HiPSC-derived 3D neural models reveal neurodevelopmental pathomechanisms of the Cockayne Syndrome B.
Humans
Induced Pluripotent Stem Cells
/ metabolism
Cockayne Syndrome
/ genetics
Oligodendroglia
/ metabolism
Cell Movement
DNA Repair Enzymes
/ metabolism
Neurons
/ metabolism
Autophagy
Brain
/ metabolism
Poly-ADP-Ribose Binding Proteins
/ metabolism
gamma-Aminobutyric Acid
/ metabolism
DNA Helicases
/ metabolism
Microcephaly
/ pathology
Demyelinating Diseases
/ pathology
Cell Differentiation
Autophagy
Brain development
Disease modeling
GABA
HDAC
In vitro
MEA
Migration
Oligodendrocytes
Personalized
Journal
Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402
Informations de publication
Date de publication:
23 Aug 2024
23 Aug 2024
Historique:
received:
08
01
2024
accepted:
09
08
2024
revised:
08
08
2024
medline:
24
8
2024
pubmed:
24
8
2024
entrez:
23
8
2024
Statut:
epublish
Résumé
Cockayne Syndrome B (CSB) is a hereditary multiorgan syndrome which-through largely unknown mechanisms-can affect the brain where it clinically presents with microcephaly, intellectual disability and demyelination. Using human induced pluripotent stem cell (hiPSC)-derived neural 3D models generated from CSB patient-derived and isogenic control lines, we here provide explanations for these three major neuropathological phenotypes. In our models, CSB deficiency is associated with (i) impaired cellular migration due to defective autophagy as an explanation for clinical microcephaly; (ii) altered neuronal network functionality and neurotransmitter GABA levels, which is suggestive of a disturbed GABA switch that likely impairs brain circuit formation and ultimately causes intellectual disability; and (iii) impaired oligodendrocyte maturation as a possible cause of the demyelination observed in children with CSB. Of note, the impaired migration and oligodendrocyte maturation could both be partially rescued by pharmacological HDAC inhibition.
Identifiants
pubmed: 39179905
doi: 10.1007/s00018-024-05406-w
pii: 10.1007/s00018-024-05406-w
doi:
Substances chimiques
DNA Repair Enzymes
EC 6.5.1.-
Poly-ADP-Ribose Binding Proteins
0
ERCC6 protein, human
EC 3.6.4.12
gamma-Aminobutyric Acid
56-12-2
DNA Helicases
EC 3.6.4.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
368Subventions
Organisme : Leibniz-Gemeinschaft
ID : K246/2019
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC 2048/1
Informations de copyright
© 2024. The Author(s).
Références
Karikkineth AC, Scheibye-Knudsen M, Fivenson E et al (2017) Cockayne syndrome: clinical features, model systems and pathways. Ageing Res Rev 33:3–17. https://doi.org/10.1016/j.arr.2016.08.002
doi: 10.1016/j.arr.2016.08.002
pubmed: 27507608
Laugel V, Dalloz C, Tobias ES et al (2008) Cerebro-oculo-facio-skeletal syndrome: three additional cases with CSB mutations, new diagnostic criteria and an approach to investigation. J Med Genet 45:564–571. https://doi.org/10.1136/jmg.2007.057141
doi: 10.1136/jmg.2007.057141
pubmed: 18628313
Schmickel RD, Chu EHY, Trosko JE, Chang CC (1977) Cockayne syndrome: a cellular sensitivity to ultraviolet light. Pediatrics 60:135–139
doi: 10.1542/peds.60.2.135
pubmed: 887325
Paddison PM, Moossy J, Derbres VJ, Klopfer W (1963) Cockayne’s syndrome. A report of five new cases with biochemical, chromosomal, dermatologic, genetic and neuropathologic observations. Dermatol Trop Ecol Geogr 15:195–203
