Involvement of the choroid plexus in Alzheimer's disease pathophysiology: findings from mouse and human proteomic studies.

Choroid Plexus / metabolism Alzheimer Disease / metabolism Animals Humans Proteomics Mice, Transgenic Mice Disease Models, Animal Amyloid beta-Protein Precursor / metabolism Proteome / metabolism Male Female Mice, Inbred C57BL
APP knock-in mice Alzheimer’s disease Amyloid-β (Aβ) Cerebrospinal fluid Choroid plexus Proteomics

Journal

Fluids and barriers of the CNS
ISSN: 2045-8118
Titre abrégé: Fluids Barriers CNS
Pays: England
ID NLM: 101553157

Informations de publication

Date de publication:
18 Jul 2024
Historique:
received: 15 04 2024
accepted: 03 06 2024
medline: 18 7 2024
pubmed: 18 7 2024
entrez: 17 7 2024
Statut: epublish

Résumé

Structural and functional changes of the choroid plexus (ChP) have been reported in Alzheimer's disease (AD). Nonetheless, the role of the ChP in the pathogenesis of AD remains largely unknown. We aim to unravel the relation between ChP functioning and core AD pathogenesis using a unique proteomic approach in mice and humans. We used an APP knock-in mouse model, APP ChP tissue proteome was dysregulated in APP Together, our findings support the hypothesis of ChP dysfunction in AD. These ChP changes were related to amyloid pathology. Therefore, the ChP could become a novel promising therapeutic target for AD.

Sections du résumé

BACKGROUND BACKGROUND
Structural and functional changes of the choroid plexus (ChP) have been reported in Alzheimer's disease (AD). Nonetheless, the role of the ChP in the pathogenesis of AD remains largely unknown. We aim to unravel the relation between ChP functioning and core AD pathogenesis using a unique proteomic approach in mice and humans.
METHODS METHODS
We used an APP knock-in mouse model, APP
RESULTS RESULTS
ChP tissue proteome was dysregulated in APP
CONCLUSIONS CONCLUSIONS
Together, our findings support the hypothesis of ChP dysfunction in AD. These ChP changes were related to amyloid pathology. Therefore, the ChP could become a novel promising therapeutic target for AD.

Identifiants

DOI: 10.1186/s12987-024-00555-3 PMID: 39020361
pubmed: 39020361
doi: 10.1186/s12987-024-00555-3
pii: 10.1186/s12987-024-00555-3
doi:

Substances chimiques

Amyloid beta-Protein Precursor 0
Proteome 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

58

Subventions

Organisme : Alzheimer Nederland
ID : WE.15-2022-01
Organisme : Fonds Wetenschappelijk Onderzoek
ID : 1295223N
Organisme : ZonMw
ID : 733050502
Pays : Netherlands

Informations de copyright

© 2024. The Author(s).

