The role of sleep deprivation in streptozotocin-induced Alzheimer's disease-like sporadic dementia in rats with respect to the serum level of oxidative and inflammatory markers.
Inflammation
Oxidative stress
Sleep deprivation (SD)
Spatial memory
Streptozotocin (STZ)
Journal
Experimental brain research
ISSN: 1432-1106
Titre abrégé: Exp Brain Res
Pays: Germany
ID NLM: 0043312
Informations de publication
Date de publication:
Dec 2022
Dec 2022
Historique:
received:
21
07
2022
accepted:
22
09
2022
pubmed:
28
10
2022
medline:
24
11
2022
entrez:
27
10
2022
Statut:
ppublish
Résumé
Numerous studies have shown the deleterious effects of sleep deprivation (SD) on memory. However, SD in various durations may induce different effects. Studies have reported that short-term or acute SD can improve cognitive functions. In addition, streptozotocin (STZ) significantly impairs learning and memory, and induces inflammation and oxidative stress. In this study, we aimed to investigate the effect of two types of SD (short term: 6 h; long term: 24 h) on STZ-induced spatial memory impairment in rats, with respect to the serum level of catalase (CAT), malondialdehyde (MDA), glutathione (GSH), superoxide dismutase (SOD), tumor necrosis factor alpha (TNF-α), interleukin-6 (IL-6), and interleukin-1beta (IL-1β). Morris water maze apparatus was used to assess spatial memory performance and STZ was injected i.c.v., twice, and at the dose of 3 mg/kg, at an interval of 48 h. The results showed that only 24 h SD impaired spatial learning and memory in rats. In addition, 24 h SD attenuated anti-oxidant activity and increased the level of pro-inflammatory markers in the serum. STZ impaired spatial learning and memory, and attenuated anti-oxidant activity and increased the level of pro-inflammatory markers in the serum of rats. Furthermore, 6 h SD slightly and partially improved spatial memory and significantly improved anti-oxidant activity in rats, with no effect on STZ-induced inflammation. We suggest that STZ has more important mechanisms that are involved in its memory impairment effect, and maybe, STZ-induced inflammation has a more important role. We also suggest more detailed studies to investigate the potential therapeutic effect of SD (in different durations) on memory function, oxidative stress, and inflammation.
Identifiants
pubmed: 36301335
doi: 10.1007/s00221-022-06471-y
pii: 10.1007/s00221-022-06471-y
doi:
Substances chimiques
Streptozocin
5W494URQ81
Antioxidants
0
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3259-3270Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Afzal M, Al-Abbasi FA, Kazmi I, Imam SS, Alshehri S, Ghoneim MM, Almalki WH, Nadeem MS, Sayyed N (2021) Fustin inhibits oxidative free radicals and inflammatory cytokines in cerebral cortex and hippocampus and protects cognitive impairment in streptozotocin-induced diabetic rats. ACS Chem Neurosci 12(24):4587–4597. https://doi.org/10.1021/acschemneuro.1c00712
doi: 10.1021/acschemneuro.1c00712
pubmed: 34860003
Alfaris NA, Alshammari GM, Altamimi JZ, Aljabryn DH, Alagal RI, Aldera H, Alkhateeb MA, Yahya MA (2021) Ellagic acid prevents streptozotocin-induced hippocampal damage and memory loss in rats by stimulating Nrf2 and nuclear factor-kappaB, and activating insulin receptor substrate/PI3K/Akt axis. J Physiol Pharmacol. https://doi.org/10.26402/jpp.2021.4.02
doi: 10.26402/jpp.2021.4.02
