scott BN, Yu MJ, Lee LW, Beyenbach KW 2004. Mechanisms of K+ transport across basolateral membranes of principal cells in Malpighian tubules of the yellow fever mosquito, Aedes aegypti. J. Exp. Biol. 207:1655–63
     [Google Scholar]
  72. 72. 
    Swale DR, Engers DW, Bollinger SR, Gross A, Inocente EA et al. 2016. An insecticide resistance-breaking mosquitocide targeting inward rectifier potassium channels in vectors of Zika virus and malaria. Sci. Rep. 6:36954Showed that Kir1 inhibitors circumvent multiple insecticide resistance mechanisms in mosquitoes.
     [Google Scholar]
  73. 73. 
    Swale DR, Li Z, Guerrero F, Perez De Leon AA, Foil LD. 2017. Role of inward rectifier potassium channels in salivary gland function and sugar feeding of the fruit fly, Drosophila melanogaster. Pestic. Biochem. Physiol. 141:41–49
     [Google Scholar]
  74. 74. 
    Swale DR, Li Z, Kraft JZ, Healy K, Liu M et al. 2018. Development of an autodissemination strategy for the deployment of novel control agents targeting the common malaria mosquito, Anopheles quadrimaculatus say (Diptera: Culicidae). PLOS Negl. Trop. Dis. 12:e0006259
     [Google Scholar]
  75. 75. 
    Taylor-Wells J, Gross AD, Jiang S, Demares F, Clements JS et al. 2018. Toxicity, mode of action, and synergist potential of flonicamid against mosquitoes. Pestic. Biochem. Physiol. 151:3–9
     [Google Scholar]
  76. 76. 
    Tompkins-Macdonald GJ, Gallin WJ, Sakarya O, Degnan B, Leys SP, Boland LM. 2009. Expression of a poriferan potassium channel: insights into the evolution of ion channels in metazoans. J. Exp. Biol. 212:761–67
     [Google Scholar]
  77. 77. 
    Tosti E, Boni R. 2004. Electrical events during gamete maturation and fertilization in animals and humans. Hum. Reprod. Update 10:53–65
     [Google Scholar]
  78. 78. 
    Wiehart UI, Klein G, Steels P, Nicolson SW, Van Kerkhove E. 2003. K+ transport in Malpighian tubules of Tenebrio molitor L: Is a KATP channel involved?. J. Exp. Biol. 206:959–65
     [Google Scholar]
  79. 79. 
    Wiehart UI, Nicolson SW, Van Kerkhove E. 2003. K+ transport in Malpighian tubules of Tenebrio molitor L: a study of electrochemical gradients and basal K+ uptake mechanisms. J. Exp. Biol. 206:949–57
     [Google Scholar]
  80. 80. 
    Wu Y, Baum M, Huang C-L, Rodan AR. 2015. Two inwardly rectifying potassium channels, Irk1 and Irk2, play redundant roles in Drosophila renal tubule function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 309:R747–56Showed that Kir1 and Kir2 play redundant roles in renal fluid and K+ secretion in D. melanogaster.
     [Google Scholar]
  81. 81. 
    Yang Z, Statler B-M, Calkins TL, Alfaro E, Esquivel CJ et al. 2017. Dynamic expression of genes encoding subunits of inward rectifier potassium (Kir) channels in the yellow fever mosquito Aedes aegypti. Comp. Biochem. Physiol. B 204:35–44
     [Google Scholar]
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The Molecular Physiology and Toxicology of Inward Rectifier Potassium Channels in Insects
Annual Review of Entomology 67, 125 (2022); https://doi.org/10.1146/annurev-ento-062121-063338
/content/journals/10.1146/annurev-ento-062121-063338
/content/journals/10.1146/annurev-ento-062121-063338
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