A microRNA-328 binding site in PAX6 is associated with centrotemporal spikes of rolandic epilepsy

Annals of Clinical and Translational Neurology

Volumn , Issue , 2016, Pages 512-522

  Panjwani, Naim ^a   Wilson, Michael D ^a,b   Addis, Laura ^c,d   Crosbie, Jennifer ^a,e   Wirrell, Elaine ^f   Auvin, Stéphane ^g   Caraballo, Roberto H ^h   Kinali, Maria ⁱ   McCormick, David ^j   Oren, Caroline ^k   Taylor, Jacqueline ^l   Trounce, John ^m   Clarke, Tara ⁿ   Akman, Cigdem I ^o   Kugler, Steven L ^p   Mandelbaum, David E ^q   McGoldrick, Patricia ^r   Wolf, Steven M ^r   Arnold, Paul ^a,e,s   Schachar, Russell ^a,e   Pal, Deb K ^c,j,t   Strug, Lisa J ^a,u,v   more..

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d ELI LILLY AND COMPANY   (United States)

^e HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^f MAYO CLINIC   (United States)

^g HÔPITAL ROBERT DEBRÉ   (France)

^h HOSPITAL DE PEDIATRÍA PROF DR JUAN P GARRAHAN   (Argentina)

ⁱ CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^j KING S COLLEGE HOSPITAL   (United Kingdom)

^k NORTHWICK PARK HOSPITAL   (United Kingdom)

^l ROYAL FREE LONDON NHS FOUNDATION TRUST   (United Kingdom)

^m Worthing Hospital   (United Kingdom)

ⁿ Columbia University Medical Centre ^*  (United States)

^o NEUROLOGICAL INSTITUTE   (United States)

^p UNIVERSITY OF PENNSYLVANIA   (United States)

^q BROWN UNIVERSITY   (United States)

^r BETH ISRAEL MEDICAL CENTER   (United States)

^s UNIVERSITY OF CALGARY   (Canada)

^t EVELINA LONDON CHILDREN S HOSPITAL   (United Kingdom)

^u UNIVERSITY OF TORONTO   (Canada)

^v HOSPITAL FOR SICK CHILDREN   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 328; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADOLESCENT; ALLELE; ARTICLE; BINDING SITE; CHILD; CONTROLLED STUDY; DOWN REGULATION; ELECTROENCEPHALOGRAPHY; FEMALE; FOLLOW UP; GENE EXPRESSION; GENE LOCUS; GENETIC ASSOCIATION; GENOTYPE; HOMOZYGOSITY; HUMAN; MAJOR CLINICAL STUDY; MALE; PIGMENT EPITHELIUM; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; ROLANDIC EPILEPSY; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84994400321     PISSN: None     EISSN: 23289503     Source Type: Journal    
DOI: 10.1002/acn3.320     Document Type: Article

References (69)

