In individuals with Williams syndrome, dysregulation of methylation in non-coding regions of neuronal and oligodendrocyte DNA is associated with pathology and cortical development


  • Morris CA. Introduction: Williams syndrome. Am J Med Genet Part C: Semin Med Genet. 2010;154C:203–8.

    Article 

    Google Scholar
     

  • Pober BR. Williams–Beuren Syndrome. N. Engl J Med. 2010;362:239–52.

    Article 

    Google Scholar
     

  • Kozel BA, Barak B, Kim CA, Mervis CB, Osborne LR, Porter M, et al. Williams syndrome. Nat Rev Dis Primers. 2021;7:42.

  • Barak B, Feng G. Neurobiology of social behavior abnormalities in autism and Williams syndrome. Nat Neurosci. 2016;19:647–55.

    Article 

    Google Scholar
     

  • Zanella M, Vitriolo A, Andirko A, Martins PT, Sturm S, O’Rourke T, et al. Dosage analysis of the 7q11.23 Williams region identifies BAZ1B as a major human gene patterning the modern human face and underlying self-domestication. Sci Adv. 2019;5:eaaw7908.

    Article 

    Google Scholar
     

  • Cha SG, Song MK, Lee SY, Kim GB, Kwak JG, Kim WH, et al. Long-term cardiovascular outcome of Williams syndrome. Congenit Heart Dis. 2019;14:684–90.

    Article 

    Google Scholar
     

  • Del Pasqua A, Rinelli G, Toscano A, Iacobelli R, Digilio C, Marino B, et al. New findings concerning cardiovascular manifestations emerging from long-term follow-up of 150 patients with the Williams-Beuren-Beuren syndrome. Cardiol Young-. 2009;19:563–7.

    Article 

    Google Scholar
     

  • Collins RT II. Cardiovascular disease in Williams syndrome. Curr Opin Pediatr. 2018;30:609–15.

    Article 

    Google Scholar
     

  • Pober BR, Wang E, Caprio S, Petersen KF, Brandt C, Stanley T, et al. High prevalence of diabetes and pre-diabetes in adults with Williams syndrome. Am J Med Genet Part C: Semin Med Genet. 2010;154C:291–8.

    Article 

    Google Scholar
     

  • Andersson SA, Olsson AH, Esguerra JLS, Heimann E, Ladenvall C, Edlund A, et al. Reduced insulin secretion correlates with decreased expression of exocytotic genes in pancreatic islets from patients with type 2 diabetes. Mol Cell Endocrinol. 2012;364:36–45.

    Article 

    Google Scholar
     

  • Frangiskakis JM, Ewart AK, Morris CA, Mervis CB, Bertrand J, Robinson BF, et al. LIM-kinase1 Hemizygosity Implicated in Impaired Visuospatial Constructive Cognition. Cell. 1996;86:59–69.

    Article 

    Google Scholar
     

  • Greiner de Magalhães C, Pitts CH, Mervis CB. Executive function as measured by the Behavior Rating Inventory of Executive Function-2: children and adolescents with Williams syndrome. J Intellect Disabil Res. 2022;66:94–107.

    Article 

    Google Scholar
     

  • Mervis CB, John AE. Cognitive and behavioral characteristics of children with Williams syndrome: Implications for intervention approaches. Am J Med Genet Part C: Semin Med Genet. 2010;154C:229–48.

    Article 

    Google Scholar
     

  • Miezah D, Porter M, Rossi A, Kazzi C, Batchelor J, Reeve J. Cognitive profile of young children with Williams syndrome. J Intellect Disabil Res. 2021;65:784–94.

    Article 

    Google Scholar
     

  • Meyer-Lindenberg A, Mervis CB, Faith Berman K. Neural mechanisms in Williams syndrome: a unique window to genetic influences on cognition and behaviour. Nat Rev Neurosci. 2006;7:380–93.

    Article 

    Google Scholar
     

  • Morris CA, Braddock SR, Council On G, Chen E, Trotter TL, Berry SA, et al. Health care supervision for children with Williams Syndrome. Pediatrics. 2020;145:2019–3761.

    Article 

    Google Scholar
     

  • Martens MA, Wilson SJ, Reutens DC. Research Review: Williams syndrome: a critical review of the cognitive, behavioral, and neuroanatomical phenotype. J Child Psychol Psychiatry. 2008;49:576–608.

    Article 

    Google Scholar
     

  • Sanders StephanJ, Ercan-Sencicek AG, Hus V, Luo R, Murtha MichaelT, Moreno-De-Luca D, et al. Multiple recurrent De Novo CNVs, Including duplications of the 7q11.23 Williams Syndrome Region, are strongly associated with Autism. Neuron. 2011;70:863–85.

    Article 

    Google Scholar
     

  • Crespi BJ, Procyshyn TL. Williams syndrome deletions and duplications: Genetic windows to understanding anxiety, sociality, autism, and schizophrenia. Neurosci Biobehav Rev. 2017;79:14–26.

