Targeted sequencing of 351 candidate genes for epileptic encephalopathy in a large cohort of patients

Molecular Genetics and Genomic Medicine

Volumn 4, Issue 5, 2016, Pages 568-580

  de Kovel, Carolien G F ^a   Brilstra, Eva H ^a   Van Kempen, Marjan J A ^a   Van‘t Slot, Ruben ^a   Nijman, Isaac J ^a   Afawi, Zaid ^b,c   De Jonghe, Peter ^d,e,f   Djémié, Tania ^d,e   Guerrini, Renzo ^g   Hardies, Katia ^d,e   Helbig, Ingo ^h,i   Hendrickx, Rik ^d   Kanaan, Moine ^c   Kramer, Uri ^j   Lehesjoki, Anna Elina E ^k   Lemke, Johannes R ^l   Marini, Carla ^g   Mei, Davide ^g   Møller, Rikke S ^m,n   Pendziwiat, Manuela ⁱ   Stamberger, Hannah ^d,e   Suls, Arvid ^d,e   Weckhuysen, Sarah ^d,e   Balling, R ^o   Barisic, N ^o   Baulac, S ^o   Caglayan, H S ^o   Craiu, D C ^o   Depienne, C ^o   Gormley, P ^o   Hjalgrim, H ^o   Hoffman Zacharska, D ^o   Jahn J ^o   Klein, K M ^o   Komarek, V ^o   LeGuern, E ^o   Lerche, H ^o   May, P ^o   Muhle, H ^o   Pal, D ^o   Palotie, A ^o   Rosenow, F ^o   Selmer, K ^o   Serratosa, J M ^o   Sisodiya, S M ^o   Stephani, U ^o   Sterbova, K ^o   Striano, P ^o   Talvik, T ^o   van Haelst, M ^o   Verbeek, N ^o   von Spiczak, S ^o   Weber, Y G ^o   Koeleman, Bobby P C ^a   more..

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e UNIVERSITY OF ANTWERP   (Belgium)

^f ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^g UNIVERSITY OF FLORENCE   (Italy)

^h CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

ⁱ UNIVERSITY OF KIEL   (Germany)

^j BETHLEHEM UNIVERSITY   (Palestine)

^k UNIVERSITY OF HELSINKI   (Finland)

^l UNIVERSITY OF LEIPZIG   (Germany)

^m DANISH EPILEPSY CENTRE   (Denmark)

ⁿ UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^o University of Southern Denmark ^*

more..

Author keywords

De novo; epileptic encephalopathy; HNRNPU; loss of function; prioritization; recessive; targeted panel sequencing; X linked

Indexed keywords

EID: 85015718168     PISSN: None     EISSN: 23249269     Source Type: Journal    
DOI: 10.1002/mgg3.235     Document Type: Article

References (51)