pubmed: 34987124
Alluri R, Ambati SR, Routhu K, Kopalli SR, Koppula S (2020) Phosphoinositide 3-kinase inhibitor AS605240 ameliorates streptozotocin-induced Alzheimer’s disease like sporadic dementia in experimental rats. EXCLI J 19:71–85. https://doi.org/10.17179/excli2019-1997
doi: 10.17179/excli2019-1997
pubmed: 32038117
pmcid: 7003642
Alzoubi KH, Malkawi BS, Khabour OF, El-Elimat T, Alali FQ (2018) Arbutus andrachne L. reverses sleep deprivation-induced memory impairments in rats. Mol Neurobiol 55(2):1150–1156. https://doi.org/10.1007/s12035-017-0387-8
doi: 10.1007/s12035-017-0387-8
pubmed: 28101814
Alzoubi KH, Al Mosabih HS, Mahasneh AF (2019a) The protective effect of edaravone on memory impairment induced by chronic sleep deprivation. Psychiatry Res 281:112577. https://doi.org/10.1016/j.psychres.2019.112577
doi: 10.1016/j.psychres.2019.112577
pubmed: 31586841
Alzoubi KH, Mayyas F, Abu Zamzam HI (2019b) Omega-3 fatty acids protects against chronic sleep-deprivation induced memory impairment. Life Sci 227:1–7. https://doi.org/10.1016/j.lfs.2019.04.028
doi: 10.1016/j.lfs.2019.04.028
pubmed: 30998938
Alzoubi KH, Al-Jamal FF, Mahasneh AF (2020) Cerebrolysin prevents sleep deprivation induced memory impairment and oxidative stress. Physiol Behav 217:112823. https://doi.org/10.1016/j.physbeh.2020.112823
doi: 10.1016/j.physbeh.2020.112823
pubmed: 31987894
Asghari AA, Hosseini M, Bafadam S, Rakhshandeh H, Farazandeh M, Mahmoudabady M (2022) Olea europaea L. (olive) leaf extract ameliorates learning and memory deficits in streptozotocin-induced diabetic rats. Avicenna J Phytomed 12(2):163–174. https://doi.org/10.22038/AJP.2021.18989
doi: 10.22038/AJP.2021.18989
pubmed: 35614890
pmcid: 9090319
Azogu I, de la Tremblaye PB, Dunbar M, Lebreton M, LeMarec N, Plamondon H (2015) Acute sleep deprivation enhances avoidance learning and spatial memory and induces delayed alterations in neurochemical expression of GR, TH, DRD1, pCREB and Ki67 in rats. Behav Brain Res 279:177–190. https://doi.org/10.1016/j.bbr.2014.11.015
doi: 10.1016/j.bbr.2014.11.015
pubmed: 25433096
Busche MA, Kekus M, Forstl H (2017) Connections between sleep and Alzheimer’s disease: insomnia, amnesia and amyloid. Nervenarzt 88(3):215–221. https://doi.org/10.1007/s00115-016-0122-0
doi: 10.1007/s00115-016-0122-0
pubmed: 27251738
Cakir A, Ocalan B, Koc C, Suyen GG, Cansev M, Kahveci N (2020) Effects of CDP-choline administration on learning and memory in REM sleep-deprived rats. Physiol Behav 213:112703. https://doi.org/10.1016/j.physbeh.2019.112703
doi: 10.1016/j.physbeh.2019.112703
pubmed: 31654682
Cheng O, Li R, Zhao L, Yu L, Yang B, Wang J, Chen B, Yang J (2015) Short-term sleep deprivation stimulates hippocampal neurogenesis in rats following global cerebral ischemia/reperfusion. PLoS One 10(6):e0125877. https://doi.org/10.1371/journal.pone.0125877
doi: 10.1371/journal.pone.0125877
pubmed: 26039740
pmcid: 4454510
Dhami M, Raj K, Singh S (2021) Neuroprotective effect of fucoxanthin against intracerebroventricular streptozotocin (ICV-STZ) induced cognitive impairment in experimental rats. Curr Alzheimer Res 18(8):623–637. https://doi.org/10.2174/1567205018666211118144602
doi: 10.2174/1567205018666211118144602
pubmed: 34792011
