Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Molecular Neurodegeneration
Published in: Molecular Neurodegeneration 1/2024

Open Access 01-12-2024 | Alzheimer's Disease | Review

Neuronal and glial vulnerability of the suprachiasmatic nucleus in tauopathies: evidence from human studies and animal models

Authors: Gowoon Son, Thomas C. Neylan, Lea T. Grinberg

Published in: Molecular Neurodegeneration | Issue 1/2024

Login to get access

Abstract

Tauopathies, a group of neurodegenerative diseases that includes Alzheimer’s disease, commonly lead to disturbances in sleep-wake patterns and circadian rhythm disorders. The circadian rhythm, a recurring 24-hour cycle governing human biological activity, is regulated by the hypothalamic suprachiasmatic nucleus (SCN) and endogenous transcriptional-translational feedback loops. Surprisingly, little attention has been given to investigating tauopathy-driven neuropathology in the SCN and the repercussions of SCN and circadian gene dysfunction in the human brain affected by tauopathies. This review aims to provide an overview of the current literature on the vulnerability of the SCN in tauopathies in humans. Emphasis is placed on elucidating the neuronal and glial changes contributing to the widespread disruption of the molecular circadian clock. Furthermore, this review identifies areas of knowledge requiring further investigation.
Literature
1.
Pollak CP, Perlick D. Sleep problems and institutionalization of the elderly. J Geriatr Psychiatry Neurol. 1991;4:204–10.PubMedCrossRef
2.
Spitznagel MB, Tremont G, Davis JD, Foster SM. Psychosocial predictors of dementia caregiver desire to institutionalize: caregiver, care recipient, and family relationship factors. J Geriatr Psychiatry Neurol. 2006;19:16–20.PubMedPubMedCentralCrossRef
3.
4.
5.
Crary JF, Trojanowski JQ, Schneider JA, Abisambra JF, Abner EL, Alafuzoff I, et al. Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol. 2014;128:755–66.PubMedPubMedCentralCrossRef
6.
7.
Kovacs GG. Molecular pathology of neurodegenerative diseases: principles and practice. J Clin Pathol. 2019;72:725–35.PubMedCrossRef
8.
Deboer T. Sleep homeostasis and the circadian clock: do the circadian pacemaker and the sleep homeostat influence each other’s functioning? Neurobiol Sleep Circadian Rhythms. 2018;5:68–77.PubMedPubMedCentralCrossRef
9.
Swaab DF, Fliers E, Partiman TS. The suprachiasmatic nucleus of the human brain in relation to sex, age and senile dementia. Brain Res. 1985;342:37–44.PubMedCrossRef
10.
Stopa EG, Volicer L, Kuo-Leblanc V, Harper D, Lathi D, Tate B, et al. Pathologic evaluation of the human Suprachiasmatic nucleus in severe dementia. J Neuropathol Exp Neurol. 1999;58:29–39.PubMedCrossRef
11.
Harper DG, Stopa EG, Kuo-Leblanc V, McKee AC, Asayama K, Volicer L, et al. Dorsomedial SCN neuronal subpopulations subserve different functions in human dementia. Brain. 2008;131:1609–17.PubMedCrossRef
12.
Zhou J-N, Hofman MA, Swaab DF. VIP neurons in the human SCN in relation to sex, age, and Alzheimer’s disease. Neurobiol Aging. 1995;16:571–6.PubMedCrossRef
13.
Wu Y-H, Zhou J-N, Van Heerikhuize J, Jockers R, Swaab DF. Decreased MT1 melatonin receptor expression in the suprachiasmatic nucleus in aging and Alzheimer’s disease. Neurobiol Aging. 2007;28:1239–47.PubMedCrossRef
