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Research Paper

A novel epigenetic marker, Ten-eleven translocation family member 2 (TET2), is identified in the intractable epileptic brain and regulates ATP binding cassette subfamily B member 1 (ABCB1) in the blood–brain barrier

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Pages 6638-6649 | Received 10 Jan 2022, Accepted 18 Feb 2022, Published online: 02 Mar 2022

References

  • Chen Z, Brodie MJ, Liew D, et al. Treatment outcomes in patients with newly diagnosed epilepsy treated with established and new antiepileptic drugs: a 30-Year longitudinal cohort study. JAMA Neurol. 2018;75(3):279–286.
  • Younus I, Reddy DS. Epigenetic interventions for epileptogenesis: a new frontier for curing epilepsy. Pharmacol Ther. 2017;177:108–122.
  • Henshall DC, Kobow K. Epigenetics and epilepsy. Cold Spring Harb Perspect Med. 2015;5(12). DOI:10.1101/cshperspect.a022731
  • Conboy K, Henshall DC, Brennan GP. Epigenetic principles underlying epileptogenesis and epilepsy syndromes. Neurobiol Dis. 2021;148:105179.
  • Henshall DC. Epigenetic changes in status epilepticus. Epilepsia. 2018;59(S2):82–86.
  • Greenberg MVC, Bourc’his D. The diverse roles of DNA methylation in mammalian development and disease. Nature Reviews Molecular Cell Biology. 2019;20(10):590–607.
  • Pensold D, Reichard J, Van Loo KMJ, et al. DNA methylation-mediated modulation of endocytosis as potential mechanism for synaptic function regulation in murine inhibitory cortical interneurons. Cerebral cortex (New York, NY: 1991). 2020;30(7): 3921–3937.
  • de Nijs L, Choe K, Steinbusch H, et al. DNA methyltransferase isoforms expression in the temporal lobe of epilepsy patients with a history of febrile seizures. Clin Epigenetics. 2019;11(1):118.
  • Zhu Q, Wang L, Zhang Y, et al. Increased expression of DNA methyltransferase 1 and 3a in human temporal lobe epilepsy. J Mol Neurosci. 2012;46(2):420–426.
  • Zhang W, Wang H, Liu B, et al. Differential DNA methylation profiles in patients with temporal lobe epilepsy and hippocampal sclerosis ILAE type I. J Mol Neurosci. 2021;71(9):1951–1966.
  • Wang L, Fu X, Peng X, et al. DNA methylation profiling reveals correlation of differential methylation patterns with gene expression in human epilepsy. J Mol Neurosci. 2016;59(1):68–77.
  • Kobow K, Ziemann M, Kaipananickal H, et al. Genomic DNA methylation distinguishes subtypes of human focal cortical dysplasia. Epilepsia. 2019;60(6):1091–1103.
  • Miller-Delaney SF, Das S, Sano T, et al. Differential DNA methylation patterns define status epilepticus and epileptic tolerance. J Neurosci. 2012;32(5):1577–1588.
  • Dębski KJ, Pitkanen A, Puhakka N, et al. Etiology matters - Genomic DNA methylation patterns in three rat models of acquired epilepsy. Sci Rep. 2016;6(1):25668.
  • Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science. 2009;324(5929):929–930.
  • Ito S, AC D, Taranova OV, et al. Role of TET proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature. 2010;466(7310):1129–1133.
  • MacArthur IC, Dawlaty MM. TET enzymes and 5-Hydroxymethylcytosine in neural progenitor cell biology and neurodevelopment. Front Cell Dev Biol. 2021;9:645335.
  • Greer CB, Wright J, Weiss JD, et al. Tet1 isoforms differentially regulate gene expression, synaptic transmission, and memory in the mammalian brain. J Neurosci. 2021;41(4):578–593.
  • Uyeda A, Onishi K, Hirayama T, et al. Suppression of DNA double-strand break formation by DNA polymerase β in active DNA demethylation is required for development of hippocampal pyramidal neurons. J Neurosci. 2020;40(47):9012–9027.
  • Kjaer C, Barzaghi G, Bak LK, et al. Transcriptome analysis in patients with temporal lobe epilepsy. Brain. 2019;142(10):e55.
  • Guelfi S, Botia JA, Thom M, et al. Transcriptomic and genetic analyses reveal potential causal drivers for intractable partial epilepsy. Brain. 2019;142(6):1616–1630.
  • Löscher W, Potschka H, Sisodiya SM, et al. Drug resistance in epilepsy: clinical impact, potential mechanisms, and new innovative treatment options. Pharmacol Rev. 2020;72(3):606–638.
  • Kwan P, Schachter SC, Brodie MJ. Drug-resistant epilepsy. N Engl J Med. 2011;365(10):919–926.
  • Kobow K, El-Osta A, Blümcke I. The methylation hypothesis of pharmacoresistance in epilepsy. Epilepsia. 2013;54(s2):41–47.
  • Arrigoni E, Galimberti S, Petrini M, et al. ATP-binding cassette transmembrane transporters and their epigenetic control in cancer: an overview. Expert Opin Drug Metab Toxicol. 2016;12(12):1419–1432.
  • Chen KG, Sikic BI. Molecular pathways: regulation and therapeutic implications of multidrug resistance. Clin Cancer Res. 2012;18(7):1863–1869.
  • Vaclavikova R, Klajic J, Brynychova V, et al. Development of high‑resolution melting analysis for ABCB1 promoter methylation: clinical consequences in breast and ovarian carcinoma. Oncol Rep. 2019;42(2):763–774.
