Transcriptional and metabolic effects of aspartate-glutamate carrier isoform 1 (AGC1) downregulation in mouse oligodendrocyte precursor cells (OPCs).
Mitochondria
Neurodevelopment
Oligodendrocytes
Omics analysis
SLC25A12/aralar1/AGC1 deficiency
White matter disorder
Journal
Cellular & molecular biology letters
ISSN: 1689-1392
Titre abrégé: Cell Mol Biol Lett
Pays: England
ID NLM: 9607427
Informations de publication
Date de publication:
29 Mar 2024
29 Mar 2024
Historique:
received:
17
10
2023
accepted:
20
03
2024
medline:
30
3
2024
pubmed:
30
3
2024
entrez:
30
3
2024
Statut:
epublish
Résumé
Aspartate-glutamate carrier isoform 1 (AGC1) is a carrier responsible for the export of mitochondrial aspartate in exchange for cytosolic glutamate and is part of the malate-aspartate shuttle, essential for the balance of reducing equivalents in the cells. In the brain, mutations in SLC25A12 gene, encoding for AGC1, cause an ultra-rare genetic disease, reported as a neurodevelopmental encephalopathy, whose symptoms include global hypomyelination, arrested psychomotor development, hypotonia and seizures. Among the biological components most affected by AGC1 deficiency are oligodendrocytes, glial cells responsible for myelination processes, and their precursors [oligodendrocyte progenitor cells (OPCs)]. The AGC1 silencing in an in vitro model of OPCs was documented to cause defects of proliferation and differentiation, mediated by alterations of histone acetylation/deacetylation. Disrupting AGC1 activity could possibly reduce the availability of acetyl groups, leading to perturbation of many biological pathways, such as histone modifications and fatty acids formation for myelin production. Here, we explore the transcriptome of mouse OPCs partially silenced for AGC1, reporting results of canonical analyses (differential expression) and pathway enrichment analyses, which highlight a disruption in fatty acids synthesis from both a regulatory and enzymatic stand. We further investigate the cellular effects of AGC1 deficiency through the identification of most affected transcriptional networks and altered alternative splicing. Transcriptional data were integrated with differential metabolite abundance analysis, showing downregulation of several amino acids, including glutamine and aspartate. Taken together, our results provide a molecular foundation for the effects of AGC1 deficiency in OPCs, highlighting the molecular mechanisms affected and providing a list of actionable targets to mitigate the effects of this pathology.
Identifiants
pubmed: 38553684
doi: 10.1186/s11658-024-00563-z
pii: 10.1186/s11658-024-00563-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
44Subventions
Organisme : Fondazione Telethon
ID : GGP19067
Organisme : Fondazione Telethon
ID : GGP19067a
Organisme : Ministero dell'Istruzione, dell'Università e della Ricerca
ID : 2022CEHEX8
Organisme : Ministero dell'Istruzione, dell'Università e della Ricerca
ID : PE0000006
Informations de copyright
© 2024. The Author(s).
Références
Wibom R, Lasorsa FM, Virpi T, Barbaro M, Sterky FH, Kucinski T, Naess K, Jonsson M, et al. AGC1 deficiency associated with global cerebral hypomyelination. N Engl J Med. 2009;361(5):489–95.
pubmed: 19641205
doi: 10.1056/NEJMoa0900591
Falk MJ, Li D, Gai X, McCormick E, Place E, Lasorsa FM, et al. AGC1 deficiency causes infantile epilepsy, abnormal myelination, and reduced N-acetylaspartate. JIMD Rep. 2014;14:77–85.
pubmed: 24515575
pmcid: 4213337
doi: 10.1007/8904_2013_287
Pfeiffer B, Sen K, Kaur S, Pappas K. Expanding phenotypic spectrum of cerebral aspartate-glutamate carrier isoform 1 (AGC1) deficiency. Neuropediatrics. 2020;51(2):160–3.