14.
Swaab DF, Grundke-Iqbal I, Iqbal K, Kremer HPH, Ravid R, van de Nes JAP. τ and ubiquitin in the human hypothalamus in aging and Alzheimer’s disease. Brain Res. 1992;590:239–49.PubMedCrossRef
15.
Wang JL, Lim AS, Chiang W-Y, Hsieh W-H, Lo M-T, Schneider JA, et al. Suprachiasmatic neuron numbers and rest-activity circadian rhythms in older humans: SCN and rest-activity rhythms. Ann Neurol. 2015;78:317–22.PubMedPubMedCentralCrossRef
16.
17.
Boone DR, Sell SL, Micci M-A, Crookshanks JM, Parsley M, Uchida T, et al. Traumatic Brain Injury-Induced Dysregulation of the Circadian Clock. Lyons LC, editor. PLoS ONE. 2012;7:e46204.PubMedPubMedCentralCrossRef
18.
Yamakawa GR, Brady RD, Sun M, McDonald SJ, Shultz SR, Mychasiuk R. The interaction of the circadian and immune system: Desynchrony as a pathological outcome to traumatic brain injury. Neurobiol Sleep Circadian Rhythms. 2020;9:100058.PubMedPubMedCentralCrossRef
19.
Brunetti V, Testani E, Iorio R, Frisullo G, Luigetti M, Di Giuda D, et al. Post-encephalitic parkinsonism and sleep disorder responsive to immunological treatment: a case report. Clin EEG Neurosci. 2016;47:324–9.PubMedCrossRef
20.
Bluett B, Pantelyat AY, Litvan I, Ali F, Apetauerova D, Bega D, et al. Best practices in the clinical Management of Progressive Supranuclear Palsy and Corticobasal Syndrome: a consensus statement of the CurePSP centers of care. Front Neurol [Internet]. 2021; [cited 2023 May 17]; 12. Available from: 10.3389/fneur.2021.694872 .
21.
De Pablo-Fernández E, Courtney R, Warner TT, Holton JL. A histologic study of the circadian system in Parkinson disease, multiple system atrophy, and progressive Supranuclear palsy. JAMA Neurology. 2018;75:1008–12.PubMedPubMedCentralCrossRef
22.
Lin W, Lin Y-K, Yang F-C, Chung C-H, Hu J-M, Tsao C-H, et al. Risk of neurodegenerative diseases in patients with sleep disorders: a nationwide population-based case-control study. Sleep Med. 2023;107:289–99.PubMedCrossRef
23.
Gemignani A, Pietrini P, Murrell JR, Glazier BS, Zolo P, Guazzelli M, et al. Slow wave and rem sleep mechanisms are differently altered in hereditary pick disease associated with the TAU G389R mutation. Arch Ital Biol. 2005;143:65–79.PubMed
24.
Walsh CM, Ruoff L, Walker K, Emery A, Varbel J, Karageorgiou E, et al. Sleepless night and day, the plight of progressive Supranuclear palsy. Sleep. 2017;40:zsx154.PubMedPubMedCentralCrossRef
25.
Peter-Derex L, Yammine P, Bastuji H, Croisile B. Sleep and Alzheimer’s disease. Sleep Med Rev. 2015;19:29–38.PubMedCrossRef
26.
27.
Aldrich MS, Foster NL, White RF, Bluemlein L, Ba GP. Sleep abnormalities in progressive supranuclear palsy. Ann Neurol. 1989;25:577–81.PubMedCrossRef
28.
Oh JY, Walsh CM, Ranasinghe K, Mladinov M, Pereira FL, Petersen C, et al. Subcortical neuronal correlates of sleep in neurodegenerative diseases. JAMA Neurol. 2022;79:498–508.PubMedPubMedCentralCrossRef
29.
Prinz PN, Peskind ER, Vitaliano PP, Raskind MA, Eisdorfer C, Zemcuznikov N, et al. Changes in the sleep and waking EEGs of nondemented and demented elderly subjects. J Am Geriatr Soc. 1982;30:86–93.PubMedCrossRef
30.
Petit D, Gagnon J-F, Fantini ML, Ferini-Strambi L, Montplaisir J. Sleep and quantitative EEG in neurodegenerative disorders. J Psychosom Res. 2004;56:487–96.PubMedCrossRef
