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Lal, Dennis ; Ruppert, Ann-Kathrin ; Trucks, Holger ; Schulz, Herbert ; Kovel, Carolien G. de ; Kasteleijn-Nolst Trenité, Dorothée G. ; Sonsma, Anja C. M. ; Koeleman, Bobby P. ; Lindhout, Dick ; Weber, Yvonne G. ; Lerche, Holger ; Kapser, Claudia ; Schankin, Christoph Josef ; Kunz, Wolfram S. ; Surges, Rainer ; Elger, Christian Erich ; Gaus, Verena ; Schmitz, Bettina ; Helbig, Ingo ; Muhle, Hiltrud ; Stephani, Ulrich ; Klein, Karl Martin ; Rosenow, Felix ; Neubauer, Bernd Axel ; Reinthaler, Eva Maria ; Zimprich, Fritz ; Feucht, Martha ; Møller, Rikke S. ; Hjalgrim, Helle ; Jonghe, Peter De ; Suls, Arvid ; Lieb, Wolfgang ; Franke, Andre ; Strauch, Konstantin ; Gieger, Christian ; Schurmann, Claudia ; Schminke, Ulf ; Nürnberg, Peter ; Sander, Thomas
Genetic generalised epilepsy (GGE) is the most common form of genetic epilepsy, accounting for 20% of all epilepsies. Genomic copy number variations (CNVs) constitute important genetic risk factors of common GGE syndromes. In our present genome-wide burden analysis, large (≥ 400 kb) and rare (< 1%) autosomal microdeletions with high calling confidence (≥ 200 markers) were assessed by the Affymetrix SNP 6.0 array in European case-control cohorts of 1,366 GGE patients and 5,234 ancestry-matched controls. We aimed to: 1) assess the microdeletion burden in common GGE syndromes, 2) estimate the relative contribution of recurrent microdeletions at genomic rearrangement hotspots and non-recurrent microdeletions, and 3) identify potential candidate genes for GGE. We found a significant excess of microdeletions in 7.3% of GGE patients compared to 4.0% in controls (P = 1.8 x 10-7; OR = 1.9). Recurrent microdeletions at seven known genomic hotspots accounted for 36.9% of all microdeletions identified in the GGE cohort and showed a 7.5-fold increased burden (P = 2.6 x 10-17) relative to controls. Microdeletions affecting either a gene previously implicated in neurodevelopmental disorders (P = 8.0 x 10-18, OR = 4.6) or an evolutionarily conserved brain-expressed gene related to autism spectrum disorder (P = 1.3 x 10-12, OR = 4.1) were significantly enriched in the GGE patients. Microdeletions found only in GGE patients harboured a high proportion of genes previously associated with epilepsy and neuropsychiatric disorders (NRXN1, RBFOX1, PCDH7, KCNA2, EPM2A, RORB, PLCB1). Our results demonstrate that the significantly increased burden of large and rare microdeletions in GGE patients is largely confined to recurrent hotspot microdeletions and microdeletions affecting neurodevelopmental genes, suggesting a strong impact of fundamental neurodevelopmental processes in the pathogenesis of common GGE syndromes.
Dongen, Jenny van ; Hagenbeek, Fiona A. ; Suderman, Matthew ; Roetman, Peter J. ; Sugden, Karen ; Geburtig-Chiocchetti, Andreas ; Ismail, Khadeeja ; Mulder, Rosa H. ; Hafferty, Jonathan D. ; Adams, Mark J. ; Walker, Rosie M. ; Morris, Stewart W. ; Lahti, Jari ; Küpers, Leanne K. ; Escaramis, Georgia ; Alemany, Silvia ; Bonder, Marc Jan ; Meijer, Mandy ; Ip, Hill F. ; Jansen, Rick ; Baselmans, Bart M. L. ; Parmar, Priyanka ; Lowry, Estelle ; Streit, Fabian ; Sirignano, Lea ; Send, Tabea S. ; Frank, Josef ; Jylhävä, Juulia ; Wang, Yunzhang ; Mishra, Pashupati Prasad ; Colins, Olivier F. ; Corcoran, David L. ; Poulton, Richie ; Mill, Jonathan ; Hannon, Eilis ; Arseneault, Louise ; Korhonen, Tellervo ; Vuoksimaa, Eero ; Felix, Janine F. ; Bakermans-Kranenburg, Marian J. ; Campbell, Archie ; Czamara, Darina ; Binder, Elisabeth ; Corpeleijn, Eva ; González Ruiz, Juan Ramon ; Grazuleviciene, Regina ; Gutzkow, Kristine B. ; Evandt, Jorunn ; Vafeiadi, Marina ; Klein, Marieke ; Meer, Dennis van der ; Ligthart, Lannie ; Heijmans, Bastiaan Theodoor ; Hoen, Peter A. C. 't ; Meurs, Joyce Berdina Josepha van ; Franke, Lude ; Boomsma, Dorret I. ; Pool, René ; Hottenga, Jouke J. ; Greevenbroek, Marleen M. J. van ; Stehouwer, Coen D. A. ; Kallen, Carla J. H. van der ; Schalkwijk, Casper G. ; Wijmenga, Cisca ; Zhernakova, Sasha ; Tigchelaar, Ettje F. ; Slagboom, P. Eline ; Beekman, Marian ; Deelen, Joris ; Heemst, Diana van ; Veldink, Jan H. ; Berg, Leonard H. van den ; Duijn, Cornelia M. van ; Hofman, Bert A. ; Isaacs, Aaron ; Uitterlinden, André G. ; Jhamai, P. Mila ; Verbiest, Michael ; Suchiman, H. Eka D. ; Verkerk, Marijn ; Breggen, Ruud van der ; Rooij, Jeroen van ; Lakenberg, Nico ; Mei, Hailiang ; Iterson, Maarten van ; Galen, Michiel van ; Bot, Jan ; Zhernakova, Dasha V. ; Hof, Peter van ’t ; Deelen, Patrick ; Nooren, Irene ; Moed, Matthijs ; Vermaat, Martijn ; Luijk, René ; Dijk, Freerk van ; Arindrarto, Wibowo ; Kielbasa, Szymon M. ; Swertz, Morris A. ; Zwet, Erik. W. van ; Hoen, Peter-Bram ’t ; Kluft, Cornelis ; Davies, Gareth E. ; Hakulinen, Christian ; Keltikangas-Järvinen, Liisa ; Franke, Barbara ; Freitag, Christine M. ; Konrad, Kerstin ; Hervás, Amaia ; Fernández-Rivas, Aranzazu ; Vetro, Agnes ; Raitakari, Olli ; Lehtimäki, Terho ; Vermeiren, Robert ; Strandberg, Timo ; Räikkönen, Katri ; Snieder, Harold ; Witt, Stephanie H. ; Deuschle, Michael ; Pedersen, Nancy L. ; Hägg, Sara ; Sunyer, Jordi ; Kaprio, Jaakko ; Ollikainen, Miina ; Moffitt, Terrie E. ; Tiemeier, Henning ; IJzendoorn, Marinus H. van ; Relton, Caroline ; Vrijheid, Martine ; Sebert, Sylvain ; Jarvelin, Marjo-Riitta ; Caspi, Avshalom ; Evans, Kathryn L. ; McIntosh, Andrew M. ; Bartels, Meike