Références

Fagan AM, Xiong C, Jasielec MS, Bateman RJ, Goate AM, Benzinger TL, et al. Longitudinal change in CSF biomarkers in autosomal-dominant Alzheimer’s disease. Sci Transl Med. 2014;6(226):226–30.
doi: 10.1126/scitranslmed.3007901
Bateman RJ, Xiong C, Benzinger TL, Fagan AM, Goate A, Fox NC, et al. Clinical and biomarker changes in dominantly inherited Alzheimer’s disease. N Engl J Med. 2012;367(9):795–804.
pubmed: 22784036 pmcid: 3474597 doi: 10.1056/NEJMoa1202753
Selkoe DJ, Hardy J. The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol Med. 2016;8(6):595–608.
pubmed: 27025652 pmcid: 4888851 doi: 10.15252/emmm.201606210
Giao T, Teixeira T, Almeida MR, Cardoso I. Choroid plexus in Alzheimer’s disease—the current state of knowledge. Biomedicines. 2022;10(2):224.
pubmed: 35203434 pmcid: 8869376 doi: 10.3390/biomedicines10020224
Balusu S, Brkic M, Libert C, Vandenbroucke RE. The choroid plexus-cerebrospinal fluid interface in Alzheimer’s disease: more than just a barrier. Neural Regen Res. 2016;11(4):534–7.
pubmed: 27212900 pmcid: 4870896 doi: 10.4103/1673-5374.180372
Ghersi-Egea JF, Strazielle N, Catala M, Silva-Vargas V, Doetsch F, Engelhardt B. Molecular anatomy and functions of the choroidal blood-cerebrospinal fluid barrier in health and disease. Acta Neuropathol. 2018;135(3):337–61.
pubmed: 29368213 doi: 10.1007/s00401-018-1807-1
Damkier HH, Brown PD, Praetorius J. Cerebrospinal fluid secretion by the choroid plexus. Physiol Rev. 2013;93(4):1847–92.
pubmed: 24137023 doi: 10.1152/physrev.00004.2013
Redzic ZB, Segal MB. The structure of the choroid plexus and the physiology of the choroid plexus epithelium. Adv Drug Deliv Rev. 2004;56(12):1695–716.
pubmed: 15381330 doi: 10.1016/j.addr.2004.07.005
Praetorius J, Damkier HH. Transport across the choroid plexus epithelium. Am J Physiol Cell Physiol. 2017;312(6):C673–86.
pubmed: 28330845 doi: 10.1152/ajpcell.00041.2017
Kaur C, Rathnasamy G, Ling EA. The choroid plexus in healthy and diseased brain. J Neuropathol Exp Neurol. 2016;75(3):198–213.
pubmed: 26888305 doi: 10.1093/jnen/nlv030
Alvira-Botero X, Carro EM. Clearance of amyloid-beta peptide across the choroid plexus in Alzheimer’s disease. Curr Aging Sci. 2010;3(3):219–29.
pubmed: 20735345 doi: 10.2174/1874609811003030219
Chebli J, Rahmati M, Lashley T, Edeman B, Oldfors A, Zetterberg H, et al. The localization of amyloid precursor protein to ependymal cilia in vertebrates and its role in ciliogenesis and brain development in zebrafish. Sci Rep. 2021;11(1):19115.
pubmed: 34580355 pmcid: 8476544 doi: 10.1038/s41598-021-98487-7
Serot JM, Bene MC, Foliguet B, Faure GC. Morphological alterations of the choroid plexus in late-onset Alzheimer’s disease. Acta Neuropathol. 2000;99(2):105–8.
pubmed: 10672315 doi: 10.1007/PL00007412
Gonzalez-Marrero I, Gimenez-Llort L, Johanson CE, Carmona-Calero EM, Castaneyra-Ruiz L, Brito-Armas JM, et al. Choroid plexus dysfunction impairs beta-amyloid clearance in a triple transgenic mouse model of Alzheimer’s disease. Front Cell Neurosci. 2015;9:17.
pubmed: 25705176 pmcid: 4319477 doi: 10.3389/fncel.2015.00017
Brkic M, Balusu S, Van Wonterghem E, Gorle N, Benilova I, Kremer A, et al. Amyloid beta oligomers disrupt blood-CSF barrier integrity by activating matrix metalloproteinases. J Neurosci. 2015;35(37):12766–78.
pubmed: 26377465 pmcid: 6795210 doi: 10.1523/JNEUROSCI.0006-15.2015