31.
32.
Van Cauter E, Leproult R, Plat L. Age-related changes in slow wave sleep and REM sleep and relationship with growth hormone and cortisol levels in healthy men. JAMA. 2000;284:861–8.PubMedCrossRef
33.
Falgàs N, Walsh CM, Yack L, Simon AJ, Allen IE, Kramer JH, et al. Alzheimer’s disease phenotypes show different sleep architecture. Alzheimers Dement. 2023;alz.12963.
34.
Arand D, Bonnet M, Hurwitz T, Mitler M, Rosa R, Sangal RB. The clinical use of the MSLT and MWT. Sleep. 2005;28:123–44.PubMedCrossRef
35.
Littner MR, Kushida C, Wise M, Davila DG, Morgenthaler T, Lee-Chiong T, et al. Practice parameters for clinical use of the multiple sleep latency test and the maintenance of wakefulness test. Sleep. 2005;28:113–21.PubMedCrossRef
36.
Cooper AD, Josephs KA. Photophobia, visual hallucinations, and REM sleep behavior disorder in progressive supranuclear palsy and corticobasal degeneration: a prospective study. Parkinsonism Relat Disord. 2009;15:59–61.PubMedCrossRef
37.
Lee SE, Rabinovici GD, Mayo MC, Wilson SM, Seeley WW, DeArmond SJ, et al. Clinicopathological correlations in corticobasal degeneration. Ann Neurol. 2011;70:327–40.PubMedPubMedCentralCrossRef
38.
Oh J, Eser RA, Ehrenberg AJ, Morales D, Petersen C, Kudlacek J, et al. Profound degeneration of wake-promoting neurons in Alzheimer’s disease. Alzheimers Dement. 2019;15:1253–63.PubMedPubMedCentralCrossRef
39.
Adams JW, Alosco ML, Mez J, Alvarez VE, Huber BR, Tripodis Y, et al. Association of probable REM sleep behavior disorder with pathology and years of contact sports play in chronic traumatic encephalopathy. Acta Neuropathol. 2020;140:851–62.PubMedPubMedCentralCrossRef
40.
41.
Lew CH, Petersen C, Neylan TC, Grinberg LT. Tau-driven degeneration of sleep- and wake-regulating neurons in Alzheimer’s disease. Sleep Med Rev. 2021;60:101541.PubMedPubMedCentralCrossRef
42.
Volicer L, Harper DG, Manning BC, Goldstein R, Satlin A. Sundowning and circadian rhythms in Alzheimer’s disease. AJP. 2001;158:704–11.CrossRef
43.
Okawa M, Mishima K, Hishikawa Y, Hozumi S, Hori H, Takahashi K. Circadian rhythm disorders in sleep-waking and body temperature in elderly patients with dementia and their treatment. Sleep. 1991;14:478–85.PubMedCrossRef
44.
Hatfield CF, Herbert J, van Someren EJW, Hodges JR, Hastings MH. Disrupted daily activity/rest cycles in relation to daily cortisol rhythms of home-dwelling patients with early Alzheimer’s dementia. Brain. 2004;127:1061–74.PubMedCrossRef
45.
Homolak J, Mudrovčić M, Vukić B, Toljan K. Circadian rhythm and Alzheimer’s disease. Med Sci (Basel). 2018;6:52.PubMed
46.
Winer JR, Morehouse A, Fenton L, Harrison TM, Ayangma L, Reed M, et al. Tau and β-amyloid burden predict Actigraphy-measured and self-reported impairment and misperception of human sleep. J Neurosci. 2021;41:7687–96.PubMedPubMedCentralCrossRef
47.
Walsh CM, Ruoff L, Varbel J, Walker K, Grinberg LT, Boxer AL, et al. Rest-activity rhythm disruption in progressive supranuclear palsy. Sleep Med. 2016;22:50–6.PubMedPubMedCentralCrossRef
48.
Suzuki K, Miyamoto T, Miyamoto M, Hirata K. The core body temperature rhythm is altered in progressive supranuclear palsy. Clin Auton Res. 2009;19:65–8.PubMedCrossRef
49.
