Requirement of brain interleukin33 for aquaporin4 expression in astrocytes and glymphatic drainage of abnormal tau.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
received:
03
06
2020
accepted:
07
12
2020
revised:
17
11
2020
pubmed:
13
1
2021
medline:
3
2
2022
entrez:
12
1
2021
Statut:
ppublish
Résumé
Defective aquaporin4 (AQP4)-mediated glymphatic drainage has been linked to tauopathy and amyloid plaque in Alzheimer's disease. We now show that brain interleukin33 (IL33) is required for regulation of AQP4 expression in astrocytes, especially those at neuron-facing membrane domain (n-AQP4). First, IL33-deficient (Il33
Identifiants
pubmed: 33432186
doi: 10.1038/s41380-020-00992-0
pii: 10.1038/s41380-020-00992-0
pmc: PMC8273186
mid: NIHMS1653404
doi:
Substances chimiques
Aquaporin 4
0
Interleukin-33
0
tau Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5912-5924Subventions
Organisme : NICHD NIH HHS
ID : R01 HD049613
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK077857
Pays : United States
Organisme : NIA NIH HHS
ID : R21 AG067311
Pays : United States
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited part of Springer Nature.
Références
Larson EB, Yaffe K, Langa KM. New insights into the dementia epidemic. N Engl J Med. 2013;369:2275–7.
doi: 10.1056/NEJMp1311405
Cutler RG, Kelly J, Storie K, Pedersen WA, Tammara A, Hatanpaa K, et al. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer’s disease. Proc Natl Acad Sci USA. 2004;101:2070–5.
doi: 10.1073/pnas.0305799101
Swerdlow RH. A brain aging, Alzheimer’s disease, and mitochondria. Biochim Biophys Acta. 2011;1812:1630–9.
doi: 10.1016/j.bbadis.2011.08.012
Barnett A, Brewer GJ. Autophagy in aging and Alzheimer’s disease: pathologic or protective? J Alzheimers Dis. 2011;25:385–94.
doi: 10.3233/JAD-2011-101989
Menzies FM, Fleming A, Rubinsztein DC. Compromised autophagy and neurodegenerative diseases. Nat Rev Neurosci. 2015;16:345–57.
doi: 10.1038/nrn3961
Wyss-Coray T. Ageing, neurodegeneration and brain rejuvenation. Nature. 2016;539:180–6.
doi: 10.1038/nature20411
Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, et al. Structural and functional features of central nervous system lymphatic vessels. Nature. 2015;523:337–41.
doi: 10.1038/nature14432
Tarasoff-Comway JM, Carare R, Osorio RS, Glodzik L, Butler T, Fieremants E, et al. Clearance systems in the brain—implications for Alzheimer disease. Nat Rev Neurol. 2015;11:457–70.
doi: 10.1038/nrneurol.2015.119
Nagelhus EA, Mathiisen TM, Ottersen OP. Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience. 2004;129:905–13.
doi: 10.1016/j.neuroscience.2004.08.053
Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med. 2012;4:147ra111.
doi: 10.1126/scitranslmed.3003748
Nagelhus E, Ottersen OP. Physiological roles of aquaporin-4 in brain. Physiol Rev. 2013;93:1543–62.
doi: 10.1152/physrev.00011.2013
Papadopoulos MC, Verkman AS. Aquaporin water channels in the nervous system. Nat Rev Neurosci. 2013;14:265–77.
doi: 10.1038/nrn3468
Szu JL, Binder DK. The role of astrocytic aquaporin-4 in synaptic plasticity and learning and memory. Front Integr Neurosci. 2016;10:8.
doi: 10.3389/fnint.2016.00008
Cayrol C, Girard JP. IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Curr Opin Immunol. 2014;31:31–7.
doi: 10.1016/j.coi.2014.09.004
Liew FY, Girard J, Turnquist HR. Interleukin-33 in health and disease. Nat Rev Immunol. 2016;16:676–89.
doi: 10.1038/nri.2016.95
Wu J, Carlock C, Zhou C, Nakae S, Hicks J, Adams HP, et al. Interleukin33 is required for disposal of unnecessary cells during ovarian atresia through regulation of autophagy and macrophage migration. J Immunol. 2015;194:2140–7.
doi: 10.4049/jimmunol.1402503
Carlock C, Wu J, Zhou C, Tatum K, Adams HP, Tan F, et al. Unique temporal and spatial expression patterns of IL-33 in ovaries during ovulation and estrous cycle are associated with ovarian tissue homeostasis. J Immunol. 2014;193:161–9.
doi: 10.4049/jimmunol.1400381
Yasuoka S, Kawanokuchi J, Parajuli B, Jin S, Doi Y, Noda M, et al. Production and functions of IL-33 in the central nervous system. Brain Res. 2011;1385:8–17.
doi: 10.1016/j.brainres.2011.02.045
Foster SL, Talbot S, Woolf CJ. CNS injury: IL-33 sounds the alarm. Immunity. 2015;42:403–5.
doi: 10.1016/j.immuni.2015.02.019
Carlock C, Wu J, Shim J, Moreno-Gonzalez I, Pitcher M, Hicks J, et al. Interleukin33 deficiency causes tau abnormality and neurodegeneration with Alzheimer-like symptoms in aged mice. Trans Psychiatry. 2017;7:e1164. https://doi.org/10.1038/tp.2017.142 .