DNA methylation profiles of aggressive behavior may capture lifetime cumulative effects of genetic, stochastic, and environmental influences associated with aggression. Here, we report the first large meta-analysis of epigenome-wide association studies (EWAS) of aggressive behavior (N = 15,324 participants). In peripheral blood samples of 14,434 participants from 18 cohorts with mean ages ranging from 7 to 68 years, 13 methylation sites were significantly associated with aggression (alpha = 1.2 × 10−7; Bonferroni correction). In cord blood samples of 2425 children from five cohorts with aggression assessed at mean ages ranging from 4 to 7 years, 83% of these sites showed the same direction of association with childhood aggression (r = 0.74, p = 0.006) but no epigenome-wide significant sites were found. Top-sites (48 at a false discovery rate of 5% in the peripheral blood meta-analysis or in a combined meta-analysis of peripheral blood and cord blood) have been associated with chemical exposures, smoking, cognition, metabolic traits, and genetic variation (mQTLs). Three genes whose expression levels were associated with top-sites were previously linked to schizophrenia and general risk tolerance. At six CpGs, DNA methylation variation in blood mirrors variation in the brain. On average 44% (range = 3–82%) of the aggression–methylation association was explained by current and former smoking and BMI. These findings point at loci that are sensitive to chemical exposures with potential implications for neuronal functions. We hope these results to be a starting point for studies leading to applications as peripheral biomarkers and to reveal causal relationships with aggression and related traits.
Pérez-Palma, Eduardo ; Helbig, Ingo ; Klein, Karl Martin ; Anttila, Verneri ; Horn, Heiko ; Maria Reinthaler, Eva ; Gormley, Padhraig ; Ganna, Andrea ; Byrnes, Andrea ; Pernhorst, Katharina ; Toliat, Mohammad Reza ; Saarentaus, Elmo ; Howrigan, Daniel P. ; Hoffman, Per ; Miquel, Juan Francisco ; De Ferrari, Giancarlo ; Nürnberg, Peter ; Lerche, Holger ; Zimprich, Fritz ; Neubauer, Bern A. ; Becker, Albert J. ; Rosenow, Felix ; Perucca, Emilio ; Zara, Federico ; Weber, Yvonne G. ; Lal, Dennis
Background Microdeletions are known to confer risk to epilepsy, particularly at genomic rearrangement “hotspot” loci. However, deciphering their role outside hotspots and risk assessment by epilepsy sub-type has not been conducted.
Methods We assessed the burden, frequency and genomic content of rare, large microdeletions found in a previously published cohort of 1,366 patients with Genetic Generalized Epilepsy (GGE) plus two sets of additional unpublished genome-wide microdeletions found in 281 Rolandic Epilepsy (RE) and 807 Adult Focal Epilepsy (AFE) patients, totaling 2,454 cases. These microdeletion sets were assessed in a combined analysis and in sub-type specific approaches against 6,746 ethnically matched controls.
Results When hotspots are considered, we detected an enrichment of microdeletions in the combined epilepsy analysis (adjusted-P= 2.00×10-7; OR = 1.89; 95%-CI: 1.51-2.35), where the implicated microdeletions overlapped with rarely deleted genes and those involved in neurodevelopmental processes. Sub-type specific analyses showed that hotspot deletions in the GGE subgroup contribute most of the signal (adjusted-P = 1.22×10-12; OR = 7.45; 95%-CI = 4.20-11.97). Outside hotspot loci, microdeletions were enriched in the GGE cohort for neurodevelopmental genes (adjusted-P = 4.78×10-3; OR = 2.30; 95%-CI = 1.42-3.70), whereas no additional signal was observed for RE and AFE. Still, gene content analysis was able to identify known (NRXN1, RBFOX1 and PCDH7) and novel (LOC102723362) candidate genes affected in more than one epilepsy sub-type but not in controls.
Conclusions Our results show a heterogeneous effect of recurrent and non-recurrent microdeletions as part of the genetic architecture of GGE and a minor to negligible contribution in the etiology of RE and AFE.