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Convergent, functionally independent signaling by mu and delta opioid receptors in hippocampal parvalbumin interneurons

View ORCID ProfileXinyi Jenny He, View ORCID ProfileJanki Patel, View ORCID ProfileConnor E. Weiss, View ORCID ProfileXiang Ma, View ORCID ProfileBrenda L. Bloodgood, View ORCID ProfileMatthew R. Banghart
doi: https://doi.org/10.1101/2021.04.23.441199
Xinyi Jenny He
1Division of Biological Sciences, Neurobiology Section, University of California San Diego, La Jolla, CA 92093, USA
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Janki Patel
1Division of Biological Sciences, Neurobiology Section, University of California San Diego, La Jolla, CA 92093, USA
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Connor E. Weiss
1Division of Biological Sciences, Neurobiology Section, University of California San Diego, La Jolla, CA 92093, USA
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Xiang Ma
1Division of Biological Sciences, Neurobiology Section, University of California San Diego, La Jolla, CA 92093, USA
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Brenda L. Bloodgood
1Division of Biological Sciences, Neurobiology Section, University of California San Diego, La Jolla, CA 92093, USA
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Matthew R. Banghart
1Division of Biological Sciences, Neurobiology Section, University of California San Diego, La Jolla, CA 92093, USA
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  • For correspondence: mbanghart@ucsd.edu
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Abstract

Functional interactions between G protein-coupled receptors are poised to enhance neuronal sensitivity to neuromodulators and therapeutic drugs. Mu and Delta opioid receptors (MORs and DORs) can interact when overexpressed in the same cells, but whether co-expression of endogenous MORs and DORs in neurons leads to functional interactions is unclear. Here, we show that both MORs and DORs inhibit parvalbumin-expressing basket cells (PV-BCs) in hippocampal CA1 through partially occlusive signaling pathways that terminate on somato-dendritic potassium channels and presynaptic calcium channels. Using photoactivatable opioid neuropeptides, we find that DORs dominate the response to enkephalin in terms of both ligand-sensitivity and kinetics, which may be due to relatively low expression levels of MOR. Opioid-activated potassium channels do not show heterologous desensitization, indicating that MORs and DORs signal independently. In a direct test for heteromeric functional interactions, the DOR antagonist TIPP-Psi does not alter the kinetics or potency of either the potassium channel or synaptic responses to photorelease of the MOR agonist DAMGO. Thus, despite largely redundant and convergent signaling, MORs and DORs do not functionally interact in PV-BCs. These findings imply that crosstalk between MORs and DORs, either in the form of physical interactions or synergistic intracellular signaling, is not a preordained outcome of co-expression in neurons.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 24, 2021.
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Convergent, functionally independent signaling by mu and delta opioid receptors in hippocampal parvalbumin interneurons
Xinyi Jenny He, Janki Patel, Connor E. Weiss, Xiang Ma, Brenda L. Bloodgood, Matthew R. Banghart
bioRxiv 2021.04.23.441199; doi: https://doi.org/10.1101/2021.04.23.441199
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Convergent, functionally independent signaling by mu and delta opioid receptors in hippocampal parvalbumin interneurons
Xinyi Jenny He, Janki Patel, Connor E. Weiss, Xiang Ma, Brenda L. Bloodgood, Matthew R. Banghart
bioRxiv 2021.04.23.441199; doi: https://doi.org/10.1101/2021.04.23.441199

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