    Article 

    Google Scholar
     

  • Mulle JG, Pulver AE, McGrath JA, Wolyniec PS, Dodd AF, Cutler DJ, et al. Reciprocal duplication of the Williams-Beuren Syndrome deletion on chromosome 7q11.23 is associated with Schizophrenia. Biol Psychiatry. 2014;75:371–7.

    Article 

    Google Scholar
     

  • Barak B, Zhang Z, Liu Y, Nir A, Trangle SS, Ennis M, et al. Neuronal deletion of Gtf2i, associated with Williams syndrome, causes behavioral and myelin alterations rescuable by a remyelinating drug. Nat Neurosci. 2019;22:700–8.

    Article 

    Google Scholar
     

  • Strong E, Butcher DT, Singhania R, Mervis CB, Morris CA, Carvalho DD, et al. Symmetrical dose-dependent DNA-methylation profiles in children with deletion or duplication of 7q11.23. Am J Hum Genet. 2015;97:216–27.

    Article 

    Google Scholar
     

  • Kimura R, Lardenoije R, Tomiwa K, Funabiki Y, Nakata M, Suzuki S, et al. Integrated DNA methylation analysis reveals a potential role for ANKRD30B in Williams syndrome. Neuropsychopharmacology. 2020;45:1627–36.

    Article 

    Google Scholar
     

  • Nir A, Barak B. White matter alterations in Williams syndrome related to behavioral and motor impairments. Glia. 2021;69:5–19.

    Article 

    Google Scholar
     

  • Grad M, Nir A, Levy G, Trangle SS, Shapira G, Shomron N, et al. Altered white matter and microRNA expression in a murine model related to Williams Syndrome suggests that miR-34b/c affects brain development via Ptpru and Dcx Modulation. Cells. 2022;11:158.

    Article 

    Google Scholar
     

  • Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. An operational definition of epigenetics. Genes Dev. 2009;23:781–3.

    Article 

    Google Scholar
     

  • Bird A. Perceptions of epigenetics. Nature. 2007;447:396–8.

    Article 

    Google Scholar
     

  • Nott A, Holtman IR, Coufal NG, Schlachetzki JCM, Yu M, Hu R, et al. Brain cell type–specific enhancer–promoter interactome maps and disease-risk association. Science. 2019;366:1134.

    Article 

    Google Scholar
     

  • Tsankova N, Renthal W, Kumar A, Nestler EJ. Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci. 2007;8:355–67.

    Article 

    Google Scholar
     

  • Cho KS, Elizondo LI, Boerkoel CF. Advances in chromatin remodeling and human disease. Curr Opin Genet Dev. 2004;14:308–15.

    Article 

    Google Scholar
     

  • Kadoch C, Crabtree GR. Mammalian SWI/SNF chromatin remodeling complexes and cancer: Mechanistic insights gained from human genomics. Sci Adv. 2015;1:e1500447.

    Article 

    Google Scholar
     

  • Culver-Cochran AE, Chadwick BP. Loss of WSTF results in spontaneous fluctuations of heterochromatin formation and resolution, combined with substantial changes to gene expression. BMC Genomics. 2013;14:740.

    Article 

    Google Scholar
     

  • Jangani M, Poolman TM, Matthews L, Yang N, Farrow SN, Berry A, et al. The Methyltransferase WBSCR22/Merm1 enhances glucocorticoid receptor function and is regulated in lung inflammation and cancer. J Biol Chem. 2014;289:8931–46.

    Article 

    Google Scholar
     

  • Schosserer M, Minois N, Angerer TB, Amring M, Dellago H, Harreither E, et al. Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan. Nat Commun. 2015;6:6158.

    Article 

    Google Scholar
     

  • Peña-Hernández R, Marques M, Hilmi K, Zhao T, Saad A, Alaoui-Jamali MA, et al. Genome-wide targeting of the epigenetic regulatory protein CTCF to gene promoters by the transcription factor TFII-I. Proc Natl Acad Sci USA. 2015;112:E677–86.

    Article 

    Google Scholar
     

  • Lazebnik MB, Tussie-Luna MI, Roy AL. Determination and functional analysis of the consensus binding site for TFII-I family member BEN, implicated in Williams-Beuren syndrome. J Biol Chem. 2008;283:11078–82.

    Article 

    Google Scholar
     

  • Makeyev AV, Bayarsaihan D. ChIP-Chip Identifies SEC23A, CFDP1, and NSD1 as TFII-I Target Genes in Human Neural Crest Progenitor Cells. Cleft Palate Craniofac J. 2013;50:347–50.

    Article 

    Google Scholar
     

  • Bayarsaihan D, Makeyev AV, Enkhmandakh B. Epigenetic modulation by TFII-I during embryonic stem cell differentiation. J Cell Biochem. 2012;113:3056–60.

    Article 

    Google Scholar
     

  • Bayarsaihan D. What role does TFII-I have to play in epigenetic modulation during embryogenesis? Epigenomics. 2013;5:9–11.

    Article 

    Google Scholar
     

  • Roy AL. Role of the multifunctional transcription factor TFII-I in DNA damage repair. DNA Repair. 2021;106:103175.