pubmed: 14156156
Moossy J (1967) The neuropathology of Cockayne’s syndrome. J Neuropathol Exp Neurol 26:654–660. https://doi.org/10.1097/00005072-196710000-00010
doi: 10.1097/00005072-196710000-00010
pubmed: 6053735
Sugarman GI, Landing BH, Reed WB (1977) Cockayne syndrome: clinical study of two patients and neuropathologic findings in one. Clin Pediatr (Phila) 16:225–232. https://doi.org/10.1177/000992287701600304
doi: 10.1177/000992287701600304
pubmed: 837626
Laugel V, Dalloz C, Durand M et al (2010) Mutation update for the CSB/ERCC6 and CSA/ERCC8 genes involved in Cockayne syndrome. Hum Mutat 31:113–126. https://doi.org/10.1002/humu.21154
doi: 10.1002/humu.21154
pubmed: 19894250
Kraemer KH, Patronas NJ, Schiffmann R et al (2008) Cockayne syndrome: a complex genotype-phenotype. Neuroscience 145:1388–1396
doi: 10.1016/j.neuroscience.2006.12.020
Chikhaoui A, Kraoua I, Calmels N et al (2022) Heterogeneous clinical features in Cockayne syndrome patients and siblings carrying the same CSA mutations. Orphanet J Rare Dis 17:121. https://doi.org/10.1186/s13023-022-02257-1
doi: 10.1186/s13023-022-02257-1
pubmed: 35248096
pmcid: 8898519
Natale V (2011) A comprehensive description of the severity groups in Cockayne syndrome. Am J Med Genet A 155A(5):1081–1095. https://doi.org/10.1002/ajmg.a.33933
doi: 10.1002/ajmg.a.33933
pubmed: 21480477
De Waard H, De Wit J, Gorgels TGMF et al (2003) Cell type-specific hypersensitivity to oxidative damage in CSB and XPA mice. DNA Repair (Amst) 2:13–25. https://doi.org/10.1016/S1568-7864(02)00188-X
doi: 10.1016/S1568-7864(02)00188-X
pubmed: 12509265
Gorgels TGMF, van der Pluijm I, Brandt RMC et al (2007) Retinal degeneration and ionizing radiation hypersensitivity in a mouse model for Cockayne syndrome. Mol Cell Biol 27:1433–1441. https://doi.org/10.1128/mcb.01037-06
doi: 10.1128/mcb.01037-06
pubmed: 17145777
Jaarsma D, van der Pluijm I, van der Horst GTJ, Hoeijmakers JHJ (2013) Cockayne syndrome pathogenesis: lessons from mouse models. Mech Ageing Dev 134:180–195. https://doi.org/10.1016/j.mad.2013.04.003
doi: 10.1016/j.mad.2013.04.003
pubmed: 23591128
Vessoni AT, Guerra CCC, Kajitani GS et al (2020) Cockayne syndrome: the many challenges and approaches to understand a multifaceted disease. Genet Mol Biol. https://doi.org/10.1590/1678-4685-GMB-2019-0085
doi: 10.1590/1678-4685-GMB-2019-0085
pubmed: 32453336
pmcid: 7250278
Xu Y, Wu Z, Liu L et al (2019) Rat model of Cockayne syndrome neurological disease. Cell Rep 29:800-809.e5. https://doi.org/10.1016/j.celrep.2019.09.028
doi: 10.1016/j.celrep.2019.09.028
pubmed: 31644904
Van der Horst GTJ, Van Steeg H, Berg RJW et al (1997) Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell 89:425–435. https://doi.org/10.1016/S0092-8674(00)80223-8
doi: 10.1016/S0092-8674(00)80223-8
pubmed: 9150142
Frouin E, Laugel V, Durand M et al (2013) Dermatologic findings in 16 patients with Cockayne syndrome and Cerebro-oculo-facial-skeletal syndrome. JAMA Dermatol 149:1414–1418. https://doi.org/10.1001/jamadermatol.2013.6683
doi: 10.1001/jamadermatol.2013.6683
pubmed: 24154677
Majora M, Sondenheimer K, Knechten M et al (2018) HDAC inhibition improves autophagic and lysosomal function to prevent loss of subcutaneous fat in a mouse model of Cockayne syndrome. Sci Transl Med. https://doi.org/10.1126/scitranslmed.aam7510
doi: 10.1126/scitranslmed.aam7510