Schmidt C, Berg D, Herting PS, Junghanns S, Schweitzer K, et al. Loss of nocturnal blood pressure fall in various extrapyramidal syndromes. Mov Disord. 2009;24:2136–42.PubMedCrossRef
50.
Blessing EM, Parekh A, Betensky RA, Babb J, Saba N, Debure L, et al. Association between lower body temperature and increased tau pathology in cognitively normal older adults. Neurobiol Dis. 2022;171:105748.PubMedPubMedCentralCrossRef
51.
Maywood ES, Chesham JE, Winsky-Sommerer R, Hastings MH. Restoring the molecular clockwork within the Suprachiasmatic hypothalamus of an otherwise Clockless mouse enables circadian phasing and stabilization of sleep-wake cycles and reverses memory deficits. J Neurosci. 2021;41:8562–76.PubMedPubMedCentralCrossRef
52.
Todd WD, Venner A, Anaclet C, Broadhurst RY, De Luca R, Bandaru SS, et al. Suprachiasmatic VIP neurons are required for normal circadian rhythmicity and comprised of molecularly distinct subpopulations. Nat Commun. 2020;11:4410.PubMedPubMedCentralCrossRef
53.
Hay-Schmidt A, Vrang N, Larsen PJ, Mikkelsen JD. Projections from the raphe nuclei to the suprachiasmatic nucleus of the rat. J Chem Neuroanat. 2003;25:293–310.PubMedCrossRef
54.
Meyer-Bernstein EL, Morin LP. Differential serotonergic innervation of the Suprachiasmatic nucleus and the lntergeniculate leaflet and its role in circadian rhythm modulation. J Neurosci. 1996;16.
55.
Cermakian N, Waddington Lamont E, Boudreau P, Boivin DB. Circadian clock gene expression in brain regions of Alzheimer ‘s disease patients and control subjects. J Biol Rhythm. 2011;26:160–70.CrossRef
56.
Dai J, Swaab DF, Van Der Vliet J, Buijs RM. Postmortem tracing reveals the organization of hypothalamic projections of the suprachiasmatic nucleus in the human brain. J Comp Neurol. 1998;400:87–102.PubMedCrossRef
57.
Simerly RB, Swanson LW. The organization of neural inputs to the medial preoptic nucleus of the rat. J Comp Neurol. 1986;246:312–42.PubMedCrossRef
58.
Watts AG, Swanson LW, Sanchez-Watts G. Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J Comp Neurol. 1987;258:204–29.PubMedCrossRef
59.
Buijs RM. Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell Tissue Res. 1978;192:423–35.PubMedCrossRef
60.
Aschoff J. Exogenous and endogenous components in circadian rhythms. Cold Spring Harb Symp Quant Biol. 1960;25:11–28.PubMedCrossRef
61.
62.
63.
Xu P, Berto S, Kulkarni A, Jeong B, Joseph C, Cox KH, et al. NPAS4 regulates the transcriptional response of the suprachiasmatic nucleus to light and circadian behavior. Neuron. 2021;109:3268–3282.e6.PubMedPubMedCentralCrossRef
64.
Wen S, Ma D, Zhao M, Xie L, Wu Q, Gou L, et al. Spatiotemporal single-cell analysis of gene expression in the mouse suprachiasmatic nucleus. Nat Neurosci. 2020;23:456–67.PubMedCrossRef
65.
Patke A, Young MW, Axelrod S. Molecular mechanisms and physiological importance of circadian rhythms. Nat Rev Mol Cell Biol. 2020;21:67–84.PubMedCrossRef
66.
Eser RA, Ehrenberg AJ, Petersen C, Dunlop S, Mejia MB, Suemoto CK, et al. Selective vulnerability of brainstem nuclei in distinct Tauopathies: a postmortem study. J Neuropathol Exp Neurol. 2018;77:149–61.PubMedPubMedCentralCrossRef
67.
Diodati D, Cyn-Ang L, Kertesz A, Finger E. Pathologic evaluation of the Supraoptic and paraventricular nuclei in dementia. Can J Neurol Sci. 2012;39:213–9.PubMedCrossRef
68.
