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Erschienen in: Inflammation Research 11/2020

18.08.2020 | Original Research Paper

Sleep deprivation aggravated lipopolysaccharide/d-galactosamine-induced acute liver injury by suppressing melatonin production

verfasst von: Lu Liu, Li Zhang, Longjiang Li, Mengting Chen, Zhe Wang, Yi Shen, Jiayi Huang, Ling Tang

Erschienen in: Inflammation Research | Ausgabe 11/2020

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Abstract

Objective

Sleep loss is common in patients with liver injury, but the effects of sleep deprivation (SD) on liver injury remain unclear. In the present study, the potential effects of SD on acute liver injury and the underlying mechanisms have been investigated.

Methods

The sleep of male BALB/c mice has been deprived by using a modified multiple platform water bath for 3 days and acute liver injury was induced by intraperitoneal injection of lipopolysaccharide (LPS) and d-galactosamine (D-Gal). The degree of liver injury was detected by aminotransferase determination, histopathology and survival rate analysis. Inflammatory response and melatonin (MT) were measured by enzyme-linked immunosorbent assay (ELISA). In addition, hepatocyte apoptosis was determined by caspase activity measurement and terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay.

Results

We observed that SD increased plasma aminotransferases, TUNEL-positive hepatocytes, histological abnormalities and mortality rates in mice with LPS/D-Gal treatment. SD also promoted LPS/D-Gal-induced production of TNF-α and upregulated hepatic caspase-8, caspase-9, and caspase-3 activities in LPS/D-Gal-exposed mice. In addition, SD significantly decreased MT contents in plasma of mice with acute liver injury, but supplementation with MT reversed these SD-promoted changes.