Erfanizadeh M, Noorafshan A, Namavar MR, Karbalay-Doust S, Talaei-Khozani T (2020) Curcumin prevents neuronal loss and structural changes in the superior cervical (sympathetic) ganglion induced by chronic sleep deprivation, in the rat model. Biol Res 53(1):31. https://doi.org/10.1186/s40659-020-00300-8
doi: 10.1186/s40659-020-00300-8
pubmed: 32650839
pmcid: 7350621
Giacobbo BL, Correa MS, Vedovelli K, de Souza CE, Spitza LM, Goncalves L, Paludo N, Molina RD, da Rosa ED, Argimon II, Bromberg E (2016) Could BDNF be involved in compensatory mechanisms to maintain cognitive performance despite acute sleep deprivation? An exploratory study. Int J Psychophysiol 99:96–102. https://doi.org/10.1016/j.ijpsycho.2015.11.008
doi: 10.1016/j.ijpsycho.2015.11.008
pubmed: 26602839
Gopalakrishnan A, Ji LL, Cirelli C (2004) Sleep deprivation and cellular responses to oxidative stress. Sleep 27(1):27–35. https://doi.org/10.1093/sleep/27.1.27
doi: 10.1093/sleep/27.1.27
pubmed: 14998234
Green TRF, Ortiz JB, Wonnacott S, Williams RJ, Rowe RK (2020) The bidirectional relationship between sleep and inflammation links traumatic brain injury and Alzheimer’s disease. Front Neurosci 14:894. https://doi.org/10.3389/fnins.2020.00894
doi: 10.3389/fnins.2020.00894
pubmed: 32982677
pmcid: 7479838
Grieb P (2016) Intracerebroventricular streptozotocin injections as a model of Alzheimer’s disease: in search of a relevant mechanism. Mol Neurobiol 53(3):1741–1752. https://doi.org/10.1007/s12035-015-9132-3
doi: 10.1007/s12035-015-9132-3
pubmed: 25744568
Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297(5580):353–356. https://doi.org/10.1126/science.1072994
doi: 10.1126/science.1072994
pubmed: 12130773
Hasan N, Zameer S, Najmi AK, Parvez S, Akhtar M (2022) Roflumilast reduces pathological symptoms of sporadic Alzheimer’s disease in rats produced by intracerebroventricular streptozotocin by inhibiting NF-kappaB/BACE-1 mediated abeta production in the hippocampus and activating the cAMP/BDNF signalling pathway. Neurotox Res 40(2):432–448. https://doi.org/10.1007/s12640-022-00482-x
doi: 10.1007/s12640-022-00482-x
pubmed: 35192144
Hennecke E, Lange D, Steenbergen F, Fronczek-Poncelet J, Elmenhorst D, Bauer A, Aeschbach D, Elmenhorst EM (2021) Adverse interaction effects of chronic and acute sleep deficits on spatial working memory but not on verbal working memory or declarative memory. J Sleep Res 30(4):e13225. https://doi.org/10.1111/jsr.13225
doi: 10.1111/jsr.13225
pubmed: 33169493
Irwin MR, Olmstead R, Carroll JE (2016) Sleep disturbance, sleep duration, and inflammation: a systematic review and meta-analysis of cohort studies and experimental sleep deprivation. Biol Psychiatry 80(1):40–52. https://doi.org/10.1016/j.biopsych.2015.05.014
doi: 10.1016/j.biopsych.2015.05.014
pubmed: 26140821
Javad-Moosavi BZ, Nasehi M, Vaseghi S, Jamaldini SH, Zarrindast MR (2020) Activation and inactivation of nicotinic receptnors in the dorsal hippocampal region restored negative effects of total (TSD) and REM sleep deprivation (RSD) on memory acquisition, locomotor activity and pain perception. Neuroscience 433:200–211. https://doi.org/10.1016/j.neuroscience.2020.03.006
doi: 10.1016/j.neuroscience.2020.03.006
pubmed: 32200080
Junek A, Rusak B, Semba K (2010) Short-term sleep deprivation may alter the dynamics of hippocampal cell proliferation in adult rats. Neuroscience 170(4):1140–1152. https://doi.org/10.1016/j.neuroscience.2010.08.018
doi: 10.1016/j.neuroscience.2010.08.018
pubmed: 20727388