1. Astradsson A, Olafsson E, Ludvigsson P, et al. Rolandic epilepsy: an incidence study in Iceland. Epilepsia 1998;39:884–886.
2. Sidenvall R, Forsgren L, Heijbel J. Prevalence and characteristics of epilepsy in children in northern Sweden. Seizure 1996;5:139–146.
3. Pal DK, Li W, Clarke T, et al. Pleiotropic effects of the 11p13 locus on developmental verbal dyspraxia and EEG centrotemporal sharp waves. Genes Brain Behav 2010;9:1004–1012.
4. Vega YH, Smith A, Cockerill H, et al. Risk factors for reading disability in families with rolandic epilepsy. Epilepsy Behav 2015;53:174–179.
5. Guerrini R, Pellacani S. Benign childhood focal epilepsies. Epilepsia 2012;53(Suppl 4):9–18.
6. Fejerman N, Caraballo R, Tenembaum SN. Atypical evolutions of benign localization-related epilepsies in children: are they predictable? Epilepsia 2000;41:380–390.
7. Eeg-Olofsson O, Petersen I, Sellden U. The development of the electroencephalogram in normal children from the age of 1 through 15 years. Paroxysmal activity. Neuropadiatrie 1971;2:375–404.
8. Ballaban-Gil K, Tuchman R. Epilepsy and epileptiform EEG: association with autism and language disorders. Ment Retard Dev Disabil Res Rev 2000;6:300–308.
9. Holtmann M, Becker K, Kentner-Figura B, Schmidt MH. Increased frequency of rolandic spikes in ADHD children. Epilepsia 2003;44:1241–1244.
10. Vears DF, Tsai MH, Sadleir LG, et al. Clinical genetic studies in benign childhood epilepsy with centrotemporal spikes. Epilepsia 2012;53:319–324.
11. Vadlamudi L, Milne RL, Lawrence K, et al. Genetics of epilepsy: the testimony of twins in the molecular era. Neurology 2014;83:1042–1048.
12. Kugler SL, Bali B, Lieberman P, et al. An autosomal dominant genetically heterogeneous variant of rolandic epilepsy and speech disorder. Epilepsia 2008;49:1086–1090.
13. Scheffer IE, Jones L, Pozzebon M, et al. Autosomal dominant rolandic epilepsy and speech dyspraxia: a new syndrome with anticipation. Ann Neurol 1995;38:633–642.
14. Guerrini R, Bonanni P, Nardocci N, et al. Autosomal recessive rolandic epilepsy with paroxysmal exercise-induced dystonia and writer’s cramp: delineation of the syndrome and gene mapping to chromosome 16p12-11.2. Ann Neurol 1999;45:344–352.
15. Epilepsy Precision Medicine Consortium. A roadmap for precision medicine in the epilepsies. Lancet Neurol 2015;14:1219–1228.
16. Lemke JR, Lal D, Reinthaler EM, et al. Mutations in GRIN2A cause idiopathic focal epilepsy with rolandic spikes. Nat Genet 2013;45:1067–1072.
17. Lal D, Reinthaler EM, Altmuller J, et al. RBFOX1 and RBFOX3 mutations in rolandic epilepsy. PLoS ONE 2013;8:e73323.
18. Lal D, Reinthaler EM, Schubert J, et al. DEPDC5 mutations in genetic focal epilepsies of childhood. Ann Neurol 2014;75:788–792.
19. Neubauer BA, Waldegger S, Heinzinger J, et al. KCNQ2 and KCNQ3 mutations contribute to different idiopathic epilepsy syndromes. Neurology 2008;71:177–183.
20. Reinthaler EM, Dejanovic B, Lal D, et al. Rare variants in gamma-aminobutyric acid type A receptor genes in rolandic epilepsy and related syndromes. Ann Neurol 2015;77:972–986.
21. Reinthaler EM, Lal D, Lebon S, et al. 16p11.2 600 kb Duplications confer risk for typical and atypical Rolandic epilepsy. Hum Mol Genet 2014;23:6069–6080.
22. Bali B, Kull LL, Strug LJ, et al. Autosomal dominant inheritance of centrotemporal sharp waves in rolandic epilepsy families. Epilepsia 2007;48:2266–2272.
23. Neubauer BA, Fiedler B, Himmelein B, et al. Centrotemporal spikes in families with rolandic epilepsy: linkage to chromosome 15q14. Neurology 1998;51:1608–1612.
24. Strug LJ, Clarke T, Chiang T, et al. Centrotemporal sharp wave EEG trait in rolandic epilepsy maps to Elongator Protein Complex 4 (ELP4). Eur J Hum Genet 2009;17:1171–1181.
25. Reinthaler EM, Lal D, Jurkowski W, et al. Analysis of ELP4, SRPX2, and interacting genes in typical and atypical rolandic epilepsy. Epilepsia 2014;55:e89–e93.
26. Derkach A, Chiang T, Gong J, et al. Association analysis using next-generation sequence data from publicly available control groups: the robust variance score statistic. Bioinformatics 2014;30:2179–2188.
27. Pal DK. Epilepsy and neurodevelopmental disorders of language. Curr Opin Neurol 2011;24:126–131.
28. Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 1989;30:389–399.
29. Boxerman JL, Hawash K, Bali B, et al. Is Rolandic epilepsy associated with abnormal findings on cranial MRI? Epilepsy Res 2007;75:180–185.
30. Clarke T, Strug LJ, Murphy PL, et al. High risk of reading disability and speech sound disorder in rolandic epilepsy families: case-control study. Epilepsia 2007;48:2258–2265.
31. Zhu X, Li S, Cooper RS, Elston RC. A unified association analysis approach for family and unrelated samples correcting for stratification. Am J Hum Genet 2008;82:352–365.
32. Crosbie J, Arnold P, Paterson A, et al. Response inhibition and ADHD traits: correlates and heritability in a community sample. J Abnorm Child Psychol 2013;41:497–507.
33. Purcell S, Neale B, Todd-Brown K, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007;81:559–575.
34. R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. 2015.