Conclusion

Our data suggested that SD exacerbated LPS/D-Gal-induced liver injury via decreasing melatonin production.
Literatur
1.
Zurück zum Zitat Perea L, Coll M, Sanjurjo L, Blaya D, Taghdouini AE, Rodrigo-Torres D, et al. Pentraxin-3 modulates lipopolysaccharide-induced inflammatory response and attenuates liver injury. Hepatology (Baltimore, MD). 2017;66(3):953–68. Perea L, Coll M, Sanjurjo L, Blaya D, Taghdouini AE, Rodrigo-Torres D, et al. Pentraxin-3 modulates lipopolysaccharide-induced inflammatory response and attenuates liver injury. Hepatology (Baltimore, MD). 2017;66(3):953–68.
2.
Zurück zum Zitat González-Terán B, Cortés JR, Manieri E, Matesanz N, Verdugo Á, Rodríguez ME, et al. Eukaryotic elongation factor 2 controls TNF-α translation in LPS-induced hepatitis. J Clin Investig. 2013;123(1):164–78.PubMed González-Terán B, Cortés JR, Manieri E, Matesanz N, Verdugo Á, Rodríguez ME, et al. Eukaryotic elongation factor 2 controls TNF-α translation in LPS-induced hepatitis. J Clin Investig. 2013;123(1):164–78.PubMed
3.
Zurück zum Zitat Deng Y, Chen C, Yu H, Diao H, Shi C, Wang Y, et al. Oridonin ameliorates lipopolysaccharide/d-galactosamine-induced acute liver injury in mice via inhibition of apoptosis. Am J Transl Res. 2017;9(9):4271–9.PubMedPubMedCentral Deng Y, Chen C, Yu H, Diao H, Shi C, Wang Y, et al. Oridonin ameliorates lipopolysaccharide/d-galactosamine-induced acute liver injury in mice via inhibition of apoptosis. Am J Transl Res. 2017;9(9):4271–9.PubMedPubMedCentral
4.
Zurück zum Zitat Bergonzi P, Bianco A, Mazza S, Mennuni G. Night sleep organization in patients with severe hepatic failure. Its modifications after l-dopa treatment. Eur Neurol. 1978;17(5):271–5.PubMed Bergonzi P, Bianco A, Mazza S, Mennuni G. Night sleep organization in patients with severe hepatic failure. Its modifications after l-dopa treatment. Eur Neurol. 1978;17(5):271–5.PubMed
5.
Zurück zum Zitat De Cruz S, Espiritu JRD, Zeidler M, Wang TS. Sleep disorders in chronic liver disease. Semin Respir Crit Care Med. 2012;33(1):26–35.PubMed De Cruz S, Espiritu JRD, Zeidler M, Wang TS. Sleep disorders in chronic liver disease. Semin Respir Crit Care Med. 2012;33(1):26–35.PubMed
6.
Zurück zum Zitat Bruyneel M, Sersté T. Sleep disturbances in patients with liver cirrhosis: prevalence, impact, and management challenges. Nat Sci Sleep. 2018;10:369–75.PubMedPubMedCentral Bruyneel M, Sersté T. Sleep disturbances in patients with liver cirrhosis: prevalence, impact, and management challenges. Nat Sci Sleep. 2018;10:369–75.PubMedPubMedCentral
7.
Zurück zum Zitat Meier-Ewert HK, Ridker PM, Rifai N, Regan MM, Price N, Dinges DF, et al. Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk. J Am Coll Cardiol. 2004;43(4):678–83.PubMed Meier-Ewert HK, Ridker PM, Rifai N, Regan MM, Price N, Dinges DF, et al. Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk. J Am Coll Cardiol. 2004;43(4):678–83.PubMed
8.
Zurück zum Zitat Ranjbaran Z, Keefer L, Farhadi A, Stepanski E, Sedghi S, Keshavarzian A. Impact of sleep disturbances in inflammatory bowel disease. J Gastroenterol Hepatol. 2007;22(11):1748–53.PubMed Ranjbaran Z, Keefer L, Farhadi A, Stepanski E, Sedghi S, Keshavarzian A. Impact of sleep disturbances in inflammatory bowel disease. J Gastroenterol Hepatol. 2007;22(11):1748–53.PubMed
9.
Zurück zum Zitat Karmann AJ, Kundermann B, Lautenbacher S. Sleep deprivation and pain: a review of the newest literature. Schmerz (Berlin, Germany). 2014;28(2):141–6. Karmann AJ, Kundermann B, Lautenbacher S. Sleep deprivation and pain: a review of the newest literature. Schmerz (Berlin, Germany). 2014;28(2):141–6.