pubmed: 30158153
Fritsche E, Tigges J, Hartmann J et al (2020) Neural in vitro models for studying substances acting on the central nervous system. Handb Exp Pharmacol. https://doi.org/10.1007/164_2020_367
doi: 10.1007/164_2020_367
Fritsche E, Haarmann-Stemmann T, Kapr J et al (2020) Stem cells for next level toxicity testing in the 21st century. Small 2006252:1–31. https://doi.org/10.1002/smll.202006252
doi: 10.1002/smll.202006252
Azar J, Bahmad HF, Daher D et al (2021) The use of stem cell-derived organoids in disease modeling: an update. Int J Mol Sci. https://doi.org/10.3390/ijms22147667
doi: 10.3390/ijms22147667
pubmed: 34768800
pmcid: 8583606
Pamies D, Wiersma D, Katt ME et al (2022) Human organotypic brain model as a tool to study chemical-induced dopaminergic neuronal toxicity. Neurobiol Dis 169:105719. https://doi.org/10.1016/j.nbd.2022.105719
doi: 10.1016/j.nbd.2022.105719
pubmed: 35398340
pmcid: 9298686
Park J, Wetzel I, Marriott I et al (2018) A 3D human triculture system modeling neurodegeneration and neuroinflammation in Alzheimer’s disease. Nat Neurosci 21:941–951. https://doi.org/10.1038/s41593-018-0175-4
doi: 10.1038/s41593-018-0175-4
pubmed: 29950669
pmcid: 6800152
Martins S, Hacheney I, Teichweyde N et al (2021) Generation of an induced pluripotent stem cell line (IUFi001) from a Cockayne syndrome patient carrying a mutation in the ERCC6 gene. Stem Cell Res. https://doi.org/10.1016/j.scr.2021.102456
doi: 10.1016/j.scr.2021.102456
pubmed: 34271225
Pasca AM, Sloan SA, Clarke LE et al (2015) Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat Methods 12:671–678. https://doi.org/10.1038/nmeth.3415
doi: 10.1038/nmeth.3415
pubmed: 26005811
pmcid: 4489980
Mayne L, Lehmann AR (1982) Failure of RNA synthesis to recover after UV irradiation: an early defect in cells from individuals with Cockayne syndrome and xeroderma pigmentosum. Mutat Res 96:140. https://doi.org/10.1016/0027-5107(82)90047-1
doi: 10.1016/0027-5107(82)90047-1
Troelstra C, van Gool A, de Wit J et al (1992) ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne’s syndrome and preferential repair of active genes. Cell 71:939–953. https://doi.org/10.1016/0092-8674(92)90390-X
doi: 10.1016/0092-8674(92)90390-X
pubmed: 1339317
Rapin I, Lindenbaum Y, Dickson DW et al (2000) Cockayne syndrome and xeroderma pigmentosum: DNA repair disorders with overlaps and paradoxes. Neurology 55:1442–1449. https://doi.org/10.1212/WNL.55.10.1442
doi: 10.1212/WNL.55.10.1442
pubmed: 11185579
Lindenbaum Y, Dickson D, Rosenbaum P et al (2001) Xeroderma pigmentosum/Cockayne syndrome complex: first neuropathological study and review of eight other cases. Eur J Paediatr Neurol 5:225–242. https://doi.org/10.1053/ejpn.2001.0523
doi: 10.1053/ejpn.2001.0523
pubmed: 11764181
Ciaffardini F, Nicolai S, Caputo M et al (2014) The Cockayne syndrome B protein is essential for neuronal differentiation and neuritogenesis. Cell Death Dis 5:e1268–e1311. https://doi.org/10.1038/cddis.2014.228
doi: 10.1038/cddis.2014.228
pubmed: 24874740
pmcid: 4047889
Wang Y, Jones-Tabah J, Chakravarty P et al (2016) Pharmacological bypass of Cockayne syndrome B function in neuronal differentiation. Cell Rep 14:2554–2561. https://doi.org/10.1016/j.celrep.2016.02.051
doi: 10.1016/j.celrep.2016.02.051
pubmed: 26972010
pmcid: 4806223
