Impairing one sensory modality enhances another by reconfiguring peptidergic signalling in Caenorhabditis elegans

Valperga G, de Bono M. 2022. Impairing one sensory modality enhances another by reconfiguring peptidergic signalling in Caenorhabditis elegans. eLife. 11, e68040.

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Abstract
Animals that lose one sensory modality often show augmented responses to other sensory inputs. The mechanisms underpinning this cross-modal plasticity are poorly understood. We probe such mechanisms by performing a forward genetic screen for mutants with enhanced O2 perception in Caenorhabditis elegans. Multiple mutants exhibiting increased O2 responsiveness concomitantly show defects in other sensory responses. One mutant, qui-1, defective in a conserved NACHT/WD40 protein, abolishes pheromone-evoked Ca2+ responses in the ADL pheromone-sensing neurons. At the same time, ADL responsiveness to pre-synaptic input from O2-sensing neurons is heightened in qui-1, and other sensory defective mutants, resulting in enhanced neurosecretion although not increased Ca2+ responses. Expressing qui-1 selectively in ADL rescues both the qui-1 ADL neurosecretory phenotype and enhanced escape from 21% O2. Profiling ADL neurons in qui-1 mutants highlights extensive changes in gene expression, notably of many neuropeptide receptors. We show that elevated ADL expression of the conserved neuropeptide receptor NPR-22 is necessary for enhanced ADL neurosecretion in qui-1 mutants, and is sufficient to confer increased ADL neurosecretion in control animals. Sensory loss can thus confer cross-modal plasticity by changing the peptidergic connectome.
Publishing Year
Date Published
2022-02-24
Journal Title
eLife
Publisher
eLife Sciences Publications
Acknowledgement
We would like to thank Gemma Chandratillake and Merav Cohen for identifying mutants and José David Moñino Sánchez for his help on neurosecretion assays. We are grateful to Kaveh Ashrafi (UCSF), Piali Sengupta (Brandeis), and the Caenorhabditis Genetic Center (funded by National Institutes of Health Infrastructure Program P40 OD010440) for strains and reagents ... and Rebecca Butcher (Univ. Florida) for C9 pheromone. We thank Tim Stevens, Paula Freire-Pritchett, Alastair Crisp, GurpreetGhattaoraya, and Fabian Amman for help with bioinformatic analysis, Ekaterina Lashmanova for help with injections, Iris Hardege for strains, and Isabel Beets (KU Leuven) and members of the de Bono Lab for comments on the manuscript. We thank the CRUK Cambridge Research Institute Genomics Core for next generation sequencing and the Flow Cytometry Facility at LMB for FACS. This research was supported by the Scientific Service Units (SSU) of IST Austria through resources provided by the Bioimaging Facility (BIF), the Life Science Facility (LSF) and Scientific Computing (SciCo-p– Bioinformatics). This work was supported by the Medical Research Council UK (Studentship to GV), an Advanced ERC grant (269,058 ACMO to MdB), and a Wellcome Investigator Award (209504/Z/17/Z to MdB).
Volume
11
Article Number
e68040
eISSN
IST-REx-ID

Cite this

Valperga G, de Bono M. Impairing one sensory modality enhances another by reconfiguring peptidergic signalling in Caenorhabditis elegans. eLife. 2022;11. doi:10.7554/eLife.68040
Valperga, G., & de Bono, M. (2022). Impairing one sensory modality enhances another by reconfiguring peptidergic signalling in Caenorhabditis elegans. ELife. eLife Sciences Publications. https://doi.org/10.7554/eLife.68040
Valperga, Giulio, and Mario de Bono. “Impairing One Sensory Modality Enhances Another by Reconfiguring Peptidergic Signalling in Caenorhabditis Elegans.” ELife. eLife Sciences Publications, 2022. https://doi.org/10.7554/eLife.68040.
G. Valperga and M. de Bono, “Impairing one sensory modality enhances another by reconfiguring peptidergic signalling in Caenorhabditis elegans,” eLife, vol. 11. eLife Sciences Publications, 2022.
Valperga G, de Bono M. 2022. Impairing one sensory modality enhances another by reconfiguring peptidergic signalling in Caenorhabditis elegans. eLife. 11, e68040.
Valperga, Giulio, and Mario de Bono. “Impairing One Sensory Modality Enhances Another by Reconfiguring Peptidergic Signalling in Caenorhabditis Elegans.” ELife, vol. 11, e68040, eLife Sciences Publications, 2022, doi:10.7554/eLife.68040.
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PMID: 35201977
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