10.
Zurück zum Zitat Jackson ML, Hughes ME, Croft RJ, Howard ME, Crewther D, Kennedy GA, et al. The effect of sleep deprivation on BOLD activity elicited by a divided attention task. Brain Imaging Behav. 2011;5(2):97–108.PubMed Jackson ML, Hughes ME, Croft RJ, Howard ME, Crewther D, Kennedy GA, et al. The effect of sleep deprivation on BOLD activity elicited by a divided attention task. Brain Imaging Behav. 2011;5(2):97–108.PubMed
11.
Zurück zum Zitat Lee YD, Kim JY, Lee KH, Kwak YJ, Lee SK, Kim OS, et al. Melatonin attenuates lipopolysaccharide-induced acute lung inflammation in sleep-deprived mice. J Pineal Res. 2009;46(1):53–7.PubMed Lee YD, Kim JY, Lee KH, Kwak YJ, Lee SK, Kim OS, et al. Melatonin attenuates lipopolysaccharide-induced acute lung inflammation in sleep-deprived mice. J Pineal Res. 2009;46(1):53–7.PubMed
12.
Zurück zum Zitat Yuan R, Guo LL, Chen HW, Li JP, Chen Z, Wei BJ, et al. Cardioprotective effects of HuoxueAnshenRecipe against myocardial Injuries Induced by sleep deprivation in rats. Evid based Complement Altern Med eCAM. 2017;2017:7359760. Yuan R, Guo LL, Chen HW, Li JP, Chen Z, Wei BJ, et al. Cardioprotective effects of HuoxueAnshenRecipe against myocardial Injuries Induced by sleep deprivation in rats. Evid based Complement Altern Med eCAM. 2017;2017:7359760.
13.
Zurück zum Zitat Arthaud S, Varin C, Gay N, Libourel PA, Chauveau F, Fort P, et al. Paradoxical (REM) sleepdeprivation in mice using the small-platforms-over-water method: polysomnographic analyses and melanin-concentrating hormone and hypocretin/orexin neuronal activation before, during and after deprivation. J Sleep Res. 2015;24(3):309–19.PubMed Arthaud S, Varin C, Gay N, Libourel PA, Chauveau F, Fort P, et al. Paradoxical (REM) sleepdeprivation in mice using the small-platforms-over-water method: polysomnographic analyses and melanin-concentrating hormone and hypocretin/orexin neuronal activation before, during and after deprivation. J Sleep Res. 2015;24(3):309–19.PubMed
14.
Zurück zum Zitat Silverstein R. d-galactosamine lethality model: scope and limitations. J Endotoxin Res. 2004;10(3):147–62.PubMed Silverstein R. d-galactosamine lethality model: scope and limitations. J Endotoxin Res. 2004;10(3):147–62.PubMed
15.
Zurück zum Zitat McGill MR, Jaeschke H. Biomarkers of drug-induced liver injury: progress and utility in research, medicine, and regulation. Expert Rev Mol Diagn. 2018;18(9):797–807.PubMedPubMedCentral McGill MR, Jaeschke H. Biomarkers of drug-induced liver injury: progress and utility in research, medicine, and regulation. Expert Rev Mol Diagn. 2018;18(9):797–807.PubMedPubMedCentral
16.
Zurück zum Zitat Tiegs G, Wolter M, Wendel A. Tumor necrosis factor is a terminal mediator in galactosamine/endotoxin-induced hepatitis in mice. Biochem Pharmacol. 1989;38(4):627–31.PubMed Tiegs G, Wolter M, Wendel A. Tumor necrosis factor is a terminal mediator in galactosamine/endotoxin-induced hepatitis in mice. Biochem Pharmacol. 1989;38(4):627–31.PubMed
17.
Zurück zum Zitat Besedovsky L, Lange T, Haack M. The sleep-immune crosstalk in health and disease. Physiol Rev. 2019;99(3):1325–80.PubMedPubMedCentral Besedovsky L, Lange T, Haack M. The sleep-immune crosstalk in health and disease. Physiol Rev. 2019;99(3):1325–80.PubMedPubMedCentral
18.