pubmed: 31766059
doi: 10.1055/s-0039-3400976
Del Arco A, Agudo M, Satrústegui J. Characterization of a second member of the subfamily of calcium-binding mitochondrial carriers expressed in human non-excitable tissues. Biochem J. 2000;345 Pt 3(Pt 3):725–32.
pubmed: 10642534
doi: 10.1042/bj3450725
Llorente-Folch I, Sahún I, Laura C, Casarejos MJ, Grau JM, Saheki T, Mena MA, et al. AGC1-malate aspartate shuttle activity is critical for dopamine handling in the nigrostriatal pathway. J Neurochem. 2013;124(3):347–62.
pubmed: 23216354
doi: 10.1111/jnc.12096
Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AMA. N-Acetylaspartate in the CNS: from neurodiagnostics to neurobiology. Prog Neurobiol. 2007;81(2):89–131.
pubmed: 17275978
pmcid: 1919520
doi: 10.1016/j.pneurobio.2006.12.003
Targett MP, Sussman J, Scolding N, O’Leary MT, Compston DA, Blakemore WF. Failure to achieve remyelination of demyelinated rat axons following transplantation of glial cells obtained from the adult human brain. Neuropathol Appl Neurobiol. 1996;22(3):199–206.
pubmed: 8804021
doi: 10.1111/j.1365-2990.1996.tb00895.x
Ramos M, Pardo B, Llorente-Folch I, Saheki T, Del Arco A, Satrústegui J. Deficiency of the mitochondrial transporter of aspartate/glutamate aralar/AGC1 causes hypomyelination and neuronal defects unrelated to myelin deficits in mouse brain. J Neurosci Res. 2011;89(12):2008–17.
pubmed: 21608011
doi: 10.1002/jnr.22639
Juaristi I, Garcia-Martin ML, Rodrigues TB, Satrústegui J, Llorente-Folch I, Pardo B. ARALAR/AGC1 deficiency, a neurodevelopmental disorder with severe impairment of neuronal mitochondrial respiration, does not produce a primary increase in brain lactate. J Neurochem. 2017;142(1):132–9.
pubmed: 28429368
doi: 10.1111/jnc.14047
Profilo E, Peña-Altamira LE, Corricelli M, Castegna A, Danese A, Agrimi G, et al. Down-regulation of the mitochondrial aspartate-glutamate carrier isoform 1 AGC1 inhibits proliferation and N-acetylaspartate synthesis in Neuro2A cells. Biochim Biophys Acta Mol Basis Dis. 2017;1863(6):1422–35.
pubmed: 28235644
doi: 10.1016/j.bbadis.2017.02.022
Petralla S, Peña-Altamira LE, Poeta E, Massenzio F, Virgili M, Barile SN, et al. Deficiency of mitochondrial aspartate-glutamate carrier 1 leads to oligodendrocyte precursor cell proliferation defects both in vitro and in vivo. Int J Mol Sci. 2019;20(18):4486.
pubmed: 31514314
pmcid: 6769484
doi: 10.3390/ijms20184486
Poeta E, Petralla S, Babini G, Renzi B, Celauro L, Magnifico MC, Barile SN, et al. Histone acetylation defects in brain precursor cells: a potential pathogenic mechanism causing proliferation and differentiation dysfunctions in mitochondrial aspartate-glutamate carrier isoform 1 deficiency. Front Cell Neurosci. 2021;15: 773709.
pubmed: 35095421
doi: 10.3389/fncel.2021.773709
Juliandi B, Abematsu M, Nakashima K. Epigenetic regulation in neural stem cell differentiation. Dev Growth Differ. 2010;52(6):493–504.
pubmed: 20608952
doi: 10.1111/j.1440-169X.2010.01175.x
Emery B, Lu QR. Transcriptional and epigenetic regulation of oligodendrocyte development and myelination in the central nervous system. Cold Spring Harb Perspect Biol. 2015;7(9): a020461.
