Developmental epileptic encephalopathy in DLG4-related synaptopathy


Por: Kassabian, B, Levy, AM, Gardella, E, Aledo-Serrano, A, Ananth, AL, Brea-Fernandez, AJ, Caumes, R, Chatron, N, Dainelli, A, De Wachter, M, Denomme-Pichon, AS, Dye, TJ, Fazzi, E, Felt, R, Fernandez-Jaen, A, Fernandez-Prieto, M, Gantz, E, Gasperowicz, P, Gil-Nagel, A, Gómez-Andrés, D, Greiner, HM, Guerrini, R, Haanpaeae, MK, Helin, M, Hoyer, J, Hurst, ACE, Kallish, S, Karkare, SN, Khan, A, Kleinendorst, L, Koch, J, Kothare, SV, Koudijs, SM, Lagae, L, Lakeman, P, Leppig, KA, Lesca, G, Lopergolo, D, Lusk, L, Mackenzie, A, Mei, DVD, Moller, RS, Pereira, EM, Platzer, K, Quelin, C, Revah-Politi, A, Rheims, S, Rodriguez-Palmero, A, Rossi, A, Santorelli, F, Seinfeld, S, Sell, E, Stephenson, D, Szczaluba, K, Trinka, E, Umair, M, Van Esch, H, van Haelst, MM, Veenma, DCM, Weber, S, Weckhuysen, S, Zacher, P, Tümer, Z and Rubboli, G

Publicada: 1 abr 2024 Ahead of Print: 1 feb 2024
Resumen:
Objective: The postsynaptic density protein of excitatory neurons PSD-95 is encoded by discs large MAGUK scaffold protein 4 (DLG4), de novo pathogenic variants of which lead to DLG4-related synaptopathy. The major clinical features are developmental delay, intellectual disability (ID), hypotonia, sleep disturbances, movement disorders, and epilepsy. Even though epilepsy is present in 50% of the individuals, it has not been investigated in detail. We describe here the phenotypic spectrum of epilepsy and associated comorbidities in patients with DLG4-related synaptopathy. Methods: We included 35 individuals with a DLG4 variant and epilepsy as part of a multicenter study. The DLG4 variants were detected by the referring laboratories. The degree of ID, hypotonia, developmental delay, and motor disturbances were evaluated by the referring clinician. Data on awake and sleep electroencephalography (EEG) and/or video-polygraphy and brain magnetic resonance imaging were collected. Antiseizure medication response was retrospectively assessed by the referring clinician. Results: A large variety of seizure types was reported, although focal seizures were the most common. Encephalopathy related to status epilepticus during slow-wave sleep (ESES)/developmental epileptic encephalopathy with spike-wave activation during sleep (DEE-SWAS) was diagnosed in >25% of the individuals. All but one individual presented with neurodevelopmental delay. Regression in verbal and/or motor domains was observed in all individuals who suffered from ESES/DEE-SWAS, as well as some who did not. We could not identify a clear genotype-phenotype relationship even between individuals with the same DLG4 variants. Significance: Our study shows that a subgroup of individuals with DLG4-related synaptopathy have DEE, and approximately one fourth of them have ESES/DEE-SWAS. Our study confirms DEE as part of the DLG4-related phenotypic spectrum. Occurrence of ESES/DEE-SWAS in DLG4-related synaptopathy requires proper investigation with sleep EEG.

Filiaciones:
Kassabian, B:
 European Reference Network EpiCARE, Danish Epilepsy Ctr Filadelfia, Dept Epilepsy Genet & Precis Med, Dianalund, Denmark

 Univ Padua, Dept Neurosci, Neurol Unit, Padua, Italy

Levy, AM:
 Copenhagen Univ Hosp, Kennedy Ctr, Dept Clin Genet, Rigshosp, Copenhagen, Denmark

Gardella, E:
 European Reference Network EpiCARE, Danish Epilepsy Ctr Filadelfia, Dept Epilepsy Genet & Precis Med, Dianalund, Denmark