    Article 

    Google Scholar
     

  • Makeyev AV, Enkhmandakh B, Hong SH, Joshi P, Shin DG, Bayarsaihan D. Diversity and complexity in chromatin recognition by TFII-I transcription factors in pluripotent embryonic stem cells and embryonic tissues. PLoS One. 2012;7:e44443.

    Article 

    Google Scholar
     

  • Tussié-Luna MI, Bayarsaihan D, Seto E, Ruddle FH, Roy AL. Physical and functional interactions of histone deacetylase 3 with TFII-I family proteins and PIASxβ. Proc Natl Acad Sci. 2002;99:12807–12.

    Article 

    Google Scholar
     

  • Crusselle-Davis VJ, Zhou Z, Anantharaman A, Moghimi B, Dodev T, Huang S, et al. Recruitment of coregulator complexes to the β-globin gene locus by TFII-I and upstream stimulatory factor. FEBS J. 2007;274:6065–73.

    Article 

    Google Scholar
     

  • Hakimi M-A, Dong Y, Lane WS, Speicher DW, Shiekhattar R. A candidate X-linked mental retardation gene is a component of a new family of Histone Deacetylase-containing complexes. J Biol Chem. 2003;278:7234–9.

    Article 

    Google Scholar
     

  • Pacaud R, Sery Q, Oliver L, Vallette FM, Tost J, Cartron P-F. DNMT3L interacts with transcription factors to target DNMT3L/DNMT3B to specific DNA sequences: Role of the DNMT3L/DNMT3B/p65-NFκB complex in the (de-)methylation of TRAF1. Biochimie. 2014;104:36–49.

    Article 

    Google Scholar
     

  • Greenberg MVC, Bourc’his D. The diverse roles of DNA methylation in mammalian development and disease. Nat Rev Mol Cell Biol. 2019;20:590–607.

    Article 

    Google Scholar
     

  • Yao B, Christian KM, He C, Jin P, Ming G-l, Song H. Epigenetic mechanisms in neurogenesis. Nat Rev Neurosci. 2016;17:537–49.

    Article 

    Google Scholar
     

  • Guo H, Zhu P, Yan L, Li R, Hu B, Lian Y, et al. The DNA methylation landscape of human early embryos. Nature. 2014;511:606–10.

    Article 

    Google Scholar
     

  • Smith ZD, Meissner A. DNA methylation: roles in mammalian development. Nat Rev Genet. 2013;14:204–20.

    Article 

    Google Scholar
     

  • Moyon S, Huynh JL, Dutta D, Zhang F, Ma D, Yoo S, et al. Functional characterization of DNA methylation in the oligodendrocyte lineage. Cell Rep. 2016;15:748–60.

    Article 

    Google Scholar
     

  • Liu J, Casaccia P. Epigenetic regulation of oligodendrocyte identity. Trends Neurosci. 2010;33:193–201.

    Article 

    Google Scholar
     

  • Liu J, Moyon S, Hernandez M, Casaccia P. Epigenetic control of oligodendrocyte development: adding new players to old keepers. Curr Opin Neurobiol. 2016;39:133–8.

    Article 

    Google Scholar
     

  • Aref-Eshghi E, Rodenhiser DI, Schenkel LC, Lin H, Skinner C, Ainsworth P, et al. Genomic DNA methylation signatures enable concurrent diagnosis and clinical genetic variant classification in neurodevelopmental syndromes. Am J Hum Genet. 2018;102:156–74.

    Article 

    Google Scholar
     

  • Corley MJ, Vargas-Maya N, Pang APS, Lum-Jones A, Li D, Khadka V, et al. Epigenetic delay in the neurodevelopmental trajectory of DNA methylation states in autism spectrum disorders. Front Genet. 2019;10:907.

    Article 

    Google Scholar
     

  • Godler DE, Amor DJ. DNA methylation analysis for screening and diagnostic testing in neurodevelopmental disorders. Essays Biochem. 2019;63:785–95.

    Article 

    Google Scholar
     

  • Moyon S, Ma D, Huynh JL, Coutts DJC, Zhao C, Casaccia P, et al. Efficient remyelination requires DNA methylation. eNeuro. 2017;4:ENEURO.0336-16.2017.

    Article 

    Google Scholar
     

  • Moyon S, Casaccia P. DNA methylation in oligodendroglial cells during developmental myelination and in disease. Neurogenesis (Austin). 2017;4:e1270381.

    Article 

    Google Scholar
     

  • Liu J, Magri L, Zhang F, Marsh NO, Albrecht S, Huynh JL, et al. Chromatin landscape defined by repressive histone methylation during oligodendrocyte differentiation. J Neurosci. 2015;35:352–65.

    Article 

    Google Scholar
     

  • Huynh JL, Casaccia P. Defining the chromatin landscape in demyelinating disorders. Neurobiol Dis. 2010;39:47–52.

    Article 

    Google Scholar
     

  • Liu J, Sandoval J, Doh ST, Cai L, López-Rodas G, Casaccia P. Epigenetic modifiers are necessary but not sufficient for reprogramming non-myelinating cells into myelin gene-expressing cells. PLoS One. 2010;5:e13023.

