University of Oulu

Immonen, E. , French, A. S., Torkkeli, P. H., Liu, H. , Vähäsöyrinki, M. and Frolov, R. V. (2017), EAG channels expressed in microvillar photoreceptors are unsuited to diurnal vision. J Physiol, 595: 5465-5479. doi:10.1113/JP273612

EAG channels expressed in microvillar photoreceptors are unsuited to diurnal vision

Saved in:
Author: Immonen, Esa‐Ville1; French, Andrew S.2; Torkkeli, Päivi H.2;
Organizations: 1Biophysics Group, Nano and Molecular Systems Research Unit, University of Oulu, Oulu FI ‑ 90014, Finland
2Department of Physiology and Biophysics, Dalhousie University, Halifax, NS, Canada
Format: article
Version: accepted version
Access: open
Online Access: PDF Full Text (PDF, 1.3 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe201804056344
Language: English
Published: John Wiley & Sons, 2017
Publish Date: 2018-02-22
Description:

Abstract

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.

see all

Series: Journal of physiology
ISSN: 0022-3751
ISSN-E: 1469-7793
ISSN-L: 0022-3751
Volume: 595
Issue: 16
Pages: 5465 - 5479
DOI: 10.1113/JP273612
OADOI: https://oadoi.org/10.1113/JP273612
Type of Publication: A1 Journal article – refereed
Field of Science: 3112 Neurosciences
1182 Biochemistry, cell and molecular biology
Subjects:
Funding: This research was supported by Academy of Finland grant #139893 to RF and by Natural Sciences and Engineering Research Council of Canada grants (NSERC) RGPIN/5565 to PHT and RGPIN 03712 to ASF.
Academy of Finland Grant Number: 139893
Detailed Information: 139893 (Academy of Finland Funding decision)
Dataset Reference: The datasets obtained and/or analysed during the present study are available from the corresponding author on reasonable request.
Copyright information: © 2017 The Authors. The Journal of Physiology © 2017 The Physiological Society.