35. Sinnwell JP, Therneau TM, Schaid DJ. The kinship2 R package for pedigree data. Hum Hered 2014;78:91–93.
36. International HapMap Consortium; Altshuler DM, Gibbs RA, et al. Integrating common and rare genetic variation in diverse human populations. Nature. 2010;467:52–58.
37. Genomes Project Consortium; Abecasis GR, Auton A, et al. An integrated map of genetic variation from 1,092 human genomes. Nature. 2012;491:56–65.
38. Cann HM, de Toma C, Cazes L, et al. A human genome diversity cell line panel. Science 2002;296:261–262.
39. Li MX, Yeung JM, Cherny SS, Sham PC. Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum Genet 2012;131:747–756.
40. Hojsgaard S. The R Package geepack for Generalized Estimating Equations. J Stat Softw 2006;15:1–11.
41. Gordon M, Lumley T. forestplot: advanced forest plot using ‘grid’ graphics. Vienna, Austria: R Foundation for Statistical Computing, 2015.
42. Pruim RJ, Welch RP, Sanna S, et al. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 2010;26:2336–2337.
43. Browning SR, Browning BL. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 2007;81:1084–1097.
44. MacDonald JR, Ziman R, Yuen RK, et al. The Database of Genomic Variants: a curated collection of structural variation in the human genome. Nucleic Acids Res 2014;42(Database issue): D986–D992.
45. Roadmap Epigenomics Consortium; Kundaje A, Meuleman W, et al. Integrative analysis of 111 reference human epigenomes. Nature. 2015;518:317–330.
46. Encode Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012;489:57–74.
47. Griffon A, Barbier Q, Dalino J, et al. Integrative analysis of public ChIP-seq experiments reveals a complex multi-cell regulatory landscape. Nucleic Acids Res 2015;43:e27.
48. Ward LD, Kellis M. HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res 2012;40(Database issue):D930–D934.
49. Mathelier A, Fornes O, Arenillas DJ, et al. JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles. Nucleic Acids Res 2015;44:D110–115.
50. Kertesz M, Iovino N, Unnerstall U, et al. The role of site accessibility in microRNA target recognition. Nat Genet 2007;39:1278–1284.
51. Coelho DJ, Sims DJ, Ruegg PJ, et al. Cell type-specific and sexually dimorphic expression of transcription factor AP-2 in the adult mouse brain. Neuroscience 2005;134:907–919.
52. Ernst J, Kellis M. Large-scale imputation of epigenomic datasets for systematic annotation of diverse human tissues. Nat Biotechnol 2015;33:364–376.
53. Yang Y, Hwang CK, D’Souza UM, et al. Three-amino acid extension loop homeodomain proteins Meis2 and TGIF differentially regulate transcription. J Biol Chem 2000;275:20734–20741.
54. Chen KC, Hsi E, Hu CY, et al. MicroRNA-328 may influence myopia development by mediating the PAX6 gene. Invest Ophthalmol Vis Sci 2012;53:2732–2739.
55. Liang CL, Hsi E, Chen KC, et al. A functional polymorphism at 3′UTR of the PAX6 gene may confer risk for extreme myopia in the Chinese. Invest Ophthalmol Vis Sci 2011;52:3500–3505.
56. Carvill GL, Regan BM, Yendle SC, et al. GRIN2A mutations cause epilepsy-aphasia spectrum disorders. Nat Genet 2013;45:1073–1076.
57. Lesca G, Rudolf G, Bruneau N, et al. GRIN2A mutations in acquired epileptic aphasia and related childhood focal epilepsies and encephalopathies with speech and language dysfunction. Nat Genet 2013;45:1061–1066.
58. Lai CS, Fisher SE, Hurst JA, et al. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 2001;413:519–523.
59. Coutinho P, Pavlou S, Bhatia S, et al. Discovery and assessment of conserved Pax6 target genes and enhancers. Genome Res 2011;21:1349–1359.
60. Stoykova A, Gotz M, Gruss P, Price J. Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 1997;124:3765–3777.
61. McBride DJ, Buckle A, van Heyningen V, Kleinjan DA. DNaseI hypersensitivity and ultraconservation reveal novel, interdependent long-range enhancers at the complex Pax6 cis-regulatory region. PLoS ONE 2011;6:e28616.
62. Sisodiya SM, Free SL, Williamson KA, et al. PAX6 haploinsufficiency causes cerebral malformation and olfactory dysfunction in humans. Nat Genet 2001;28:214–216.
63. Manuel M, Georgala PA, Carr CB, et al. Controlled overexpression of Pax6 in vivo negatively autoregulates the Pax6 locus, causing cell-autonomous defects of late cortical progenitor proliferation with little effect on cortical arealization. Development 2007;134:545–555.
64. Garcia-Ramos C, Jackson DC, Lin JJ, et al. Cognition and brain development in children with benign epilepsy with centrotemporal spikes. Epilepsia 2015;56:1615–1622.
65. Woods JO, Singh-Blom UM, Laurent JM, et al. Prediction of gene-phenotype associations in humans, mice, and plants using phenologs. BMC Bioinformatics 2013;14:203.
66. Pasquinelli AE, Reinhart BJ, Slack F, et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000;408:86–89.
67. Agoston Z, Heine P, Brill MS, et al. Meis2 is a Pax6 co-factor in neurogenesis and dopaminergic periglomerular fate specification in the adult olfactory bulb. Development 2014;141:28–38.
68. Jimenez-Mateos EM, Engel T, Merino-Serrais P, et al. Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat Med 2012;18:1087–1094.
69. Blanchette M, Kent WJ, Riemer C, et al. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res 2004;14:708–715.