 Univ Southern Denmark, Dept Reg Hlth Res, Odense, Denmark

Aledo-Serrano, A:
 Vithas La Milagrosa Univ Hosp, Vithas Hosp Grp, Epilepsy & Neurogenet Unit, Madrid, Spain

Ananth, AL:
 Univ Alabama Birmingham, Div Pediat Neurol, Birmingham, AL USA

Brea-Fernandez, AJ:
 Univ Santiago de Compostela, Ctr Singular Invest Med Mol & Enfermedades Cron C, Ctr Invest Biomed Red Enfermedades Raras Inst Sal, Grp Genom & Bioinformat, Santiago De Compostela, Spain

 Fdn Publ Galega Med Xen, Inst Invest Sanitaria IDIS, Santiago De Compostela, Spain

Caumes, R:
 CHU Lille, Clin Genet, Lille, France

Chatron, N:
 Hosp Civils Lyon, Serv Genet, Bron, France

 Univ Lyon, Univ Claude Bernard Lyon 1, Inst NeuroMyoGene, INSERM U1315, Lyon, France

Dainelli, A:
 Meyer Childrens Hosp IRCCS, Ist Ricovero & Cura Carattere Sci, Neurosci Dept, European Reference Network EpiCARE, Florence, Italy

De Wachter, M:
 Univ Antwerp, Antwerp Univ Hosp, Dept Pediat Neurol, Edegem, Belgium

Denomme-Pichon, AS:
 Dijon Bourgogne Univ Hosp, Funct Unit Diagnost Innovat Rare Dis, Federat Hosp Univ Medecine TRANSLat & Anomalies D, Dijon, France

 Univ Burgundy, INSERM, UMR 1231, Genet Anomalies Dev GAD, Dijon, France

Dye, TJ:
 Cincinnati Childrens Hosp Med Ctr, Div Neurol, Cincinnati, OH USA

 Univ Cincinnati, Coll Med, Dept Pediat, Cincinnati, OH USA

Fazzi, E:
 Univ Brescia, Dept Clin & Expt Sci, Brescia, Italy

 Unit Child Neurol & Psychiat, Azienda Socio Sanit Terr ASST Spedali Civili Bres, Brescia, Italy

Felt, R:
 Kaiser Permanente Bellevue Med Ctr, Dept Neurol, Bellevue, WA USA

Fernandez-Jaen, A:
 Hosp Univ Quironsalud, Dept Pediat Neurol, Neurogenet Sect, Madrid, Spain

 Univ Europea, Fac Med, Madrid, Spain

Fernandez-Prieto, M:
 Univ Santiago de Compostela, Ctr Singular Invest Med Mol & Enfermedades Cron C, Ctr Invest Biomed Red Enfermedades Raras Inst Sal, Grp Genom & Bioinformat, Santiago De Compostela, Spain

 Fdn Publ Galega Med Xen, Inst Invest Sanitaria IDIS, Santiago De Compostela, Spain

Gantz, E:
 Univ Alabama Birmingham, Div Pediat Neurol, Birmingham, AL USA

Gasperowicz, P:
 Med Univ Warsaw, Dept Med Genet, Warsaw, Poland

Gil-Nagel, A:
 Ruber Int Hosp, Neurol Dept, Epilepsy Program, Madrid, Spain

Gómez-Andrés, D:
 Hosp Universitari Vall dHebron, Vall dHebron Res Inst, Child Neurol Unit, Barcelona, Spain

Greiner, HM:
 Cincinnati Childrens Hosp Med Ctr, Div Neurol, Cincinnati, OH USA

 Univ Cincinnati, Coll Med, Dept Pediat, Cincinnati, OH USA

Guerrini, R:
 Meyer Childrens Hosp IRCCS, Ist Ricovero & Cura Carattere Sci, Neurosci Dept, European Reference Network EpiCARE, Florence, Italy

