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Nitric oxide feedback to ciliary photoreceptor cells gates a UV avoidance circuit

Nitric oxide feedback to ciliary photoreceptor cells gates a UV avoidance circuit
Nitric oxide feedback to ciliary photoreceptor cells gates a UV avoidance circuit
Nitric oxide (NO) produced by nitric-oxide synthase (NOS) is a key regulator of animal physiology. Here we uncover a function for NO in the integration of UV exposure and the gating of a UV-avoidance circuit. We studied UV/violet avoidance mediated by brain ciliary photoreceptors (cPRCs) in larvae of the annelid Platynereis dumerilii. In the larva, NOS is expressed in interneurons (INNOS) postsynaptic to cPRCs. UV stimulation of cPRCs triggers INNOS activation and NO production. NO signals retrogradely to cPRCs to induce their sustained post-stimulus activation through an unconventional guanylate cyclase. This late activation inhibits serotonergic ciliomotor neurons to induce downward swimming. In NOS mutants, retrograde signalling, circuit output and UV avoidance are defective. By mathematical modelling, we recapitulate phototransduction and circuit dynamics in wild-type and mutant larvae. Our results reveal how NO-mediated retrograde signalling gates a synaptic circuit and induces short-term memory of UV exposure to orchestrate light-avoidance behaviour.
eLife Sciences Publications
Jokura, Kei
0485cc2c-385a-4402-bd1e-26b2a0549f33
Ueda, Nobuo
649ce8f6-4752-4f91-93bf-1d059649a1b9
Gühmann, Martin
141bce04-ff8b-409b-8f50-847fc3e37c1f
Yañez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Słowiński, Piotr
5c49ee0a-0052-4486-b0a7-6a5185debee2
Wedgwood, Kyle C.A.
7695339e-0d99-496f-bbfc-99e358d4a81c
Jékely, Gáspár
94f0485f-2d93-4df4-b287-1e5b01295578
Jokura, Kei
0485cc2c-385a-4402-bd1e-26b2a0549f33
Ueda, Nobuo
649ce8f6-4752-4f91-93bf-1d059649a1b9
Gühmann, Martin
141bce04-ff8b-409b-8f50-847fc3e37c1f
Yañez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Słowiński, Piotr
5c49ee0a-0052-4486-b0a7-6a5185debee2
Wedgwood, Kyle C.A.
7695339e-0d99-496f-bbfc-99e358d4a81c
Jékely, Gáspár
94f0485f-2d93-4df4-b287-1e5b01295578

Jokura, Kei, Ueda, Nobuo, Gühmann, Martin, Yañez-Guerra, Luis Alfonso, Słowiński, Piotr, Wedgwood, Kyle C.A. and Jékely, Gáspár (2023) Nitric oxide feedback to ciliary photoreceptor cells gates a UV avoidance circuit eLife Sciences Publications 52pp. (doi:10.7554/eLife.91258.1).

Record type: Monograph (Working Paper)

Abstract

Nitric oxide (NO) produced by nitric-oxide synthase (NOS) is a key regulator of animal physiology. Here we uncover a function for NO in the integration of UV exposure and the gating of a UV-avoidance circuit. We studied UV/violet avoidance mediated by brain ciliary photoreceptors (cPRCs) in larvae of the annelid Platynereis dumerilii. In the larva, NOS is expressed in interneurons (INNOS) postsynaptic to cPRCs. UV stimulation of cPRCs triggers INNOS activation and NO production. NO signals retrogradely to cPRCs to induce their sustained post-stimulus activation through an unconventional guanylate cyclase. This late activation inhibits serotonergic ciliomotor neurons to induce downward swimming. In NOS mutants, retrograde signalling, circuit output and UV avoidance are defective. By mathematical modelling, we recapitulate phototransduction and circuit dynamics in wild-type and mutant larvae. Our results reveal how NO-mediated retrograde signalling gates a synaptic circuit and induces short-term memory of UV exposure to orchestrate light-avoidance behaviour.

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e-pub ahead of print date: 19 September 2023

Identifiers

Local EPrints ID: 488169
URI: http://eprints.soton.ac.uk/id/eprint/488169
PURE UUID: 5a5089bc-d4fc-4e8a-96ee-5344c140e5cf
ORCID for Luis Alfonso Yañez-Guerra: ORCID iD orcid.org/0000-0002-2523-1310

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Date deposited: 17 Mar 2024 05:20
Last modified: 18 Mar 2024 04:15

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Contributors

Author: Kei Jokura
Author: Nobuo Ueda
Author: Martin Gühmann
Author: Luis Alfonso Yañez-Guerra ORCID iD
Author: Piotr Słowiński
Author: Kyle C.A. Wedgwood
Author: Gáspár Jékely

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