Roemer SF, Grinberg LT, Crary JF, Seeley WW, McKee AC, Kovacs GG, et al. Rainwater Charitable Foundation criteria for the neuropathologic diagnosis of progressive supranuclear palsy. Acta Neuropathol. 2022;144:603–14.PubMedPubMedCentralCrossRef
69.
Han SM, Jang YJ, Kim EY, Park SA. The change in circadian rhythms in P301S transgenic mice is linked to variability in Hsp70-related tau disaggregation. Exp Neurobiol. 2022;31:196–207.PubMedPubMedCentralCrossRef
70.
Stevanovic K, Yunus A, Joly-Amado A, Gordon M, Morgan D, Gulick D, et al. Disruption of normal circadian clock function in a mouse model of tauopathy. Exp Neurol. 2017;294:58–67.PubMedCrossRef
71.
72.
Juste YR, Kaushik S, Bourdenx M, Aflakpui R, Bandyopadhyay S, Garcia F, et al. Reciprocal regulation of chaperone-mediated autophagy and the circadian clock. Nat Cell Biol. 2021;23:1255–70.PubMedPubMedCentralCrossRef
73.
74.
Busino L, Bassermann F, Maiolica A, Lee C, Nolan PM, Godinho SIH, et al. SCF Fbxl3 controls the oscillation of the circadian clock by directing the degradation of Cryptochrome proteins. Science. 2007;316:900–4.PubMedCrossRef
75.
Lu R, Dong Y, Li JD. Necdin regulates BMAL1 stability and circadian clock through SGT1-HSP90 chaperone machinery. Nucleic Acids Res. 2020;48:7944–57.PubMedPubMedCentralCrossRef
76.
77.
Hight K, Hallett H, Churchill L, De A, Boucher A, Krueger JM. Time of day differences in the number of cytokine-, neurotrophin- and NeuN-immunoreactive cells in the rat somatosensory or visual cortex. Brain Res. 2010;1337:32–40.PubMedPubMedCentralCrossRef
78.
Hastings MH, Brancaccio M, Gonzalez-Aponte MF, Herzog ED. Circadian rhythms and astrocytes: the good, the bad, and the ugly. Annu Rev Neurosci. 2023;46 null.
79.
Patton AP, Smyllie NJ, Chesham JE, Hastings MH. Astrocytes sustain circadian oscillation and Bidirectionally determine circadian period, but do not regulate circadian phase in the Suprachiasmatic nucleus. J Neurosci. 2022;42:5522–37.PubMedPubMedCentralCrossRef
80.
Tso CF, Simon T, Greenlaw AC, Puri T, Mieda M, Herzog ED. Astrocytes regulate daily rhythms in the suprachiasmatic nucleus and behavior. Curr Biol. 2017;27:1055–61.PubMedPubMedCentralCrossRef
81.
Leone MJ, Marpegan L, Bekinschtein TA, Costas MA, Golombek DA. Suprachiasmatic astrocytes as an interface for immune-circadian signalling. J Neurosci Res. 2006;84:1521–7.PubMedCrossRef
82.
Brancaccio M, Edwards MD, Patton AP, Smyllie NJ, Chesham JE, Maywood ES, et al. Cell-autonomous clock of astrocytes drives circadian behavior in mammals. Science. 2019;363:187–92.PubMedPubMedCentralCrossRef
83.
Brancaccio M, Patton AP, Chesham JE, Maywood ES, Hastings MH. Astrocytes control circadian timekeeping in the Suprachiasmatic nucleus via glutamatergic signaling. Neuron. 2017;93:1420–1435.e5.PubMedPubMedCentralCrossRef
84.
Patton AP, Morris EL, McManus D, Wang H, Li Y, Chin JW, et al. Astrocytic control of extracellular GABA drives circadian timekeeping in the suprachiasmatic nucleus. Proc Natl Acad Sci. 2023;120:e2301330120.PubMedPubMedCentralCrossRef
85.
Coomans C, Saaltink D-J, Deboer T, Tersteeg M, Lanooij S, Schneider AF, et al. Doublecortin-like expressing astrocytes of the suprachiasmatic nucleus are implicated in the biosynthesis of vasopressin and influences circadian rhythms. Glia. 2021;69:2752–66.PubMedPubMedCentralCrossRef
86.