1. Adzhubei, I., D. M. Jordan, and S. R. Sunyaev. 2013. Predicting functional effect of human missense mutations using PolyPhen-2. Curr. Protoc. Hum. Genet. Chapter 7:20.
2. Backx, L., B. Ceulemans, J. R. Vermeesch, K. Devriendt, and H. Van Esch. 2009. Early myoclonic encephalopathy caused by a disruption of the neuregulin-1 receptor ErbB4. Eur. J. Hum. Genet. 17:378-382.
3. Banne, E., O. Atawneh, M. Henneke, K. Brockmann, J. Gartner, O. Elpeleg, et al. 2013. West syndrome, microcephaly, grey matter heterotopia and hypoplasia of corpus callosum due to a novel ARFGEF2 mutation. J. Med. Genet. 50:772-775.
4. Basel-Vanagaite, L., T. Hershkovitz, E. Heyman, M. Raspall-Chaure, N. Kakar, P. Smirin-Yosef, et al. 2013. Biallelic SZT2 mutations cause infantile encephalopathy with epilepsy and dysmorphic corpus callosum. Am. J. Hum. Genet. 93:524-529.
5. Caliebe, A., H. Y. Kroes, der van Smagt J. J., J. I. Martin-Subero, H. Tonnies, van‘t Slot R., et al. 2010. Four patients with speech delay, seizures and variable corpus callosum thickness sharing a 0.440 Mb deletion in region 1q44 containing the HNRPU gene. Eur. J. Med. Genet. 53:179-185.
6. Campeau, P. M., D. Kasperaviciute, J. T. Lu, L. C. Burrage, C. Kim, M. Hori, et al. 2014. The genetic basis of DOORS syndrome: an exome-sequencing study. Lancet Neurol. 13:44-58.
7. Carvill, G. L., S. B. Heavin, S. C. Yendle, J. M. McMahon, B. J. O'Roak, J. Cook, et al. 2013. Targeted resequencing in epileptic encephalopathies identifies de novo mutations in CHD2 and SYNGAP1. Nat. Genet. 45:825-830.
8. Chen, Y. I., R. E. Moore, H. Y. Ge, M. K. Young, T. D. Lee, and S. W. Stevens. 2007. Proteomic analysis of in vivo-assembled pre-mRNA splicing complexes expands the catalog of participating factors. Nucleic Acids Res. 35:3928-3944.
9. Claes, L., J. Del-Favero, B. Ceulemans, L. Lagae, C. Van Broeckhoven, and P. De Jonghe. 2001. De novo mutations in the sodium-channel gene SCN1A cause severe myoclonic epilepsy of infancy. Am. J. Hum. Genet. 68:1327-1332.
10. Consortium E.E.R, Project EPG, Consortium E.K. 2014. De novo mutations in synaptic transmission genes including DNM1 cause epileptic encephalopathies. Am. J. Hum. Genet. 95:360-370.
11. Cooper, G. M., E. A. Stone, G. Asimenos, N. C. S. Program, E. D. Green, S. Batzoglou, et al. 2005. Distribution and intensity of constraint in mammalian genomic sequence. Genome Res. 15:901-913.
12. Dong, C., P. Wei, X. Jian, R. Gibbs, E. Boerwinkle, K. Wang, et al. 2015. Comparison and integration of deleteriousness prediction methods for nonsynonymous SNVs in whole exome sequencing studies. Hum. Mol. Genet. 24:2125-2137.
13. Engel, J Jr., International League Against E. 2001. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia 42:796-803.
14. Epi4K-Consortium, Epilepsy Phenome/Genome, P., A. S. Allen, S. F. Berkovic, P. Cossette, N. Delanty, D. Dlugos, et al. 2013. De novo mutations in epileptic encephalopathies. Nature 501:217-221.
15. Frühmesser, A., J. Blake, E. Haberlandt, B. Baying, B. Raeder, H. Runz, et al. 2013. Disruption of EXOC6B in a patient with developmental delay, epilepsy, and a de novo balanced t(2;8) translocation. Eur. J. Hum. Genet. 21:1177-1180.
16. Gandomi, S. K., K. D. Farwell Gonzalez, M. Parra, L. Shahmirzadi, J. Mancuso, P. Pichurin, et al. 2014. Diagnostic exome sequencing identifies two novel IQSEC2 mutations associated with X-linked intellectual disability with seizures: implications for genetic counseling and clinical diagnosis. J. Genet. Couns. 23:289-298.
17. Grantham, R. 1974. Amino acid difference formula to help explain protein evolution. Science 185:862-864.
