Sleep Loss Can Cause Death through Accumulation of Reactive Oxygen Species in the Gut

Vaccaro, Alexandra; Kaplan Dor, Yosef; Nambara, Keishi; Pollina, Elizabeth A.; Lin, Cindy; Greenberg, Michael E.; Rogulja, Dragana

doi:10.1016/j.cell.2020.04.049

Cited by 542Genetics, Aging, and Longevity in Model OrganismsCircadian rhythm and melatoninSleep and Wakefulness Research

Sleep Loss Can Cause Death through Accumulation of Reactive Oxygen Species in the Gut

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Vaccaro, Alexandra, Kaplan Dor, Yosef, Nambara, Keishi, Pollina, Elizabeth A., Lin, Cindy, Greenberg, Michael E., Rogulja, Dragana·2020·Cell

DOI 10.1016/j.cell.2020.04.049

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Abstract

The view that sleep is essential for survival is supported by the ubiquity of this behavior, the apparent existence of sleep-like states in the earliest animals, and the fact that severe sleep loss can be lethal. The cause of this lethality is unknown. Here we show, using flies and mice, that sleep deprivation leads to accumulation of reactive oxygen species (ROS) and consequent oxidative stress, specifically in the gut. ROS are not just correlates of sleep deprivation but drivers of death: their neutralization prevents oxidative stress and allows flies to have a normal lifespan with little to no sleep. The rescue can be achieved with oral antioxidant compounds or with gut-targeted transgenic expression of antioxidant enzymes. We conclude that death upon severe sleep restriction can be caused by oxidative stress, that the gut is central in this process, and that survival without sleep is possible when ROS accumulation is prevented. VIDEO ABSTRACT.

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Severe sleep loss causes accumulation of ROS in the gut (but not the brain) of both flies and mice, associated with death of flies.
“severe sleep loss causes accumulation of ROS in the gut (but not the brain) of both flies and mice, which was associated with death of the flies”
From Effects of Coffee and Its Components on the Gastrointestinal Tract and the Brain–Gut Axis (2020) · cites this paper as [225]
These effects could be prevented by oral administration of antioxidant compounds or through gut-targeted transgenic expression of antioxidant enzymes.
“all these effects could be prevented by oral administration of antioxidant compounds or through gut-targeted transgenic expression of antioxidant enzymes.”
From Effects of Coffee and Its Components on the Gastrointestinal Tract and the Brain–Gut Axis (2020) · cites this paper as [225]
The antioxidant components of coffee (like melatonin) may prevent accumulation of ROS in the gut and avoid deleterious effect of voluntary sleep restriction.
“the antioxidant components of coffee (like melatonin, one of the antioxidant compounds used in the mentioned study by Rogulja and collaborators, [225]) may prevent accumulation of ROS in the gut and avoid the deleterious effect of voluntary sleep restriction.”
From Effects of Coffee and Its Components on the Gastrointestinal Tract and the Brain–Gut Axis (2020) · cites this paper as [225]
Sleep deprivation causes death in mice and flies through accumulation of reactive oxygen species in the gut.