Kang X, Jiang L, Lan F, Tang YY, Zhang P, Zou W, Chen YJ, Tang XQ (2021) Hydrogen sulfide antagonizes sleep deprivation-induced depression- and anxiety-like behaviors by inhibiting neuroinflammation in a hippocampal Sirt1-dependent manner. Brain Res Bull 177:194–202. https://doi.org/10.1016/j.brainresbull.2021.10.002
doi: 10.1016/j.brainresbull.2021.10.002
pubmed: 34624463
Konakanchi S, Raavi V, Ml HK, Shankar Ms V (2021) Effect of chronic sleep deprivation and sleep recovery on hippocampal CA3 neurons, spatial memory and anxiety-like behavior in rats. Neurobiol Learn Mem 187:107559. https://doi.org/10.1016/j.nlm.2021.107559
doi: 10.1016/j.nlm.2021.107559
pubmed: 34808338
Konakanchi S, Raavi V, Ml HK, Shankar Ms V (2022) Effect of chronic sleep deprivation and sleep recovery on hippocampal CA3 neurons, spatial memory and anxiety-like behavior in rats. Neurobiol Learn Mem 187:107559. https://doi.org/10.1016/j.nlm.2021.107559
doi: 10.1016/j.nlm.2021.107559
pubmed: 34808338
Lee Y, Kim YH, Park SJ, Huh JW, Kim SH, Kim SU, Kim JS, Jeong KJ, Lee KM, Hong Y, Lee SR, Chang KT (2014) Insulin/IGF signaling-related gene expression in the brain of a sporadic Alzheimer’s disease monkey model induced by intracerebroventricular injection of streptozotocin. J Alzheimers Dis 38(2):251–267. https://doi.org/10.3233/JAD-130776
doi: 10.3233/JAD-130776
pubmed: 23948941
Lima AM, de Bruin VM, Rios ER, de Bruin PF (2014) Differential effects of paradoxical sleep deprivation on memory and oxidative stress. Naunyn Schmiedebergs Arch Pharmacol 387(5):399–406. https://doi.org/10.1007/s00210-013-0955-z
doi: 10.1007/s00210-013-0955-z
pubmed: 24424716
Liu P, Zhao B, Wei M, Li Y, Liu J, Ma L, Shang S, Huo K, Wang J, Li R, Qu Q (2020) Activation of inflammation is associated with amyloid-beta accumulation induced by chronic sleep restriction in rats. J Alzheimers Dis 74(3):759–773. https://doi.org/10.3233/JAD-191317
doi: 10.3233/JAD-191317
pubmed: 32083588
Liu W, Li J, Yang M, Ke X, Dai Y, Lin H, Wang S, Chen L, Tao J (2022) Chemical genetic activation of the cholinergic basal forebrain hippocampal circuit rescues memory loss in Alzheimer’s disease. Alzheimers Res Ther 14(1):53. https://doi.org/10.1186/s13195-022-00994-w
doi: 10.1186/s13195-022-00994-w
pubmed: 35418161
pmcid: 9006585
LootiBashiyan M, Nasehi M, Vaseghi S, Khalifeh S (2021) Investigating the effect of crocin on memory deficits induced by total sleep deprivation (TSD) with respect to the BDNF, TrkB and ERK levels in the hippocampus of male Wistar rats. J Psychopharmacol. https://doi.org/10.1177/02698811211000762
doi: 10.1177/02698811211000762
Maglasang MNA, Frolov A, Guzman M, Echols S, Daly D (2022) Cerebral vascular density and its possible correlation with Alzheimer disease progression in elderly individuals with rheumatoid arthritis. FASEB J 36(Suppl):1. https://doi.org/10.1096/fasebj.2022.36.S1.L6386
doi: 10.1096/fasebj.2022.36.S1.L6386
Mahboubi S, Nasehi M, Imani A, Sadat-Shirazi MS, Zarrindast MR, Vousooghi N, Noroozian M (2019) Benefit effect of REM-sleep deprivation on memory impairment induced by intensive exercise in male wistar rats: with respect to hippocampal BDNF and TrkB. Nat Sci Sleep 11:179–188. https://doi.org/10.2147/NSS.S207339
doi: 10.2147/NSS.S207339
pubmed: 31576186
pmcid: 6767759