    Article 

    Google Scholar
     

  • Jang HS, Shin WJ, Lee JE, Do JT. CpG and non-CpG methylation in epigenetic gene regulation and brain function. Genes. 2017;8:148.

    Article 

    Google Scholar
     

  • Wang Z, Tang B, He Y, Jin P. DNA methylation dynamics in neurogenesis. Epigenomics. 2016;8:401–14.

    Article 

    Google Scholar
     

  • Sandoval J, Heyn H, Moran S, Serra-Musach J, Pujana MA, Bibikova M, et al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics. 2011;6:692–702.

    Article 

    Google Scholar
     

  • Ladd-Acosta C, Hansen KD, Briem E, Fallin MD, Kaufmann WE, Feinberg AP. Common DNA methylation alterations in multiple brain regions in autism. Mol Psychiatry. 2014;19:862–71.

    Article 

    Google Scholar
     

  • Numata S, Ye T, Herman M, Lipska BK. DNA methylation changes in the postmortem dorsolateral prefrontal cortex of patients with schizophrenia. Front Genet. 2014;5:280.

    Article 

    Google Scholar
     

  • Veyrac A, Besnard A, Caboche J, Davis S, Laroche S. Chapter Four – The Transcription Factor Zif268/Egr1, Brain Plasticity, and Memory, in Progress in Molecular Biology and Translational Science, ZU Khan and EC Muly, Editors. 2014, Academic Press. 89–129.

  • O’Donovan KJ, Tourtellotte WG, Millbrandt J, Baraban JM. The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci. 1999;22:167–73.

    Article 

    Google Scholar
     

  • Bacon C, Rappold GA. The distinct and overlapping phenotypic spectra of FOXP1 and FOXP2 in cognitive disorders. Hum Genet. 2012;131:1687–98.

    Article 

    Google Scholar
     

  • Lee B-K, Iyer VR. Genome-wide studies of CCCTC-binding Factor (CTCF) and cohesin provide insight into chromatin structure and regulation. J Biol Chem. 2012;287:30906–13.

    Article 

    Google Scholar
     

  • Semick SA, Bharadwaj RA, Collado-Torres L, Tao R, Shin JH, Deep-Soboslay A, et al. Integrated DNA methylation and gene expression profiling across multiple brain regions implicate novel genes in Alzheimerʼs disease. Acta Neuropathol. 2019;137:557–69.

  • Marin-Husstege M, He Y, Li J, Kondo T, Sablitzky F, Casaccia-Bonnefil P. Multiple roles of Id4 in developmental myelination: Predicted outcomes and unexpected findings. Glia. 2006;54:285–96.

    Article 

    Google Scholar
     

  • Kondo T, Raff M. The Id4 HLH protein and the timing of oligodendrocyte differentiation. EMBO J. 2000;19:1998–2007.

    Article 

    Google Scholar
     

  • Guillemain A, Laouarem Y, Cobret L, Štefok D, Chen W, Bloch S, et al. LINGO family receptors are differentially expressed in the mouse brain and form native multimeric complexes. FASEB J. 2020;34:13641–53.

    Article 

    Google Scholar
     

  • Mi S, Hu B, Hahm K, Luo Y, Kam Hui ES, Yuan Q, et al. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat Med. 2007;13:1228–33.

    Article 

    Google Scholar
     

  • Mi S, Miller RH, Lee X, Scott ML, Shulag-Morskaya S, Shao Z, et al. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci. 2005;8:745–51.

    Article 

    Google Scholar
     

  • Chen Y, Pal B, Visvader JE, Smyth GK. Differential methylation analysis of reduced representation bisulfite sequencing experiments using edgeR. F1000Research. 2017;6:2055.

    Article 

    Google Scholar
     

  • Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D’Souza C, Fouse SD, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature. 2010;466:253–7.

    Article 

    Google Scholar
     

  • Spindola LM, Santoro ML, Pan PM, Ota VK, Xavier G, Carvalho CM, et al. Detecting multiple differentially methylated CpG sites and regions related to dimensional psychopathology in youths. Clin Epigenetics. 2019;11:146.

    Article 

    Google Scholar
     

  • Jeong H, Mendizabal I, Berto S, Chatterjee P, Layman T, Usui N, et al. Evolution of DNA methylation in the human brain. Nat Commun. 2021;12:2021.

    Article 

    Google Scholar
     

  • Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38:576–89.

    Article 

    Google Scholar
     

  • Roth RB, Hevezi P, Lee J, Willhite D, Lechner SM, Foster AC, et al. Gene expression analyses reveal molecular relationships among 20 regions of the human CNS. Neurogenetics. 2006;7:67–80.

    Article 

    Google Scholar
     

  • Lin A, Wang RT, Ahn S, Park CC, Smith DJ. A genome-wide map of human genetic interactions inferred from radiation hybrid genotypes. Genome Res. 2010;20:1122–32.

    Article 

    Google Scholar
     

  • Beckmann AM, Wilce PA. Egr transcription factors in the nervous system. Neurochemistry Int. 1997;31:477–510.