“sleep deprivation caused mice and flies death through the accumulation of reactive oxygen species (ROS) in the gut [20]”
From Healthy Human Fecal Microbiota Transplantation into Mice Attenuates MPTP-Induced Neurotoxicity via AMPK/SOD2 Pathway (2023) · cites this paper as [20]

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Wu, S.-C., Liao, C.-W., Pan, R., & Juang, J. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.03.004 · Cited by 111 · see citing works
Reactive Oxygen Species: Radical Factors in the Evolution of Animal Life
Taverne, Y. J. H. J., Merkus, D., Bogers, A. J. J. C., Halliwell, B. B., Duncker, D. J., & Lyons, T. W. (2018) · BioEssays · doi:10.1002/bies.201700158 · Cited by 110 · see citing works
No Organ Left Behind: Tales of Gut Development and Evolution
Stainier, D. Y. R. (2005) · Science · doi:10.1126/science.1108709 · Cited by 109 · see citing works
Identification of Redeye, a new sleep-regulating protein whose expression is modulated by sleep amount
Shi, M., Yue, Z., Kuryatov, A., Lindstrom, J. M., & Sehgal, A. (2014) · eLife · doi:10.7554/elife.01473 · Cited by 108 · see citing works
Evolution of oxygen utilization in multicellular organisms and implications for cell signalling in tissue engineering
Stamati, K., Mudera, V., & Cheema, U. (2011) · Journal of Tissue Engineering · doi:10.1177/2041731411432365 · Cited by 107 · see citing works
Detection and Characterization of Reactive Oxygen and Nitrogen Species in Biological Systems by Monitoring Species-Specific Products
Hardy, M., Zielonka, J., Karoui, H., Sikora, A., Michalski, R., Podsiadły, R., López, M., Vasquez-Vivar, J. M., Kalyanaraman, B., & Ouari, O. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7398 · Cited by 106 · see citing works
Tumor-promoting function of apoptotic caspases by an amplification loop involving ROS, macrophages and JNK in Drosophila
Pérez, E., Lindblad, J. L., & Bergmann, A. (2017) · eLife · doi:10.7554/elife.26747 · Cited by 101 · see citing works
Sleep, aging, and lifespan in Drosophila
Bushey, D., Hughes, K. A., Tononi, G., & Cirelli, C. (2010) · BMC Neuroscience · doi:10.1186/1471-2202-11-56 · Cited by 100 · see citing works
Sleep Dysfunction and Gastrointestinal Diseases.
Khanijow, V., Prakash, P., Emsellem, H. A., Borum, M. L., & Doman, D. B. (2015) · PubMed Central · Cited by 100 · see citing works
A Role for the Molecular Chaperone Protein BiP/GRP78 in Drosophila Sleep Homeostasis
Naidoo, N. N., Casiano, V., Cater, J. R., Zimmerman, J. E., & Pack, A. I. (2007) · SLEEP · doi:10.1093/sleep/30.5.557 · Cited by 98 · see citing works
Oxidative stress induces stem cell proliferation via TRPA1/RyR-mediated Ca2+ signaling in the Drosophila midgut
Xu, C., Luo, J., He, L., Montell, C., & Perrimon, N. (2017) · eLife · doi:10.7554/elife.22441 · Cited by 96 · see citing works
Contribution of sleep to the repair of neuronal DNA double-strand breaks: evidence from flies and mice
Bellesi, M., Bushey, D., Chini, M., Tononi, G., & Cirelli, C. (2016) · Scientific Reports · doi:10.1038/srep36804 · Cited by 95 · see citing works
Chronic Sleep Fragmentation During the Sleep Period Induces Hypothalamic Endoplasmic Reticulum Stress and PTP1b-Mediated Leptin Resistance in Male Mice
Hakim, F., Wang, Y., Carreras, A., Hirotsu, C., Zhang, J., Peris, E., & Gozal, D. (2015) · Sleep · doi:10.5665/sleep.4320 · Cited by 90 · see citing works
Molecular correlates of sleep and wakefulness in the brain of the white‐crowned sparrow