Mahdavi MS, Nasehi M, Vaseghi S, Mousavi Z, Zarrindast MR (2021) The effect of alpha lipoic acid on passive avoidance and social interaction memory, pain perception, and locomotor activity in REM sleep-deprived rats. Pharmacol Rep 73(1):102–110. https://doi.org/10.1007/s43440-020-00161-8
doi: 10.1007/s43440-020-00161-8
pubmed: 33000413
Manchanda S, Singh H, Kaur T, Kaur G (2018) Low-grade neuroinflammation due to chronic sleep deprivation results in anxiety and learning and memory impairments. Mol Cell Biochem 449(1–2):63–72. https://doi.org/10.1007/s11010-018-3343-7
doi: 10.1007/s11010-018-3343-7
pubmed: 29549603
Mander BA, Winer JR, Jagust WJ, Walker MP (2016) Sleep: a novel mechanistic pathway, biomarker, and treatment target in the pathology of Alzheimer’s disease? Trends Neurosci 39(8):552–566. https://doi.org/10.1016/j.tins.2016.05.002
doi: 10.1016/j.tins.2016.05.002
pubmed: 27325209
pmcid: 4967375
Massadeh AM, Alzoubi KH, Milhem AM, Rababa’h AM, Khabour OF (2022) Evaluating the effect of selenium on spatial memory impairment induced by sleep deprivation. Physiol Behav 244:113669. https://doi.org/10.1016/j.physbeh.2021.113669
doi: 10.1016/j.physbeh.2021.113669
pubmed: 34871651
Mehla J, Pahuja M, Gupta YK (2013) Streptozotocin-induced sporadic Alzheimer’s disease: selection of appropriate dose. J Alzheimers Dis 33(1):17–21. https://doi.org/10.3233/JAD-2012-120958
doi: 10.3233/JAD-2012-120958
pubmed: 22886014
Misrani A, Tabassum S, Yang L (2021) Mitochondrial dysfunction and oxidative stress in Alzheimer’s disease. Front Aging Neurosci 13:617588. https://doi.org/10.3389/fnagi.2021.617588
doi: 10.3389/fnagi.2021.617588
pubmed: 33679375
pmcid: 7930231
Moldovan M, Constantinescu AO, Balseanu A, Oprescu N, Zagrean L, Popa-Wagner A (2010) Sleep deprivation attenuates experimental stroke severity in rats. Exp Neurol 222(1):135–143. https://doi.org/10.1016/j.expneurol.2009.12.023
doi: 10.1016/j.expneurol.2009.12.023
pubmed: 20045410
Moreira-Silva D, Vizin RCL, Martins TMS, Ferreira TL, Almeida MC, Carrettiero DC (2019) Intracerebral injection of streptozotocin to model Alzheimer disease in rats. Bio Protoc 9(20):e3397. https://doi.org/10.21769/BioProtoc.3397
doi: 10.21769/BioProtoc.3397
pubmed: 33654898
pmcid: 7853929
Norozpour Y, Nasehi M, Sabouri-Khanghah V, Nami M, Vaseghi S, Zarrindast MR (2020) The effect of alpha-2 adrenergic receptors on memory retention deficit induced by rapid eye movement sleep deprivation. Iran J Basic Med Sci 23(12):1571–1575. https://doi.org/10.22038/ijbms.2020.44891.10468
doi: 10.22038/ijbms.2020.44891.10468
pubmed: 33489031
pmcid: 7811809
Olonode ET, Aderibigbe AO, Adeoluwa OA, Eduviere AT, Ben-Azu B (2019) Morin hydrate mitigates rapid eye movement sleep deprivation-induced neurobehavioural impairments and loss of viable neurons in the hippocampus of mice. Behav Brain Res 356:518–525. https://doi.org/10.1016/j.bbr.2017.12.024
doi: 10.1016/j.bbr.2017.12.024
pubmed: 29284109
Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Academic Press, London
Ramanathan L, Siegel JM (2011) Sleep deprivation under sustained hypoxia protects against oxidative stress. Free Radic Biol Med 51(10):1842–1848. https://doi.org/10.1016/j.freeradbiomed.2011.08.016
doi: 10.1016/j.freeradbiomed.2011.08.016
pubmed: 21907278
pmcid: 3197752
Ramanathan L, Hu S, Frautschy SA, Siegel JM (2010) Short-term total sleep deprivation in the rat increases antioxidant responses in multiple brain regions without impairing spontaneous alternation behavior. Behav Brain Res 207(2):305–309. https://doi.org/10.1016/j.bbr.2009.10.014