Vessoni AT, Herai RH, Karpiak JV et al (2016) Cockayne syndrome-derived neurons display reduced synapse density and altered neural network synchrony. Hum Mol Genet 25:1271–1280. https://doi.org/10.1093/hmg/ddw008
doi: 10.1093/hmg/ddw008
pubmed: 26755826
pmcid: 4787902
Liang F, Li B, Xu Y et al (2023) Identification and characterization of necdin as a target for the Cockayne syndrome B protein in promoting neuronal differentiation and maintenance. Pharmacol Res 187:106637. https://doi.org/10.1016/j.phrs.2022.106637
doi: 10.1016/j.phrs.2022.106637
pubmed: 36586641
Szepanowski L-P, Wruck W, Kapr J et al (2024) Cockayne syndrome patient iPSC-derived brain organoids and neurospheres show early transcriptional dysregulation of biological processes associated with brain development and metabolism. Cells 13(7):591. https://doi.org/10.3390/cells13070591
doi: 10.3390/cells13070591
pubmed: 38607030
pmcid: 11011893
Brunner JW, Lammertse HCA, van Berkel AA et al (2023) Power and optimal study design in iPSC-based brain disease modelling. Mol Psychiatry 28:1545–1556. https://doi.org/10.1038/s41380-022-01866-3
doi: 10.1038/s41380-022-01866-3
pubmed: 36385170
Hofrichter M, Nimtz L, Tigges J et al (2017) Comparative performance analysis of human iPSC-derived and primary neural progenitor cells (NPC) grown as neurospheres in vitro. Stem Cell Res 25:72–82. https://doi.org/10.1016/j.scr.2017.10.013
doi: 10.1016/j.scr.2017.10.013
pubmed: 29112887
Nimtz L, Hartmann J, Tigges J et al (2020) Characterization and application of electrically active neuronal networks established from human induced pluripotent stem cell-derived neural progenitor cells for neurotoxicity evaluation. Stem Cell Res 45:101761. https://doi.org/10.1016/j.scr.2020.101761
doi: 10.1016/j.scr.2020.101761
pubmed: 32244191
Pamies D, Chesnut M, Smirnova L et al (2021) Human 3D iPSC-derived brain model to study chemical-induced myelin disruption. Glia 69:E392–E394
Hartmann J, Henschel N, Bartmann K et al (2023) Molecular and functional characterization of different brainsphere models for use in neurotoxicity testing on microelectrode arrays. Cells. https://doi.org/10.3390/cells12091270
doi: 10.3390/cells12091270
pubmed: 37508538
pmcid: 10378241
Hofrichter M (2016) Establishment of a hiPSC-based in vitro model to study environmental and genetic disturbances of neurodevelopmental processes. PhD Diss. Heinrich-Heine-University Duesseldorf. urn:nbn:de:hbz:061-20170424-091020-5
Ramachandran H, Martins S, Kontarakis Z et al (2021) Fast but not furious: a streamlined selection method for genome-edited cells. Life Sci Alliance. https://doi.org/10.26508/lsa.202101051
doi: 10.26508/lsa.202101051
pubmed: 33903218
pmcid: 8127327
Nguyen T, Ramachandran H, Martins S et al (2022) Identification of genome edited cells using CRISPRnano. Nucleic Acids Res 50:W199–W203. https://doi.org/10.1093/nar/gkac440
doi: 10.1093/nar/gkac440
pubmed: 35640601
pmcid: 9252781
Tigges J, Bielec K, Brockerhoff G et al (2021) Academic application of good cell culture practice for induced pluripotent stem cells. Altex. https://doi.org/10.14573/altex.2101221
doi: 10.14573/altex.2101221
pubmed: 33963415
Pamies D, Barreras P, Block K et al (2017) A human brain microphysiological system derived from induced pluripotent stem cells to study neurological diseases and toxicity. Altex 34:362–376. https://doi.org/10.14573/altex.1609122
doi: 10.14573/altex.1609122
pubmed: 27883356
