Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair
Abstract Neuronal communication involves small-molecule transmitters, gap junctions, and neuropeptides. While neurons often express multiple neuropeptides, our understanding of the coordination of their actions and their mutual interactions remains limited. Here, we demonstrate that two neuropeptide...
Saved in:
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2024-11-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-53899-7 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850179521683128320 |
|---|---|
| author | Ichiro Aoki Luca Golinelli Eva Dunkel Shripriya Bhat Erschad Bassam Isabel Beets Alexander Gottschalk |
| author_facet | Ichiro Aoki Luca Golinelli Eva Dunkel Shripriya Bhat Erschad Bassam Isabel Beets Alexander Gottschalk |
| author_sort | Ichiro Aoki |
| collection | DOAJ |
| description | Abstract Neuronal communication involves small-molecule transmitters, gap junctions, and neuropeptides. While neurons often express multiple neuropeptides, our understanding of the coordination of their actions and their mutual interactions remains limited. Here, we demonstrate that two neuropeptides, NLP-10 and FLP-1, released from the same interneuron pair, AVKL/R, exert antagonistic effects on locomotion speed in Caenorhabditis elegans. NLP-10 accelerates locomotion by activating the G protein-coupled receptor NPR-35 on premotor interneurons that promote forward movement. Notably, we establish that NLP-10 is crucial for the aversive response to mechanical and noxious light stimuli. Conversely, AVK-derived FLP-1 slows down locomotion by suppressing the secretion of NLP-10 from AVK, through autocrine feedback via activation of its receptor DMSR-7 in AVK neurons. Our findings suggest that peptidergic autocrine motifs, exemplified by the interaction between NLP-10 and FLP-1, might represent a widespread mechanism in nervous systems across species. These mutual functional interactions among peptidergic co-transmitters could fine-tune brain activity. |
| format | Article |
| id | doaj-art-0ab9ffd10df04fba8cfb9c077a8e77ec |
| institution | OA Journals |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-0ab9ffd10df04fba8cfb9c077a8e77ec2025-08-20T02:18:28ZengNature PortfolioNature Communications2041-17232024-11-0115111910.1038/s41467-024-53899-7Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pairIchiro Aoki0Luca Golinelli1Eva Dunkel2Shripriya Bhat3Erschad Bassam4Isabel Beets5Alexander Gottschalk6Buchmann Institute for Molecular Life Sciences, Goethe UniversityDepartment of Biology, KU LeuvenBuchmann Institute for Molecular Life Sciences, Goethe UniversityBuchmann Institute for Molecular Life Sciences, Goethe UniversityBuchmann Institute for Molecular Life Sciences, Goethe UniversityDepartment of Biology, KU LeuvenBuchmann Institute for Molecular Life Sciences, Goethe UniversityAbstract Neuronal communication involves small-molecule transmitters, gap junctions, and neuropeptides. While neurons often express multiple neuropeptides, our understanding of the coordination of their actions and their mutual interactions remains limited. Here, we demonstrate that two neuropeptides, NLP-10 and FLP-1, released from the same interneuron pair, AVKL/R, exert antagonistic effects on locomotion speed in Caenorhabditis elegans. NLP-10 accelerates locomotion by activating the G protein-coupled receptor NPR-35 on premotor interneurons that promote forward movement. Notably, we establish that NLP-10 is crucial for the aversive response to mechanical and noxious light stimuli. Conversely, AVK-derived FLP-1 slows down locomotion by suppressing the secretion of NLP-10 from AVK, through autocrine feedback via activation of its receptor DMSR-7 in AVK neurons. Our findings suggest that peptidergic autocrine motifs, exemplified by the interaction between NLP-10 and FLP-1, might represent a widespread mechanism in nervous systems across species. These mutual functional interactions among peptidergic co-transmitters could fine-tune brain activity.https://doi.org/10.1038/s41467-024-53899-7 |
| spellingShingle | Ichiro Aoki Luca Golinelli Eva Dunkel Shripriya Bhat Erschad Bassam Isabel Beets Alexander Gottschalk Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair Nature Communications |
| title | Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair |
| title_full | Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair |
| title_fullStr | Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair |
| title_full_unstemmed | Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair |
| title_short | Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair |
| title_sort | hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair |
| url | https://doi.org/10.1038/s41467-024-53899-7 |
| work_keys_str_mv | AT ichiroaoki hierarchicalregulationoffunctionallyantagonisticneuropeptidesexpressedinasingleneuronpair AT lucagolinelli hierarchicalregulationoffunctionallyantagonisticneuropeptidesexpressedinasingleneuronpair AT evadunkel hierarchicalregulationoffunctionallyantagonisticneuropeptidesexpressedinasingleneuronpair AT shripriyabhat hierarchicalregulationoffunctionallyantagonisticneuropeptidesexpressedinasingleneuronpair AT erschadbassam hierarchicalregulationoffunctionallyantagonisticneuropeptidesexpressedinasingleneuronpair AT isabelbeets hierarchicalregulationoffunctionallyantagonisticneuropeptidesexpressedinasingleneuronpair AT alexandergottschalk hierarchicalregulationoffunctionallyantagonisticneuropeptidesexpressedinasingleneuronpair |