pubmed: 26134004
pmcid: 4563712
doi: 10.1101/cshperspect.a020461
Hernandez M, Casaccia P. Interplay between transcriptional control and chromatin regulation in the oligodendrocyte lineage. Glia. 2015;63(8):1357–75.
pubmed: 25970296
pmcid: 4470782
doi: 10.1002/glia.22818
Long PM, Moffett JR, Namboodiri AMA, Viapiano MS, Lawler SE, Jaworski DM. N-acetylaspartate (NAA) and N-acetylaspartylglutamate (NAAG) promote growth and inhibit differentiation of glioma stem-like cells. J Biol Chem. 2013;288(36):26188–200.
pubmed: 23884408
pmcid: 3764823
doi: 10.1074/jbc.M113.487553
Bogner-Strauss JG. N-Acetylaspartate metabolism outside the brain: lipogenesis, histone acetylation, and cancer. Front Endocrinol. 2017;8:240.
doi: 10.3389/fendo.2017.00240
Mercatelli D, Bortolotti M, Giorgi FM. Transcriptional network inference and master regulator analysis of the response to ribosome-inactivating proteins in leukemia cells. Toxicology. 2020;441: 152531.
pubmed: 32593706
doi: 10.1016/j.tox.2020.152531
Protti M, Cirrincione M, Palano S, Poeta E, Babini G, Magnifico MC, et al. Targeted quantitative metabolic profiling of brain-derived cell cultures by semi-automated MEPS and LC–MS/MS. J Pharm Biomed Anal. 2023;236: 115757.
pubmed: 37801818
doi: 10.1016/j.jpba.2023.115757
Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7): e47.
pubmed: 25605792
pmcid: 4402510
doi: 10.1093/nar/gkv007
Benjamini Y. Discovering the false discovery rate. J R Stat Soc Series B Stat Methodol. 2010;72(4):405–16.
doi: 10.1111/j.1467-9868.2010.00746.x
Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14(4):417–9.
pubmed: 28263959
pmcid: 5600148
doi: 10.1038/nmeth.4197
Balboni N, Giorgi FM. GitHub. https://github.com/Nbalb/agc1_OliNeu . Accessed 26 Oct 2023.
Love MI, Soneson C, Hickey PF, Johnson LK, Pierce NT, Shepherd L, et al. Tximeta: reference sequence checksums for provenance identification in RNA-seq. PLoS Comput Biol. 2020;16(2): e1007664.
pubmed: 32097405
pmcid: 7059966
doi: 10.1371/journal.pcbi.1007664
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Zhu A, Ibrahim JG, Love MI. Heavy-tailed prior distributions for sequence count data: removing the noise and preserving large differences. Bioinformatics. 2019;35(12):2084–92.
pubmed: 30395178
doi: 10.1093/bioinformatics/bty895
Balboni N, Giorgi FM. Agc1 Transcriptome Explorer. https://giorglab.unibo.it/Agc1 . Accessed 26 Oct 2023.
Mercatelli D, Triboli L, Fornasari E, Ray F, Giorgi FM. Coronapp: a web application to annotate and monitor SARS-CoV-2 mutations. J Med Virol. 2021;93(5):3238–45.
pubmed: 33205830
doi: 10.1002/jmv.26678
Giorgi FM, Ceraolo C, Mercatelli D. The R language: an engine for bioinformatics and data science. Life. 2022;12(5):648.
pubmed: 35629316
pmcid: 9148156
doi: 10.3390/life12050648
Balboni N, Giorgi FM. Gene Epression Omnibus series GSE236054. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE236054 . Accessed 26 Oct 2023. Token:cbqtgksmhjohdyr.
Dolgalev I. MSigDB Gene Sets for Multiple Organisms in a Tidy Data Format [R package msigdbr version 7.5.1]. 2022.