Jones, S., Pfister‐Genskow, M., Benca, R. M., & Cirelli, C. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05089.x · Cited by 90 · see citing works

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Underestimated health risks: polystyrene micro- and nanoplastics jointly induce intestinal barrier dysfunction by ROS-mediated epithelial cell apoptosis
Liang, B., Zhong, Y., Huang, Y., Lin, X., Liu, J., Lin, L., Hu, M., Jiang, J., Dai, M., Wang, B., et al. (2021) · Particle and Fibre Toxicology · doi:10.1186/s12989-021-00414-1 · Cited by 508 · see citing works
A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection
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 · see citing works
Oxidative eustress: On constant alert for redox homeostasis
Sies, H. (2021) · Redox Biology · doi:10.1016/j.redox.2021.101867 · Cited by 333 · see citing works
Prolonged sleep deprivation induces a cytokine-storm-like syndrome in mammals
Sang, D., Lin, K., Yang, Y., Ran, G., Li, B., Chen, C., Li, Q., Ma, Y., Lu, L., Cui, X., et al. (2023) · Cell · doi:10.1016/j.cell.2023.10.025 · Cited by 278 · see citing works
New insights in intestinal oxidative stress damage and the health intervention effects of nutrients: A review
Wang, Y., Chen, Y., Zhang, X., Lu, Y., & Chen, H. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.104248 · Cited by 265 · see citing works
Copper Clusters: An Effective Antibacterial for Eradicating Multidrug‐Resistant Bacterial Infection In Vitro and In Vivo
Zhang, X., Zhang, Z.-C., Shu, Q., Xu, C., Zheng, Q., Guo, Z. J., Wang, C., Hao, Z., Liu, X., Wang, G., et al. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202008720 · Cited by 230 · see citing works
Self-Driven Electron Transfer Biomimetic Enzymatic Catalysis of Bismuth-Doped PCN-222 MOF for Rapid Therapy of Bacteria-Infected Wounds
Wu, L., Luo, Y. Y., Wang, C., Wu, S., Zheng, Y., Li, Z., Cui, Z., Liang, Y., Zhu, S., Shen, J., et al. (2023) · ACS Nano · doi:10.1021/acsnano.2c10203 · Cited by 182 · see citing works
Circadian rhythm regulates the function of immune cells and participates in the development of tumors
Zeng, Y., Guo, Z., Wu, M., Chen, F., & Chen, L. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-01960-1 · Cited by 184 · see citing works
Microbiota and sleep: awakening the gut feeling
Sen, P., Molinero-Perez, A., O’Riordan, K. J., McCafferty, C. P., O’Halloran, K. D., & Cryan, J. F. (2021) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2021.07.004 · Cited by 162 · see citing works
Circadian rhythms and cancers: the intrinsic links and therapeutic potentials
Zhou, L., Zhang, Z., Nice, E. C., Huang, C., Zhang, W., & Tang, Y. C. (2022) · Journal of Hematology & Oncology · doi:10.1186/s13045-022-01238-y · Cited by 156 · see citing works
Role of Food Antioxidants in Modulating Gut Microbial Communities: Novel Understandings in Intestinal Oxidative Stress Damage and Their Impact on Host Health
Rajoka, M. S. R., Thirumdas, R., Mehwish, H. M., Umair, M., Khurshid, M., Hayat, H. F., Phimolsiripol, Y., Pallarés, N., Martí-Quijal, F. J., & Barba, F. J. (2021) · Antioxidants · doi:10.3390/antiox10101563 · Cited by 157 · see citing works
Effects of Coffee and Its Components on the Gastrointestinal Tract and the Brain–Gut Axis
Iriondo-DeHond, A., Uranga, J. A., del Castillo, M. D., & Abalo, R. (2020) · Nutrients · doi:10.3390/nu13010088 · Cited by 126 · see citing works
“During the last stage of preparation of this manuscript, a report by the group of Rogulja [225] was published showing that there is a key connection between beneficial effects of sleep and gut health.”