Haanpaeae, MK:
 Turku Univ Hosp, Dept Genom, Turku, Finland

Helin, M:
 Turku Univ Hosp, Dept Pediat Neurol, Turku, Finland

Hoyer, J:
 Friedrich Alexander Univ Erlangen Nurnberg, Inst Human Genet, Erlangen, Germany

Hurst, ACE:
 Univ Alabama Birmingham, Dept Genet, Birmingham, AL USA

Kallish, S:
 Univ Penn, Dept Med, Div Translat Med & Human Genet, Philadelphia, PA USA

Karkare, SN:
 Cohen Childrens Med Ctr, Dept Pediat, Div Pediat Neurol, New Hyde Pk, NY USA

Khan, A:
 Univ Lakki Marwat, Fac Biol Sci, Dept Zool, Lakki Marwat, Pakistan

 Univ Tubingen, Inst Med Genet & Appl Genom, Tubingen, Germany

Kleinendorst, L:
 Amsterdam Univ Med Ctr UMC, Univ Amsterdam, Dept Human Genet, Amsterdam, Netherlands

 Univ Amsterdam, Amsterdam Univ Med Ctr UMC, Emma Ctr Personalized Med, Amsterdam, Netherlands

Koch, J:
 Paracelsus Med Univ, Univ Childrens Hosp, Salzburg, Austria

Kothare, SV:
 Cohen Childrens Med Ctr, Dept Pediat, Div Pediat Neurol, New Hyde Pk, NY USA

Koudijs, SM:
 Erasmus MC Sophia Childrens Hosp, Univ Med Ctr Rotterdam, Dept Neurol, Rotterdam, Netherlands

 Erasmus Med Ctr ENCORE, GRIN Expertise Ctr, Erfelijke Neurocognitieve Ontwikkelingsstoornisse, Rotterdam, Netherlands

Lagae, L:
 Univ Hosp Leuven, Dept Dev & Regenerat, Sect Paediat Neurol, European Reference Network EpiCARE, Leuven, Belgium

Lakeman, P:
 Amsterdam Univ Med Ctr UMC, Univ Amsterdam, Dept Human Genet, Amsterdam, Netherlands

Leppig, KA:
 Kaiser Permanente Washington, Genet Serv, Seattle, WA USA

Lesca, G:
 Hosp Civils Lyon, Serv Genet, Bron, France

 Univ Lyon, Univ Claude Bernard Lyon 1, Inst NeuroMyoGene, INSERM U1315, Lyon, France

Lopergolo, D:
 Univ Siena, Dept Med Surg & Neurosci, Siena, Italy

 IRCCS Stella Maris Fdn, Mol Med Neurodegenerat & Neuromuscular Dis Unit, Pisa, Italy

Lusk, L:
 Childrens Hosp Philadelphia, Div Neurol, Epilepsy Neurogenet Initiat, Philadelphia, PA USA

Mackenzie, A:
 Childrens Hosp Eastern Ontario, Res Inst, Ottawa, ON, Canada

 Univ Ottawa, Fac Med, Ottawa, ON, Canada

Mei, DVD:
 Meyer Childrens Hosp IRCCS, Ist Ricovero & Cura Carattere Sci, Neurosci Dept, European Reference Network EpiCARE, Florence, Italy

Moller, RS:
 European Reference Network EpiCARE, Danish Epilepsy Ctr Filadelfia, Dept Epilepsy Genet & Precis Med, Dianalund, Denmark

 Univ Southern Denmark, Dept Reg Hlth Res, Odense, Denmark

Pereira, EM:
 Columbia Univ, Vagelos Coll Phys & Surg, New York Presbyterian Morgan Stanley Childrens Ho, Div Clin Genet,Dept Pediat, New York, NY USA

Platzer, K:
 Univ Leipzig, Med Ctr, Inst Human Genet, Leipzig, Germany

Quelin, C:
 CHU Rennes, Dept Med Genet, Rennes, France

Revah-Politi, A:
 Columbia Univ, Irving Med Ctr, Inst Genom Med, New York, NY USA

