Effects of combined sleep deprivation and noise exposure on hippocampal neuroinflammation and pyroptosis

Abstract

Abstract: Objective To explore the effects of sleep deprivation and noise combined exposure on hippocampal neuroinflammation and pyroptosis,and to provide clues for clarifying the synergistic effects and mechanisms of these factors on the nervous system. Methods Forty-eight male C57BL/6J mice were randomly divided into four groups：the control(C) group,the sleep deprivation(SD) group,the noise exposure(NE) group,and the sleep deprivation combined with noise exposure(SN) group. The sleep deprivation paradigm was established by employing the curling prevention by water(CPW) paradigm. The noise intensity was 115 dB SPL,and the duration lasted for 4 hours. The activity level of superoxide dismutase(SOD) and the content level of malonaldehyde(MDA) in the hippocampal tissues of the mice were determined using kits. The level of corticosterone(CORT) in the serum of the mice was detected by enzyme-linked immunosorbent assay(ELISA). The expressions of inflammatory factors and genes and proteins related to pyroptosis in the hippocampal tissues of the mice were measured by quantitative real-time PCR(RT-qPCR) and Western Blot. Results Following sleep deprivation and noise exposure,the serum CORT levels in SD group of mice were significantly increased in comparison to C group(P<0.05). The serum CORT levels in NE group demonstrated an upward trend,yet the difference was not statistically significant(P>0.05). The serum CORT levels in SN group were significantly increased(P<0.05). Compared with C group,the SOD activity in the hippocampus tissue of SD,NE and SN groups were significantly decreased(all P<0.05),and the MDA content were significantly increased(all P<0.05). These findings suggested that sleep deprivation and noise exposure could induce disturbances in the oxidation-reduction balance of hippocampal tissues. Additionally,the expression levels of tumor necrosis factor-α(TNF-α),interleukin-6(IL-6),interleukin-18(IL-18) and interleukin-1β(IL-1β) mRNA in the hippocampal tissues of SD,NE and SN groups were observed to have increased significantly in comparison to that of C group(all P<0.05). Further analysis revealed that compared to C group,SD,NE and SN groups exerted a pronounced influence on the hippocampal NOD-like receptor thermal protein domian associated protein 3(NLRP3)/cysteine aspartate-specific protease1(Caspase-1)/gasdermin-D(GSDMD) pathway associated with pyroptosis(all P<0.05). Additionally,factorial analysis indicated that sleep deprivation and combined noise exposure exerted an interactive effect on the expression of pyroptosis-related proteins(P<0.05). Conclusion Sleep deprivation and noise exposure alone and in combination can cause neuroinflammatory responses in the hippocampus,leading to neuronal pyroptosis,and the two have a synergistic effect,ultimately increasing the risk of neurological damage.

Key words: Sleep deprivation, Noise, NLRP3/Caspase-1/GSDMD pathway, Pyroptosis

CLC Number:

R-332

SONG Xiaoqiong, CHENG Mengzhu, MA Kefeng, SHE Xiaojun, CUI Bo. Effects of combined sleep deprivation and noise exposure on hippocampal neuroinflammation and pyroptosis. [J]OCCUPATION AND HEALTH, 2025, 41(22): 3074-3080.

