Cyclic nucleotide-dependent ionic currents in olfactory receptor neurons of the hawkmoth Manduca sexta suggest pull-push sensitivity modulation

Dolzer, Jan and Schroeder, Katrin and Stengl, Monika (2021) Cyclic nucleotide-dependent ionic currents in olfactory receptor neurons of the hawkmoth Manduca sexta suggest pull-push sensitivity modulation. EUROPEAN JOURNAL OF NEUROSCIENCE, 54 (3). pp. 4804-4826. ISSN 0953-816X, 1460-9568

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Abstract

Olfactory receptor neurons (ORNs) of the hawkmoth Manduca sexta sensitize via cAMP- and adapt via cGMP-dependent mechanisms. Perforated patch clamp recordings distinguished 11 currents in these ORNs. Derivatives of cAMP and/or cGMP antagonistically affected three of five K+ currents and two non-specific cation currents. The Ca2+-dependent K+ current I-K(Ca())2+ and the sensitive pheromone-dependent K+ current IK(cGMP-), which both express fast kinetics, were inhibited by 8bcGMP, while a slow K+ current, IK(cGMP+), was activated by 8bcGMP. Furthermore, application of 8bcAMP blocked slowly activating, zero mV-reversing, non-specific cation currents, I-LL and I-cat(PKC?), which remained activated in the presence of 8bcGMP. Their activations pull the membrane potential towards their 0-mV reversal potentials, in addition to increasing intracellular Ca2+ levels voltage- and I-LL-dependently. Twenty minutes after application, 8bcGMP blocked a TEA-independent K+ current, I-K(noTEA), and a fast cation current, I-cat(nRP), which both shift the membrane potential to negative values. We conclude that conditions of sensitization are maintained at high levels of cAMP, via specific opening/closure of ion channels that allow for fast kinetics, hyperpolarized membrane potentials, and low intracellular Ca2+ levels. In contrast, adaptation is supported via cGMP, which antagonizes cAMP, opening Ca2+-permeable channels with slow kinetics that stabilize depolarized resting potentials. The antagonistic modulation of peripheral sensory neurons by cAMP or cGMP is reminiscent of pull-push mechanisms of neuromodulation at central synapses underlying metaplasticity.

Item Type: Article
Uncontrolled Keywords: PROTEIN-KINASE-C; FUNCTIONAL EXPRESSION; POTASSIUM CHANNELS; ANTENNAL SENSILLA; TRICHOID SENSILLA; INSECT OLFACTION; K+ CHANNEL; PHEROMONE; DROSOPHILA; CALCIUM; cAMP; cGMP; insects; metaplasticity; olfactory transduction
Subjects: 500 Science > 590 Zoological sciences
Divisions: Biology, Preclinical Medicine > Institut für Zoologie
Depositing User: Dr. Gernot Deinzer
Date Deposited: 13 Sep 2022 07:08
Last Modified: 13 Sep 2022 07:08
URI: https://pred.uni-regensburg.de/id/eprint/47234

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