Rare variants in γ-aminobutyric acid type A receptor genes in rolandic epilepsy and related syndromes

Annals of Neurology

Volumn 77, Issue 6, 2015, Pages 972-986

  Reinthaler, Eva M ^a   Dejanovic, Borislav ^b   Lal, Dennis ^b,c,d   Semtner, Marcus ^e   Merkler, Yvonne ^b   Reinhold, Annika ^e   Pittrich, Dorothea A ^a   Hotzy, Christoph ^a   Feucht, Martha ^a   Steinböck, Hannelore ^f   Gruber Sedlmayr, Ursula ^g   Ronen, Gabriel M ^h   Neophytou, Birgit ⁱ   Geldner, Julia ^j   Haberlandt, Edda ^k   Muhle, Hiltrud ^l   Ikram, M Arfan ^m   Van Duijn, Cornelia M ^m   Uitterlinden, Andre G ^m   Hofman, Albert ^m   Altmüller, Janine ^b,d   Kawalia, Amit ^d   Toliat, Mohammad R ^d   Nürnberg, Peter ^b,d   Lerche, Holger ⁿ   Nothnagel, Michael ^d   Thiele, Holger ^d   Sander, Thomas ^d   Meier, Jochen C ^e,o   Schwarz, Günter ^b   Neubauer, Bernd A ^c   Zimprich, Fritz ^a   more..

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY HOSPITAL GIESSEN   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^f Private Practice for Pediatrics   (Austria)

^g MEDICAL UNIVERSITY OF GRAZ   (Austria)

^h MCMASTER UNIVERSITY   (Canada)

ⁱ ST ANNA CHILDREN S HOSPITAL   (Austria)

^j KAISER FRANZ JOSEF HOSPITAL   (Austria)

^k INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^l UNIVERSITY OF KIEL   (Germany)

^m ERASMUS MEDICAL CENTER   (Netherlands)

ⁿ UNIVERSITY OF TÜBINGEN   (Germany)

^o TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; POSTSYNAPTIC RECEPTOR; PROTEIN VARIANT; GABRG2 PROTEIN, HUMAN;

ADULT; ARTICLE; CELL MEMBRANE; COMPUTER MODEL; EVOKED RESPONSE; EXOME; FEMALE; FUNCTIONAL ASSESSMENT; GENE MUTATION; GENETIC SCREENING; GENETIC VARIABILITY; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN STABILITY; RISK ASSESSMENT; ROLANDIC EPILEPSY; SEGREGATION ANALYSIS; CAUCASIAN; GENETICS; HEK293 CELL LINE; LANDAU KLEFFNER SYNDROME; LIPOYLATION; MUTATION; PEDIGREE; SYNDROME;

EPILEPSY, ROLANDIC; EUROPEAN CONTINENTAL ANCESTRY GROUP; EXOME; FEMALE; HEK293 CELLS; HUMANS; LANDAU-KLEFFNER SYNDROME; LIPOYLATION; MALE; MUTATION; PEDIGREE; RECEPTORS, GABA-A; SYNDROME;

EID: 84930035622     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24395     Document Type: Article

References (62)