    Article 

    Google Scholar
     

  • Kim SH, Song JY, Joo EJ, Lee KY, Shin SY, Lee YH, et al. Genetic association of the EGR2 gene with bipolar disorder in Korea. Exp Mol Med. 2012;44:121–9.

    Article 

    Google Scholar
     

  • Morris ME, Viswanathan N, Kuhlman S, Davis FC, Weitz CJ. A screen for genes induced in the suprachiasmatic nucleus by light. Science. 1998;279:1544–7.

    Article 

    Google Scholar
     

  • Hu VW, Frank BC, Heine S, Lee NH, Quackenbush J. Gene expression profiling of lymphoblastoid cell lines from monozygotic twins discordant in severity of autism reveals differential regulation of neurologically relevant genes. BMC Genomics. 2006;7:118.

    Article 

    Google Scholar
     

  • Wang T, Xiong J-Q. The orphan nuclear receptor TLX/NR2E1 in neural stem cells and diseases. Neurosci Bull. 2016;32:108–14.

    Article 

    Google Scholar
     

  • Zhang C-L, Zou Y, He W, Gage FH, Evans RM. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature. 2008;451:1004–7.

    Article 

    Google Scholar
     

  • Kumar RA, McGhee KA, Leach S, Bonaguro R, Maclean A, Aguirre-Hernandez R, et al. Initial association of NR2E1 with bipolar disorder and identification of candidate mutations in bipolar disorder, schizophrenia, and aggression through resequencing. Am J Med Genet Part B: Neuropsychiatr Genet. 2008;147B:880–9.

    Article 

    Google Scholar
     

  • O’Leary JD, Kozareva DA, Hueston CM, O’Leary OF, Cryan JF, Nolan YM. The nuclear receptor Tlx regulates motor, cognitive and anxiety-related behaviours during adolescence and adulthood. Behav Brain Res. 2016;306:36–47.

    Article 

    Google Scholar
     

  • Yamakawa H, Cheng J, Penney J, Gao F, Rueda R, Wang J, et al. The Transcription Factor Sp3 cooperates with HDAC2 to regulate synaptic function and plasticity in neurons. Cell Rep. 2017;20:1319–34.

    Article 

    Google Scholar
     

  • Thumfart KM, Jawaid A, Bright K, Flachsmann M, Mansuy IM. Epigenetics of childhood trauma: Long term sequelae and potential for treatment. Neurosci Biobehav Rev. 2022;132:1049–66.

    Article 

    Google Scholar
     

  • Day JJ, Kennedy AJ, Sweatt JD. DNA Methylation and its implications and accessibility for neuropsychiatric therapeutics. Annu Rev Pharmacol Toxicol. 2015;55:591–611.

    Article 

    Google Scholar
     

  • Meaney MJ, Szyf M. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin Neurosci. 2005;7:103–23.

    Article 

    Google Scholar
     

  • Rajarajan P, Gil SE, Brennand KJ, Akbarian S. Spatial genome organization and cognition. Nat Rev Neurosci. 2016;17:681–91.

    Article 

    Google Scholar
     

  • Kempfer R, Pombo A. Methods for mapping 3D chromosome architecture. Nat Rev Genet. 2020;21:207–26.

    Article 

    Google Scholar
     

  • Bernstein BE, Stamatoyannopoulos Ja, Costello Jf, Ren B, Milosavljevic A, Meissner A, et al. The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol. 2010;28:1045–8.

    Article 

    Google Scholar
     

  • Irimia M, Weatheritt RJ, Ellis JD, Parikshak NN, Gonatopoulos-Pournatzis T, Babor M, et al. A highly conserved program of neuronal microexons is misregulated in autistic brains. Cell. 2014;159:1511–23.

    Article 

    Google Scholar
     

  • Chailangkarn T, Trujillo CA, Freitas BC, Hrvoj-Mihic B, Herai RH, Yu DX, et al. A human neurodevelopmental model for Williams syndrome. Nature. 2016;536:338–43.

    Article 

    Google Scholar
     

  • Zhou J, Sears RL, Xing X, Zhang B, Li D, Rockweiler NB, et al. Tissue-specific DNA methylation is conserved across human, mouse, and rat, and driven by primary sequence conservation. BMC Genomics. 2017;18:724.

    Article 

    Google Scholar
     

  • Lokk K, Modhukur V, Rajashekar B, Märtens K, Mägi R, Kolde R, et al. DNA methylome profiling of human tissues identifies global and tissue-specific methylation patterns. Genome Biol. 2014;15:3248.

    Article 

    Google Scholar
     

  • Andrews SV, Ellis SE, Bakulski KM, Sheppard B, Croen LA, Hertz-Picciotto I, et al. Cross-tissue integration of genetic and epigenetic data offers insight into autism spectrum disorder. Nat Commun. 2017;8:1011.

    Article 

    Google Scholar
     

  • Pott S, Lieb JD. What are super-enhancers? Nat Genet. 2015;47:8–12.

