Multicenter Study

. 2024 Apr;65(4):1029-1045.

doi: 10.1111/epi.17876. Epub 2024 Feb 29.

Developmental epileptic encephalopathy in DLG4-related synaptopathy

Benedetta Kassabian^#^{1

2}, Amanda M Levy^#³, Elena Gardella^{1

4}, Angel Aledo-Serrano⁵, Amitha L Ananth⁶, Alejandro J Brea-Fernández^{7

8}, Roseline Caumes⁹, Nicolas Chatron^{10

11}, Alice Dainelli¹², Matthias De Wachter¹³, Anne-Sophie Denommé-Pichon^{14

15}, Thomas J Dye^{16

17}, Elisa Fazzi^{18

19}, Roxanne Felt²⁰, Alberto Fernández-Jaén^{21

22}, Montse Fernández-Prieto^{7

8}, Emily Gantz⁶, Piotr Gasperowicz²³, Antonio Gil-Nagel²⁴, David Gómez-Andrés²⁵, Hansel M Greiner^{16

17}, Renzo Guerrini¹², Maria K Haanpää²⁶, Minttu Helin²⁷, Juliane Hoyer²⁸, Anna C E Hurst²⁹, Staci Kallish³⁰, Shefali N Karkare³¹, Amjad Khan^{32

33}, Lotte Kleinendorst^{34

35}, Johannes Koch³⁶, Sanjeev V Kothare³¹, Suzanna M Koudijs^{37

38}, Lieven Lagae³⁹, Phillis Lakeman³⁴, Kathleen A Leppig⁴⁰, Gaetan Lesca^{10

11}, Diego Lopergolo^{41

42}, Laina Lusk⁴³, Alex Mackenzie^{44

45}, Davide Mei¹², Rikke S Møller^{1

4}, Elaine M Pereira⁴⁶, Konrad Platzer⁴⁷, Chloe Quelin⁴⁸, Anya Revah-Politi⁴⁹, Sylvain Rheims⁵⁰, Agustí Rodríguez-Palmero^{51

52}, Andrea Rossi¹⁹, Filippo Santorelli⁴², Syndi Seinfeld⁵³, Erick Sell⁵⁴, Donna Stephenson⁵⁵, Krzysztof Szczaluba^{23