Steeland S, Gorle N, Vandendriessche C, Balusu S, Brkic M, Van Cauwenberghe C, et al. Counteracting the effects of TNF receptor-1 has therapeutic potential in Alzheimer’s disease. EMBO Mol Med. 2018;10(4):e8300.
pubmed: 29472246 pmcid: 5887909 doi: 10.15252/emmm.201708300
Silverberg GD, Heit G, Huhn S, Jaffe RA, Chang SD, Bronte-Stewart H, et al. The cerebrospinal fluid production rate is reduced in dementia of the Alzheimer’s type. Neurology. 2001;57(10):1763–6.
pubmed: 11723260 doi: 10.1212/WNL.57.10.1763
Serot JM, Peltier J, Fichten A, Ledeme N, Bourgeois AM, Jouanny P, et al. Reduced CSF turnover and decreased ventricular Abeta42 levels are related. BMC Neurosci. 2011;12:42.
pubmed: 21569454 pmcid: 3117747 doi: 10.1186/1471-2202-12-42
Serot JM, Zmudka J, Jouanny P. A possible role for CSF turnover and choroid plexus in the pathogenesis of late onset Alzheimer’s disease. J Alzheimers Dis. 2012;30(1):17–26.
pubmed: 22349684 doi: 10.3233/JAD-2012-111964
Wostyn P, Audenaert K, De Deyn PP. Choroidal proteins involved in cerebrospinal fluid production may be potential drug targets for Alzheimer’s disease therapy. Perspect Medicin Chem. 2011;5:11–7.
pubmed: 21487536 pmcid: 3072647 doi: 10.4137/PMC.S6509
Kalaria RN, Premkumar DR, Pax AB, Cohen DL, Lieberburg I. Production and increased detection of amyloid beta protein and amyloidogenic fragments in brain microvessels, meningeal vessels and choroid plexus in Alzheimer’s disease. Brain Res Mol Brain Res. 1996;35(1–2):58–68.
pubmed: 8717340 doi: 10.1016/0169-328X(95)00180-Z
Premkumar DR, Kalaria RN. Altered expression of amyloid beta precursor mRNAs in cerebral vessels, meninges, and choroid plexus in Alzheimer’s disease. Ann N Y Acad Sci. 1996;777:288–92.
pubmed: 8624100 doi: 10.1111/j.1749-6632.1996.tb34434.x
Sousa JC, Cardoso I, Marques F, Saraiva MJ, Palha JA. Transthyretin and Alzheimer’s disease: where in the brain? Neurobiol Aging. 2007;28(5):713–8.
pubmed: 16698124 doi: 10.1016/j.neurobiolaging.2006.03.015
Kant S, Stopa EG, Johanson CE, Baird A, Silverberg GD. Choroid plexus genes for CSF production and brain homeostasis are altered in Alzheimer’s disease. Fluids Barriers CNS. 2018;15(1):34.
pubmed: 30541599 pmcid: 6291926 doi: 10.1186/s12987-018-0120-7
Stopa EG, Tanis KQ, Miller MC, Nikonova EV, Podtelezhnikov AA, Finney EM, et al. Comparative transcriptomics of choroid plexus in Alzheimer’s disease, frontotemporal dementia and Huntington’s disease: implications for CSF homeostasis. Fluids Barriers CNS. 2018;15(1):18.
pubmed: 29848382 pmcid: 5977762 doi: 10.1186/s12987-018-0102-9
Leitner DF, Kanshin E, Faustin A, Thierry M, Friedman D, Devore S, et al. Localized proteomic differences in the choroid plexus of Alzheimer’s disease and epilepsy patients. Front Neurol. 2023;14:1221775.
pubmed: 37521285 pmcid: 10379643 doi: 10.3389/fneur.2023.1221775
Carna M, Onyango IG, Katina S, Holub D, Novotny JS, Nezvedova M, et al. Pathogenesis of Alzheimer’s disease: involvement of the choroid plexus. Alzheimers Dement. 2023;19(8):3537–54.
pubmed: 36825691 doi: 10.1002/alz.12970
Tijms BM, Vromen EM, Mjaavatten O, Holstege H, Reus LM, van der Lee S, et al. Cerebrospinal fluid proteomics in patients with Alzheimer’s disease reveals five molecular subtypes with distinct genetic risk profiles. Nat Aging. 2024. https://doi.org/10.1038/s43587-023-00550-7 .
doi: 10.1038/s43587-023-00550-7 pubmed: 38195725 pmcid: 10798889