Rheims, S:
 Hosp Civils Lyon & Lyon 1 Univ, Dept Funct Neurol & Epileptol, European Reference Network EpiCARE, Lyon, France

:
 Univ Autonoma Barcelona, Hosp Univ Germans Trias & Pujol, Dept Pediat, Paediat Neurol Unit, Barcelona, Spain

 Inst Salud Carlos III, Grp Invest Biomed Red Enfermedades Raras, Madrid, Spain

Rossi, A:
 Unit Child Neurol & Psychiat, Azienda Socio Sanit Terr ASST Spedali Civili Bres, Brescia, Italy

Santorelli, F:
 IRCCS Stella Maris Fdn, Mol Med Neurodegenerat & Neuromuscular Dis Unit, Pisa, Italy

Seinfeld, S:
 Joe DiMaggio Childrens Hosp, Neurosci Ctr, Dept Pediat Neurol, Hollywood, FL USA

Sell, E:
 Childrens Hosp Eastern Ontario, Div Neurol, Ottawa, ON, Canada

Stephenson, D:
 Childrens Hosp Philadelphia, Div Neurol, Philadelphia, PA USA

Szczaluba, K:
 Med Univ Warsaw, Dept Med Genet, Warsaw, Poland

 Med Univ Warsaw, Ctr Excellence Rare & Undiagnosed Dis, Warsaw, Poland

Trinka, E:
 Paracelsus Med Univ, Ctr Cognit Neurosci, Salzburg, Austria

Umair, M:
 King Saud Bin Abdulaziz Univ Hlth Sci, King Abdullah Int Med Res Ctr, Med Genom Res Dept, Minist Natl Guard Hlth Affairs, Riyadh, Saudi Arabia

 Univ Management & Technol, Sch Sci, Dept Life Sci, Lahore, Pakistan

Van Esch, H:
 Univ Hosp Leuven, Ctr Human Genet, Leuven, Belgium

van Haelst, MM:
 Amsterdam Univ Med Ctr UMC, Univ Amsterdam, Dept Human Genet, Amsterdam, Netherlands

 Univ Amsterdam, Amsterdam Univ Med Ctr UMC, Emma Ctr Personalized Med, Amsterdam, Netherlands

Veenma, DCM:
 Erasmus Med Ctr ENCORE, GRIN Expertise Ctr, Erfelijke Neurocognitieve Ontwikkelingsstoornisse, Rotterdam, Netherlands

 Sophia Hosp, Erasmus Med Ctr MC, Dept Pediat, Rotterdam, Netherlands

Weber, S:
 Ctr Hosp Univ Caen Normandie, Dept Neurol, Caen, France

 Ctr Hospitalier Univ Caen Normandie, Dept Neurol, Caen, France

Weckhuysen, S:
 VIB Ctr Mol Neurol, Vlaams Inst Biotechnol, Appl & Translat Neurogen Grp, Antwerp, Belgium

 Antwerp Univ Hosp, Dept Neurol, Antwerp, Belgium

Zacher, P:
 Epilepsy Ctr Kleinwachau, Radeberg, Germany

Tümer, Z:
 Copenhagen Univ Hosp, Kennedy Ctr, Dept Clin Genet, Rigshosp, Copenhagen, Denmark

 Univ Copenhagen, Fac Hlth & Med Sci, Dept Clin Med, Copenhagen, Denmark

Rubboli, G:
 European Reference Network EpiCARE, Danish Epilepsy Ctr Filadelfia, Dept Epilepsy Genet & Precis Med, Dianalund, Denmark

 Univ Copenhagen, Fac Hlth & Med Sci, Dept Clin Med, Copenhagen, Denmark
ISSN: 00139580





Epilepsia
Editorial
Blackwell Publishing Inc., 111 RIVER ST, HOBOKEN 07030-5774, NJ USA, Reino Unido
Tipo de documento: Article
Volumen: 65 Número: 4
Páginas: 1029-1045
WOS Id: 001176458900001
ID de PubMed: 38135915
imagen Green Published

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