18. Grozeva, D., K. Carss, O. Spasic-Boskovic, M. I. Tejada, J. Gecz, M. Shaw, et al. 2015. Targeted next-generation sequencing analysis of 1,000 individuals with intellectual disability. Hum. Mutat. 36:1197-1204.
19. Haack, T. B., P. Hogarth, M. C. Kruer, A. Gregory, T. Wieland, T. Schwarzmayr, et al. 2012. Exome sequencing reveals de novo WDR45 mutations causing a phenotypically distinct, X-linked dominant form of NBIA. Am. J. Hum. Genet. 91:1144-1149.
20. Hamdan, F. F., M. Srour, J. M. Capo-Chichi, H. Daoud, C. Nassif, L. Patry, et al. 2014. De novo mutations in moderate or severe intellectual disability. PLoS Genet. 10:e1004772.
21. Harkin, L. A., J. M. McMahon, X. Iona, L. Dibbens, J. T. Pelekanos, S. M. Zuberi, et al. 2007. The spectrum of SCN1A-related infantile epileptic encephalopathies. Brain 130:843-852.
22. Hirose, S., and A. Mitsudome. 2003. X-linked mental retardation and epilepsy: pathogenetic significance of ARX mutations. Brain Dev. 25:161-165.
23. Hu, J., and P. C. Ng. 2012. Predicting the effects of frameshifting indels. Genome Biol. 13:R9.
24. Janer, A., H. Antonicka, E. Lalonde, T. Nishimura, F. Sasarman, G. K. Brown, et al. 2012. An RMND1 Mutation causes encephalopathy associated with multiple oxidative phosphorylation complex deficiencies and a mitochondrial translation defect. Am. J. Hum. Genet. 91:737-743.
25. Kalscheuer, V. M., V. M. James, M. L. Himelright, P. Long, R. Oegema, C. Jensen, et al. 2015. Novel missense mutation A789V in IQSEC2 underlies X-linked intellectual disability in the MRX78 family. Front. Mol. Neurosci. 8:85.
26. Kircher, M., D. M. Witten, P. Jain, B. J. O'Roak, G. M. Cooper, and J. Shendure. 2014. A general framework for estimating the relative pathogenicity of human genetic variants. Nat. Genet. 46:310-315.
27. Kodera, H., M. Kato, A. S. Nord, T. Walsh, M. Lee, G. Yamanaka, et al. 2013. Targeted capture and sequencing for detection of mutations causing early onset epileptic encephalopathy. Epilepsia 54:1262-1269.
28. Kumar, P., S. Henikoff, and P. C. Ng. 2009. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4:1073-1081.
29. Lemke, J. R., K. Geider, K. L. Helbig, H. O. Heyne, H. Schutz, J. Hentschel, et al. 2016. Delineating the GRIN1 phenotypic spectrum: a distinct genetic NMDA receptor encephalopathy. Neurology 86:2171-8.
30. Lionel, A. C., A. K. Vaags, D. Sato, M. J. Gazzellone, E. B. Mitchell, H. Y. Chen, et al. 2013. Rare exonic deletions implicate the synaptic organizer Gephyrin (GPHN) in risk for autism, schizophrenia and seizures. Hum. Mol. Genet. 22:2055-2066.
31. McKenna, A., M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, et al. 2010. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20:1297-1303.
32. McRae, J. F., S. Clayton, T. W. Fitzgerald, J. Kaplanis, E. Prigmore, D. Rajan, et al. 2016. Prevalence, phenotype and architecture of developmental disorders caused by de novo mutation. bioRxiv 049056; doi: http://dx.doi.org/10.1101/049056
33. Morleo, M., D. Iaconis, D. Chitayat, I. Peluso, R. Marzella, A. Renieri, et al. 2008. Disruption of the IQSEC2 transcript in a female with X; autosome translocation t(X;20)(p11.2;q11.2) and a phenotype resembling X-linked infantile spasms (ISSX) syndrome. Mol. Med. Rep. 1:33-39.
34. Nakamura, K., H. Kodera, T. Akita, M. Shiina, M. Kato, H. Hoshino, et al. 2013. De novo mutations in GNAO1, encoding a Galpha subunit of heterotrimeric G proteins, cause epileptic encephalopathy. Am. J. Hum. Genet. 93:496-505.
35. Need, A. C., V. Shashi, Y. Hitomi, K. Schoch, K. V. Shianna, M. T. McDonald, et al. 2012. Clinical application of exome sequencing in undiagnosed genetic conditions. J. Med. Genet. 49:353-361.