Background
Bioactive peptides and gut microbiota: Candidates for a novel strategy for reduction and control of neurodegenerative diseases
Wu, S., Bekhit, A. E. A., Wu, Q., Chen, M., Liao, X., Wang, J., & Ding, Y. (2020) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2020.12.019 · Cited by 123 · see citing works
Recent advances in ultrathin two-dimensional materials and biomedical applications for reactive oxygen species generation and scavenging
Wang, L., Li, Y., Zhao, L., Qi, Z., Gou, J., Zhang, S., & Zhang, J. Z. (2020) · Nanoscale · doi:10.1039/d0nr05746k · Cited by 123 · see citing works
Sleep and Oxidative Stress: Current Perspectives on the Role of NRF2
Davinelli, S., Medoro, A., Savino, R., & Scapagnini, G. (2024) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-024-01487-0 · Cited by 116 · see citing works
Behavioral States
Flavell, S. W., Raizen, D. M., & You, Y. (2020) · Genetics · doi:10.1534/genetics.120.303539 · Cited by 88 · see citing works
Commensal microbe-derived SCFA alleviates atrial fibrillation via GPR43/NLRP3 signaling
Zuo, K., Chen, F., Liu, Z., Fu, Y., Liu, Y., Liu, L., Wang, Y., Yin, X., Liu, X., Li, J., et al. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.70644 · Cited by 89 · see citing works
Healthy Human Fecal Microbiota Transplantation into Mice Attenuates MPTP-Induced Neurotoxicity via AMPK/SOD2 Pathway
Xie, Z., Zhang, M., Luo, Y., Jin, D., Guo, X., Yang, W., Zheng, J., Zhang, H., Zhang, L., Deng, C., et al. (2023) · Aging and disease · doi:10.14336/ad.2023.0309 · Cited by 80 · see citing works
A gut-secreted peptide suppresses arousability from sleep
Titos, I., Juginović, A., Vaccaro, A., Nambara, K., Gorelik, P., Mazor, O., & Rogulja, D. (2023) · Cell · doi:10.1016/j.cell.2023.02.022 · Cited by 80 · see citing works
Self-citation
Identification and Screening of Potential Bioactive Peptides with Sleep-Enhancing Effects in Bovine Milk Casein Hydrolysate
Qian, J., Zheng, L. P., Su, G., Huang, M., Luo, D., & Zhao, M. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c03937 · Cited by 72 · see citing works
Aucubin Attenuates Liver Ischemia-Reperfusion Injury by Inhibiting the HMGB1/TLR-4/NF-κB Signaling Pathway, Oxidative Stress, and Apoptosis
Zhang, S., Feng, Z., Gao, W., Duan, Y., Fan, G., Geng, X., Wu, B., Li, K., Liu, K., & Peng, C. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.544124 · Cited by 74 · see citing works
Diosmetin has therapeutic efficacy in colitis regulating gut microbiota, inflammation, and oxidative stress via the circ-Sirt1/Sirt1 axis
Li, H., Wei, Y., Li, X., Zhang, S., Zhang, R., Li, J.-H., Ma, B., Shao, S., Lv, Z., Ruan, H., et al. (2021) · Acta Pharmacologica Sinica · doi:10.1038/s41401-021-00726-0 · Cited by 69 · see citing works
Increased physical activity improves gut microbiota composition and reduces short-chain fatty acid concentrations in older adults with insomnia
Magzal, F., Shochat, T., Haimov, I., Tamir, S., Asraf, K., Arieli, M., Even, C., & Agmon, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-05099-w · Cited by 70 · see citing works
Hypoxia in Aging and Aging-Related Diseases: Mechanism and Therapeutic Strategies
Wei, Y., Giunta, S., & Xia, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158165 · Cited by 69 · see citing works
Bifidobacterium adolescentis regulates catalase activity and host metabolism and improves healthspan and lifespan in multiple species
Chen, S., Chen, L., Qi, Y., Xu, J., Ge, Q., Fan, Y., Chen, D., Zhang, Y., Wang, L., Hou, T., et al. (2021) · Nature Aging · doi:10.1038/s43587-021-00129-0 · Cited by 66 · see citing works