Baumann J, Gassmann K, Masjosthusmann S et al (2016) Comparative human and rat neurospheres reveal species differences in chemical effects on neurodevelopmental key events. Arch Toxicol 90:1415–1427. https://doi.org/10.1007/s00204-015-1568-8
doi: 10.1007/s00204-015-1568-8
pubmed: 26216354
Kong L, Zhang Y, Ye ZQ et al (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. https://doi.org/10.1093/nar/gkm391
doi: 10.1093/nar/gkm391
pubmed: 17991683
pmcid: 2238837
Gu J, Weber K, Klemp E et al (2012) Identifying core features of adaptive metabolic mechanisms for chronic heat stress attenuation contributing to systems robustness. Integr Biol 4:480–493. https://doi.org/10.1039/c2ib00109h
doi: 10.1039/c2ib00109h
Shim SH, Lee SK, Lee DW et al (2020) Loss of function of rice plastidic glycolate/glycerate translocator 1 impairs photorespiration and plant growth. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01726
doi: 10.3389/fpls.2019.01726
pubmed: 32765572
pmcid: 7378735
Poirier K, Lebrun N, Broix L et al (2013) Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat Genet 45:639–647. https://doi.org/10.1038/ng.2613
doi: 10.1038/ng.2613
pubmed: 23603762
Becerra-Solano LE, Mateos-Sánchez L, López-Muñoz E (2021) Microcephaly, an etiopathogenic vision. Pediatr Neonatol 62:354–360. https://doi.org/10.1016/j.pedneo.2021.05.008
doi: 10.1016/j.pedneo.2021.05.008
pubmed: 34112604
Laugel V, Dalloz C, Stary A et al (2008) Deletion of 5′ sequences of the CSB gene provides insight into the pathophysiology of Cockayne syndrome. Eur J Hum Genet 16:320–327. https://doi.org/10.1038/sj.ejhg.5201991
doi: 10.1038/sj.ejhg.5201991
pubmed: 18183039
Bartmann K, Bendt F, Dönmez A et al (2023) A human iPSC-based in vitro neural network formation assay to investigate neurodevelopmental toxicity of pesticides. bioRxiv. https://doi.org/10.1101/2023.01.12.523741
doi: 10.1101/2023.01.12.523741
Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728–739. https://doi.org/10.1038/nrn920
doi: 10.1038/nrn920
pubmed: 12209121
de Lange ECM, Hammarlund-Udenaes M (2015) Translational aspects of blood-brain barrier transport and central nervous system effects of drugs: from discovery to patients. Clin Pharmacol Ther 97:380–394. https://doi.org/10.1002/CPT.76
doi: 10.1002/CPT.76
pubmed: 25670219
Arrowsmith J, Miller P (2013) Trial watch: phase II and phase III attrition rates 2011–2012. Nat Rev Drug Discov 12:569. https://doi.org/10.1038/nrd4090
doi: 10.1038/nrd4090
pubmed: 23903212
Cummings JL, Morstorf T, Zhong K (2014) Alzheimer’s disease drug-development pipeline: few candidates, frequent failures. Alzheimer’s Res Ther. https://doi.org/10.1186/alzrt269
doi: 10.1186/alzrt269
Ashmawi NS, Hammoda MA (2022) Early prediction and evaluation of risk of autism spectrum disorders. Cureus. https://doi.org/10.7759/cureus.23465
doi: 10.7759/cureus.23465
pubmed: 36408300
pmcid: 9668347
Kenific CM, Wittmann T, Debnath J (2016) Autophagy in adhesion and migration. J Cell Sci 129:3685–3693. https://doi.org/10.1242/jcs.188490
doi: 10.1242/jcs.188490
pubmed: 27672021
pmcid: 5087656
Kenific CM, Stehbens SJ, Goldsmith J et al (2016) NBR 1 enables autophagy-dependent focal adhesion turnover. J Cell Biol 212:577–590. https://doi.org/10.1083/jcb.201503075
doi: 10.1083/jcb.201503075
pubmed: 26903539
pmcid: 4772495