Mercatelli D, Lopez-Garcia G, Giorgi FM. corto: a lightweight R package for gene network inference and master regulator analysis. Bioinformatics. 2020;36(12):3916–7.
pubmed: 32232425
doi: 10.1093/bioinformatics/btaa223
Vaquero-Garcia J, Barrera A, Gazzara MR, González-Vallinas J, Lahens NF, Hogenesch JB, et al. A new view of transcriptome complexity and regulation through the lens of local splicing variations. Elife. 2016;5: e11752.
pubmed: 26829591
pmcid: 4801060
doi: 10.7554/eLife.11752
Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, Anderson S, et al. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol. 2003;161(1):169–86.
pubmed: 12682089
pmcid: 2172886
doi: 10.1083/jcb.200210110
Gerdes J, Li L, Schlueter C, Duchrow M, Wohlenberg C, Gerlach C, et al. Immunobiochemical and molecular biologic characterization of the cell proliferation-associated nuclear antigen that is defined by monoclonal antibody Ki-67. Am J Pathol. 1991;138(4):867–73.
pubmed: 2012175
pmcid: 1886092
Dimas P, Montani L, Pereira JA, Moreno D, Trötzmüller M, Gerber J, Semenkovich CF, et al. CNS myelination and remyelination depend on fatty acid synthesis by oligodendrocytes. Elife. 2019;8: e44702.
pubmed: 31063129
pmcid: 6504237
doi: 10.7554/eLife.44702
Eberlé D, Hegarty B, Bossard P, Ferré P, Foufelle F. SREBP transcription factors: master regulators of lipid homeostasis. Biochimie. 2004;86(11):839–48.
pubmed: 15589694
doi: 10.1016/j.biochi.2004.09.018
Monnerie H, Romer M, Jensen BK, Millar JS, Jordan-Sciutto KL, Kim SF, et al. Reduced sterol regulatory element-binding protein (SREBP) processing through site-1 protease (S1P) inhibition alters oligodendrocyte differentiation in vitro. J Neurochem. 2017;140(1):53–67.
pubmed: 27385127
doi: 10.1111/jnc.13721
Porstmann T, Griffiths B, Chung YL, Delpuech O, Griffiths JR, Downward J, et al. PKB/Akt induces transcription of enzymes involved in cholesterol and fatty acid biosynthesis via activation of SREBP. Oncogene. 2005;24(43):6465–81.
pubmed: 16007182
doi: 10.1038/sj.onc.1208802
Xia Z, Ouyang D, Li Q, Li M, Zou Q, Li L, et al. The expression, functions, interactions and prognostic values of PTPRZ1: a review and bioinformatic analysis. J Cancer. 2019;10(7):1663–74.
pubmed: 31205522
pmcid: 6548002
doi: 10.7150/jca.28231
Kuboyama K, Fujikawa A, Suzuki R, Tanga N, Noda M. Role of chondroitin sulfate (CS) modification in the regulation of protein-tyrosine phosphatase receptor type Z (PTPRZ) activity: pleiotrophin-PTPRZ—a signaling is involved in oligodendrocyte differentiation. J Biol Chem. 2016;291(35):18117–28.
pubmed: 27445335
pmcid: 5000061
doi: 10.1074/jbc.M116.742536
Nielsen JA, Berndt JA, Hudson LD, Armstrong RC. Myelin transcription factor 1 (Myt1) modulates the proliferation and differentiation of oligodendrocyte lineage cells. Mol Cell Neurosci. 2004;25(1):111–23.
pubmed: 14962745
doi: 10.1016/j.mcn.2003.10.001
Lee X, Hu Y, Zhang Y, Yang Z, Shao Z, Qiu M, Pepinsky B, et al. Oligodendrocyte differentiation and myelination defects in OMgp null mice. Mol Cell Neurosci. 2011;46(4):752–61.
pubmed: 21352918
doi: 10.1016/j.mcn.2011.02.008
Vana AC, Lucchinetti CF, Le TQ, Armstrong RC. Myelin transcription factor 1 (Myt1) expression in demyelinated lesions of rodent and human CNS. Glia. 2007;55(7):687–97.