36. Ohba, C., H. Osaka, M. Iai, S. Yamashita, Y. Suzuki, N. Aida, et al. 2013. Diagnostic utility of whole exome sequencing in patients showing cerebellar and/or vermis atrophy in childhood. Neurogenetics 14:225-232.
37. Ohba, C., S. Nabatame, Y. Iijima, K. Nishiyama, Y. Tsurusaki, M. Nakashima, et al. 2014. De novo WDR45 mutation in a patient showing clinically Rett syndrome with childhood iron deposition in brain. J. Hum. Genet. 59:292-295.
38. Olson, H. E., D. Tambunan, C. LaCoursiere, M. Goldenberg, R. Pinsky, E. Martin, et al. 2015. Mutations in epilepsy and intellectual disability genes in patients with features of Rett syndrome. Am. J. Med. Genet. A 167A:2017-2025.
39. Ozawa, T., R. Koide, Y. Nakata, H. Saitsu, N. Matsumoto, K. Takahashi, et al. 2014. A novel WDR45 mutation in a patient with static encephalopathy of childhood with neurodegeneration in adulthood (SENDA). Am. J. Med. Genet. A 164A:2388-2390.
40. Paciorkowski, A. R., J. Weisenberg, J. B. Kelley, A. Spencer, E. Tuttle, D. Ghoneim, et al. 2014. Autosomal recessive mutations in nuclear transport factor KPNA7 are associated with infantile spasms and cerebellar malformation. Eur. J. Hum. Genet. 22:587-593.
41. Poulton, C., R. Oegema, D. Heijsman, J. Hoogeboom, R. Schot, H. Stroink, et al. 2013. Progressive cerebellar atrophy and polyneuropathy: expanding the spectrum of PNKP mutations. Neurogenetics 14:43-51.
42. Reiss, J., S. Gross-Hardt, E. Christensen, P. Schmidt, R. R. Mendel, and G. Schwarz. 2001. A mutation in the gene for the neurotransmitter receptor-clustering protein gephyrin causes a novel form of molybdenum cofactor deficiency. Am. J. Hum. Genet. 68:208-213.
43. Saitsu, H., T. Nishimura, K. Muramatsu, H. Kodera, S. Kumada, K. Sugai, et al. 2013. De novo mutations in the autophagy gene WDR45 cause static encephalopathy of childhood with neurodegeneration in adulthood. Nat. Genet. 45:445-449, 449e1.
44. Samocha, K. E., E. B. Robinson, S. J. Sanders, C. Stevens, A. Sabo, L. M. McGrath, et al. 2014. A framework for the interpretation of de novo mutation in human disease. Nat. Genet. 46:944-950.
45. Shoubridge, C., P. S. Tarpey, F. Abidi, S. L. Ramsden, S. Rujirabanjerd, J. A. Murphy, et al. 2010. Mutations in the guanine nucleotide exchange factor gene IQSEC2 cause nonsyndromic intellectual disability. Nat. Genet. 42:486-488.
46. Simpson, M. A., H. Cross, C. Proukakis, D. A. Priestman, D. C. Neville, G. Reinkensmeier, et al. 2004. Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat. Genet. 36:1225-1229.
47. Striano, P., N. Specchio, R. Biancheri, N. Cannelli, A. Simonati, D. Cassandrini, et al. 2007. Clinical and electrophysiological features of epilepsy in Italian patients with CLN8 mutations. Epilepsy Behav. 10:187-191.
48. Thierry, G., C. Beneteau, O. Pichon, E. Flori, B. Isidor, F. Popelard, et al. 2012. Molecular characterization of 1q44 microdeletion in 11 patients reveals three candidate genes for intellectual disability and seizures. Am. J. Med. Genet. A 158A:1633-1640.
49. Tran Mau-Them, F., M. Willems, B. Albrecht, E. Sanchez, J. Puechberty, S. Endele, et al. 2014. Expanding the phenotype of IQSEC2 mutations: truncating mutations in severe intellectual disability. Eur. J. Hum. Genet. 22:289-292.
50. Veeramah, K. R., L. Johnstone, T. M. Karafet, D. Wolf, R. Sprissler, J. Salogiannis, et al. 2013. Exome sequencing reveals new causal mutations in children with epileptic encephalopathies. Epilepsia 54:1270-1281.
51. Ware, J. S., K. E. Samocha, J. Homsy, and M. J. Daly. 2015. Interpreting de novo variation in human disease using denovolyzeR. Curr. Protoc. Hum. Genet. 87:7.25.1-7.2515.