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Journal article

Sleep pressure accumulates in a voltage-gated lipid peroxidation memory

Abstract:

Voltage-gated potassium (KV) channels contain cytoplasmically exposed β-subunits1,2,3,4,5 whose aldo-keto reductase activity6,7,8 is required for the homeostatic regulation of sleep9. Here we show that Hyperkinetic, the β-subunit of the KV1 channel Shaker in Drosophila7, forms a dynamic lipid peroxidation memory. Information is stored in the oxidation state of Hyperkinetic’s nicotinamide adenine dinucleotide phosphate (NADPH) cofactor, which changes when lipid-derived carbonyls10,11,12,13, such as 4-oxo-2-nonenal or an endogenous analogue generated by illuminating a membrane-bound photosensitizer9,14, abstract an electron pair. NADP+ remains locked in the active site of KVβ until membrane depolarization permits its release and replacement with NADPH. Sleep-inducing neurons15,16,17 use this voltage-gated oxidoreductase cycle to encode their recent lipid peroxidation history in the collective binary states of their KVβ subunits; this biochemical memory influences—and is erased by—spike discharges driving sleep. The presence of a lipid peroxidation sensor at the core of homeostatic sleep control16,17 suggests that sleep protects neuronal membranes against oxidative damage. Indeed, brain phospholipids are depleted of vulnerable polyunsaturated fatty acyl chains after enforced waking, and slowing the removal of their carbonylic breakdown products increases the demand for sleep.

Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1038/s41586-025-08734-4

Authors

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Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Role:
Author
ORCID:
0000-0002-8263-2460
More by this author
Role:
Author
ORCID:
0000-0002-9960-5020
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Role:
Author
ORCID:
0000-0001-9663-8233
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Role:
Author
ORCID:
0009-0009-5933-3081
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Role:
Author


More from this funder
Funder identifier:
https://ror.org/029chgv08
Grant:
084655/Z/08/Z
More from this funder
Funder identifier:
https://ror.org/03x94j517
Grant:
MR/V013238/1
More from this funder
Funder identifier:
https://ror.org/0472cxd90
Grant:
832467


Publisher:
Springer Nature
Journal:
Nature More from this journal
Volume:
641
Issue:
8061
Pages:
232-239
Publication date:
2025-03-19
Acceptance date:
2025-02-03
DOI:
EISSN:
1476-4687
ISSN:
0028-0836
Pmid:
40108451


Language:
English
Keywords:
Pubs id:
2098109
Local pid:
pubs:2098109
Deposit date:
2025-03-25
ARK identifier:

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