pubmed: 17330875
pmcid: 2789289
doi: 10.1002/glia.20492
Kim SY, Kelland EE, Kim JH, Lund BT, Chang X, Wang K, et al. The influence of retinoic acid on the human oligodendrocyte precursor cells by RNA-sequencing. Biochem Biophys Rep. 2017;9:166–72.
pubmed: 29114585
Latasa MJ, Ituero M, Moran-Gonzalez A, Aranda A, Cosgaya JM. Retinoic acid regulates myelin formation in the peripheral nervous system. Glia. 2010;58(12):1451–64.
pubmed: 20648638
doi: 10.1002/glia.21020
Hallows WC, Lee S, Denu JM. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA. 2006;103(27):10230–5.
pubmed: 16790548
pmcid: 1480596
doi: 10.1073/pnas.0604392103
Miao T, Kim J, Kang P, Fujiwara H, Hsu FF, Bai H. Acetyl-CoA-mediated autoacetylation of fatty acid synthase as a metabolic switch of de novo lipogenesis in Drosophila. Proc Natl Acad Sci USA. 2022;119(49): e2212220119.
pubmed: 36459649
pmcid: 9894184
doi: 10.1073/pnas.2212220119
Luong A, Hannah VC, Brown MS, Goldstein JL. Molecular characterization of human acetyl-CoA synthetase, an enzyme regulated by sterol regulatory element-binding proteins. J Biol Chem. 2000;275(34):26458–66.
pubmed: 10843999
doi: 10.1074/jbc.M004160200
Wellen KE, Thompson CB. A two-way street: reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol. 2012;13(4):270–6.
pubmed: 22395772
doi: 10.1038/nrm3305
Lin HP, Cheng ZL, He RY, Song L, Tian MX, Zhou LS, Groh BS, et al. Destabilization of fatty acid synthase by acetylation inhibits de novo lipogenesis and tumor cell growth. Cancer Res. 2016;76(23):6924–36.
pubmed: 27758890
pmcid: 5135623
doi: 10.1158/0008-5472.CAN-16-1597
Camargo N, Smit AB, Verheijen MHG. SREBPs: SREBP function in glia-neuron interactions. FEBS J. 2009;276(3):628–36.
pubmed: 19143832
doi: 10.1111/j.1742-4658.2008.06808.x
Alvarez MJ, Shen Y, Giorgi FM, Lachmann A, Ding BB, Ye BH, et al. Functional characterization of somatic mutations in cancer using network-based inference of protein activity. Nat Genet. 2016;48(8):838–47.
pubmed: 27322546
pmcid: 5040167
doi: 10.1038/ng.3593
Lachmann A, Giorgi FM, Lopez G, Califano A. ARACNe-AP: gene network reverse engineering through adaptive partitioning inference of mutual information. Bioinformatics. 2016;32(14):2233–5.
pubmed: 27153652
pmcid: 4937200
doi: 10.1093/bioinformatics/btw216
Genetic effects on gene expression across human tissues. Nature. 2017;550(7675):204–13.
Beccacece L, Costa F, Pascali JP, Giorgi FM. Cross-species transcriptomics analysis highlights conserved molecular responses to per- and polyfluoroalkyl substances. Toxics. 2023;11(7):567.
pubmed: 37505532
pmcid: 10385990
doi: 10.3390/toxics11070567
Bunk EC, Ertaylan G, Ortega F, Pavlou MA, Gonzalez Cano L, Stergiopoulos A, et al. Prox1 is required for oligodendrocyte cell identity in adult neural stem cells of the subventricular zone. Stem Cells. 2016;34(8):2115–29.
pubmed: 27068685
doi: 10.1002/stem.2374
Chang W, Teng J. Prox1 is essential for oligodendrocyte survival and regulates oligodendrocyte apoptosis via the regulation of NOXA. Acta Biochim Biophys Sin. 2018;50(7):709–17.
