Alzheimer’s disease (AD) is the most common age-associated neurodegenerative disease featured by progressive learning and memory deficit, and Aβ was identified as playing a key role in the process of AD and was theorized to be caused by the imbalance of production and clearance. Increasing evidence suggested an association between sleep deprivation and AD. Our recent study found that chronic sleep restriction (CSR) caused cognitive impairment and Aβ accumulation in rats, but the underlining mechanism was unclear. In the present study, we investigated the effects of inflammation on Aβ accumulation induced by CSR. We found that CSR significantly increased the expression of interleukin-1β (IL-1β), tumor necrosis factor-α (TNF-α), inducible nitric oxide synthase (iNOS), and nitric oxide (NO) in brain, and the inflammatory factors levels were positively correlated with Aβ42 deposition. Additionally, the inflammatory factors were correlated with BACE1, LRP-1, and RAGE levels in both the hippocampus and the prefrontal cortex. Furthermore, the plasma levels of IL-1β, TNF-α, and NO were elevated after CSR, and the concentration of plasma inflammatory mediators were correlated with plasma levels of sLRP1 and sRAGE. These results suggested that the inflammation in brain and plasma might be involved in the CSR-induced Aβ accumulation.
MuirSW, SpeechleyM, WellsJ, BorrieM, GopaulK, Montero-OdassoM (2012) Gait assessment in mild cognitive impairment and Alzheimer’s disease: The effect of dual-task challenges across the cognitive spectrum. Gait Posture35, 96–100.
2.
PlantLD, WebsterNJ, BoyleJP, RamsdenM, FreirDB, PeersC, PearsonHA (2006) Amyloid beta peptide as a physiological modulator of neuronal ‘A’-type+current. Neurobiol Aging27, 1673–1683.
3.
BarageSH, SonawaneKD (2015) Amyloid cascade hypothesis: Pathogenesis and therapeutic strategies in Alzheimer’s disease. Neuropeptides52, 1–18.
4.
MastersCL, SelkoeDJ (2012) Biochemistry of amyloid beta-protein and amyloid deposits in Alzheimer disease. Cold Spring Harb Perspect Med2, a006262.
DeaneR, BellRD, SagareA, ZlokovicBV (2009) Clearance of amyloid-beta peptide across the blood-brain barrier: Implication for therapies in Alzheimer’s disease. CNS Neurol Disord Drug Targets8, 16–30.
7.
BellRD (2012) The imbalance of vascular molecules in Alzheimer’s disease. J Alzheimers Dis32, 699–709.
8.
CaiZ, LiuN, WangC, QinB, ZhouY, XiaoM, ChangL, YanLJ, ZhaoB (2016) Role of RAGE in Alzheimer’s disease. Cell Mol Neurobiol36, 483–495.
Shokri-KojoriE, WangGJ, WiersCE, DemiralSB, GuoM, KimSW, LindgrenE, RamirezV, ZehraA, FreemanC, MillerG, ManzaP, SrivastavaT, De SantiS, TomasiD, BenvenisteH, VolkowND (2018) beta-Amyloid accumulation in the human brain after one night of sleep deprivation. Proc Natl Acad Sci U S A115, 4483–4488.
16.
LuceyBP, HicksTJ, McLelandJS, ToedebuschCD, BoydJ, ElbertDL, PattersonBW, BatyJ, MorrisJC, OvodV, MawuenyegaKG, BatemanRJ (2018) Effect of sleep on overnight cerebrospinal fluid amyloid beta kinetics. Ann Neurol83, 197–204.
17.
ZhaoB, LiuP, WeiM, LiY, LiuJ, MaL, ShangS, JiangY, HuoK, WangJ, QuQ (2019) Chronic sleep restriction induces Abeta accumulation by disrupting the balance of Abeta production and clearance in rats. Neurochem Res44, 859–873.
18.