References

[1] WEI R,DUAN X,GUO L.Effects of sleep deprivation on coronary heart disease[J].Korean J Physiol Pha,2022,26(5):297-305.
[2] DELL' AQUILA J T,SOTI V.Sleep deprivation:A risk for epileptic seizures[J].Sleep Sci,2022,15(2):245-249.
[3] DELIC V,RATLIFF W A,CITRON B A.Sleep deprivation,a link between post-traumatic stress disorder and Alzheimer's disease[J].J Alzheimer's Dis,2021,79(4):1443-1449.
[4] ZHANG L,ZHANG H Q,LIANG X Y,et al.Melatonin ameliorates cognitive impairment induced by sleep deprivation in rats:Role of oxidative stress,BDNF and CaMKII[J].Behav Brain Res,2013,256:72-81.
[5] KILLGORE W D.Effects of sleep deprivation on cognition[J].Prog Brain Res,2010,185:105-129.
[6] LIAN W W,ZHOU W,ZHANG B Y,et al.DL0410 ameliorates cognitive disorder in SAMP8 mice by promoting mitochondrial dynamics and the NMDAR-CREB-BDNF pathway[J].Acta Pharmacol Sin,2021,42(7):1055-1068.
[7] THOMPSON R,SMITH R B,BOU K Y,et al.Noise pollution and human cognition:An updated systematic review and meta-analysis of recent evidence[J].Environ Int,2022,158:106905.
[8] MANIKANDAN S,PADMA M K,SRIKUMAR R,et al.Effects of chronic noise stress on spatial memory of rats in relation to neuronal dendritic alteration and free radical-imbalance in hippocampus and medial prefrontal cortex[J].Neurosci Lett,2006,399(1/2):17-22.
[9] DAIBER A,KROLLER-SCHON S,FRENIS K,et al.Environmental noise induces the release of stress hormones and inflammatory signaling molecules leading to oxidative stress and vascular dysfunction-signatures of the internal exposome[J].Biofactors,2019,45(4):495.
[10] HAHAD O,PROCHASKA J H,DAIBER A,et al.Environmental noise-induced effects on stress hormones,oxidative stress,and vascular dysfunction:Key factors in the relationship between cerebrocardiovascular and psychological disorders[J].Oxid Med Cell Longev,2019,2019:4623109.
[11] BASNER M,BABISCH W,DAVIS A,et al.Auditory and non-auditory effects of noise on health[J].The Lancet,2014,383(9925):1325-1332.
[12] 胡俊杰,朱英文,付波,等.某部装备长时作业物理环境及军人睡眠节律调查分析[J].军事医学,2023,47(11):801-804.
[13] YANG S H.Cellular and molecular mediators of neuroinflammation in Alzheimer disease[J].Int Neurourol J,2019,23(S2):54-62.
[14] ZIELINSKI M R,GERASHCHENKO D,KARPOVA S A,et al.The NLRP3 inflammasome modulates sleep and NREM sleep delta power induced by spontaneous wakefulness,sleep deprivation and lipopolysa ccharide[J].Brain Behav Immun,2017,62:137-150.
[15] ZHOU H,WU J,GONG Y,et al.Isoquercetin alleviates sleep deprivation dependent hippocampal neurons damage by suppressing NLRP3-induced pyroptosis[J].Immunopharmacol Immunotoxicol,2022,44(5):766-772.
[16] SU D,LI W,SHE X,et al.Chronic noise exposure exacerbates AD-like neuropathology in SAMP8 mice in relation to Wnt signaling in the PFC and hippocampus[J].Sci Rep,2018,8(1):14622.
[17] LUO L,LIN S,HU G,et al.Molecular mechanism of rolupram reducing neuroinflammation in noise induced tinnitus mice through TLR4/NF-κB/NLRP3 protein/caspase-1/IL-1 β signaling pathway[J].Int J Biol Macromol, 2024,278:134987.
[18] SANG D,LIN K,YANG Y,et al.Prolonged sleep deprivation induces a cytokine-storm-like syndrome in mammals[J].Cell,2023,186(25):5500-5516.
[19] SALEHPOUR F,FARAJDOKHT F,ERFANI M,et al.Transcranial near-infrared photobiomodulation attenuates memory impairment and hippocampal oxidative stress in sleep-deprived mice[J].Brain Res,2018, 1682:36-43.
[20] BOYACIOGLU N,OZKAN S.The effect of noise in the intensive care unit on the oxidative stress response in rats[J].Biol Res Nurs,2020, 22(3):397-402.
[21] NABAEE E,KESMATI M,SHAHRIARI A,et al.Cognitive and hippocampus biochemical changes following sleep deprivation in the adult male rat[J].Biomed Pharmacother,2018,104:69-76.
[22] MANCHANDA S,SINGH H,KAUR T,et al.Low-grade neuroinflammation due to chronic sleep deprivation results in anxiety and learning and memory impairments[J].Mol Cell Biochem,2018,449(1/2):63-72.
[23] SHUKLA M,MANI K V,DEEPSHIKHA A,et al.Moderate noise associated oxidative stress with concomitant memory impairment,neuro-inflammation and neurodegeneration[J].Brain Behav Immun Health,2020,5:100089.
[24] 付一鸣,张鑫垚,佘晓俊,等.长期睡眠期噪声暴露对小鼠认知功能的影响及生物钟相关机制[J].环境与职业医学,2024,41(2):119-124,132.
[25] WANG S,YUAN Y H,CHEN N H,et al.The mechanisms of NLRP3 inflammasome/pyroptosis activation and their role in Parkinson's disease[J].Int Immunopharmacol,2019,67:458-464.
[26] FUSCO R,SIRACUSA R,GENOVESE T,et al.Focus on the role of NLRP3 inflammasome in diseases[J].Int J Mol Sci,2020,21(12):4223.
[27] HENEKA M T,MCMANUS R M,LATZ E.Inflammasome signalling in brain function and neurodegenerative disease[J].Nat Rev Neurosci,2018,19:610-621.
[28] SHAO B Z,WANG S L,PAN P,et al.Targeting NLRP3 inflammasome in inflammatory bowel disease:Putting out the fire of inflammation[J].Inflammation,2019,42(4):1147-1159.
[29] YANG K L,LI W H,LIU Y J,et al.Hydrogen sulfide attenuates neuroinflammation by inhibiting the NLRP3/Caspase-1/GSDMD pathway in retina or brain neuron following rat ischemia/reperfusion[J].Brain Sci,2022,12(9):1245.