56}, Eugen Trinka^{57

58}, Muhammad Umair^{59

60}, Hilde Van Esch⁶¹, Mieke M van Haelst^{34

35}, Danielle C M Veenma^{38

62}, Sacha Weber^{63

64}, Sarah Weckhuysen^{65

66}, Pia Zacher⁶⁷, Zeynep Tümer^#^{3

68}, Guido Rubboli^#^{1

68}

Affiliations

¹ Department of Epilepsy Genetics and Precision Medicine, Danish Epilepsy Center Filadelfia, member of the European Reference Network EpiCARE, Dianalund, Denmark.
² Neurology Unit, Department of Neurosciences, University of Padua, Padua, Italy.
³ Department of Clinical Genetics, Kennedy Center, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
⁴ Department of Regional Health Research, University of Southern Denmark, Odense, Denmark.
⁵ Epilepsy and Neurogenetics Unit, Vithas la Milagrosa University Hospital, Vithas Hospital Group, Madrid, Spain.
⁶ Division of Pediatric Neurology, University of Alabama at Birmingham, Birmingham, Alabama, USA.
⁷ Grupo de Genómica y Bioinformática, Centro Singular de Investigación en Medicina Molecular y Enfermedades Crónicas (CiMUS), Centro de Investigación Biomédica en Red de Enfermedades Raras del Instituto de Salud Carlos III (CIBERER-ISCIII), Universidade de Santiago de Compostela, Santiago de Compostela, Spain.
⁸ Grupo de Genética, Fundación Pública Galega de Medicina Xenómica, Instituto de Investigación Biomédica de Santiago (IDIS), Santiago de Compostela, Spain.
⁹ CHU de Lille, Clinique de Génétique, Lille, France.
¹⁰ Service de Genetique, Hospices Civils de Lyon, Bron, France.
¹¹ Institute NeuroMyoGène, Laboratoire Physiopathologie et Génétique du Neurone et du Muscle, Centre National de la recherche scientifique (CNRS) Unité mixte de recherche (UMR) 5261- L'Institut national de la santé et de la recherche médicale (INSERM) U1315, Université de Lyon-Université Claude Bernard Lyon 1, Lyon, France.
¹² Neuroscience Department, Meyer Children's Hospital IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico), member of the European Reference Network EpiCARE, Florence, Italy.
¹³ Department of Pediatric Neurology, Antwerp University Hospital, University of Antwerp, Edegem, Belgium.
¹⁴ Functional Unit for Diagnostic Innovation in Rare Diseases, Fédération Hospitalo-Universitaire Médecine TRANSLationnelle et Anomalies du Développement (FHU-TRANSLAD), Dijon Bourgogne University Hospital, Dijon, France.
¹⁵ L'Institut national de la santé et de la recherche médicale (INSERM) Unité mixte de recherche (UMR) 1231, Génétique des Anomalies du Développement (GAD), Fédération Hospitalo-Universitaire Médecine TRANSLationnelle et Anomalies du Développement (FHU-TRANSLAD), University of Burgundy, Dijon, France.
¹⁶ Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA.
¹⁷ Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA.
¹⁸ Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy.
¹⁹ Unit of Child Neurology and Psychiatry, Azienda Socio Sanitaria Territoriale (ASST) Spedali Civili of Brescia, Brescia, Italy.
²⁰ Department of Neurology, Kaiser Permanente Bellevue Medical Center, Bellevue, Washington, USA.
²¹ Department of Pediatric Neurology, Neurogenetics Section, Hospital Universitario Quirónsalud, Madrid, Spain.
²² Facultad de Medicina, Universidad Europea, Madrid, Spain.
²³ Department of Medical Genetics, Medical University of Warsaw, Warsaw, Poland.
²⁴ Neurology Department, Epilepsy Program, Ruber Internacional Hospital, Madrid, Spain.
²⁵ Child Neurology Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Research Institute, Barcelona, Spain.
²⁶ Department of Genomics, Turku University Hospital, Turku, Finland.
²⁷ Department of Pediatric Neurology, Turku University Hospital, Turku, Finland.
²⁸ Friedrich-Alexander-Universität Erlangen Nürnberg, Institute of Human Genetics, Erlangen, Germany.
²⁹ Department of Genetics, University of Alabama at Birmingham, Birmingham, Alabama, USA.
³⁰ Division of Translational Medicine and Human Genetics, Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
³¹ Division of Pediatric Neurology, Department of Pediatrics, Cohen Children's Medical Center, New Hyde Park, New York, USA.
³² Department of Zoology, Faculty of Biological Sciences, University of Lakki Marwat, Lakki Marwat, Pakistan.