Costa R, Montagnese S. The role of astrocytes in generating circadian rhythmicity in health and disease. J Neurochem. 2021;157:42–52.PubMedCrossRef
87.
McKee CA, Lananna BV, Musiek ES. Circadian regulation of astrocyte function: implications for Alzheimer’s disease. Cell Mol Life Sci. 2020;77:1049–58.PubMedCrossRef
88.
Lananna BV, McKee CA, King MW, Del-Aguila JL, Dimitry JM, Farias FHG, et al. Chi3l1/YKL-40 is controlled by the astrocyte circadian clock and regulates neuroinflammation and Alzheimer’s disease pathogenesis. Sci Transl Med. 2020;12.
89.
Gerstner JR, Perron IJ, Riedy SM, Yoshikawa T, Kadotani H, Owada Y, et al. Normal sleep requires the astrocyte brain-type fatty acid binding protein FABP7. Sci Adv. 2017;3:e1602663.PubMedPubMedCentralCrossRef
90.
Gerstner JR, Bremer QZ, Vander Heyden WM, Lavaute TM, Yin JC, Landry CF. Brain fatty acid binding protein (Fabp7) is diurnally regulated in astrocytes and hippocampal granule cell precursors in adult rodent brain. PLoS One. 2008;3:e1631.PubMedPubMedCentralCrossRef
91.
Muthukumarasamy I, Buel SM, Hurley JM, Dordick JS. NOX2 inhibition enables retention of the circadian clock in BV2 microglia and primary macrophages. Front Immunol [Internet]. 2023; [cited 2023 Apr 3];14. Available from: 10.3389/fimmu.2023.1106515 .
92.
Fonken LK, Frank MG, Kitt MM, Barrientos RM, Watkins LR, Maier SF. Microglia inflammatory responses are controlled by an intrinsic circadian clock. Brain Behav Immun. 2015;45:171–9.PubMedCrossRef
93.
Liu H, Wang X, Chen L, Chen L, Tsirka SE, Ge S, et al. Microglia modulate stable wakefulness via the thalamic reticular nucleus in mice. Nat Commun. 2021;12:4646.PubMedPubMedCentralCrossRef
94.
Deng X-H, Bertini G, Palomba M, Xu Y-Z, Bonaconsa M, Nygård M, et al. Glial transcripts and immune-challenged glia in the Suprachiasmatic nucleus of Young and aged mice. Chronobiol Int. 2010;27:742–67.PubMedCrossRef
95.
Matsui F, Yamaguchi ST, Kobayashi R, Ito S, Nagashima S, Zhou Z, et al. Ablation of microglia does not alter circadian rhythm of locomotor activity. Mol Brain. 2023;16:34.PubMedPubMedCentralCrossRef
96.
Sominsky L, Dangel T, Malik S, De Luca SN, Singewald N, Spencer SJ. Microglial ablation in rats disrupts the circadian system. FASEB J. 2021;35:e21195.PubMedCrossRef
97.
Yoshiyama Y, Higuchi M, Zhang B, Huang S-M, Iwata N, Saido TC, et al. Synapse loss and microglial activation precede tangles in a P301S Tauopathy mouse model. Neuron. 2007;53:337–51.PubMedCrossRef
98.
Song H, Moon M, Choe HK, Han D-H, Jang C, Kim A, et al. Aβ-induced degradation of BMAL1 and CBP leads to circadian rhythm disruption in Alzheimer’s disease. Mol Neurodegener. 2015;10:13.PubMedPubMedCentralCrossRef
99.
Nam Y, Kim S, Kim J, Hoe H-S, Moon M. Mesoscopic mapping of visual pathway in a female 5XFAD mouse model of Alzheimer’s disease. Cells. 2022;11:3901.PubMedPubMedCentralCrossRef
100.
Paul JR, Munir HA, van Groen T, Gamble KL. Behavioral and SCN neurophysiological disruption in the Tg-SwDI mouse model of Alzheimer’s disease. Neurobiol Dis. 2018;114:194–200.PubMedPubMedCentralCrossRef
101.
Parhizkar S, Gent G, Chen Y, Rensing N, Gratuze M, Strout G, et al. Sleep deprivation exacerbates microglial reactivity and Aβ deposition in a TREM2-dependent manner in mice. Sci Transl Med. 2023;15:eade6285.PubMedCrossRef
102.