Reducing complement activation during sleep deprivation yields cognitive improvement by dexmedetomidine
Zhai, Q., Zhang, Y., Ye, M., Zhu, S., Sun, J., Wang, Y., Deng, B., Ma, D., & Wang, Q. (2023) · British Journal of Anaesthesia · doi:10.1016/j.bja.2023.04.044 · Cited by 66 · see citing works
Melatonin as a Chronobiotic with Sleep-promoting Properties
Sanabria, F. C., Carmassi, C., Bruno, S., Bazzani, A., Carli, M., Scarselli, M., & Faraguna, U. (2022) · Current Neuropharmacology · doi:10.2174/1570159x20666220217152617 · Cited by 68 · see citing works
Antioxidative Stress Mechanisms behind Resveratrol: A Multidimensional Analysis
Gu, T., Wang, N., Wu, T., Ge, Q., & Chen, L. (2021) · Journal of Food Quality · doi:10.1155/2021/5571733 · Cited by 64 · see citing works
Construction of a “Bacteria-Metabolites” Co-Expression Network to Clarify the Anti–Ulcerative Colitis Effect of Flavonoids of Sophora flavescens Aiton by Regulating the “Host–Microbe” Interaction
Shao, J., Li, Z., Gao, Y., Zhao, K., Lin, M., Li, Y., Wang, S., Liu, Y., & Chen, L. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.710052 · Cited by 63 · see citing works
Sleep Deprivation Promotes Endothelial Inflammation and Atherogenesis by Reducing Exosomal miR-182-5p
Li, X., Cao, Y., Xu, X., Wang, C., Ni, Q., Lv, X., Yang, C., Zhang, Z., Qi, X., & Song, G. (2023) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.123.319026 · Cited by 65 · see citing works
Sleep Deprivation-Induced Oxidative Stress in Rat Models: A Scoping Systematic Review
Neculicioiu, V. S., Colosi, I. A., Costache, C. A., Țoc, D. A., Sevastre-Berghian, A., Colosi, H. A., & Clichici, S. V. (2023) · Antioxidants · doi:10.3390/antiox12081600 · Cited by 59 · see citing works
Probiotics Supplementation Attenuates Inflammation and Oxidative Stress Induced by Chronic Sleep Restriction
Zheng, Y., Zhang, L., Bonfili, L., de Vivo, L., Eleuteri, A. M., & Bellesi, M. (2023) · Nutrients · doi:10.3390/nu15061518 · Cited by 58 · see citing works
A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection
Hulse, 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 · see citing works
“, 2006), and several metabolic processes (Kempf et al., 2019; Vaccaro et al., 2020).”
Background
Mild sleep restriction increases endothelial oxidative stress in female persons
Shah, R., Shah, V. K., Emin, M. T., Gao, S., Sampogna, R. V., Aggarwal, B., Chang, A., St‐Onge, M., Malik, V., Wang, J., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-42758-y · Cited by 52 · see citing works
Effects of Coffee on Gut Microbiota and Bowel Functions in Health and Diseases: A Literature Review
Saygili, S., Hegde, S., & Shi, X.-Z. P. (2024) · Nutrients · doi:10.3390/nu16183155 · Cited by 52 · see citing works
Poria cocos water-soluble polysaccharide modulates anxiety-like behavior induced by sleep deprivation by regulating the gut dysbiosis, metabolic disorders and TNF-α/NF-κB signaling pathway
Zhang, D., Li, H.-J., Zhang, H., & Ye, X. (2022) · Food & Function · doi:10.1039/d2fo00811d · Cited by 52 · see citing works
Microenvironment‐Adaptive Nanozyme for Accelerating Drug‐Resistant Bacteria‐Infected Wound Healing
Lei, Y., Sun, Y., Niu, Y., Zhang, P., Hu, J., Chen, Z., Zhang, G., & Xu, Y. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202202596 · Cited by 51 · see citing works
Beyond the symptom: the biology of fatigue
Raizen, D. M., Mullington, J. M., Anaclet, C., Clarke, G. A., Critchley, H., Dantzer, R., Davis, R. W., Drew, K. L., Fessel, J. P., Fuller, P. M., et al. (2023) · SLEEP · doi:10.1093/sleep/zsad069 · Cited by 51 · see citing works