Saito T, Matsuba Y, Mihira N, Takano J, Nilsson P, Itohara S, et al. Single App knock-in mouse models of Alzheimer’s disease. Nat Neurosci. 2014;17(5):661–3.
pubmed: 24728269 doi: 10.1038/nn.3697
Nilsson P, Saito T, Saido TC. New mouse model of Alzheimer’s. ACS Chem Neurosci. 2014;5(7):499–502.
pubmed: 24852598 pmcid: 4102956 doi: 10.1021/cn500105p
Xie J, Gorle N, Vandendriessche C, Van Imschoot G, Van Wonterghem E, Van Cauwenberghe C, et al. Low-grade peripheral inflammation affects brain pathology in the App(NL-G-F)mouse model of Alzheimer’s disease. Acta Neuropathol Commun. 2021;9(1):163.
pubmed: 34620254 pmcid: 8499584 doi: 10.1186/s40478-021-01253-z
Sasaguri H, Nilsson P, Hashimoto S, Nagata K, Saito T, De Strooper B, et al. APP mouse models for Alzheimer’s disease preclinical studies. EMBO J. 2017;36(17):2473–87.
pubmed: 28768718 pmcid: 5579350 doi: 10.15252/embj.201797397
Noor Z, Ahn SB, Baker MS, Ranganathan S, Mohamedali A. Mass spectrometry-based protein identification in proteomics-a review. Brief Bioinform. 2021;22(2):1620–38.
pubmed: 32047889 doi: 10.1093/bib/bbz163
Delvenne A, Gobom J, Tijms B, Bos I, Reus LM, Dobricic V, et al. Cerebrospinal fluid proteomic profiling of individuals with mild cognitive impairment and suspected non-Alzheimer’s disease pathophysiology. Alzheimers Dement. 2022;19:807–20.
doi: 10.1002/alz.12713
Mehla J, Lacoursiere SG, Lapointe V, McNaughton BL, Sutherland RJ, McDonald RJ, et al. Age-dependent behavioral and biochemical characterization of single APP knock-in mouse (APP(NL-G-F/NL-G-F)) model of Alzheimer’s disease. Neurobiol Aging. 2019;75:25–37.
pubmed: 30508733 doi: 10.1016/j.neurobiolaging.2018.10.026
Liu L, Duff K. A technique for serial collection of cerebrospinal fluid from the cisterna magna in mouse. J Vis Exp. 2008. https://doi.org/10.3791/960 .
doi: 10.3791/960 pubmed: 19066529 pmcid: 2762909
Van Wonterghem E, Van Hoecke L, Van Imschoot G, Verhaege D, Burgelman M, Vandenbroucke RE. Microdissection and whole mount scanning electron microscopy visualization of mouse choroid plexus. J Vis Exp. 2022;190: e64733.
Boeddrich A, Haenig C, Neuendorf N, Blanc E, Ivanov A, Kirchner M, et al. A proteomics analysis of 5xFAD mouse brain regions reveals the lysosome-associated protein Arl8b as a candidate biomarker for Alzheimer’s disease. Genome Med. 2023;15(1):50.
pubmed: 37468900 pmcid: 10357615 doi: 10.1186/s13073-023-01206-2
Marques F, Sousa JC, Coppola G, Gao F, Puga R, Brentani H, et al. Transcriptome signature of the adult mouse choroid plexus. Fluids Barriers CNS. 2011;8(1):10.
pubmed: 21349147 pmcid: 3042978 doi: 10.1186/2045-8118-8-10
Booij JC, van Soest S, Swagemakers SM, Essing AH, Verkerk AJ, van der Spek PJ, et al. Functional annotation of the human retinal pigment epithelium transcriptome. BMC Genomics. 2009;10:164.
pubmed: 19379482 pmcid: 2679759 doi: 10.1186/1471-2164-10-164
Kramer A, Green J, Pollard J Jr, Tugendreich S. Causal analysis approaches in ingenuity pathway analysis. Bioinformatics. 2014;30(4):523–30.
pubmed: 24336805 doi: 10.1093/bioinformatics/btt703
Mi H, Muruganujan A, Huang X, Ebert D, Mills C, Guo X, et al. Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0). Nat Protoc. 2019;14(3):703–21.
pubmed: 30804569 pmcid: 6519457 doi: 10.1038/s41596-019-0128-8
Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25(8):1091–3.
pubmed: 19237447 pmcid: 2666812 doi: 10.1093/bioinformatics/btp101