doi: 10.1016/j.bbr.2009.10.014
pubmed: 19850085
Sahin L, Cevik OS, Cevik K, Guven C, Taskin E, Kocahan S (2021) Mild regular treadmill exercise ameliorated the detrimental effects of acute sleep deprivation on spatial memory. Brain Res 1759:147367. https://doi.org/10.1016/j.brainres.2021.147367
doi: 10.1016/j.brainres.2021.147367
pubmed: 33582122
Scheff SW, Price DA, Schmitt FA, Mufson EJ (2006) Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging 27(10):1372–1384. https://doi.org/10.1016/j.neurobiolaging.2005.09.012
doi: 10.1016/j.neurobiolaging.2005.09.012
pubmed: 16289476
Shang J, Che S, Zhu M (2022) Oleuropein improves cognitive dysfunction and neuroinflammation in diabetic rats through the PI3K/Akt/mTOR pathway. Appl Bionics Biomech 2022:5892463. https://doi.org/10.1155/2022/5892463
doi: 10.1155/2022/5892463
pubmed: 35528541
pmcid: 9071920
Shi HS, Luo YX, Xue YX, Wu P, Zhu WL, Ding ZB, Lu L (2011) Effects of sleep deprivation on retrieval and reconsolidation of morphine reward memory in rats. Pharmacol Biochem Behav 98(2):299–303. https://doi.org/10.1016/j.pbb.2011.01.006
doi: 10.1016/j.pbb.2011.01.006
pubmed: 21255602
Spano GM, Banningh SW, Marshall W, de Vivo L, Bellesi M, Loschky SS, Tononi G, Cirelli C (2019) Sleep deprivation by exposure to novel objects increases synapse density and axon-spine interface in the hippocampal CA1 region of adolescent mice. J Neurosci 39(34):6613–6625. https://doi.org/10.1523/JNEUROSCI.0380-19.2019
doi: 10.1523/JNEUROSCI.0380-19.2019
pubmed: 31263066
pmcid: 6703893
Sun L, Dou X, Yang W (2022) Propofol protects rats against intra-cerebroventricular streptozotocin-induced cognitive dysfunction and neuronal damage. Folia Morphol (Warsz). https://doi.org/10.5603/FM.a2022.0027
doi: 10.5603/FM.a2022.0027
Tang H, Li K, Dou X, Zhao Y, Huang C, Shu F (2020) The neuroprotective effect of osthole against chronic sleep deprivation (CSD)-induced memory impairment in rats. Life Sci 263:118524. https://doi.org/10.1016/j.lfs.2020.118524
doi: 10.1016/j.lfs.2020.118524
pubmed: 33011218
Torabi Z, Rezaie M, Aramvash A, Nasiri-Khalili MA, Nasehi M, Abedi B, Vaseghi S (2022) Interaction of lithium and sleep deprivation on memory performance and anxiety-like behavior in male Wistar rats. Behav Brain Res. https://doi.org/10.1016/j.bbr.2022.113890
doi: 10.1016/j.bbr.2022.113890
pubmed: 35413328
Turkez H, Arslan ME, Barboza JN, Kahraman CY, de Sousa DP, Mardinoglu A (2021) Therapeutic potential of ferulic acid in Alzheimer’s disease. Curr Drug Deliv. https://doi.org/10.2174/1567201819666211228153801
doi: 10.2174/1567201819666211228153801
pubmed: 33109049
Urrestarazu E, Iriarte J (2016) Clinical management of sleep disturbances in Alzheimer’s disease: current and emerging strategies. Nat Sci Sleep 8:21–33. https://doi.org/10.2147/NSS.S76706
doi: 10.2147/NSS.S76706
pubmed: 26834500
pmcid: 4716729
Vaseghi S, Babapour V, Nasehi M, Zarrindast MR (2018) The role of CA1 CB1 receptors on lithium-induced spatial memory impairment in rats. EXCLI J 17:916–934. https://doi.org/10.17179/excli2018-1511
doi: 10.17179/excli2018-1511
pubmed: 30564071
pmcid: 6295625
Vaseghi S, Babapour V, Nasehi M, Zarrindast MR (2020) Synergistic but not additive effect between ACPA and lithium in the dorsal hippocampal region on spatial learning and memory in rats: isobolographic analyses. Chem Biol Interact 315:108895. https://doi.org/10.1016/j.cbi.2019.108895