Self-citation
Prefrontal synaptic regulation of homeostatic sleep pressure revealed through synaptic chemogenetics
Sawada, T., Iino, Y., Yoshida, K., Okazaki, H., Nomura, S., Shimizu, C., Arima, T., Juichi, M., Zhou, S., Kurabayashi, N., et al. (2024) · Science · doi:10.1126/science.adl3043 · Cited by 50 · see citing works
Dehydroepiandrosterone alleviates intestinal inflammatory damage via GPR30-mediated Nrf2 activation and NLRP3 inflammasome inhibition in colitis mice
Cao, J., Lu, M., Yan, W., Li, L., & Ma, H. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.06.025 · Cited by 51 · see citing works
The role of probiotics in children with autism spectrum disorders: A study protocol for a randomised controlled trial
Zhang, L., Xu, Y., Li, H., Li, B., Duan, G., & Zhu, C. (2022) · PLoS ONE · doi:10.1371/journal.pone.0263109 · Cited by 49 · see citing works
Potential Role of Sleep Deficiency in Inducing Immune Dysfunction
Kuna, K., Szewczyk, K., Gabryelska, A., Białasiewicz, P., Ditmer, M., Strzelecki, D., & Sochal, M. (2022) · Biomedicines · doi:10.3390/biomedicines10092159 · Cited by 49 · see citing works
Dome1–JAK–STAT signaling between parasite and host integrates vector immunity and development
Rana, V. S., Kitsou, C., Dutta, S., Ronzetti, M. H., Zhang, M., Bernard, Q., Smith, A. A., Tomás‐Cortázar, J., Yang, X., Wu, M.-J., et al. (2023) · Science · doi:10.1126/science.abl3837 · Cited by 49 · see citing works
Dynamics of oxidative stress and immune responses in neonatal calves during diarrhea
Fu, Z., Yang, Y. M., Ma, L., Malmuthuge, N., Guan, L. L., & Bu, D. (2023) · Journal of Dairy Science · doi:10.3168/jds.2023-23630 · Cited by 47 · see citing works
Gut microbiota–bile acid‐vitamin D axis plays an important role in determining oocyte quality and embryonic development
Li, A., Li, F., Song, W., Lei, Z., Sha, Q., Liu, S., Zhou, C., Zhang, X., Li, X., Schatten, H., et al. (2023) · Clinical and Translational Medicine · doi:10.1002/ctm2.1236 · Cited by 46 · see citing works
Gut Microbiota: An Important Participant in Childhood Obesity
Luo, Y., Li, M., Luo, D., & Tang, B. (2024) · Advances in Nutrition · doi:10.1016/j.advnut.2024.100362 · Cited by 48 · see citing works
The metabolome of Mexican cavefish shows a convergent signature highlighting sugar, antioxidant, and Ageing-Related metabolites
Medley, K., Persons, J. L., Biswas, T., Olsen, L. A., Peuß, R., Krishnan, J., Xiong, S., & Rohner, N. (2022) · eLife · doi:10.7554/elife.74539 · Cited by 45 · see citing works
Apigenin: a natural molecule at the intersection of sleep and aging
Kramer, D. J., & Johnson, A. A. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1359176 · Cited by 45 · see citing works
The hypothalamic link between arousal and sleep homeostasis in mice
Yamagata, T., Kahn, M. C., Prius-Mengual, J., Meijer, E. J., Šabanović, M., Guillaumin, M. C. C., van der Vinne, V., Huang, Y., McKillop, L. E., Jagannath, A., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2101580118 · Cited by 45 · see citing works
Relationship between Dietary Polyphenols and Gut Microbiota: New Clues to Improve Cognitive Disorders, Mood Disorders and Circadian Rhythms
Liu, S., Cheng, L., Liu, Y., Zhan, S., Wu, Z., & Zhang, X. (2023) · Foods · doi:10.3390/foods12061309 · Cited by 44 · see citing works
Temozolomide-based sonodynamic therapy induces immunogenic cell death in glioma
Zhou, Y., Jiao, J., Yang, R., Wen, B., Wu, Q., Xu, L., Tong, X., & Yan, H. (2023) · Clinical Immunology · doi:10.1016/j.clim.2023.109772 · Cited by 43 · see citing works