Hernandez SJ, Fote G, Reyes-Ortiz AM et al (2021) Cooperation of cell adhesion and autophagy in the brain: functional roles in development and neurodegenerative disease. Matrix Biol Plus 12:100089. https://doi.org/10.1016/j.mbplus.2021.100089
doi: 10.1016/j.mbplus.2021.100089
pubmed: 34786551
pmcid: 8579148
Clawson GA (2016) Histone deacetylase inhibitors as cancer therapeutics. Ann Transl Med. https://doi.org/10.21037/atm.2016.07.22
doi: 10.21037/atm.2016.07.22
pubmed: 27568481
pmcid: 4980376
Hartlaub AM, McElroy CA, Maitre NL, Hester ME (2019) Modeling human brain circuitry using pluripotent stem cell platforms. Front Pediatr 7:1–8. https://doi.org/10.3389/fped.2019.00057
doi: 10.3389/fped.2019.00057
Pelkonen A, Pistono C, Klecki P et al (2022) Functional characterization of human pluripotent stem cell-derived models of the brain with microelectrode arrays. Cells. https://doi.org/10.3390/cells11010106
doi: 10.3390/cells11010106
Silbereis JC, Pochareddy S, Zhu Y et al (2016) The cellular and molecular landscapes of the developing human central nervous system. Neuron 89:248. https://doi.org/10.1016/j.neuron.2015.12.008
doi: 10.1016/j.neuron.2015.12.008
pubmed: 26796689
pmcid: 4959909
Budday S, Steinmann P, Kuhl E (2015) Physical biology of human brain development. Front Cell Neurosci 9:1–17. https://doi.org/10.3389/fncel.2015.00257
doi: 10.3389/fncel.2015.00257
Vasudevan P, Suri M (2017) A clinical approach to developmental delay and intellectual disability. Clin Med J R Coll Physicians Lond 17:558–561. https://doi.org/10.7861/clinmedicine.17-6-558
doi: 10.7861/clinmedicine.17-6-558
Peerboom C, Wierenga CJ (2021) The postnatal GABA shift: a developmental perspective. Neurosci Biobehav Rev 124:179–192. https://doi.org/10.1016/j.neubiorev.2021.01.024
doi: 10.1016/j.neubiorev.2021.01.024
pubmed: 33549742
Pozzi D, Rasile M, Corradini I, Matteoli M (2020) Environmental regulation of the chloride transporter KCC2: switching inflammation off to switch the GABA on? Transl Psychiatry. https://doi.org/10.1038/s41398-020-01027-6
doi: 10.1038/s41398-020-01027-6
pubmed: 33293520
pmcid: 7723989
Gitiaux C, Blin-Rochemaure N, Hully M et al (2015) Progressive demyelinating neuropathy correlates with clinical severity in Cockayne syndrome. Clin Neurophysiol 126:1435–1439. https://doi.org/10.1016/j.clinph.2014.10.014
doi: 10.1016/j.clinph.2014.10.014
pubmed: 25453614
Ying Y-Q, Yan X-Q, Jin S-J et al (2018) Inhibitory effect of LPS on the proliferation of oligodendrocyte precursor cells through the notch signaling pathway in intrauterine infection-induced rats. Curr Med Sci 38:840–846. https://doi.org/10.1007/s11596-018-1951-9
doi: 10.1007/s11596-018-1951-9
pubmed: 30341518
Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA (2011) The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci 29:423–440. https://doi.org/10.1016/j.ijdevneu.2011.02.012
doi: 10.1016/j.ijdevneu.2011.02.012
pubmed: 21382469
pmcid: 3099053
Dach K, Bendt F, Huebenthal U et al (2017) BDE-99 impairs differentiation of human and mouse NPCs into the oligodendroglial lineage by species-specific modes of action. Sci Rep. https://doi.org/10.1038/srep44861
doi: 10.1038/srep44861
pubmed: 28317842
pmcid: 5357893
Ehrlich M, Mozafari S, Glatza M et al (2017) Rapid and efficient generation of oligodendrocytes from human induced pluripotent stem cells using transcription factors. Proc Natl Acad Sci USA 114:E2243–E2252. https://doi.org/10.1073/pnas.1614412114