Zurück zum Zitat Irwin MR, Olmstead R, Carroll JE. Sleep disturbance, sleep duration, and inflammation: a systematic review and meta-analysis of cohort studies and experimental sleep deprivation. Biol Psychiatry. 2016;80(1):40–52.PubMed Irwin MR, Olmstead R, Carroll JE. Sleep disturbance, sleep duration, and inflammation: a systematic review and meta-analysis of cohort studies and experimental sleep deprivation. Biol Psychiatry. 2016;80(1):40–52.PubMed
19.
Zurück zum Zitat Gozal D, Khalyfa A, Qiao Z, Akbarpour M, Maccari R, Ottanà R. Protein-tyrosine phosphatase-1B mediates sleep fragmentation-induced insulin resistance and visceral adipose tissue inflammation in mice. Sleep. 2017;40(9). Gozal D, Khalyfa A, Qiao Z, Akbarpour M, Maccari R, Ottanà R. Protein-tyrosine phosphatase-1B mediates sleep fragmentation-induced insulin resistance and visceral adipose tissue inflammation in mice. Sleep. 2017;40(9).
20.
Zurück zum Zitat Park YS, Chung SH, Lee SK, Kim JH, Kim JB, Kim TK, et al. Melatonin improves experimental colitis with sleep deprivation. Int J Mol Med. 2015;35(4):979–86.PubMedPubMedCentral Park YS, Chung SH, Lee SK, Kim JH, Kim JB, Kim TK, et al. Melatonin improves experimental colitis with sleep deprivation. Int J Mol Med. 2015;35(4):979–86.PubMedPubMedCentral
21.
Zurück zum Zitat Wang Y, Yang F, Jiao FZ, Chen Q, Zhang WB, Wang LW, et al. Modulations of histone deacetylase 2 offer a protective effect through the mitochondrial apoptosis pathway in acute liver failure. Oxid Med Cell Longev. 2019;2019:8173016.PubMedPubMedCentral Wang Y, Yang F, Jiao FZ, Chen Q, Zhang WB, Wang LW, et al. Modulations of histone deacetylase 2 offer a protective effect through the mitochondrial apoptosis pathway in acute liver failure. Oxid Med Cell Longev. 2019;2019:8173016.PubMedPubMedCentral
22.
Zurück zum Zitat Nowak M, Gaines GC, Rosenberg J, Minter R, Bahjat FR, Rectenwald J, et al. LPS-induced liver injury in d-galactosamine-sensitized mice requires secreted TNF-alpha and the TNF-p55 receptor. Am J Physiol Regul Integr Comp Physiol. 2000;278(5):R1202–R12091209.PubMed Nowak M, Gaines GC, Rosenberg J, Minter R, Bahjat FR, Rectenwald J, et al. LPS-induced liver injury in d-galactosamine-sensitized mice requires secreted TNF-alpha and the TNF-p55 receptor. Am J Physiol Regul Integr Comp Physiol. 2000;278(5):R1202–R12091209.PubMed
23.
Zurück zum Zitat Zhou H, Tang L, Yang Y, Lin L, Dai J, Ge P, et al. Dopamine alleviated acute liver injury induced by lipopolysaccharide/d-galactosamine in mice. Int Immunopharmacol. 2018;61:249–55.PubMed Zhou H, Tang L, Yang Y, Lin L, Dai J, Ge P, et al. Dopamine alleviated acute liver injury induced by lipopolysaccharide/d-galactosamine in mice. Int Immunopharmacol. 2018;61:249–55.PubMed
24.
Zurück zum Zitat Kim JY, Lee YD, Kim BJ, Kim SP, Kim DH, Jo KJ, Lee SK, et al. Melatonin improves inflammatory cytokine profiles in lung inflammation associated with sleep deprivation. Mol Med Rep. 2012;5(5):1281–4.PubMed Kim JY, Lee YD, Kim BJ, Kim SP, Kim DH, Jo KJ, Lee SK, et al. Melatonin improves inflammatory cytokine profiles in lung inflammation associated with sleep deprivation. Mol Med Rep. 2012;5(5):1281–4.PubMed
25.
Zurück zum Zitat Pasparakis M, Alexopoulou L, Episkopou V, Kollias G. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J Exp Med. 1996;184(4):1397–411.PubMed Pasparakis M, Alexopoulou L, Episkopou V, Kollias G. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J Exp Med. 1996;184(4):1397–411.PubMed
26.