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Methodol). 1995;57(1):289–300.
doi: 10.1111/j.2517-6161.1995.tb02031.x
UniProt C. UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res. 2023;51(D1):D523–31.
doi: 10.1093/nar/gkac1052
Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419.
pubmed: 25613900 doi: 10.1126/science.1260419
Bos I, Vos S, Vandenberghe R, Scheltens P, Engelborghs S, Frisoni G, et al. The EMIF-AD multimodal biomarker discovery study: design, methods and cohort characteristics. Alzheimers Res Ther. 2018;10(1):64.
pubmed: 29980228 pmcid: 6035398 doi: 10.1186/s13195-018-0396-5
Morris JC, Schindler SE, McCue LM, Moulder KL, Benzinger TLS, Cruchaga C, et al. Assessment of racial disparities in biomarkers for Alzheimer disease. JAMA Neurol. 2019;76(3):264–73.
pubmed: 30615028 pmcid: 6439726 doi: 10.1001/jamaneurol.2018.4249
Bos I, Verhey FR, Ramakers I, Jacobs HIL, Soininen H, Freund-Levi Y, et al. Cerebrovascular and amyloid pathology in predementia stages: the relationship with neurodegeneration and cognitive decline. Alzheimers Res Ther. 2017;9(1):101.
pubmed: 29284531 pmcid: 5747152 doi: 10.1186/s13195-017-0328-9
Batth TS, Francavilla C, Olsen JV. Off-line high-pH reversed-phase fractionation for in-depth phosphoproteomics. J Proteome Res. 2014;13(12):6176–86.
pubmed: 25338131 doi: 10.1021/pr500893m
Magdalinou NK, Noyce AJ, Pinto R, Lindstrom E, Holmen-Larsson J, Holtta M, et al. Identification of candidate cerebrospinal fluid biomarkers in parkinsonism using quantitative proteomics. Parkinsonism Relat Disord. 2017;37:65–71.
pubmed: 28214264 doi: 10.1016/j.parkreldis.2017.01.016
Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature. 2012;489(7416):391–9.
pubmed: 22996553 pmcid: 4243026 doi: 10.1038/nature11405
Rouillard AD, Gundersen GW, Fernandez NF, Wang Z, Monteiro CD, McDermott MG, et al. The harmonizome: a collection of processed datasets gathered to serve and mine knowledge about genes and proteins. Database Oxford. 2016;2016:baw100.
pubmed: 27374120 pmcid: 4930834 doi: 10.1093/database/baw100
Grote S, Prufer K, Kelso J, Dannemann M. ABAEnrichment: an R package to test for gene set expression enrichment in the adult and developing human brain. Bioinformatics. 2016;32(20):3201–3.
pubmed: 27354695 pmcid: 5048072 doi: 10.1093/bioinformatics/btw392
Mesquita SD, Ferreira AC, Gao F, Coppola G, Geschwind DH, Sousa JC, et al. The choroid plexus transcriptome reveals changes in type I and II interferon responses in a mouse model of Alzheimer’s disease. Brain Behav Immun. 2015;49:280–92.
pubmed: 26092102 doi: 10.1016/j.bbi.2015.06.008
Liu R, Zhang Z, Chen Y, Liao J, Wang Y, Liu J, et al. Choroid plexus epithelium and its role in neurological diseases. Front Mol Neurosci. 2022;15: 949231.
pubmed: 36340696 pmcid: 9633854 doi: 10.3389/fnmol.2022.949231
Serot JM, Bene MC, Foliguet B, Faure GC. Altered choroid plexus basement membrane and epithelium in late-onset Alzheimer’s disease: an ultrastructural study. Ann N Y Acad Sci. 1997;826:507–9.
pubmed: 9329734 doi: 10.1111/j.1749-6632.1997.tb48514.x
Marques F, Sousa JC. The choroid plexus is modulated by various peripheral stimuli: implications to diseases of the central nervous system. Front Cell Neurosci. 2015;9:136.
pubmed: 26236190 pmcid: 4394702 doi: 10.3389/fncel.2015.00136
Whyte LS, Hassiotis S, Hattersley KJ, Hemsley KM, Hopwood JJ, Lau AA, et al. Lysosomal dysregulation in the murine App(NL-G-F/NL-G-F) model of Alzheimer’s disease. Neuroscience. 2020;429:143–55.