pubmed: 29931031
doi: 10.1093/abbs/gmy061
Kato K, Konno D, Berry M, Matsuzaki F, Logan A, Hidalgo A. Prox1 inhibits proliferation and is required for differentiation of the oligodendrocyte cell lineage in the mouse. PLoS ONE. 2015;10(12): e0145334.
pubmed: 26709696
pmcid: 4692484
doi: 10.1371/journal.pone.0145334
Ampofo E, Schmitt BM, Menger MD, Laschke MW. The regulatory mechanisms of NG2/CSPG4 expression. Cell Mol Biol Lett. 2017;22(1):4.
pubmed: 28536635
pmcid: 5415841
doi: 10.1186/s11658-017-0035-3
Narayanan R, Pirouz M, Kerimoglu C, Pham L, Wagener RJ, Kiszka KA, et al. Loss of BAF (mSWI/SNF) complexes causes global transcriptional and chromatin state changes in forebrain development. Cell Rep. 2015;13(9):1842–54.
pubmed: 26655900
doi: 10.1016/j.celrep.2015.10.046
Abbas E, Hassan MA, Sokpor G, Kiszka K, Pham L, Kerimoglu C, et al. Conditional loss of BAF (mSWI/SNF) scaffolding subunits affects specification and proliferation of oligodendrocyte precursors in developing mouse forebrain. Front Cell Dev Biol. 2021;9: 619538.
pubmed: 34336815
pmcid: 8320002
doi: 10.3389/fcell.2021.619538
Berry K, Wang J, Lu QR. Epigenetic regulation of oligodendrocyte myelination in developmental disorders and neurodegenerative diseases. F1000 Res. 2020;9:105.
doi: 10.12688/f1000research.20904.1
de Ferra F, Engh H, Hudson L, Kamholz J, Puckett C, Molineaux S, et al. Alternative splicing accounts for the four forms of myelin basic protein. Cell. 1985;43(3 Pt 2):721–7.
pubmed: 2416470
doi: 10.1016/0092-8674(85)90245-4
Campagnoni AT. Molecular biology of myelin proteins from the central nervous system. J Neurochem. 1988;51(1):1–14.
pubmed: 2454292
doi: 10.1111/j.1471-4159.1988.tb04827.x
Delarasse C, Della Gaspera B, Lu CW, Lachapelle F, Gelot A, Rodriguez D, Dautigny A, et al. Complex alternative splicing of the myelin oligodendrocyte glycoprotein gene is unique to human and non-human primates. J Neurochem. 2006;98(6):1707–17.
pubmed: 16903876
doi: 10.1111/j.1471-4159.2006.04053.x
Naef R, Suter U. Many facets of the peripheral myelin protein PMP22 in myelination and disease. Microsc Res Tech. 1998;41(5):359–71.
pubmed: 9672419
doi: 10.1002/(SICI)1097-0029(19980601)41:5<359::AID-JEMT3>3.0.CO;2-L
Li J, Parker B, Martyn C, Natarajan C, Guo J. The PMP22 gene and its related diseases. Mol Neurobiol. 2013;47(2):673–98.
pubmed: 23224996
doi: 10.1007/s12035-012-8370-x
Wang DS, Wu X, Bai Y, Zaidman C, Grider T, Kamholz J, Lupski JR, et al. PMP22 exon 4 deletion causes ER retention of PMP22 and a gain-of-function allele in CMT1E. Ann Clin Transl Neurol. 2017;4(4):236–45.
pubmed: 28382305
pmcid: 5376752
doi: 10.1002/acn3.395
Mollard R, Viville S, Ward SJ, Décimo D, Chambon P, Dollé P. Tissue-specific expression of retinoic acid receptor isoform transcripts in the mouse embryo. Mech Dev. 2000;94(1–2):223–32.
pubmed: 10842077
doi: 10.1016/S0925-4773(00)00303-8
Noll E, Miller RH. Regulation of oligodendrocyte differentiation: a role for retinoic acid in the spinal cord. Development. 1994;120(3):649–60.
