title: EAG channels expressed in microvillar photoreceptors are unsuited to diurnal vision.
abstract: The principles underlying the evolutionary selection of ion channels for expression in sensory neurons are unclear. Photoreceptor depolarization in the diurnal Drosophila melanogaster is predominantly provided by light-activated transient receptor potential (TRP) channels, whereas repolarization is mediated by sustained voltage-gated K+channels of the Shab family. In the present study, we show that phototransduction in the nocturnal cockroach Periplaneta americana is predominantly mediated by TRP-like channels, whereas membrane repolarization is based on EAG channels. Although bright light stimulates Shab channels in Drosophila, further restricting depolarization and improving membrane bandwidth, it strongly suppresses EAG conductance in Periplaneta. This light-dependent inhibition (LDI) is caused by calcium and is abolished by chelating intracellular calcium or suppressing eag gene expression. LDI increases membrane resistance, augments gain and reduces the signalling bandwidth. This makes EAG unsuitable for light response conditioning during the day and might have resulted in the evolutionary replacement of EAG by other delayed rectifiers in diurnal insects.
  
  
  
  The principles underlying evolutionary selection of ion channels for expression in sensory neurons are unclear. Among species possessing microvillar photoreceptors, the major ionic conductances have only been identified in Drosophila melanogaster. In Drosophila, depolarization is provided by light-activated transient receptor potential (TRP) channels with a minor contribution from TRP-like (TRPL) channels, whereas repolarization is mediated by sustained voltage-gated K+(Kv) channels of the Shab family. Bright light stimulates Shab channels, further restricting depolarization and improving membrane bandwidth. In the present study, data obtained using a combination of electrophysiological, pharmacological and molecular knockdown techniques strongly suggest that in photoreceptors of the nocturnal cockroach Periplaneta americana the major excitatory channel is TRPL, whereas the predominant delayed rectifier is EAG, a ubiquitous but enigmatic Kv channel. By contrast to the diurnal Drosophila, bright light strongly suppresses EAG conductance in Periplaneta. This light-dependent inhibition (LDI) is caused by calcium entering the cytosol and is amplified following inhibition of calcium extrusion, and it can also be abolished by chelating intracellular calcium or suppressing eag gene expression by RNA interference. LDI increases membrane resistance, augments gain and reduces the signalling bandwidth, impairing information transfer. LDI is also observed in the nocturnal cricket Gryllus integer, whereas, in the diurnal water strider Gerris lacustris, the delayed rectifier is up-regulated by light. Although LDI is not expected to reduce delayed rectifier current in the normal illumination environment of nocturnal cockroaches and crickets, it makes EAG unsuitable for light response conditioning during the day, and might have resulted in the evolutionary replacement of EAG by other delayed rectifiers in diurnal insects.
authors.affiliation: Biophysics group, Nano and Molecular Systems Research Unit, University of Oulu, Oulu, Finland.
authors.forename: Esa-Ville
authors.identifier: 0000-0002-5576-0627
authors.initials: EV
authors.lastname: Immonen
authors.affiliation: Department of Physiology and Biophysics, Dalhousie University, Halifax, NS, Canada.
authors.forename: Andrew S
authors.identifier: 0000-0001-8190-4084
authors.initials: AS
authors.lastname: French
authors.affiliation: Department of Physiology and Biophysics, Dalhousie University, Halifax, NS, Canada.
authors.forename: Päivi H
authors.identifier: 0000-0002-8205-7339
authors.initials: PH
authors.lastname: Torkkeli
authors.affiliation: Department of Physiology and Biophysics, Dalhousie University, Halifax, NS, Canada.
authors.forename: Hongxia
authors.initials: H
authors.lastname: Liu
authors.affiliation: Biophysics group, Nano and Molecular Systems Research Unit, University of Oulu, Oulu, Finland.
authors.forename: Mikko
authors.initials: M
authors.lastname: Vähäsöyrinki
authors.affiliation: Biophysics group, Nano and Molecular Systems Research Unit, University of Oulu, Oulu, Finland.
authors.forename: Roman V
authors.identifier: 0000-0002-7431-5297
authors.initials: RV
authors.lastname: Frolov
mesh_terms: D000818:Animals; D002940:Circadian Rhythm; D051638:Ether-A-Go-Go Potassium Channels / Q000235:genetics / Q000502:physiology*; D006135:Gryllidae / Q000502:physiology; D020062:Heteroptera / Q000502:physiology; D051656:KCNQ Potassium Channels / Q000235:genetics / Q000502:physiology; D008027:Light; D008297:Male; D008871:Microvilli; D010526:Periplaneta / Q000502:physiology; D017956:Photoreceptor Cells, Invertebrate / Q000502:physiology* / Q000648:ultrastructure; D034622:RNA Interference; D012333:RNA, Messenger / Q000378:metabolism; D050051:Transient Receptor Potential Channels / Q000235:genetics / Q000502:physiology; D014785:Vision, Ocular / Q000502:physiology*
chemical_list: D051638:Ether-A-Go-Go Potassium Channels; D051656:KCNQ Potassium Channels; D012333:RNA, Messenger; D050051:Transient Receptor Potential Channels
keywords: EAG channel; Periplaneta americana; TRP channels; TRPL channel; photoreceptor