SeongKJ, LeeHG, KookMS, KoHM, JungJY, KimWJ (2016) Epigallocatechin-3-gallate rescues LPS-impaired adult hippocampal neurogenesis through suppressing the TLR4-NF-kappaB signaling pathway in mice. Korean J Physiol Pharmacol20, 41–51.
19.
ShearerWT, ReubenJM, MullingtonJM, PriceNJ, LeeBN, SmithEO, SzubaMP, Van DongenHP, DingesDF (2001) Soluble TNF-alpha receptor 1 and IL-6 plasma levels in humans subjected to the sleep deprivation model of spaceflight. J Allergy Clin Immunol107, 165–170.
20.
AminFU, ShahSA, BadshahH, KhanM, KimMO (2017) Anthocyanins encapsulated by PLGA@PEG nanoparticles potentially improved its free radical scavenging capabilities via p38/JNK pathway against Abeta1-42-induced oxidative stress. J Nanobiotechnology15, 12.
21.
LiuQ, ChenY, ShenC, XiaoY, WangY, LiuZ, LiuX (2017) Chicoric acid supplementation prevents systemic inflammation-induced memory impairment and amyloidogenesis via inhibition of NF-kappaB. FASEB J31, 1494–1507.
22.
McGeerPL, RogersJ, McGeerEG (2006) Inflammation, anti-inflammatory agents and Alzheimer disease: The last 12 years. J Alzheimers Dis9, 271–276.
23.
AsiimweN, YeoSG, KimMS, JungJ, JeongNY (2016) Nitric oxide: Exploring the contextual link with Alzheimer’s disease. Oxid Med Cell Longev2016, 7205747.
GalimbertiD, FenoglioC, LovatiC, VenturelliE, GuidiI, CorraB, ScalabriniD, ClericiF, MarianiC, BresolinN, ScarpiniE (2006) Serum MCP-1 levels are increased in mild cognitive impairment and mild Alzheimer’s disease. Neurobiol Aging27, 1763–1768.
26.
ZhaoJ, O’ConnorT, VassarR (2011) The contribution of activated astrocytes to Abeta production: Implications for Alzheimer’s disease pathogenesis. J Neuroinflammation8, 150.
27.
JinP, KimJA, ChoiDY, LeeYJ, JungHS, HongJT (2013) Anti-inflammatory and anti-amyloidogenic effects of a small molecule, 2,4-bis(p-hydroxyphenyl)-2-butenal in Tg2576 Alzheimer’s disease mice model. J Neuroinflammation10, 2.
28.
JaegerLB, DohguS, SultanaR, LynchJL, OwenJB, EricksonMA, ShahGN, PriceTO, Fleegal-DemottaMA, ButterfieldDA, BanksWA (2009) Lipopolysaccharide alters the blood-brain barrier transport of amyloid beta protein: A mechanism for inflammation in therogression of Alzheimer’s disease. Brain Behav Immun23, 507–517.
29.
RomanV, HagewoudR, LuitenPG, MeerloP (2006) Differential effects of chronic partial sleep deprivation and stress on serotonin-1A and muscarinic acetylcholine receptor sensitivity. J Sleep Res15, 386–394.
30.
ZielinskiMR, DavisJM, FadelJR, YoungstedtSD (2013) Influence of chronic moderate sleep restriction and exercise training on anxiety, spatial memory, and associated neurobiological measures in mice. Behav Brain Res250, 74–80.
31.
BaiY, ShaJ, KannoT, MiyamotoK, HideshimaK, MatsuzakiY (2019) Comparison of the bone regenerative capacity of three-dimensional uncalcined and unsintered hydroxyapatite/Poly-d/l-Lactide and beta-tricalcium phosphate used as bone graft substitutes. J Invest Surg, doi: 10.1080/08941939.2019.1616859.
32.
Seyed JafariSM, HungerRE (2017) IHC optical density score: A new practical method for quantitative immunohistochemistry image analysis. Appl Immunohistochem Mol Morphol25, e12–e13.