doi: 10.1038/tp.2017.142
Chapuis J, Hot D, Hansmannel F, Kerdraon O, Ferreira S, Maurage CA, et al. Transcriptomic and genetic studies identify IL-33 as a candidate gene for Alzheimer’s disease. Mol Psychiatry. 2009;14:1004–16.
doi: 10.1038/mp.2009.10
Fu AKY, Hung K, Yuen MYF, Zhou X, Mak DSY, Chan ICW, et al. IL-33 ameliorates Alzheimer’s disease-like pathology and cognitive decline. Proc Natl Acad Sci USA. 2016;113:E2705–13.
doi: 10.1073/pnas.1604032113
Valenzuela DM, Murphy AJ, Frendewey D, Gale NW, Economides AN, Auerbach W, et al. High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat Biotechnol. 2003;21:652–9.
doi: 10.1038/nbt822
Kim HY, Lee DK, Chung BR, Kim H, Kim KS. Intracerebroventricular injection of amyloid-β peptides in normal mice to acutely induce Alzheimer-like cognitive deficits. J Vis Exp. 2016;109:53308.
Wu J, Borillo J, Glass WF II, Hicks J, Ou CN, Lou Y. T cell epitope of α3 chain of Type IV collagen induces severe glomerulonephritis. Kidney Int. 2003;64:1292–301.
doi: 10.1046/j.1523-1755.2003.00227.x
Terris J, Ecelbarger CA, Marples D, Knepper MA, Nielsen S. Distribution of aquaporin-4 water channel expression within rat kidney. Am J Physiol. 1995;269:F775–85.
doi: 10.1152/ajpcell.1995.269.3.C775
Iliff JJ, Chen MJ, Plog BA, Zeppenfeld DM, Soltero M, Yang L, et al. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci. 2014;34:16180–93.
doi: 10.1523/JNEUROSCI.3020-14.2014
Wang J, Jin WS, Bu XL, Zen F, Huang ZL, Li WW, et al. Physiological clearance of tau in the periphery and its therapeutic potential for tauopathies. Acta Neuropathol. 2018;136:525–36.
doi: 10.1007/s00401-018-1891-2
Xu W, Ge Y, Liu Z, Gong R. Glycogen synthase kinase 3β orchestrates microtubule remodeling in compensatory glomerular adaptation to podocyte depletion. J Biol Chem. 2014;290:1348–63.
doi: 10.1074/jbc.M114.593830
Caillet-Boudin ML, Buee L, Sergeant N, Lefebvre B. Regulation of human MAPT gene expression. Mol Neurodegener. 2015;10:28.
doi: 10.1186/s13024-015-0025-8
Fairlie-Clark K, Barbour M, Wilson C, Hridi SU, Allan D, Jiang H. Expression and function of IL-33/ST2 axis in the central nervous system under normal and diseased conditions. Front Immunol. 2018;9:2596.
doi: 10.3389/fimmu.2018.02596
Verkman AS, Binder DK, Bloch O, Auguste K, Papadopoulos MC. Three distinct roles of aquaporin-4 in brain function revealed by knockout mice. Biochim Biophys Acta. 2006;1758:1085–93.
doi: 10.1016/j.bbamem.2006.02.018
Sykova E, Nicholson C. Diffusion in brain extracellular space. Physiol Rev. 2008;88:1277–340.
doi: 10.1152/physrev.00027.2007
Nedergaard M. Garbage truck of the brain. Science. 2013;340:1529–30.
doi: 10.1126/science.1240514
Xu Z, Xiao N, Chen Y, Huang H, Marshall C, Gao J, et al. Deletion of aquaporin-4 in APP/PS1 mice exacerbates brain Aβ accumulation and memory deficits. Mol Neurodegeneration. 2015;10:58.
doi: 10.1186/s13024-015-0056-1
Zetterberg H, Wilson D, Andreasson U, Minthon L, Blennow K, Randall J, et al. Plasma tau levels in Alzheimer’s disease. Alzheimers Res Ther. 2013;5:9.
doi: 10.1186/alzrt163
Kimura T, Sharma G, Ishiguro K, Hisanaga SI. Phospho-Tau bar code: analysis of phosphoisotypes of tau and its application to tauopathy. Front Neurosci. 2018;12:44.
doi: 10.3389/fnins.2018.00044
Bateman RJ, Barthélemy NR, Horie K. Another step forward in blood-based diagnostics for Alzheimer’s disease. Nat Med. 2020;26:314–6.
doi: 10.1038/s41591-020-0797-4
Schlondorff D. The glomerular mesangial cell: an expanding role for a specialized pericyte. FASEB J. 1987;1:272–81.
doi: 10.1096/fasebj.1.4.3308611
Sterzel RB, Perfetto M, Biemesderfer D, Kashgarian M. Disposal of ferritin in the glomerular mesangium of rats. Kidney Int. 1983;23:480–8.
doi: 10.1038/ki.1983.45
Lonneborg A. Biomarkers for Alzheimer disease in cerebrospinal fluid, urine, and blood. Mol Diagn Ther. 2008;12:307–20.
doi: 10.1007/BF03256296