    Article 

    Google Scholar
     

  • Simons M, Trajkovic K. Neuron-glia communication in the control of oligodendrocyte function and myelin biogenesis. J Cell Sci. 2006;119:4381–9.

    Article 

    Google Scholar
     

  • Barres BA, Schmid R, Sendnter M, Raff MC. Multiple extracellular signals are required for long-term oligodendrocyte survival. Development. 1993;118:283–95.

    Article 

    Google Scholar
     

  • Fields RD, Stevens-Graham B. New insights into neuron-glia communication. Science. 2002;298:556–62.

    Article 

    Google Scholar
     

  • Mitew S, Hay CM, Peckham H, Xiao J, Koenning M, Emery B. Mechanisms regulating the development of oligodendrocytes and central nervous system myelin. Neuroscience. 2014;276:29–47.

    Article 

    Google Scholar
     

  • Bilican B, Fiore-Heriche C, Compston A, Allen ND, Chandran S. Induction of Olig2+ precursors by FGF involves BMP signalling blockade at the smad level. PLOS ONE. 2008;3:e2863.

    Article 

    Google Scholar
     

  • Michailov Galin V, Sereda Michael W, Brinkmann Bastian G, Fischer Tobias M, Haug B, Birchmeier C, et al. Axonal Neuregulin-1 regulates myelin sheath thickness. Science. 2004;304:700–3.

    Article 

    Google Scholar
     

  • Xiao J, Ferner AH, Wong AW, Denham M, Kilpatrick TJ, Murray SS. Extracellular signal-regulated kinase 1/2 signaling promotes oligodendrocyte myelination in vitro. J Neurochemistry. 2012;122:1167–80.

    Article 

    Google Scholar
     

  • Xiao J, Wong AW, Willingham MM, van den Buuse M, Kilpatrick TJ, Murray SS. Brain-derived neurotrophic factor promotes central nervous system myelination via a direct effect upon oligodendrocytes. Neurosignals. 2010;18:186–202.

    Article 

    Google Scholar
     

  • Gendron-Maguire M, Mallo M, Zhang M, Gridley T. Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell. 1993;75:1317–31.

    Article 

    Google Scholar
     

  • Santagati F, Minoux M, Ren S-Y, Rijli FM. Temporal requirement of Hoxa2 in cranial neural crest skeletal morphogenesis. Development. 2005;132:4927–36.

    Article 

    Google Scholar
     

  • Tavella S, Bobola N. Expressing Hoxa2 across the entire endochondral skeleton alters the shape of the skeletal template in a spatially restricted fashion. Differentiation. 2010;79:194–202.

    Article 

    Google Scholar
     

  • Boeckx, C and Benítez-Burraco A, Osteogenesis and neurogenesis: a robust link also for language evolution. Front Cell Neurosci., 2015. 9.

  • Fukushima N, Furuta D, Hidaka Y, Moriyama R, Tsujiuchi T. Post-translational modifications of tubulin in the nervous system. J Neurochemistry. 2009;109:683–93.

    Article 

    Google Scholar
     

  • Gadadhar S, Alvarez Viar G, Hansen JN, Gong A, Kostarev A, Ialy-Radio C, et al. Tubulin glycylation controls axonemal dynein activity, flagellar beat, and male fertility. Science. 2021;371:6525.

    Article 

    Google Scholar
     

  • Jang S-W, Srinivasan R, Jones EA, Sun G, Keles S, Krueger C, et al. Locus-wide identification of Egr2/Krox20 regulatory targets in myelin genes. J Neurochemistry. 2010;115:1409–20.

    Article 

    Google Scholar
     

  • Kuhlbrodt K, Herbarth B, Sock E, Hermans-Borgmeyer I, Wegner M. Sox10, a novel transcriptional modulator in glial cells. J Neurosci. 1998;18:237.

    Article 

    Google Scholar
     

  • LeBlanc SE, Jang S-W, Ward RM, Wrabetz L, Svaren J. Direct regulation of myelin protein zero expression by the Egr2 transactivator. J Biol Chem. 2006;281:5453–60.

    Article 

    Google Scholar
     

  • Swanberg SE, Nagarajan RP, Peddada S, Yasui DH, LaSalle JM. Reciprocal co-regulation of EGR2 and MECP2 is disrupted in Rett syndrome and autism. Hum Mol Genet. 2009;18:525–34.

    Article 

    Google Scholar
     

  • Mager GM, Ward RM, Srinivasan R, Jang S-W, Wrabetz L, Svaren J. Active gene repression by the Egr2-NAB complex during peripheral nerve myelination. J Biol Chem. 2008;283:18187–97.

    Article 

    Google Scholar
     

  • Le N, Nagarajan R, Wang JYT, Svaren J, LaPash C, Araki T, et al. Nab proteins are essential for peripheral nervous system myelination. Nat Neurosci. 2005;8:932–40.

    Article 

    Google Scholar
     

  • Okano M, Bell DW, Haber DA, Li E. DNA Methyltransferases Dnmt3a and Dnmt3b are essential for De Novo methylation and mammalian development. Cell. 1999;99:247–57.