pubmed: 31917339 doi: 10.1016/j.neuroscience.2019.12.042
Szabo MP, Mishra S, Knupp A, Young JE. The role of Alzheimer’s disease risk genes in endolysosomal pathways. Neurobiol Dis. 2022;162: 105576.
pubmed: 34871734 doi: 10.1016/j.nbd.2021.105576
Van Acker ZP, Bretou M, Annaert W. Endo-lysosomal dysregulations and late-onset Alzheimer’s disease: impact of genetic risk factors. Mol Neurodegener. 2019;14(1):20.
pubmed: 31159836 pmcid: 6547588 doi: 10.1186/s13024-019-0323-7
Zhang W, Xu C, Sun J, Shen HM, Wang J, Yang C. Impairment of the autophagy-lysosomal pathway in Alzheimer’s diseases: pathogenic mechanisms and therapeutic potential. Acta Pharm Sin B. 2022;12(3):1019–40.
pubmed: 35530153 pmcid: 9069408 doi: 10.1016/j.apsb.2022.01.008
Joshi G, Bekier ME 2nd, Wang Y. Golgi fragmentation in Alzheimer’s disease. Front Neurosci. 2015;9:340.
pubmed: 26441511 pmcid: 4585163 doi: 10.3389/fnins.2015.00340
Li JQ, Yu JT, Jiang T, Tan L. Endoplasmic reticulum dysfunction in Alzheimer’s disease. Mol Neurobiol. 2015;51(1):383–95.
pubmed: 24715417 doi: 10.1007/s12035-014-8695-8
Krzyzanowska A, Carro E. Pathological alteration in the choroid plexus of Alzheimer’s disease: implication for new therapy approaches. Front Pharmacol. 2012;3:75.
pubmed: 22563316 pmcid: 3342675 doi: 10.3389/fphar.2012.00075
Cottrell DA, Blakely EL, Johnson MA, Ince PG, Turnbull DM. Mitochondrial enzyme-deficient hippocampal neurons and choroidal cells in AD. Neurology. 2001;57(2):260–4.
pubmed: 11468310 doi: 10.1212/WNL.57.2.260
Vargas T, Ugalde C, Spuch C, Antequera D, Moran MJ, Martin MA, et al. Abeta accumulation in choroid plexus is associated with mitochondrial-induced apoptosis. Neurobiol Aging. 2010;31(9):1569–81.
pubmed: 18838197 doi: 10.1016/j.neurobiolaging.2008.08.017
Pifferi F, Laurent B, Plourde M. Lipid transport and metabolism at the blood-brain interface: implications in health and disease. Front Physiol. 2021;12: 645646.
pubmed: 33868013 pmcid: 8044814 doi: 10.3389/fphys.2021.645646
Yin C, Ackermann S, Ma Z, Mohanta SK, Zhang C, Li Y, et al. ApoE attenuates unresolvable inflammation by complex formation with activated C1q. Nat Med. 2019;25(3):496–506.
pubmed: 30692699 pmcid: 6420126 doi: 10.1038/s41591-018-0336-8
Serot JM, Bene MC, Faure GC. Comparative immunohistochemical characteristics of human choroid plexus in vascular and Alzheimer’s dementia. Hum Pathol. 1994;25(11):1185–90.
pubmed: 7959663 doi: 10.1016/0046-8177(94)90035-3
Solar P, Zamani A, Kubickova L, Dubovy P, Joukal M. Choroid plexus and the blood-cerebrospinal fluid barrier in disease. Fluids Barriers CNS. 2020;17(1):35.
pubmed: 32375819 pmcid: 7201396 doi: 10.1186/s12987-020-00196-2
Choi JD, Moon Y, Kim HJ, Yim Y, Lee S, Moon WJ. Choroid plexus volume and permeability at brain MRI within the Alzheimer disease clinical spectrum. Radiology. 2022;304(3):635–45.
pubmed: 35579521 doi: 10.1148/radiol.212400
Dietrich MO, Spuch C, Antequera D, Rodal I, de Yebenes JG, Molina JA, et al. Megalin mediates the transport of leptin across the blood-CSF barrier. Neurobiol Aging. 2008;29(6):902–12.
pubmed: 17324488 doi: 10.1016/j.neurobiolaging.2007.01.008
Masuda A, Kobayashi Y, Kogo N, Saito T, Saido TC, Itohara S. Cognitive deficits in single App knock-in mouse models. Neurobiol Learn Mem. 2016;135:73–82.
pubmed: 27377630 doi: 10.1016/j.nlm.2016.07.001