pubmed: 8162861
doi: 10.1242/dev.120.3.649
Joubert L, Foucault I, Sagot Y, Bernasconi L, Duval F, Alliod C, Frossard MJ, et al. Chemical inducers and transcriptional markers of oligodendrocyte differentiation. J Neurosci Res. 2010;88(12):2546–57.
pubmed: 20544820
doi: 10.1002/jnr.22434
Dahlin M, Martin DA, Hedlund Z, Jonsson M, von Döbeln U, Wedell A. The ketogenic diet compensates for AGC1 deficiency and improves myelination. Epilepsia. 2015;56(11):e176–81.
pubmed: 26401995
doi: 10.1111/epi.13193
Cavicchioli MV, Santorsola M, Balboni N, Mercatelli D, Giorgi FM. Prediction of metabolic profiles from transcriptomics data in human cancer cell lines. Int J Mol Sci. 2022;23(7):3867.
pubmed: 35409231
pmcid: 8998886
doi: 10.3390/ijms23073867
Marde VS, Tiwari PL, Wankhede NL, Taksande BG, Upaganlawar AB, Umekar Milind J, Kale MB. Neurodegenerative disorders associated with genes of mitochondria. Futur J Pharm Sci. 2021;7(1):66.
doi: 10.1186/s43094-021-00215-5
Sanna PP, Cabrelle C, Kawamura T, Mercatelli D, O’Connor N, Roberts Amanda J and Repunte-Canonigo V, et al. A history of repeated alcohol intoxication promotes cognitive impairment and gene expression signatures of disease progression in the 3xTg mouse model of Alzheimer’s disease. eNeuro. 2023;10(7).
Nasrabady SE, Rizvi B, Goldman JE, Brickman AM. White matter changes in Alzheimer’s disease: a focus on myelin and oligodendrocytes. Acta Neuropathol Commun. 2018;6(1):22.
pubmed: 29499767
pmcid: 5834839
doi: 10.1186/s40478-018-0515-3
Lorenzini L, Fernandez M, Baldassarro VA, Bighinati A, Giuliani A, Calzà L, et al. White matter and neuroprotection in Alzheimer’s dementia. Molecules. 2020;25(3):503.
pubmed: 31979414
pmcid: 7038211
doi: 10.3390/molecules25030503
Pu A, Stephenson EL, Yong VW. The extracellular matrix: focus on oligodendrocyte biology and targeting CSPGs for remyelination therapies. Glia. 2018;66(9):1809–25.
pubmed: 29603376
doi: 10.1002/glia.23333
Fragoso YD, Stoney PN, Shearer Kirsty D, Sementilli A, Nanescu SE, Sementilli P, McCaffery P. Expression in the human brain of retinoic acid induced 1, a protein associated with neurobehavioural disorders. Brain Struct Funct. 2015;220(2):1195–203.
pubmed: 24519454
doi: 10.1007/s00429-014-0712-1
Rinaldi B, Villa R, Sironi A, Garavelli L, Finelli P, Bedeschi MF. Smith-magenis syndrome-clinical review, biological background and related disorders. Genes (Basel). 2022;13(2):335.
pubmed: 35205380
doi: 10.3390/genes13020335
Yokoyama C, Wang X, Briggs MR, Admon A, Wu J, Hua X, Goldstein JL, et al. SREBP-1, a basic-helix–loop–helix-leucine zipper protein that controls transcription of the low density lipoprotein receptor gene. Cell. 1993;75(1):187–97.
pubmed: 8402897
doi: 10.1016/S0092-8674(05)80095-9
Jayakumar A, Tai MH, Huang WY, Al-Feel W, Hsu M, Abu-Elheiga L, et al. Human fatty acid synthase: properties and molecular cloning. Proc Natl Acad Sci USA. 1995;92(19):8695–9.