doi: 10.1016/j.cbi.2019.108895
pubmed: 31715133
Vaseghi S, Arjmandi-Rad S, Kholghi G, Nasehi M (2021) Inconsistent effects of sleep deprivation on memory function. EXCLI J 20:1011–1027. https://doi.org/10.17179/excli2021-3764
doi: 10.17179/excli2021-3764
pubmed: 34267613
pmcid: 8278215
Villafuerte G, Miguel-Puga A, Rodriguez EM, Machado S, Manjarrez E, Arias-Carrion O (2015) Sleep deprivation and oxidative stress in animal models: a systematic review. Oxid Med Cell Longev 2015:234952. https://doi.org/10.1155/2015/234952
doi: 10.1155/2015/234952
pubmed: 25945148
pmcid: 4402503
Wadhwa M, Kumari P, Chauhan G, Roy K, Alam S, Kishore K, Ray K, Panjwani U (2017) Sleep deprivation induces spatial memory impairment by altered hippocampus neuroinflammatory responses and glial cells activation in rats. J Neuroimmunol 312:38–48. https://doi.org/10.1016/j.jneuroim.2017.09.003
doi: 10.1016/j.jneuroim.2017.09.003
pubmed: 28912034
Wadhwa M, Prabhakar A, Anand JP, Ray K, Prasad D, Kumar B, Panjwani U (2019) Complement activation sustains neuroinflammation and deteriorates adult neurogenesis and spatial memory impairment in rat hippocampus following sleep deprivation. Brain Behav Immun 82:129–144. https://doi.org/10.1016/j.bbi.2019.08.004
doi: 10.1016/j.bbi.2019.08.004
pubmed: 31408672
Wang D, Kowalewski EK, Koch G (2022) Application of meta-analysis to evaluate relationships among ARIA-E rate, amyloid reduction rate, and clinical cognitive response in amyloid therapeutic clinical trials for early Alzheimer’s disease. Ther Innov Regul Sci 56(3):501–516. https://doi.org/10.1007/s43441-022-00390-4
doi: 10.1007/s43441-022-00390-4
pubmed: 35320578
Weil ZM, Norman GJ, Karelina K, Morris JS, Barker JM, Su AJ, Walton JC, Bohinc S, Nelson RJ, DeVries AC (2009) Sleep deprivation attenuates inflammatory responses and ischemic cell death. Exp Neurol 218(1):129–136. https://doi.org/10.1016/j.expneurol.2009.04.018
doi: 10.1016/j.expneurol.2009.04.018
pubmed: 19409382
pmcid: 2696570
Wu M, Zhang M, Yin X, Chen K, Hu Z, Zhou Q, Cao X, Chen Z, Liu D (2021) The role of pathological tau in synaptic dysfunction in Alzheimer’s diseases. Transl Neurodegener 10(1):45. https://doi.org/10.1186/s40035-021-00270-1
doi: 10.1186/s40035-021-00270-1
pubmed: 34753506
pmcid: 8579533
Yao ZY, Li XH, Zuo L, Xiong Q, He WT, Li DX, Dong ZF (2022) Maternal sleep deprivation induces gut microbial dysbiosis and neuroinflammation in offspring rats. Zool Res 43(3):380–390. https://doi.org/10.24272/j.issn.2095-8137.2022.023
doi: 10.24272/j.issn.2095-8137.2022.023
pubmed: 35362675
pmcid: 9113977
Yeo HG, Lee Y, Jeon CY, Jeong KJ, Jin YB, Kang P, Kim SU, Kim JS, Huh JW, Kim YH, Sim BW, Song BS, Park YH, Hong Y, Lee SR, Chang KT (2015) Characterization of cerebral damage in a monkey model of Alzheimer’s disease induced by intracerebroventricular injection of streptozotocin. J Alzheimers Dis 46(4):989–1005. https://doi.org/10.3233/JAD-143222
doi: 10.3233/JAD-143222
pubmed: 25881906
Zhao HL, Cui SY, Qin Y, Liu YT, Cui XY, Hu X, Kurban N, Li MY, Li ZH, Xu J, Zhang YH (2021) Prophylactic effects of sporoderm-removed Ganoderma lucidum spores in a rat model of streptozotocin-induced sporadic Alzheimer’s disease. J Ethnopharmacol 269:113725. https://doi.org/10.1016/j.jep.2020.113725
doi: 10.1016/j.jep.2020.113725
pubmed: 33352241