Auteurs

Aurore Delvenne (A)

Department of Psychiatry and Neuropsychology, Alzheimer Centrum Limburg, School for Mental Health and Neuroscience, Maastricht University, P.O. Box 616, Maastricht, 6200 MD, The Netherlands. a.delvenne@maastrichtuniversity.nl.

Charysse Vandendriessche (C)

VIB Center for Inflammation Research, VIB, Ghent, Belgium.
Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium.

Johan Gobom (J)

Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden.
Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden.

Marlies Burgelman (M)

VIB Center for Inflammation Research, VIB, Ghent, Belgium.
Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium.

Pieter Dujardin (P)

VIB Center for Inflammation Research, VIB, Ghent, Belgium.
Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium.

Clint De Nolf (C)

Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium.
Department of Internal Medicine and Pediatrics, Ghent University, Ghent, Belgium.

Betty M Tijms (BM)

Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.

Charlotte E Teunissen (CE)

Neurochemistry Laboratory, Department of Clinical Chemistry, Amsterdam University Medical Centers (AUMC), Amsterdam Neuroscience, Amsterdam, Netherlands.

Suzanne E Schindler (SE)

Department of Neurology, Washington University School of Medicine, St. Louis, USA.
Knight Alzheimer's Disease Research Center, Washington University School of Medicine, St. Louis, USA.

Frans Verhey (F)

Department of Psychiatry and Neuropsychology, Alzheimer Centrum Limburg, School for Mental Health and Neuroscience, Maastricht University, P.O. Box 616, Maastricht, 6200 MD, The Netherlands.

Inez Ramakers (I)

Department of Psychiatry and Neuropsychology, Alzheimer Centrum Limburg, School for Mental Health and Neuroscience, Maastricht University, P.O. Box 616, Maastricht, 6200 MD, The Netherlands.

Pablo Martinez-Lage (P)

Fundación CITA-Alzhéimer Fundazioa, San Sebastian, Spain.

Mikel Tainta (M)

Fundación CITA-Alzhéimer Fundazioa, San Sebastian, Spain.

Rik Vandenberghe (R)

Neurology Service, University Hospitals Leuven, Louvain, Belgium.
Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Louvain, Belgium.

Jolien Schaeverbeke (J)

Neurology Service, University Hospitals Leuven, Louvain, Belgium.
Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Louvain, Belgium.

Sebastiaan Engelborghs (S)

Reference Center for Biological Markers of Dementia (BIODEM), Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.
Department of Neurology and Bru-BRAIN, Universitair Ziekenhuis Brussel, Brussels, Belgium.
NEUR Research Group, Center for Neurosciences (C4N), Vrije Universiteit Brussel, Brussels, Belgium.

Ellen De Roeck (E)

Reference Center for Biological Markers of Dementia (BIODEM), Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.
Department of Neurology and Memory Clinic, Hospital Network Antwerp (ZNA) Middelheim and Hoge Beuken, Antwerp, Belgium.

Julius Popp (J)

Old Age Psychiatry, University Hospital Lausanne, Lausanne, Switzerland.
Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatry University Hospital Zürich, Zurich, Switzerland.