pubmed: 7567999
pmcid: 41033
doi: 10.1073/pnas.92.19.8695
Bitto E, Bingman CA, Wesenberg GE, McCoy JG, Phillips GN Jr. Structure of aspartoacylase, the brain enzyme impaired in Canavan disease. Proc Natl Acad Sci USA. 2007;104(2):456–61.
pubmed: 17194761
doi: 10.1073/pnas.0607817104
Flores AI, Narayanan SP, Morse Emily N, Shick HE, Yin X, Kidd G, Avila RL, et al. Constitutively active Akt induces enhanced myelination in the CNS. J Neurosci. 2008;28(28):7174–83.
pubmed: 18614687
pmcid: 4395496
doi: 10.1523/JNEUROSCI.0150-08.2008
Jaegle M, Ghazvini M, Mandemakers W, Piirsoo M, Driegen S, Levavasseur F, et al. The POU proteins Brn-2 and Oct-6 share important functions in Schwann cell development. Genes Dev. 2003;17(11):1380–91.
pubmed: 12782656
pmcid: 196070
doi: 10.1101/gad.258203
Schepers GE, Bullejos M, Hosking BM, Koopman P. Cloning and characterisation of the Sry-related transcription factor gene Sox8. Nucleic Acids Res. 2000;28(6):1473–80.
pubmed: 10684944
pmcid: 111037
doi: 10.1093/nar/28.6.1473
Ming Z, Vining B, Bagheri-Fam S, Harley V. SOX9 in organogenesis: shared and unique transcriptional functions. Cell Mol Life Sci. 2022;79(10):522.
pubmed: 36114905
pmcid: 9482574
doi: 10.1007/s00018-022-04543-4
Stolt CC, Lommes P, Sock E, Chaboissier MC, Schedl A, Wegner M. The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev. 2003;17(13):1677–89.
pubmed: 12842915
pmcid: 196138
doi: 10.1101/gad.259003
Turnescu T, Arter J, Reiprich S, Tamm ER, Waisman A, Wegner M. Sox8 and Sox10 jointly maintain myelin gene expression in oligodendrocytes. Glia. 2018;66(2):279–94.
pubmed: 29023979
doi: 10.1002/glia.23242
Zhou W, He Y, Rehman AU, Kong Y, Hong S, Ding G, Yalamanchili HK, et al. Loss of function of NCOR1 and NCOR2 impairs memory through a novel GABAergic hypothalamus-CA3 projection. Nat Neurosci. 2019;22(2):205–17.
pubmed: 30664766
pmcid: 6361549
doi: 10.1038/s41593-018-0311-1
Castelo-Branco G, Lilja T, Wallenborg K, Falcão AM, Marques SC, Gracias A, et al. Neural stem cell differentiation is dictated by distinct actions of nuclear receptor corepressors and histone deacetylases. Stem Cell Rep. 2014;3(3):502–15.
doi: 10.1016/j.stemcr.2014.07.008
Iemolo A, Montilla-Perez P, Lai IC, Meng Y, Nolan S, Wen J, et al. A cell type-specific expression map of NCoR1 and SMRT transcriptional co-repressors in the mouse brain. J Comp Neurol. 2020;528(13):2218–38.
pubmed: 32072640
pmcid: 7368833
doi: 10.1002/cne.24886
Kerkhofs M. Cytosolic Ca
pubmed: 32505042
doi: 10.1016/j.ceca.2020.102223
Chen JC, Alvarez MJ, Talos F, Dhruv H, Rieckhof GE, Iyer A, et al. Identification of causal genetic drivers of human disease through systems-level analysis of regulatory networks. Cell. 2014;159(2):402–14.
pubmed: 25303533
pmcid: 4194029
doi: 10.1016/j.cell.2014.09.021
Wishart DS, Feunang YD, Guo AC, Lo EJ, Marcu A, Grant JR, et al. DrugBank 5.0: a major update to the DrugBank database for 2018. Nucleic Acids Res. 2018;46(D1):D1074–82.
pubmed: 29126136
doi: 10.1093/nar/gkx1037