HeppnerFL, RansohoffRM, BecherB (2015) Immune attack: The role of inflammation in Alzheimer disease. Nat Rev Neurosci16, 358–372.
39.
McGeerPL, McGeerEG (2007) NSAIDs and Alzheimer disease: Epidemiological, animal model and clinical studies. Neurobiol Aging28, 639–647.
40.
MarchesiVT (2011) Alzheimer’s dementia begins as a disease of small blood vessels, damaged by oxidative-induced inflammation and dysregulated amyloid metabolism: Implications for early detection and therapy. FASEB J25, 5–13.
41.
HenekaMT, SastreM, Dumitrescu-OzimekL, DewachterI, WalterJ, KlockgetherT, Van LeuvenF (2005) Focal glial activation coincides with increased BACE1 activation and precedes amyloid plaque deposition in APP[V717I] transgenic mice. J Neuroinflammation2, 22.
42.
AldertonWK, CooperCE, KnowlesRG (2001) Nitric oxide synthases: Structure, function and inhibition. Biochem J357, 593–615.
43.
KarranE, MerckenM, De StrooperB (2011) The amyloid cascade hypothesis for Alzheimer’s disease: An appraisal for the development of therapeutics. Nat Rev Drug Discov10, 698–712.
44.
HuangW, LiZ, ZhaoL, ZhaoW (2017) Simvastatin ameliorate memory deficits and inflammation in clinical and mouse model of Alzheimer’s disease via modulating the expression of miR-106b. Biomed Pharmacother92, 46–57.
45.
Del ReyA, VerdenhalvenM, LorwaldAC, MeyerC, HernangomezM, RandolfA, RoggeroE, KonigAM, HeverhagenJT, GuazaC, BesedovskyHO (2016) Brain-borne IL-1 adjusts glucoregulation and provides fuel support to astrocytes and neurons in an autocrine/paracrine manner. Mol Psychiatry21, 1309–1320.
46.
da Cruz-HöflingMA, RapôsoC, VerinaudL, ZagoGM (2009) Neuroinflammation and astrocytic reaction in the course of Phoneutria nigriventer (armed-spider) blood–brain barrier (BBB) opening. Neurotoxicology30, 636–646.
VivianiB, BartesaghiS, CorsiniE, GalliCL, MarinovichM (2004) Cytokines role in neurodegenerative events. Toxicol Lett149, 85–89.
49.
SastreM, DewachterI, LandrethGE, WillsonTM, KlockgetherT, van LeuvenF, HenekaMT (2003) Nonsteroidal anti-inflammatory drugs and peroxisome proliferator-activated receptor-gamma agonists modulate immunostimulated processing of amyloid precursor protein through regulation of beta-secretase. J Neurosci23, 9796–9804.
50.
KitazawaM, HsuHW, MedeirosR (2016) Copper exposure perturbs brain inflammatory responses and impairs clearance of amyloid-beta. Toxicol Sci152, 194–204.
51.
RealeM, IarloriC, FelicianiC, GambiD (2008) Peripheral chemokine receptors, their ligands, cytokines and Alzheimer’s disease. J Alzheimers Dis14, 147–159.
52.
LeeKS, ChungJH, ChoiTK, SuhSY, OhBH, HongCH (2009) Peripheral cytokines and chemokines in Alzheimer’s disease. Dement Geriatr Cogn Disord28, 281–287.
53.
KruegerJM, WalterJ, DinarelloCA, WolffSM, ChedidL (1984) Sleep-promoting effects of endogenous pyrogen (interleukin-1). Am J Physiol246, R994–999.
54.
Di MecoA, JoshiYB, PraticoD (2014) Sleep deprivation impairs memory, tau metabolism, and synaptic integrity of a mouse model of Alzheimer’s disease with plaques and tangles. Neurobiol Aging35, 1813–1820.
55.
ChenDW, WangJ, ZhangLL, WangYJ, GaoCY (2018) Cerebrospinal fluid amyloid-beta levels are increased in patients with insomnia. J Alzheimers Dis61, 645–651.