1. Gobbi G, Boni A, Filippini M,. The spectrum of idiopathic Rolandic epilepsy syndromes and idiopathic occipital epilepsies: from the benign to the disabling. Epilepsia 2006; 47 (suppl 2): 62-66.
2. Guerrini R, Pellacani S,. Benign childhood focal epilepsies. Epilepsia 2012; 53 (suppl 4): 9-18.
3. Fejerman N,. Atypical rolandic epilepsy. Epilepsia 2009; 50 (suppl 7): 9-12.
4. 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.
5. Tovia E, Goldberg-Stern H, Ben Zeev B, et al., The prevalence of atypical presentations and comorbidities of benign childhood epilepsy with centrotemporal spikes. Epilepsia 2011; 52: 1483-1488.
6. Kavros PM, Clarke T, Strug LJ, et al., Attention impairment in rolandic epilepsy: systematic review. Epilepsia 2008; 49: 1570-1580.
7. Vears DF, Tsai MH, Sadleir LG, et al., Clinical genetic studies in benign childhood epilepsy with centrotemporal spikes. Epilepsia 2012; 53: 319-324.
8. Lemke JR, Lal D, Reinthaler EM, et al., Mutations in GRIN2A cause idiopathic focal epilepsy with rolandic spikes. Nat Genet 2013; 45: 1067-1072.
9. 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.
10. Carvill GL, Regan BM, Yendle SC, et al., GRIN2A mutations cause epilepsy-aphasia spectrum disorders. Nat Genet 2013; 45: 1073-1076.
11. Lal D, Reinthaler EM, Schubert J, et al., DEPDC5 mutations in genetic focal epilepsies of childhood. Ann Neurol 2014; 75: 788-792.
12. Lal D, Reinthaler EM, Altmuller J, et al., RBFOX1 and RBFOX3 mutations in rolandic epilepsy. PLoS One 2013; 8: e73323.
13. 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.
14. Winkelmann A, Maggio N, Eller J, et al., Changes in neural network homeostasis trigger neuropsychiatric symptoms. J Clin Invest 2014; 124: 696-711.
15. Meier JC, Semtner M, Winkelmann A, Wolfart J,. Presynaptic mechanisms of neuronal plasticity and their role in epilepsy. Front Cell Neurosci 2014; 8: 164.
16. Luscher B, Fuchs T, Kilpatrick CL,. GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 2011; 70: 385-409.
17. Galanopoulou AS,. GABA(A) receptors in normal development and seizures: friends or foes? Curr Neuropharmacol 2008; 6: 1-20.
18. Olsen RW, DeLorey TM, Gordey M, Kang MH,. GABA receptor function and epilepsy. Adv Neurol 1999; 79: 499-510.
19. De Deyn PP, Marescau B, MacDonald RL,. Epilepsy and the GABA-hypothesis: a brief review and some examples. Acta Neurol Belg 1990; 90: 65-81.
20. Macdonald RL, Kang JQ, Gallagher MJ,. GABAA receptor subunit mutations and genetic epilepsies. In:, Noebels JL, Avoli M, Rogawski MA, et al, eds. Jasper's basic mechanisms of the epilepsies. 4th ed. Bethesda, MD: National Center for Biotechnology Information, 2012.
21. Allen AS, Berkovic SF, Cossette P, et al., De novo mutations in epileptic encephalopathies. Nature 2013; 501: 217-221.
22. Schweizer C, Balsiger S, Bluethmann H, et al., The gamma 2 subunit of GABA(A) receptors is required for maintenance of receptors at mature synapses. Mol Cell Neurosci 2003; 24: 442-450.
23. Dejanovic B, Schwarz G,. Neuronal nitric oxide synthase-dependent S-nitrosylation of gephyrin regulates gephyrin clustering at GABAergic synapses. J Neurosci 2014; 34: 7763-7768.
24. Berg AT, Berkovic SF, Brodie MJ, et al., Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia 2010; 51: 676-685.
25. Aicardi J, Chevrie JJ,. Atypical benign partial epilepsy of childhood. Dev Med Child Neurol 1982; 24: 281-292.
26. Doose H, Hahn A, Neubauer BA, et al., Atypical "benign" partial epilepsy of childhood or pseudo-Lennox syndrome. Part II: family study. Neuropediatrics 2001; 32: 9-13.
27. Hahn A, Pistohl J, Neubauer BA, Stephani U,. Atypical "benign" partial epilepsy or pseudo-Lennox syndrome. Part I: symptomatology and long-term prognosis. Neuropediatrics 2001; 32: 1-8.
28. Hofman A, van Duijn CM, Franco OH, et al., The Rotterdam Study: 2012 objectives and design update. Eur J Epidemiol 2011; 26: 657-686.
29. Purcell SM, Moran JL, Fromer M, et al., A polygenic burden of rare disruptive mutations in schizophrenia. Nature 2014; 506: 185-190.
30. Yeo G, Burge CB,. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 2004; 11: 377-394.
31. Liu X, Jian X, Boerwinkle E,. dbNSFP v2.0: a database of human non-synonymous SNVs and their functional predictions and annotations. Hum Mutat 2013; 34: E2393-E2402.
32. Jacob TC, Bogdanov YD, Magnus C, et al., Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J Neurosci 2005; 25: 10469-10478.
33. Dejanovic B, Semtner M, Ebert S, et al., Palmitoylation of gephyrin controls receptor clustering and plasticity of GABAergic synapses. PLoS Biol 2014; 12: e1001908.