Zurück zum Zitat Cao Y, Li Q, Liu L, Wu H, Huang F, Wang C, et al. Modafinil protects hippocampal neurons by suppressing excessive autophagy and apoptosis in mice with sleep deprivation. Br J Pharmacol. 2019;176(9):1282–97.PubMedPubMedCentral Cao Y, Li Q, Liu L, Wu H, Huang F, Wang C, et al. Modafinil protects hippocampal neurons by suppressing excessive autophagy and apoptosis in mice with sleep deprivation. Br J Pharmacol. 2019;176(9):1282–97.PubMedPubMedCentral
27.
Zurück zum Zitat Periasamya S, Hsua DZ, Fu HY, Liu MY. Sleep deprivation-induced multi-organ injury: role of oxidative stress and inflammation. EXCLI J. 2015;14:672–83. Periasamya S, Hsua DZ, Fu HY, Liu MY. Sleep deprivation-induced multi-organ injury: role of oxidative stress and inflammation. EXCLI J. 2015;14:672–83.
28.
Zurück zum Zitat Amaral FGD, Cipolla-Neto J. A brief review about melatonin, a pineal hormone. Arch Endocrinol Metab. 2018;62(4):472–9.PubMed Amaral FGD, Cipolla-Neto J. A brief review about melatonin, a pineal hormone. Arch Endocrinol Metab. 2018;62(4):472–9.PubMed
29.
Zurück zum Zitat Hardeland R, Madrid JA, Tan DX, Reiter RJ. Melatonin, the circadian multioscillator system and health: the need for detailed analyses of peripheral melatonin signaling. J Pineal Res. 2012;52(2):139–66.PubMed Hardeland R, Madrid JA, Tan DX, Reiter RJ. Melatonin, the circadian multioscillator system and health: the need for detailed analyses of peripheral melatonin signaling. J Pineal Res. 2012;52(2):139–66.PubMed
30.
Zurück zum Zitat Katkar GD, Sundaram MS, Hemshekhar M, Sharma DR, Santhosh MS, Sunitha K, et al. Melatonin alleviates Echis carinatus venom-induced toxicities by modulating inflammatory mediators and oxidative stress. J Pineal Res. 2014;56(3):295–312.PubMed Katkar GD, Sundaram MS, Hemshekhar M, Sharma DR, Santhosh MS, Sunitha K, et al. Melatonin alleviates Echis carinatus venom-induced toxicities by modulating inflammatory mediators and oxidative stress. J Pineal Res. 2014;56(3):295–312.PubMed
31.
Zurück zum Zitat Xu J, Sun S, Wei W, Fu J, Qi W, Manchester LC, et al. Melatonin reduces mortality and oxidatively mediated hepatic and renal damage due to diquat treatment. J Pineal Res. 2007;42(2):166–71.PubMed Xu J, Sun S, Wei W, Fu J, Qi W, Manchester LC, et al. Melatonin reduces mortality and oxidatively mediated hepatic and renal damage due to diquat treatment. J Pineal Res. 2007;42(2):166–71.PubMed
32.
Zurück zum Zitat Huang CT, Chiang RP, Chen CL, Tsai YJ. Sleep deprivation aggravates median nerve injury-induced neuropathic pain and enhances microglial activation by suppressing melatonin secretion. Sleep. 2014;37(9):1513–23.PubMedPubMedCentral Huang CT, Chiang RP, Chen CL, Tsai YJ. Sleep deprivation aggravates median nerve injury-induced neuropathic pain and enhances microglial activation by suppressing melatonin secretion. Sleep. 2014;37(9):1513–23.PubMedPubMedCentral
33.
Zurück zum Zitat Acuña-Castroviejo D, Rahim I, Acuña-Fernández C, Fernández-Ortiz M, Solera-Marín J, Sayed RKA, et al. Melatonin, clock genes and mitochondria in sepsis. Cell Mol Life Sci CMLS. 2017;74(21):3965–87.PubMed Acuña-Castroviejo D, Rahim I, Acuña-Fernández C, Fernández-Ortiz M, Solera-Marín J, Sayed RKA, et al. Melatonin, clock genes and mitochondria in sepsis. Cell Mol Life Sci CMLS. 2017;74(21):3965–87.PubMed
34.
Zurück zum Zitat Yaprak M, Altun A, Vardar A, Aktoz M, Ciftci S, Ozbay G. Decreased nocturnal synthesis of melatonin in patients with coronary artery disease. Int J Cardiol. 2003;89(1):103–7.PubMed Yaprak M, Altun A, Vardar A, Aktoz M, Ciftci S, Ozbay G. Decreased nocturnal synthesis of melatonin in patients with coronary artery disease. Int J Cardiol. 2003;89(1):103–7.PubMed
35.