Melatonin improves skin barrier damage caused by sleep restriction through gut microbiota
Li, W., Wang, Z., Cao, J., Dong, Y., & Chen, Y. (2023) · Journal of Pineal Research · doi:10.1111/jpi.12874 · Cited by 42 · see citing works
Recent progress in the preparation of bioactive peptides using simulated gastrointestinal digestion processes
Du, C., Gong, H., Zhao, H., & Wang, P. (2024) · Food Chemistry · doi:10.1016/j.foodchem.2024.139587 · Cited by 41 · see citing works
Sleep deprivation causes gut dysbiosis impacting on systemic metabolomics leading to premature ovarian insufficiency in adolescent mice
Yan, J., Zhang, X., Zhu, K., Yu, M., Liu, Q., Felici, M. D., Zhang, T., Wang, J., & Shen, W. (2024) · Theranostics · doi:10.7150/thno.95197 · Cited by 41 · see citing works
LONP1-mediated mitochondrial quality control safeguards metabolic shifts in heart development
Zhao, K., Huang, X., Zhao, W., Lü, B., & Yang, Z. (2022) · Development · doi:10.1242/dev.200458 · Cited by 40 · see citing works
Structural characterization and antioxidant activity of processed polysaccharides PCP-F1 from Polygonatum cyrtonema Hua.
Zhao, Y., Wang, Z., Fu, R., Xie, R., Wang, B., & Li, Q. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1272977 · Cited by 40 · see citing works
Activation of locus coeruleus noradrenergic neurons rapidly drives homeostatic sleep pressure
Silverman, D., Chen, C., Chang, S., Bui, L., Zhang, Y., Raghavan, R., Jiang, A., Le, A. N., Darmohray, D. M., Sima, J., et al. (2025) · Science Advances · doi:10.1126/sciadv.adq0651 · Cited by 39 · see citing works
l ‐Carnosine Protects Against Deoxynivalenol‐Induced Oxidative Stress in Intestinal Stem Cells by Regulating the Keap1/Nrf2 Signaling Pathway
Zhou, J., Lin, H., Qin, Y., Li, X., Gao, C., Yan, H., & Wang, X. (2021) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202100406 · Cited by 39 · see citing works
Drinking Water Supplemented with Acidifiers Improves the Growth Performance of Weaned Pigs and Potentially Regulates Antioxidant Capacity, Immunity, and Gastrointestinal Microbiota Diversity
Xu, Q., Liu, C., Mo, X.-J., Chen, M., Zhao, X., Liu, M.-Z., Wang, S., Zhou, B., & Zhao, C.-X. (2022) · Antioxidants · doi:10.3390/antiox11050809 · Cited by 39 · see citing works
Recent Advancement in Sleep Technologies: A Literature Review on Clinical Standards, Sensors, Apps, and AI Methods
Cay, G., Ravichandran, V., Sadhu, S., Zisk, A. H., Salisbury, A. L., Solanki, D., & Mankodiya, K. (2022) · IEEE Access · doi:10.1109/access.2022.3210518 · Cited by 44 · see citing works
JNK Signaling in Drosophila Aging and Longevity
Gan, T., Fan, L., Zhao, L., Misra, M., Liu, M., Zhang, M., & Su, Y. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179649 · Cited by 36 · see citing works
DNA Nanostructures Treat Inflammatory Bowel Disease through ROS Scavenging and Gut Microbiota Modulation
Ge, J., Jia, B., Wang, Y., Ma, Y., Sun, X., Dong, J., Jiang, S., & Li, Z. (2024) · Advanced Functional Materials · doi:10.1002/adfm.202402781 · Cited by 37 · see citing works
A high-protein diet-responsive gut hormone regulates behavioral and metabolic optimization in Drosophila melanogaster
Yoshinari, Y., Nishimura, T., Yoshii, T., Kondo, S., Tanimoto, H., Kobayashi, T., Matsuyama, M., & Niwa, R. (2024) · Nature Communications · doi:10.1038/s41467-024-55050-y · Cited by 39 · see citing works
Non-REM and REM/paradoxical sleep dynamics across phylogeny