den Haan J, Morrema THJ, Verbraak FD, de Boer JF, Scheltens P, Rozemuller AJ, et al. Amyloid-beta and phosphorylated tau in post-mortem Alzheimer’s disease retinas. Acta Neuropathol Commun. 2018;6:147.CrossRef
103.
La Morgia C, Ross-Cisneros FN, Koronyo Y, Hannibal J, Gallassi R, Cantalupo G, et al. Melanopsin retinal ganglion cell loss in A lzheimer disease. Ann Neurol. 2016;79:90–109.PubMedCrossRef
104.
105.
Hart de Ruyter FJ, Morrema THJ, den Haan J, Twisk JWR, de Boer JF, Scheltens P, et al. Phosphorylated tau in the retina correlates with tau pathology in the brain in Alzheimer’s disease and primary tauopathies. Acta Neuropathol. 2023;145:197–218.PubMedCrossRef
106.
Koronyo Y, Rentsendorj A, Mirzaei N, Regis GC, Sheyn J, Shi H, et al. Retinal pathological features and proteome signatures of Alzheimer’s disease. Acta Neuropathol. 2023;145:409–38.PubMedPubMedCentralCrossRef
107.
Schön C, Hoffmann NA, Ochs SM, Burgold S, Filser S, Steinbach S, et al. Long-term in vivo imaging of Fibrillar tau in the retina of P301S transgenic mice. PLoS One. 2012;7:e53547.PubMedPubMedCentralCrossRef
108.
Montine TJ, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Dickson DW, et al. National Institute on Aging-Alzheimer’s association guidelines for the neuropathologic assessment of Alzheimer’s disease: a practical approach. Acta Neuropathol. 2012;123:1–11.PubMedCrossRef
109.
Kovacs GG, Lukic MJ, Irwin DJ, Arzberger T, Respondek G, Lee EB, et al. Distribution patterns of tau pathology in progressive supranuclear palsy. Acta Neuropathol. 2020;140:99–119.PubMedPubMedCentralCrossRef
110.
Mckee AC, Abdolmohammadi B, Stein TD. The neuropathology of chronic traumatic encephalopathy. Handb Clin Neurol. 2018;158:297–307.PubMedCrossRef
111.
Wyss-Coray T, Mucke L. Inflammation in neurodegenerative disease--a double-edged sword. Neuron. 2002;35:419–32.PubMedCrossRef
112.
Wang C, Holtzman DM. Bidirectional relationship between sleep and Alzheimer’s disease: role of amyloid, tau, and other factors. Neuropsychopharmacol. 2020;45:104–20.CrossRef
113.
114.
Hoyt KR, Obrietan K. Circadian clocks, cognition, and Alzheimer’s disease: synaptic mechanisms, signaling effectors, and chronotherapeutics. Mol Neurodegener. 2022;17:35.PubMedPubMedCentralCrossRef
Metadata
Title
Neuronal and glial vulnerability of the suprachiasmatic nucleus in tauopathies: evidence from human studies and animal models
Authors
Gowoon Son
Thomas C. Neylan
Lea T. Grinberg
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Molecular Neurodegeneration / Issue 1/2024
Electronic ISSN: 1750-1326
DOI
https://doi.org/10.1186/s13024-023-00695-4

Other articles of this Issue 1/2024

Molecular Neurodegeneration 1/2024 Go to the issue

Research article

Adaptive immune changes associate with clinical progression of Alzheimer’s disease

Research article

Unravelling cell type-specific responses to Parkinson’s Disease at single cell resolution

Guideline

Alzheimer blood biomarkers: practical guidelines for study design, sample collection, processing, biobanking, measurement and result reporting

Commentary

Blood platelet factor 4: the elixir of brain rejuvenation

Review

Updates on mouse models of Alzheimer’s disease

Review

Nuclear-import receptors as gatekeepers of pathological phase transitions in ALS/FTD