Zurück zum Zitat Pontes GN, Cardoso EC, Carneiro-Sampaio MM, Markus RP. Pineal melatonin and the innate immune response: the TNF-alpha increase after cesarean section suppresses nocturnal melatonin production. J Pineal Res. 2007;43(4):365–71.PubMed Pontes GN, Cardoso EC, Carneiro-Sampaio MM, Markus RP. Pineal melatonin and the innate immune response: the TNF-alpha increase after cesarean section suppresses nocturnal melatonin production. J Pineal Res. 2007;43(4):365–71.PubMed
36.
Zurück zum Zitat da Silveira C-M, Carvalho-Sousa CE, Tamura EK, Pinato L, Cecon E, Fernandes PACM, et al. TLR4 and CD14 receptors expressed in rat pineal gland trigger NFKB pathway. J Pineal Res. 2010;49(2):183–92. da Silveira C-M, Carvalho-Sousa CE, Tamura EK, Pinato L, Cecon E, Fernandes PACM, et al. TLR4 and CD14 receptors expressed in rat pineal gland trigger NFKB pathway. J Pineal Res. 2010;49(2):183–92.
37.
Zurück zum Zitat da Silveira C-M, Pinato L, Tamura EK, Carvalho-Sousa CE, Markus RP. Glia-pinealocyte network: the paracrine modulation of melatonin synthesis by tumor necrosis factor (TNF). PLoS ONE. 2012;7(7):e40142. da Silveira C-M, Pinato L, Tamura EK, Carvalho-Sousa CE, Markus RP. Glia-pinealocyte network: the paracrine modulation of melatonin synthesis by tumor necrosis factor (TNF). PLoS ONE. 2012;7(7):e40142.
38.
Zurück zum Zitat Wang H, Wei W, Zhang SY, Shen YX, Yue L, Wang NP, et al. Melatonin-selenium nanoparticles inhibit oxidative stress and protect against hepatic injury induced by Bacillus Calmette-Guérin/lipopolysaccharide in mice. J Pineal Res. 2005;39(2):156–63.PubMed Wang H, Wei W, Zhang SY, Shen YX, Yue L, Wang NP, et al. Melatonin-selenium nanoparticles inhibit oxidative stress and protect against hepatic injury induced by Bacillus Calmette-Guérin/lipopolysaccharide in mice. J Pineal Res. 2005;39(2):156–63.PubMed
39.
Zurück zum Zitat Wang H, Xu DX, Lv JW, Ning H, Wei W. Melatonin attenuates lipopolysaccharide (LPS)-induced apoptotic liver damage in d-galactosamine-sensitized mice. Toxicology. 2007;237:49–57.PubMed Wang H, Xu DX, Lv JW, Ning H, Wei W. Melatonin attenuates lipopolysaccharide (LPS)-induced apoptotic liver damage in d-galactosamine-sensitized mice. Toxicology. 2007;237:49–57.PubMed
40.
Zurück zum Zitat Puig Á, Rancan L, Paredes SD, Carrasco A, Escames G, Vara E, et al. Melatonin decreases the expression of inflammation and apoptosis markers in the lung of a senescence-accelerated mice model. Exp Gerontol. 2016;75:1–7.PubMed Puig Á, Rancan L, Paredes SD, Carrasco A, Escames G, Vara E, et al. Melatonin decreases the expression of inflammation and apoptosis markers in the lung of a senescence-accelerated mice model. Exp Gerontol. 2016;75:1–7.PubMed
41.
Zurück zum Zitat Gao T, Wang Z, Dong Y, Cao J, Lin R, Wang X, et al. Role of melatonin in sleep deprivation-induced intestinal barrier dysfunction in mice. J Pineal Res. 2019;67(1):e12574.PubMed Gao T, Wang Z, Dong Y, Cao J, Lin R, Wang X, et al. Role of melatonin in sleep deprivation-induced intestinal barrier dysfunction in mice. J Pineal Res. 2019;67(1):e12574.PubMed
Metadaten
Titel
Sleep deprivation aggravated lipopolysaccharide/d-galactosamine-induced acute liver injury by suppressing melatonin production
verfasst von
Lu Liu
Li Zhang
Longjiang Li
Mengting Chen
Zhe Wang
Yi Shen
Jiayi Huang
Ling Tang
Publikationsdatum
18.08.2020
Verlag
Springer International Publishing
Erschienen in
Inflammation Research / Ausgabe 11/2020
Print ISSN: 1023-3830
Elektronische ISSN: 1420-908X
DOI
https://doi.org/10.1007/s00011-020-01393-3

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