    Article 

    Google Scholar
     

  • Gertz J, Varley KE, Reddy TE, Bowling KM, Pauli F, Parker SL, et al. Analysis of DNA methylation in a three-generation family reveals widespread genetic influence on epigenetic regulation. PLOS Genet. 2011;7:e1002228.

    Article 

    Google Scholar
     

  • Gölzenleuchter M, Kanwar R, Zaibak M, Al Saiegh F, Hartung T, Klukas J, et al. Plasticity of DNA methylation in a nerve injury model of pain. Epigenetics. 2015;10:200–12.

    Article 

    Google Scholar
     

  • Nohara K, Nakabayashi K, Okamura K, Suzuki T, Suzuki S, Hata K. Gestational arsenic exposure induces site-specific DNA hypomethylation in active retrotransposon subfamilies in offspring sperm in mice. Epigenetics Chromatin. 2020;13:53.

    Article 

    Google Scholar
     

  • Voisin A-S, Suarez Ulloa V, Stockwell P, Chatterjee A, Silvestre F, Genome-wide DNA. methylation of the liver reveals delayed effects of early-life exposure to 17-α-ethinylestradiol in the self-fertilizing mangrove rivulus. Epigenetics. 2022;17:473–97.

    Article 

    Google Scholar
     

  • Baker Frost D, da Silveira W, Hazard ES, Atanelishvili I, Wilson RC, Flume J, et al. Differential DNA methylation landscape in skin fibroblasts from African Americans with systemic Sclerosis. Genes. 2021;12:129.

    Article 

    Google Scholar
     

  • Raff MC, Miller RH, Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature. 1983;303:390–6.

    Article 

    Google Scholar
     

  • Raff MC, Abney ER, Fok-Seang J. Reconstitution of a developmental clock in vitro: a critical role for astrocytes in the timing of oligodendrocyte differentiation. Cell. 1985;42:61–9.

    Article 

    Google Scholar
     

  • Raff MC, Lillien LE, Richardson WD, Burne JF, Noble MD. Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture. Nature. 1988;333:562–5.

    Article 

    Google Scholar
     

  • Mi S, Lee X, Shao Z, Thill G, Ji B, Relton J, et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci. 2004;7:221–8.

    Article 

    Google Scholar
     

  • Riechmann V, van Crüchten I, Sablitzky F. The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, 1d2 and Id3. Nucleic Acids Res. 1994;22:749–55.

    Article 

    Google Scholar
     

  • Jen Y, Manova K, Benezra R. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev Dyn: Off Publ Am Assoc Anatomists. 1996;207:235–52.

    Article 

    Google Scholar
     

  • Norton JD, Deed RW, Craggs G, Sablitzky F. Id helix—loop—helix proteins in cell growth and differentiation. Trends Cell Biol. 1998;8:58–65.


    Google Scholar
     

  • Norton JD, Atherton GT. Coupling of cell growth control and apoptosis functions of Id proteins. Mol Cell Biol. 1998;18:2371–81.

    Article 

    Google Scholar
     

  • Emery B. Regulation of oligodendrocyte differentiation and myelination. Science. 2010;330:779–82.

    Article 

    Google Scholar
     

  • Plemel JR, Manesh SB, Sparling JS, Tetzlaff W. Myelin inhibits oligodendroglial maturation and regulates oligodendrocytic transcription factor expression. Glia. 2013;61:1471–87.

    Article 

    Google Scholar
     

  • Huang H-S, Akbarian S. GAD1 mRNA expression and DNA methylation in prefrontal cortex of subjects with Schizophrenia. PLOS ONE. 2007;2:e809.

    Article 

    Google Scholar
     

  • Tao R, Davis KN, Li C, Shin JH, Gao Y, Jaffe AE, et al. GAD1 alternative transcripts and DNA methylation in human prefrontal cortex and hippocampus in brain development, schizophrenia. Mol Psychiatry. 2018;23:1496–505.

    Article 

    Google Scholar
     

  • Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O’Shea DJ, et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature. 2011;477:171–8.

    Article 

    Google Scholar
     

  • Levy DR, Tamir T, Kaufman M, Parabucki A, Weissbrod A, Schneidman E, et al. Dynamics of social representation in the mouse prefrontal cortex. Nat Neurosci. 2019;22:2013–22.

    Article 

    Google Scholar
     

  • Yizhar O, Levy DR. The social dilemma: prefrontal control of mammalian sociability. Curr Opin Neurobiol. 2021;68:67–75.

    Article 

    Google Scholar
     

  • Chew L-J, Coley W, Cheng Y, Gallo V. Mechanisms of regulation of oligodendrocyte development by p38 Mitogen-activated Protein Kinase. J Neurosci. 2010;30:11011–27.

    Article 

    Google Scholar
     

  • Liang X, Draghi NA, Resh MD. Signaling from Integrins to Fyn to Rho Family GTPases regulates morphologic differentiation of Oligodendrocytes. J Neurosci. 2004;24:7140.