Jaggard, J. B., Wang, G. X., & Mourrain, P. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.08.004 · Cited by 37 · see citing works
The Impact of Instant Coffee and Decaffeinated Coffee on the Gut Microbiota and Depression-Like Behaviors of Sleep-Deprived Rats
Gu, X., Zhang, S., Ma, W., Wang, Q., Li, Y., Xia, C., Xu, Y., Zhang, T., Yang, L., & Zhou, M. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.778512 · Cited by 37 · see citing works
Redox Control of the Dormant Cancer Cell Life Cycle
Li, B., Huang, Y., Ming, H., Nice, E. C., Xuan, R., & Huang, C. (2021) · Cells · doi:10.3390/cells10102707 · Cited by 36 · see citing works
Sleep Loss Causes Dysfunction in Murine Extraorbital Lacrimal Glands
Huang, S., Si, H., Liu, J., Qi, D., Pei, X., Lu, D., Zou, S., & Li, Z. (2022) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.63.6.19 · Cited by 37 · see citing works
Sleep pressure accumulates in a voltage-gated lipid peroxidation memory
Rorsman, H. O., Müller, M. A., Liu, P. Z., Sanchez, L. G., Kempf, A., Gerbig, S., Spengler, B., & Miesenböck, G. (2025) · Nature · doi:10.1038/s41586-025-08734-4 · Cited by 34 · see citing works
Oxidase Mimic Graphdiyne for Efficient Superoxide Generation in Wide pH Ranges
Gu, Y., Fan, C., Hao, X., Hu, F., Zhang, C., Yang, H., Li, C. M., & Guo, C. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202110192 · Cited by 35 · see citing works
Sleep loss is a metabolic disorder
Feeney, S. P., McCarthy, J. M., Petruconis, C. R., & Tudor, J. C. (2025) · Science Signaling · doi:10.1126/scisignal.adp9358 · Cited by 34 · see citing works
Selenium metabolism and regulation of immune cells in immune‐associated diseases
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Farnesol Exerts Protective Effects against Chronic Sleep Deprivation‐Induced Cognitive Impairment via Activation SIRT1/Nrf2 Pathway in the Hippocampi of Adult Mice
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Self-citation
A bidirectional relationship between sleep and oxidative stress in Drosophila
Hill, V. M., O'Connor, R. M., Sissoko, G. B., Irobunda, I., Leong, S., Canman, J. C., Stavropoulos, N., & Shirasu‐Hiza, M. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2005206 · Cited by 196 · see citing works

Authors: Vaccaro, A., Kaplan Dor, Y., Nambara, K., Pollina, E. A., Lin, C., Greenberg, M. E., & Rogulja, D.
Affiliations: Harvard University (US)
Corresponding author: Rogulja, Dragana
ORCID: Vaccaro, Alexandra
Nambara, Keishi
Pollina, Elizabeth A.
Greenberg, Michael E.
Rogulja, Dragana
Venue: Cell
Publisher: Elsevier BV
Published: 2020-06
Volume: 181
Issue: 6
Pages: 1307-1328.e15
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2020.04.049
OpenAlex: W3033924751
Cited by: 541
References: 252
Citations by year: 2026: 79 · 2025: 127 · 2024: 109 · 2023: 92 · 2022: 63 · 2021: 53 · 2020: 18
FWCI: 18.77
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 375 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Funders: Pew Charitable Trusts
New York Stem Cell Foundation
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Keywords: sleep deprivation, reactive oxygen species, oxidative stress, intestine, antioxidant enzymes, lifespan, oral antioxidants, Drosophila, mice
MeSH terms: Animals, Antioxidants, Drosophila, Male, Mice, Inbred CBA, Mice, Inbred C57BL, Sleep, Sleep Deprivation, Reactive Oxygen Species, Oxidative Stress, Gastrointestinal Tract, Mice

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Sleep Loss Can Cause Death through Accumulation of Reactive Oxygen Species in the Gut

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