doi: 10.1073/pnas.1614412114
pubmed: 28246330
pmcid: 5358375
Chesnut M, Hartung T, Hogberg H, Pamies D (2021) Human oligodendrocytes and myelin in vitro to evaluate developmental neurotoxicity. Int J Mol Sci 22:7929. https://doi.org/10.3390/ijms22157929
doi: 10.3390/ijms22157929
pubmed: 34360696
pmcid: 8347131
Douvaras P, Fossati V (2015) Generation and isolation of oligodendrocyte progenitor cells from human pluripotent stem cells. Nat Protoc 10:1143–1154. https://doi.org/10.1038/nprot.2015.075
doi: 10.1038/nprot.2015.075
pubmed: 26134954
Noack M, Leyk J, Richter-Landsberg C (2014) HDAC6 inhibition results in tau acetylation and modulates tau phosphorylation and degradation in oligodendrocytes. Glia 62:535–547. https://doi.org/10.1002/glia.22624
doi: 10.1002/glia.22624
pubmed: 24464872
Liu B, Chen X, Wang ZQ, Tong WM (2014) Nbn gene inactivation in the CNS of mouse inhibits the myelinating ability of the mature cortical oligodendrocytes. Glia 62:133–144. https://doi.org/10.1002/glia.22593
doi: 10.1002/glia.22593
pubmed: 24272708
Tauheed AM, Ayo JO, Kawu MU (2016) Regulation of oligodendrocyte differentiation: insights and approaches for the management of neurodegenerative disease. Pathophysiology 23:203–210. https://doi.org/10.1016/j.pathophys.2016.05.007
doi: 10.1016/j.pathophys.2016.05.007
pubmed: 27342760
Yadav R, Mishra P, Yadav D (2019) Histone deacetylase inhibitors: a prospect in drug discovery. Turk J Pharm Sci 16:101–114. https://doi.org/10.4274/tjps.75047
doi: 10.4274/tjps.75047
pubmed: 32454703
Smalley JP, Cowley SM, Hodgkinson JT (2020) Bifunctional HDAC therapeutics: one drug to rule them all? Molecules. https://doi.org/10.3390/molecules25194394
doi: 10.3390/molecules25194394
pubmed: 32987782
pmcid: 7583022
Bondarev AD, Attwood MM, Jonsson J et al (2021) Recent developments of HDAC inhibitors: emerging indications and novel molecules. Br J Clin Pharmacol 87:4577–4597. https://doi.org/10.1111/bcp.14889
doi: 10.1111/bcp.14889
pubmed: 33971031
Tang X, Kim J, Zhou L et al (2016) KCC2 rescues functional deficits in human neurons derived from patients with Rett syndrome. Proc Natl Acad Sci USA 113:751–756. https://doi.org/10.1073/pnas.1524013113
doi: 10.1073/pnas.1524013113
pubmed: 26733678
pmcid: 4725523
Toritsuka M, Yoshino H, Makinodan M et al (2021) Developmental dysregulation of excitatory-to-inhibitory GABA-polarity switch may underlie schizophrenia pathology: a monozygotic-twin discordant case analysis in human iPS cell-derived neurons. Neurochem Int. https://doi.org/10.1016/j.neuint.2021.105179
doi: 10.1016/j.neuint.2021.105179
pubmed: 34500023
Menassa DA, Gomez-Nicola D (2018) Microglial dynamics during human brain development. Front Immunol. https://doi.org/10.3389/fimmu.2018.01014
doi: 10.3389/fimmu.2018.01014
pubmed: 29881376
pmcid: 5976733
Allen NJ, Lyons DA (2018) Glia as architects of central nervous system formation and function. Science 185:181–185
doi: 10.1126/science.aat0473
Bar E, Barak B (2019) Microglia roles in synaptic plasticity and myelination in homeostatic conditions and neurodevelopmental disorders. Glia 67:2125–2141. https://doi.org/10.1002/glia.23637
doi: 10.1002/glia.23637
pubmed: 31058364
Tau GZ, Peterson BS (2010) Normal development of brain circuits. Neuropsychopharmacology 35:147–168. https://doi.org/10.1038/npp.2009.115
doi: 10.1038/npp.2009.115
pubmed: 19794405