    Article 

    Google Scholar
     

  • Chen Y, Wu H, Wang S, Koito H, Li J, Ye F, et al. The oligodendrocyte-specific G protein–coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat Neurosci. 2009;12:1398–406.

    Article 

    Google Scholar
     

  • Boda E, Viganò F, Rosa P, Fumagalli M, Labat-Gest V, Tempia F, et al. The GPR17 receptor in NG2 expressing cells: Focus on in vivocell maturation and participation in acute trauma and chronic damage. Glia. 2011;59:1958–73.

    Article 

    Google Scholar
     

  • Carter CS, Grippo AJ, Pournajafi-Nazarloo H, Ruscio MG, and Porges SW, Oxytocin, vasopressin and sociality, in Progress in Brain Research, ID Neumann and R Landgraf, Editors. 2008, Elsevier. 331–6.

  • Heinrichs M, von Dawans B, Domes G. Oxytocin, vasopressin, and human social behavior. Front Neuroendocrinol. 2009;30:548–57.

    Article 

    Google Scholar
     

  • Dai L, Carter CS, Ying J, Bellugi U, Pournajafi-Nazarloo H, Korenberg JR. Oxytocin and Vasopressin are dysregulated in williams syndrome, a genetic disorder affecting social behavior. PLOS ONE. 2012;7:e38513.

    Article 

    Google Scholar
     

  • Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci. 2011;12:524–38.

    Article 

    Google Scholar
     

  • Johnson ZV, Young LJ. Oxytocin and vasopressin neural networks: Implications for social behavioral diversity and translational neuroscience. Neurosci Biobehav Rev. 2017;76:87–98.

    Article 

    Google Scholar
     

  • Ebstein RP, Knafo A, Mankuta D, Chew SH, Lai PS. The contributions of oxytocin and vasopressin pathway genes to human behavior. Hormones Behav. 2012;61:359–79.

    Article 

    Google Scholar
     

  • Landgraf R, Neumann ID. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front Neuroendocrinol. 2004;25:150–76.

    Article 

    Google Scholar
     

  • Sue Carter C. Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology. 1998;23:779–818.

    Article 

    Google Scholar
     

  • Insel TR. The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron. 2010;65:768–79.

    Article 

    Google Scholar
     

  • Haas BW and Smith AK, Oxytocin, vasopressin, and Williams syndrome: epigenetic effects on abnormal social behavior. Front Genet., 2015. 6.

  • Bakulski KM, Halladay A, Hu VW, Mill J, Fallin MD. Epigenetic research in neuropsychiatric disorders: the “Tissue Issue”. Curr Behav Neurosci Rep. 2016;3:264–74.

    Article 

    Google Scholar
     

  • Nestler EJ, Peña CJ, Kundakovic M, Mitchell A, Akbarian S. Epigenetic basis of mental illness. Neuroscientist. 2015;22:447–63.

    Article 

    Google Scholar
     

  • Tekendo-Ngongang C, Dahoun S, Nguefack S, Gimelli S, Sloan-Béna F, Wonkam A. Challenges in clinical diagnosis of williams-beuren syndrome in sub-saharan africans: case reports from cameroon. Mol Syndromol. 2014;5:287–92.

    Article 

    Google Scholar
     

  • Lumaka A, Lukoo R, Mubungu G, Lumbala P, Mbayabo G, Mupuala A, et al. Williams-Beuren syndrome: pitfalls for diagnosis in limited resources setting. Clin Case Rep. 2016;4:294–7.

    Article 

    Google Scholar
     

  • Jühling F, Kretzmer H, Bernhart SH, Otto C, Stadler PF, Hoffmann S. metilene: fast and sensitive calling of differentially methylated regions from bisulfite sequencing data. Genome Res. 2016;26:256–62.

    Article 

    Google Scholar
     

  • Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38:576–89.

    Article 

    Google Scholar
     

  • Shen L. Gene Overlap: Test and visualize gene overlaps. 0.99.0. 2013. https://doi.org/10.18129/B9.bioc.GeneOverlap.

    Article 

    Google Scholar
     

  • Zhou Y, Zhou B, Pache L, Chang MA-OX, Khodabakhshi AH, Tanaseichuk O, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10:1523.

    Article 

    Google Scholar
     

  • Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24–26.

    Article 

    Google Scholar
     

  • Kumar K, Oli A, Hallikeri K, Shilpasree AS, Goni M. An optimized protocol for total RNA isolation from archived formalin-fixed paraffin-embedded tissues to identify the long non-coding RNA in oral squamous cell carcinomas. MethodsX. 2021;9:101602.

    Article 

    Google Scholar
     

  • Oudelaar AM, Downes DJ, Davies JOJ, Hughes JR. Low-input Capture-C: A chromosome conformation capture assay to analyze chromatin architecture in small numbers of cells. Bio Protoc. 2017;7:e2645.

    Article 

    Google Scholar
     

  • Splinter E, Grosveld F, de Laat W. 3C technology: analyzing the spatial organization of genomic loci in vivo. Methods Enzymol. 2004;375:493–507.

    Article 

    Google Scholar
     



  • Source link

    Leave a Comment