34. Fukata M, Fukata Y, Adesnik H, et al., Identification of PSD-95 palmitoylating enzymes. Neuron 2004; 44: 987-996.
35. Dejanovic B, Lal D, Catarino CB, et al., Exonic microdeletions of the gephyrin gene impair GABAergic synaptic inhibition in patients with idiopathic generalized epilepsy. Neurobiol Dis 2014; 67: 88-96.
36. Tanaka M, Olsen RW, Medina MT, et al., Hyperglycosylation and reduced GABA currents of mutated GABRB3 polypeptide in remitting childhood absence epilepsy. Am J Hum Genet 2008; 82: 1249-1261.
37. Dibbens LM, Feng HJ, Richards MC, et al., GABRD encoding a protein for extra- or peri-synaptic GABAA receptors is a susceptibility locus for generalized epilepsies. Hum Mol Genet 2004; 13: 1315-1319.
38. Miller PS, Aricescu AR,. Crystal structure of a human GABAA receptor. Nature 2014; 512: 270-275.
39. Kang JQ, Macdonald RL,. The GABAA receptor gamma2 subunit R43Q mutation linked to childhood absence epilepsy and febrile seizures causes retention of alpha1beta2gamma2S receptors in the endoplasmic reticulum. J Neurosci 2004; 24: 8672-8677.
40. Keller CA, Yuan X, Panzanelli P, et al., The gamma2 subunit of GABA(A) receptors is a substrate for palmitoylation by GODZ. J Neurosci 2004; 24: 5881-5891.
41. Fang C, Deng L, Keller CA, et al., GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses. J Neurosci 2006; 26: 12758-12768.
42. De Rubeis S, He X, Goldberg AP, et al., Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 2014; 515: 209-215.
43. Johnston AJ, Kang JQ, Shen W, et al., A novel GABRG2 mutation, p.R136∗, in a family with GEFS+ and extended phenotypes. Neurobiol Dis 2014; 64: 131-141.
44. de Kovel CG, Trucks H, Helbig I, et al., Recurrent microdeletions at 15q11.2 and 16p13.11 predispose to idiopathic generalized epilepsies. Brain 2010; 133 (pt 1): 23-32.
45. Lal D, Trucks H, Moller RS, et al., Rare exonic deletions of the RBFOX1 gene increase risk of idiopathic generalized epilepsy. Epilepsia 2013; 54: 265-271.
46. Moller RS, Weber YG, Klitten LL, et al., Exon-disrupting deletions of NRXN1 in idiopathic generalized epilepsy. Epilepsia 2013; 54: 256-264.
47. Ottman R,. Analysis of genetically complex epilepsies. Epilepsia 2005; 46 (suppl 10): 7-14.
48. Audenaert D, Schwartz E, Claeys KG, et al., A novel GABRG2 mutation associated with febrile seizures. Neurology 2006; 67: 687-690.
49. Huang X, Hernandez CC, Hu N, Macdonald RL,. Three epilepsy-associated GABRG2 missense mutations at the gamma+/beta- interface disrupt GABAA receptor assembly and trafficking by similar mechanisms but to different extents. Neurobiol Dis 2014; 68: 167-179.
50. Fisher JL, Macdonald RL,. Single channel properties of recombinant GABAA receptors containing gamma 2 or delta subtypes expressed with alpha 1 and beta 3 subtypes in mouse L929 cells. J Physiol 1997; 505 (pt 2): 283-297.
51. Angelotti TP, Macdonald RL,. Assembly of GABAA receptor subunits: alpha 1 beta 1 and alpha 1 beta 1 gamma 2S subunits produce unique ion channels with dissimilar single-channel properties. J Neurosci 1993; 13: 1429-1440.
52. Essrich C, Lorez M, Benson JA, et al., Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci 1998; 1: 563-571.
53. Li RW, Yu W, Christie S, et al., Disruption of postsynaptic GABA receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J Neurochem 2005; 95: 756-770.
54. Rathenberg J, Kittler JT, Moss SJ,. Palmitoylation regulates the clustering and cell surface stability of GABAA receptors. Mol Cell Neurosci 2004; 26: 251-257.
55. Todd E, Gurba KN, Botzolakis EJ, et al., GABAA receptor biogenesis is impaired by the gamma2 subunit febrile seizure-associated mutation, GABRG2(R177G). Neurobiol Dis 2014; 69: 215-224.
56. Mody I, Pearce RA,. Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci 2004; 27: 569-575.
57. Reid CA, Kim T, Phillips AM, et al., Multiple molecular mechanisms for a single GABAA mutation in epilepsy. Neurology 2013; 80: 1003-1008.
58. Luscher B, Shen Q, Sahir N,. The GABAergic deficit hypothesis of major depressive disorder. Mol Psychiatry 2011; 16: 383-406.
59. Shen Q, Fuchs T, Sahir N, Luscher B,. GABAergic control of critical developmental periods for anxiety- and depression-related behavior in mice. PloS One 2012; 7: e47441.
60. Laurie DJ, Wisden W, Seeburg PH,. The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 1992; 12: 4151-4172.
61. Noebels JL,. The biology of epilepsy genes. Annu Rev Neurosci 2003; 26: 599-625.
62. Goldberg EM, Coulter DA,. Mechanisms of epileptogenesis: a convergence on neural circuit dysfunction. Nat Rev Neurosci 2013; 14: 337-349.