  • Thom M, Sisodiya SM, Beckett A, et al. Cytoarchitectural abnormalities in hippocampal sclerosis. J Neuropathol Exp Neurol. 2002;61(6):510–519.
  • Hartz AMS, Schulz JA, and Sokola BS, et al. Isolation of cerebral capillaries from fresh human brain tissue. J Vis Exp. 2018. 139.
  • Hoshi Y, Uchida Y, Tachikawa M, et al. Oxidative stress-induced activation of Abl and Src kinases rapidly induces P-glycoprotein internalization via phosphorylation of caveolin-1 on tyrosine-14, decreasing cortisol efflux at the blood-brain barrier. J Cereb Blood Flow Metab. 2020;40(2):420–436.
  • Zhang C, Chanteux H, Zuo Z, et al. Potential role for human P-glycoprotein in the transport of lacosamide. Epilepsia. 2013;54(7):1154–1160.
  • Tishler DM, Weinberg KI, Hinton DR, et al. MDR1 gene expression in brain of patients with medically intractable epilepsy. Epilepsia. 1995;36(1):1–6.
  • Weksler B, Romero IA, Couraud PO. The hCMEC/D3 cell line as a model of the human blood brain barrier. Fluids Barriers CNS. 2013;10(1):16.
  • Fontaine M, Elmquist WF, Miller DW. Use of rhodamine 123 to examine the functional activity of P-glycoprotein in primary cultured brain microvessel endothelial cell monolayers. Life Sci. 1996;59(18):1521–1531.
  • Cong B, Zhang Q, and Cao X. The function and regulation of TET2 in innate immunity and inflammation. Protein Cell. 2020;12(3):165–173.
  • Marshall LL, Killinger BA, Ensink E, et al. Epigenomic analysis of Parkinson’s disease neurons identifies Tet2 loss as neuroprotective. Nat Neurosci. 2020;23(10):1203–1214.
  • Wu TT, Liu T, Li X, et al. TET2-mediated Cdkn2A DNA hydroxymethylation in midbrain dopaminergic neuron injury of Parkinson’s disease. Hum Mol Genet. 2020;29(8):1239–1252.
  • Carrillo-Jimenez A, Deniz O, Niklison-Chirou MV, et al. TET2 regulates the neuroinflammatory response in microglia. Cell Rep. 2019;29(3):697–713 e698.
  • Kobow K, Jeske I, Hildebrandt M, et al. Increased reelin promoter methylation is associated with granule cell dispersion in human temporal lobe epilepsy. J Neuropathol Exp Neurol. 2009;68(4):356–364.
  • Martínez-Levy GA, Rocha L, Lubin FD, et al. Increased expression of BDNF transcript with exon VI in hippocampi of patients with pharmaco-resistant temporal lobe epilepsy. Neuroscience. 2016;314:12–21.
  • Lio CJ, Shukla V, Samaniego-Castruita D, et al. TET enzymes augment activation-induced deaminase (AID) expression via 5-hydroxymethylcytosine modifications at the Aicda superenhancer. Sci Immunol. 2019;4(34). DOI:10.1126/sciimmunol.aau7523.
  • Caldwell BA, Liu MY, Prasasya RD, et al. Functionally distinct roles for TET-oxidized 5-methylcytosine bases in somatic reprogramming to pluripotency. Mol Cell. 2021;81(4):859–869.e858.
  • Soubrier F. TET2: a bridge between DNA methylation and vascular inflammation. Circulation. 2020;141(24):2001–2003.
  • Potus F, Pauciulo Michael W, Cook Elina K, et al. Novel mutations and decreased expression of the epigenetic regulator TET2 in pulmonary arterial hypertension. Circulation. 2020;141(24):1986–2000.
  • Vezzani A, Balosso S, Ravizza T. Neuroinflammatory pathways as treatment targets and biomarkers in epilepsy. Nat Rev Neurol. 2019;15(8):459–472.
  • Weidner LD, Kannan P, Mitsios N, et al. The expression of inflammatory markers and their potential influence on efflux transporters in drug-resistant mesial temporal lobe epilepsy tissue. Epilepsia. 2018;59(8):1507–1517.
  • van Vliet EA, Zibell G, Pekcec A, et al. COX-2 inhibition controls P-glycoprotein expression and promotes brain delivery of phenytoin in chronic epileptic rats. Neuropharmacology. 2010;58(2):404–412.
  • Sun L. Low-dose cyclooxygenase-2 (COX-2) inhibitor celecoxib plays a protective role in the rat model of neonatal necrotizing enterocolitis. Bioengineered. 2021;12(1):7223–7234.
  • Deng X, Shao Y, Xie Y, et al. MicroRNA-146a-5p downregulates the expression of P-Glycoprotein in rats with Lithium-Pilocarpine-induced status epilepticus. Biol Pharm Bull. 2019;42(5):744–750.
  • Shan Y, Li Y, Han H, et al. Insulin reverses choriocarcinoma 5- fluorouracil resistance. Bioengineered. 2021;12(1):2087–2094.
  • Dong T, Li M, Gao F, et al. Construction and imaging of a neurovascular unit model. Neural Regen Res. 2022;17(8):1685–1694.
  • Potschka H. Modulating P-glycoprotein regulation: future perspectives for pharmacoresistant epilepsies? Epilepsia. 2010;51(8):1333–1347.
  • Soldner ELB, Hartz AMS, Akanuma SI, et al. Inhibition of human microsomal PGE2 synthase-1 reduces seizure-induced increases of P-glycoprotein expression and activity at the blood-brain barrier. FASEB J. 2019;33(12):13966–13981.
  • Hartz AM, Pekcec A, Soldner EL, et al. P-gp protein expression and transport activity in rodent Seizure models and human epilepsy. Mol. Pharmaceutics. 2017;14(4):999–1011.
  • Barker-Haliski M, White HS. Glutamatergic mechanisms associated with Seizures and epilepsy. Cold Spring Harb Perspect Med. 2015;5(8):a022863.