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SLO BK Potassium Channels Couple Gap Junctions to Inhibition of Calcium Signaling in Olfactory Neuron Diversification.

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Title: SLO BK Potassium Channels Couple Gap Junctions to Inhibition of Calcium Signaling in Olfactory Neuron Diversification.
Author(s): Alqadah A; Hsieh YW; Schumacher JA; Wang X; Merrill SA; Millington G; Bayne B; Jorgensen EM; Chuang CF
Abstract: The C. elegans AWC olfactory neuron pair communicates to specify asymmetric subtypes AWCOFF and AWCON in a stochastic manner. Intercellular communication between AWC and other neurons in a transient NSY-5 gap junction network antagonizes voltage-activated calcium channels, UNC-2 (CaV2) and EGL-19 (CaV1), in the AWCON cell, but how calcium signaling is downregulated by NSY-5 is only partly understood. Here, we show that voltage- and calcium-activated SLO BK potassium channels mediate gap junction signaling to inhibit calcium pathways for asymmetric AWC differentiation. Activation of vertebrate SLO-1 channels causes transient membrane hyperpolarization, which makes it an important negative feedback system for calcium entry through voltage-activated calcium channels. Consistent with the physiological roles of SLO-1, our genetic results suggest that slo-1 BK channels act downstream of NSY-5 gap junctions to inhibit calcium channel-mediated signaling in the specification of AWCON. We also show for the first time that slo-2 BK channels are important for AWC asymmetry and act redundantly with slo-1 to inhibit calcium signaling. In addition, nsy-5-dependent asymmetric expression of slo-1 and slo-2 in the AWCON neuron is necessary and sufficient for AWC asymmetry. SLO-1 and SLO-2 localize close to UNC-2 and EGL-19 in AWC, suggesting a role of possible functional coupling between SLO BK channels and voltage-activated calcium channels in AWC asymmetry. Furthermore, slo-1 and slo-2 regulate the localization of synaptic markers, UNC-2 and RAB-3, in AWC neurons to control AWC asymmetry. We also identify the requirement of bkip-1, which encodes a previously identified auxiliary subunit of SLO-1, for slo-1 and slo-2 function in AWC asymmetry. Together, these results provide an unprecedented molecular link between gap junctions and calcium pathways for terminal differentiation of olfactory neurons.
Issue Date: 2016-01-15
Publisher: Public Library of Science
Citation Info: Alqadah, A., Hsieh, Y. W., Schumacher, J. A., Wang, X. H., Merrill, S. A., Millington, G., Bayne, B., Jorgensen, E. M. and Chuang, C. F. SLO BK Potassium Channels Couple Gap Junctions to Inhibition of Calcium Signaling in Olfactory Neuron Diversification. Plos Genetics. 2016. 12(1). DOI: 10.1371/journal.pgen.1005654.
Type: Article
Description: This is a copy of an article published in PLoS Genetics. © 2016 Public Library of Science Publications. © 2016 Alqadah et al.
URI: http://hdl.handle.net/10027/21005
ISSN: 1553-7390
Sponsor: AA is supported by a Choose Ohio First Scholarship (https://www.chooseohiofirst.org/), YWH by a National Institute of Health Organogenesis Training Grant (https://researchtraining.nih.gov/programs/training-grants), JAS by an American Cancer Society Postdoctoral Fellowship PF-11-028-01-CSM (http://www.cancer.org/research/applyforaresearchgrant/granttypes/postdoctoral-fellowships), SAM by a National Institute of Health National Research Service Award 5F31NS084826-03 (http://www.nidcd.nih.gov/funding/types/pages/training.aspx), EMJ by a National Institute of Health Grant NS034307 (http://www.nih.gov/), and CFC by a Whitehall Foundation Research Grant 2008-05-21 (http://www.whitehall.org/grants/), an Alfred P. Sloan Research Fellowship BR5060 (http://www.sloan.org/) and a National Institute of Health Grant R01GM098026 (http://www.nigms.nih.gov/Pages/default.aspx). EMJ is an Investigator of HHMI.
Date Available in INDIGO: 2016-08-02
 

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