³³ Institute for Medical Genetics and Applied Genomics, University of Tübingen, Tübingen, Germany.
³⁴ Department of Human Genetics, Amsterdam University Medical Center (UMC), University of Amsterdam, Amsterdam, the Netherlands.
³⁵ Emma Center for Personalized Medicine, Amsterdam University Medical Center (UMC), University of Amsterdam, Amsterdam, the Netherlands.
³⁶ University Children's Hospital, Paracelsus Medical University, Salzburg, Austria.
³⁷ Department of Neurology, Erasmus Medical Center (MC) Sophia Children's Hospital, Rotterdam, the Netherlands.
³⁸ Erfelijke Neuro-Cognitieve Ontwikkelingsstoornissen, Rotterdam, Erasmus Medical Center (ENCORE)-GRIN Expertise Center, Rotterdam, the Netherlands.
³⁹ Department of Development and Regeneration, Section Paediatric Neurology, member of the European Reference Network EpiCARE, University Hospitals Leuven, Leuven, Belgium.
⁴⁰ Genetic Services, Kaiser Permanente of Washington, Seattle, Washington, USA.
⁴¹ Department of Medicine, Surgery, and Neurosciences, University of Siena, Siena, Italy.
⁴² Molecular Medicine for Neurodegenerative and Neuromuscular Diseases Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Stella Maris Foundation, Pisa, Italy.
⁴³ Division of Neurology, Epilepsy Neurogenetics Initiative, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
⁴⁴ Research Institute, Children's Hospital of Eastern Ontario, Ottawa, Ontario, Canada.
⁴⁵ Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada.
⁴⁶ Division of Clinical Genetics, Department of Pediatrics, Columbia University Vagelos College of Physicians and Surgeons and New York-Presbyterian Morgan Stanley Children's Hospital, New York, New York, USA.
⁴⁷ Institute of Human Genetics, University of Leipzig Medical Center, Leipzig, Germany.
⁴⁸ Department of Medical Genetics, CHU de Rennes, Rennes, France.
⁴⁹ Institute for Genomic Medicine, Columbia University Irving Medical Center, New York, New York, USA.
⁵⁰ Department of Functional Neurology and Epileptology, member of the European Reference Network EpiCARE, Hospices Civils de Lyon and Lyon 1 University, Lyon, France.
⁵¹ Paediatric Neurology Unit, Department of Pediatrics, Hospital Universitari Germans Trias i Pujol, Universitat Autònoma de Barcelona, Barcelona, Spain.
⁵² Grupo de Investigación Biomédica en Red de Enfermedades Raras, Instituto de Salud Carlos III, Madrid, Spain.
⁵³ Department of Pediatric Neurology, Neuroscience Center, Joe DiMaggio Children's Hospital, Hollywood, Florida, USA.
⁵⁴ Division of Neurology, Children's Hospital of Eastern Ontario, Ottawa, Ontario, Canada.
⁵⁵ Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
⁵⁶ Center of Excellence for Rare and Undiagnosed Diseases, Medical University of Warsaw, Warsaw, Poland.
⁵⁷ Department of Neurology, Neurointensive Care and Neurorehabilitation, Christian Doppler University Hospital, member of the European Reference Network EpiCARE, Paracelsus Medical University, Center for Cognitive Neuroscience, Salzburg, Austria.
⁵⁸ Neuroscience Institute, Christian Doppler University Hospital, member of the European Reference Network EpiCARE, Paracelsus Medical University, Center for Cognitive Neuroscience, Salzburg, Austria.
⁵⁹ Medical Genomics Research Department, King Abdullah International Medical Research Center, King Saud Bin Abdulaziz University for Health Sciences, Ministry of National Guard Health Affairs, Riyadh, Saudi Arabia.
⁶⁰ Department of Life Sciences, School of Science, University of Management and Technology, Lahore, Pakistan.
⁶¹ Center for Human Genetics, University Hospitals Leuven, Leuven, Belgium.
⁶² Department of Pediatrics, Erasmus Medical Center (MC)-Sophia Hospital, Rotterdam, the Netherlands.
⁶³ Service de Génétique, Centre Hospitalier Universitaire (CHU) de Caen-Normandie, Caen, France.
⁶⁴ Service de Neurologie, Centre Hospitalier Universitaire (CHU) de Caen-Normandie, Caen, France.
⁶⁵ Applied and Translational Neurogenomics Group, Vlaams Instituut voor Biotechnologie (VIB) Center for Molecular Neurology, Antwerp, Belgium.
⁶⁶ Department of Neurology, Antwerp University Hospital, Antwerp, Belgium.
⁶⁷ Center for Adults with Disability (MZEB), Epilepsy Center Kleinwachau, Radeberg, Germany.
⁶⁸ Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