Gwendoline Peyratout (G)

Old Age Psychiatry, University Hospital Lausanne, Lausanne, Switzerland.

Magda Tsolaki (M)

1st Department of Neurology, AHEPA University Hospital, Medical School, Faculty of Health Sciences, Aristotle University of Thessaloniki, Makedonia, Thessaloniki, Greece.

Yvonne Freund-Levi (Y)

Department of Neurobiology, Caring Sciences and Society (NVS), Division of Clinical Geriatrics, Karolinska Institutet, Stockholm, Sweden.
Department of Psychiatry in Region Örebro County and School of Medical Sciences, Faculty of Medicine and Health, Örebro University, Örebro, Sweden.
Department of Old Age Psychiatry, Psychology & Neuroscience, King's College, London, UK.

Simon Lovestone (S)

University of Oxford, Oxford, UK.
Johnson and Johnson Medical Ltd., Wokingham, UK.

Johannes Streffer (J)

Reference Center for Biological Markers of Dementia (BIODEM), Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.
H. Lundbeck A/S, Valby, Denmark.

Lars Bertram (L)

Lübeck Interdisciplinary Platform for Genome Analytics, University of Lübeck, Lübeck, Germany.

Kaj Blennow (K)

Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden.
Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden.
Paris Brain Institute, ICM, Pitié-Salpêtrière Hospital, Sorbonne University, Paris, France.
Neurodegenerative Disorder Research Center, Division of Life Sciences and Medicine, and Department of Neurology, Institute on Aging and Brain Disorders, University of Science and Technology of China and First Affiliated Hospital of USTC, Hefei, People's Republic of China.

Henrik Zetterberg (H)

Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden.
Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden.
Department of Neurodegenerative Disease, UCL Institute of Neurology, London, UK.
UK Dementia Research Institute at UCL, London, UK.
Hong Kong Center for Neurodegenerative Diseases, Clear Water Bay, Hong Kong, China.
Wisconsin Alzheimer's Disease Research Center, University of Wisconsin School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI, 53792, USA.

Pieter Jelle Visser (PJ)

Department of Psychiatry and Neuropsychology, Alzheimer Centrum Limburg, School for Mental Health and Neuroscience, Maastricht University, P.O. Box 616, Maastricht, 6200 MD, The Netherlands.
Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.
Department of Neurobiology, Care Sciences and Society, Division of Neurogeriatrics, Karolinska Institutet, Stockholm, Sweden.

Roosmarijn E Vandenbroucke (RE)

VIB Center for Inflammation Research, VIB, Ghent, Belgium.
Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium.

Stephanie J B Vos (SJB)

Department of Psychiatry and Neuropsychology, Alzheimer Centrum Limburg, School for Mental Health and Neuroscience, Maastricht University, P.O. Box 616, Maastricht, 6200 MD, The Netherlands.

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Classifications MeSH

questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Ventricules cérébraux › Plexus choroïde › Involvement of the choroid plexus in...
questionsmedicales.fr › Troubles mentaux › Troubles neurocognitifs › Démence › Maladie d'Alzheimer › Involvement of the choroid plexus in...
questionsmedicales.fr › Eucaryotes › Animaux › Involvement of the choroid plexus in...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Involvement of the choroid plexus in...
questionsmedicales.fr › Disciplines des sciences naturelles › Chimie › Biochimie › Protéomique › Involvement of the choroid plexus in...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Souris transgéniques › Involvement of the choroid plexus in...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Involvement of the choroid plexus in...
questionsmedicales.fr › Techniques d'investigation › Modèles théoriques › Modèles biologiques › Modèles animaux de maladie humaine › Involvement of the choroid plexus in...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines sécrétoires inhibitrices de protéinases › Protéase nexines › Précurseur de la protéine bêta-amyloïde › Involvement of the choroid plexus in...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéome › Involvement of the choroid plexus in...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Lignées consanguines de souris › Souris de lignée C57BL › Involvement of the choroid plexus in...