The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.
A potassium channel β-subunit couples mitochondrial electron transport to sleep
Open accessAbstract
The essential but enigmatic functions of sleep1,2 must be reflected in molecular changes sensed by the brain’s sleep-control systems. In the fruitfly Drosophila, about two dozen sleep-inducing neurons3 with projections to the dorsal fan-shaped body (dFB) adjust their electrical output to sleep need4, via the antagonistic regulation of two potassium conductances: the leak channel Sandman imposes silence during waking, whereas increased A-type currents through Shaker support tonic firing during sleep5. Here we show that oxidative byproducts of mitochondrial electron transport6,7 regulate the activity of dFB neurons through a nicotinamide adenine dinucleotide phosphate (NADPH) cofactor bound to the oxidoreductase domain8,9 of Shaker’s KVβ subunit, Hyperkinetic10,11. Sleep loss elevates mitochondrial reactive oxygen species in dFB neurons, which register this rise by converting Hyperkinetic to the NADP+-bound form. The oxidation of the cofactor slows the inactivation of the A-type current and boosts the frequency of action potentials, thereby promoting sleep. Energy metabolism, oxidative stress, and sleep—three processes implicated independently in lifespan, ageing, and degenerative disease6,12–14—are thus mechanistically connected. KVβ substrates8,15,16 or inhibitors that alter the ratio of bound NADPH to NADP+ (and hence the record of sleep debt or waking time) represent prototypes of potential sleep-regulatory drugs. Sleep deprivation in Drosophila elevates reactive oxygen species in sleep-promoting neurons, leading to changes in potassium currents and spiking activity and thereby connecting energy metabolism, oxidative stress, and sleep.
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Citations
Cites
How mitochondria produce reactive oxygen species
Murphy, M. P. (2009) · Biochemical Journal · doi:10.1042/bj20081386 · Cited by 8,207
A GAL4-Driver Line Resource for Drosophila Neurobiology
Jenett, A., Rubin, G. M., Ngo, T.-T. B., Shepherd, D., Murphy, C., Dionne, H., Pfeiffer, B. D., Cavallaro, A., Hall, D., Jeter, J., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.011 · Cited by 1,449
Structure of a voltage-dependent K+ channel β subunit
Gulbis, J. M., Mann, S., & MacKinnon, R. (1999) · Cell · doi:10.1016/s0092-8674(00)80805-3 · Cited by 283
RNAi-mediated suppression of the mitochondrial iron chaperone, frataxin, in Drosophila
Anderson, P. R., Kirby, K., Hilliker, A. J., & Phillips, J. P. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi367 · Cited by 144
Cited by
Reactive oxygen species (ROS) as pleiotropic physiological signalling agents
Sies, H., & Jones, D. P. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0230-3 · Cited by 5,335
Sleep Loss Can Cause Death through Accumulation of Reactive Oxygen Species in the Gut
Vaccaro, A., Kaplan Dor, Y., Nambara, K., Pollina, E. A., Lin, C., Greenberg, M. E., & Rogulja, D. (2020) · Cell · doi:10.1016/j.cell.2020.04.049 · Cited by 541
Hulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D., Takemura, S.-Y., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al. (2021) · eLife · doi:10.7554/elife.66039 · Cited by 392
Building an allocentric travelling direction signal via vector computation
Lyu, C., Abbott, L. F., & Maimon, G. (2022) · Nature · doi:10.1038/s41586-021-04067-0 · Cited by 215
Cao, J., Herman, A. B., West, G. B., Poe, G., & Savage, V. M. (2020) · Science Advances · doi:10.1126/sciadv.aba0398 · Cited by 105
The MARCHF6 E3 ubiquitin ligase acts as an NADPH sensor for the regulation of ferroptosis
Nguyen, K. T., Mun, S.-H., Yang, J., Lee, J., Seok, O.-H., Kim, E., Kim, D., An, S. Y., Seo, D.-Y., Suh, J.-Y., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00973-1 · Cited by 92
Sleep, circadian rhythms, and type 2 diabetes mellitus
Parameswaran, G., & Ray, D. W. (2022) · Clinical Endocrinology · doi:10.1111/cen.14607 · Cited by 85
The inescapable drive to sleep: Overlapping mechanisms of sleep and sedation
Franks, N. P., & Wisden, W. (2021) · Science · doi:10.1126/science.abi8372 · Cited by 74
Mitochondrial origins of the pressure to sleep
Sarnataro, R., Velasco, C. D., Monaco, N., Kempf, A., & Miesenböck, G. (2025) · Nature · doi:10.1038/s41586-025-09261-y · Cited by 62
Self-citationHulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D. B., Takemura, S., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al. (2020) · doi:10.1101/2020.12.08.413955 · Cited by 392
“, 2006), and several metabolic processes (Kempf et al., 2019; Vaccaro et al., 2020).”
BackgroundRe-examining the role of the dorsal fan-shaped body in promoting sleep in Drosophila
De, J., Wu, M., Lambatan, V., Hua, Y., & Joiner, W. J. (2023) · Current Biology · doi:10.1016/j.cub.2023.07.043 · Cited by 42
Hamid, A., Gattuso, H., Caglar, A. N., Pillai, M., Steele, T., Gonzalez, A., Nagel, K., & Syed, M. H. (2024) · Current Biology · doi:10.1016/j.cub.2023.12.020 · Cited by 24
The zebrafish mutant dreammist implicates sodium homeostasis in sleep regulation
(2020) · doi:10.1101/2020.11.18.388736 · Cited by 4
The zebrafish mutant dreammist implicates sodium homeostasis in sleep regulation
Barlow, I. L., Mackay, E., Wheater, E., Goel, A., Lim, S., Zimmerman, S., Woods, I., Prober, D. A., & Rihel, J. (2023) · doi:10.7554/elife.87521.2
Metadata
- Authors
- Kempf, A., Song, S. M., Talbot, C. B., & Miesenböck, G.
- Venue
- Nature
- Published
- 2019-03-20
- Volume
- 568
- Issue
- 7751
- Pages
- 230-234
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2925034948
- Cited by
- 189
- References
- 4
- FWCI
- 9.87
- Type
- journal article
- Language
- en
- Open access
- green
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