Hydrogen Peroxide and Phosphoinositide Metabolites Synergistically Regulate a Cation Current to Influence Neuroendocrine Cell Bursting
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Authors
Chauhan-Puri, Alamjeet K.
Lee, Kelly H.
Magoski, Neil
Date
2021-10-22
Type
journal article
Language
en
Keyword
Aplysia , Peptidergic neuron , Diacylglycerol , H2O2 , Inositol trisphosphate , Mollusc , Reproduction
Alternative Title
Abstract
In various neurons, including neuroendocrine cells, non-selective cation channels elicit plateau potentials and persistent firing. Reproduction in the marine snail, Aplysia californica, is initiated when the neuroendocrine bag cell neurons undergo an afterdischarge, i.e., a prolonged period of enhanced excitability and spiking during which egg-laying hormone is released into the blood. The afterdischarge is associated with both the production of hydrogen peroxide (H2O2) and activation of phospholipase C (PLC), which hydrolyzes phosphatidylinositol-4,5-bisphosphate into diacylglycerol (DAG) and inositol trisphosphate (IP3). We previously demonstrated that H2O2 gates a voltage-dependent cation current and evokes spiking in bag cell neurons. The present study tests if DAG and IP3 impact the H2O2-induced current and excitability. In whole-cell voltage-clamped cultured bag cell neurons, bath-application of 1-oleoyl-2-acetyl-sn-glycerol (OAG), a DAG analogue, enhanced the H2O2-induced current, which was amplified by the inclusion of IP3 in the pipette. A similar outcome was produced by the PLC activator, N-(3-trifluoromethylphenyl)-2,4,6-trimethylbenzenesulfonamide. In current-clamp, OAG or OAG plus IP3, elevated the frequency of H2O2-induced bursting. PKC is also triggered during the afterdischarge; when PKC was stimulated with phorbol 12-myristate 13-acetate, it caused a voltage-dependent inward current with a reversal potential similar to the H2O2-induced current. Furthermore, PKC activation followed by H2O2 reduced the onset latency and increased the duration of action potential firing. Finally, inhibiting nicotinamide adenine dinucleotide phosphate oxidase with 3-benzyl-7-(2-benzoxazolyl)thio-1,2,3-triazolo[4,5-d]pyrimidine diminished evoked bursting in isolated bag cell neuron clusters. These results suggest that reactive oxygen species and phosphoinostide metabolites may synergize, and contribute to reproductive behaviour by promoting neuroendocrine cell firing.
Description
This is the peer reviewed version of the following article: Chauhan-Puri, A.K., Lee, K.H. and Magoski, N.S. (2021), Hydrogen peroxide and phosphoinositide metabolites synergistically regulate a cation current to influence neuroendocrine cell bursting. J Physiol. Accepted Author Manuscript. https://doi.org/10.1113/JP282302, which has been published in final form at https://doi.org/10.1113/JP282302. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions.
Citation
Chauhan-Puri, A.K., Lee, K.H. and Magoski, N.S. (2021), Hydrogen peroxide and phosphoinositide metabolites synergistically regulate a cation current to influence neuroendocrine cell bursting. J Physiol. Accepted Author Manuscript. https://doi.org/10.1113/JP282302
Publisher
Wiley