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Antioxidants
Volume 13
Issue 7
10.3390/antiox13070833
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Article

Sleep Deprivation Triggers Mitochondrial DNA Release in Microglia to Induce Neural Inflammation: Preventative Effect of Hydroxytyrosol Butyrate

by
Yachong Hu
1,
Yongyao Wang
1,
Yifang Wang
1,
Yuxia Zhang
1,
Zhen Wang
1,
Xiaohong Xu
2,
Tinghua Zhang
2,
Tiantian Zhang
1,
Shuangxi Zhang
1,
Ranrui Hu
1,
Le Shi
1,
Xudong Wang
1,
Jin Li
3,
Hui Shen
4,
Jiankang Liu
1,5,
Mami Noda
1,6,
Yunhua Peng
1,* and
Jiangang Long
1,*
1
Center for Mitochondrial Biology and Medicine, The Key Laboratory of Biomedical Information Engineering of Ministry of Education, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, China
2
School of Pharmacy, Chengdu Medical College, Chengdu 610500, China
3
State Key Laboratory of Toxicology and Medical Countermeasures, Beijing Institute of Pharmacology and Toxicology, Beijing 100850, China
4
Department of Nutrition and Food Hygiene, Faculty of Naval Medicine, Naval Medical University, Shanghai 200433, China
5
School of Health and Life Science, University of Health and Rehabilitation Sciences, Qingdao 266071, China
6
Research and Educational Resource Center for Immunophenotyping, RUDN University, 6 Miklukho-Maklaya St, 117198 Moscow, Russia
*
Authors to whom correspondence should be addressed.
Antioxidants 2024, 13(7), 833; https://doi.org/10.3390/antiox13070833
Submission received: 30 May 2024 / Revised: 5 July 2024 / Accepted: 10 July 2024 / Published: 12 July 2024
(This article belongs to the Section Health Outcomes of Antioxidants and Oxidative Stress)
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Abstract

Sleep deprivation (SD) triggers mitochondrial dysfunction and neural inflammation, leading to cognitive impairment and mental issues. However, the mechanism involving mitochondrial dysfunction and neural inflammation still remains unclear. Here, we report that SD rats exhibited multiple behavioral disorders, brain oxidative stress, and robust brain mitochondrial DNA (mtDNA) oxidation. In particular, SD activated microglia and microglial mtDNA efflux to the cytosol and provoked brain pro-inflammatory cytokines. We observed that the mtDNA efflux and pro-inflammatory cytokines significantly reduced with the suppression of the mtDNA oxidation. With the treatment of a novel mitochondrial nutrient, hydroxytyrosol butyrate (HTHB), the SD-induced behavioral disorders were significantly ameliorated while mtDNA oxidation, mtDNA release, and NF-κB activation were remarkably alleviated in both the rat brain and the N9 microglial cell line. Together, these results indicate that microglial mtDNA oxidation and the resultant release induced by SD mediate neural inflammation and HTHB prevents mtDNA oxidation and efflux, providing a potential treatment for SD-induced mental issues.
Keywords: sleep deprivation; mtDNA release; oxidative stress; hydroxytyrosol butyrate; microglia; neural inflammation sleep deprivation; mtDNA release; oxidative stress; hydroxytyrosol butyrate; microglia; neural inflammation
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MDPI and ACS Style

Hu, Y.; Wang, Y.; Wang, Y.; Zhang, Y.; Wang, Z.; Xu, X.; Zhang, T.; Zhang, T.; Zhang, S.; Hu, R.; et al. Sleep Deprivation Triggers Mitochondrial DNA Release in Microglia to Induce Neural Inflammation: Preventative Effect of Hydroxytyrosol Butyrate. Antioxidants 2024, 13, 833. https://doi.org/10.3390/antiox13070833

AMA Style

Hu Y, Wang Y, Wang Y, Zhang Y, Wang Z, Xu X, Zhang T, Zhang T, Zhang S, Hu R, et al. Sleep Deprivation Triggers Mitochondrial DNA Release in Microglia to Induce Neural Inflammation: Preventative Effect of Hydroxytyrosol Butyrate. Antioxidants. 2024; 13(7):833. https://doi.org/10.3390/antiox13070833

Chicago/Turabian Style

Hu, Yachong, Yongyao Wang, Yifang Wang, Yuxia Zhang, Zhen Wang, Xiaohong Xu, Tinghua Zhang, Tiantian Zhang, Shuangxi Zhang, Ranrui Hu, and et al. 2024. "Sleep Deprivation Triggers Mitochondrial DNA Release in Microglia to Induce Neural Inflammation: Preventative Effect of Hydroxytyrosol Butyrate" Antioxidants 13, no. 7: 833. https://doi.org/10.3390/antiox13070833

APA Style

Hu, Y., Wang, Y., Wang, Y., Zhang, Y., Wang, Z., Xu, X., Zhang, T., Zhang, T., Zhang, S., Hu, R., Shi, L., Wang, X., Li, J., Shen, H., Liu, J., Noda, M., Peng, Y., & Long, J. (2024). Sleep Deprivation Triggers Mitochondrial DNA Release in Microglia to Induce Neural Inflammation: Preventative Effect of Hydroxytyrosol Butyrate. Antioxidants, 13(7), 833. https://doi.org/10.3390/antiox13070833

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