^# Contributed equally.

PMID: 38135915
DOI: 10.1111/epi.17876

Multicenter Study

Developmental epileptic encephalopathy in DLG4-related synaptopathy

Benedetta Kassabian et al. Epilepsia. 2024 Apr.

. 2024 Apr;65(4):1029-1045.

doi: 10.1111/epi.17876. Epub 2024 Feb 29.

Authors

Affiliations

¹ Department of Epilepsy Genetics and Precision Medicine, Danish Epilepsy Center Filadelfia, member of the European Reference Network EpiCARE, Dianalund, Denmark.
² Neurology Unit, Department of Neurosciences, University of Padua, Padua, Italy.
³ Department of Clinical Genetics, Kennedy Center, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
⁴ Department of Regional Health Research, University of Southern Denmark, Odense, Denmark.
⁵ Epilepsy and Neurogenetics Unit, Vithas la Milagrosa University Hospital, Vithas Hospital Group, Madrid, Spain.
⁶ Division of Pediatric Neurology, University of Alabama at Birmingham, Birmingham, Alabama, USA.
⁷ Grupo de Genómica y Bioinformática, Centro Singular de Investigación en Medicina Molecular y Enfermedades Crónicas (CiMUS), Centro de Investigación Biomédica en Red de Enfermedades Raras del Instituto de Salud Carlos III (CIBERER-ISCIII), Universidade de Santiago de Compostela, Santiago de Compostela, Spain.
⁸ Grupo de Genética, Fundación Pública Galega de Medicina Xenómica, Instituto de Investigación Biomédica de Santiago (IDIS), Santiago de Compostela, Spain.
⁹ CHU de Lille, Clinique de Génétique, Lille, France.
¹⁰ Service de Genetique, Hospices Civils de Lyon, Bron, France.
¹¹ Institute NeuroMyoGène, Laboratoire Physiopathologie et Génétique du Neurone et du Muscle, Centre National de la recherche scientifique (CNRS) Unité mixte de recherche (UMR) 5261- L'Institut national de la santé et de la recherche médicale (INSERM) U1315, Université de Lyon-Université Claude Bernard Lyon 1, Lyon, France.
¹² Neuroscience Department, Meyer Children's Hospital IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico), member of the European Reference Network EpiCARE, Florence, Italy.
¹³ Department of Pediatric Neurology, Antwerp University Hospital, University of Antwerp, Edegem, Belgium.
¹⁴ Functional Unit for Diagnostic Innovation in Rare Diseases, Fédération Hospitalo-Universitaire Médecine TRANSLationnelle et Anomalies du Développement (FHU-TRANSLAD), Dijon Bourgogne University Hospital, Dijon, France.
¹⁵ L'Institut national de la santé et de la recherche médicale (INSERM) Unité mixte de recherche (UMR) 1231, Génétique des Anomalies du Développement (GAD), Fédération Hospitalo-Universitaire Médecine TRANSLationnelle et Anomalies du Développement (FHU-TRANSLAD), University of Burgundy, Dijon, France.
¹⁶ Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA.
¹⁷ Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA.
¹⁸ Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy.
¹⁹ Unit of Child Neurology and Psychiatry, Azienda Socio Sanitaria Territoriale (ASST) Spedali Civili of Brescia, Brescia, Italy.
²⁰ Department of Neurology, Kaiser Permanente Bellevue Medical Center, Bellevue, Washington, USA.
²¹ Department of Pediatric Neurology, Neurogenetics Section, Hospital Universitario Quirónsalud, Madrid, Spain.
²² Facultad de Medicina, Universidad Europea, Madrid, Spain.
²³ Department of Medical Genetics, Medical University of Warsaw, Warsaw, Poland.
²⁴ Neurology Department, Epilepsy Program, Ruber Internacional Hospital, Madrid, Spain.
²⁵ Child Neurology Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Research Institute, Barcelona, Spain.
²⁶ Department of Genomics, Turku University Hospital, Turku, Finland.
²⁷ Department of Pediatric Neurology, Turku University Hospital, Turku, Finland.
²⁸ Friedrich-Alexander-Universität Erlangen Nürnberg, Institute of Human Genetics, Erlangen, Germany.
²⁹ Department of Genetics, University of Alabama at Birmingham, Birmingham, Alabama, USA.
³⁰ Division of Translational Medicine and Human Genetics, Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
³¹ Division of Pediatric Neurology, Department of Pediatrics, Cohen Children's Medical Center, New Hyde Park, New York, USA.
³² Department of Zoology, Faculty of Biological Sciences, University of Lakki Marwat, Lakki Marwat, Pakistan.
³³ Institute for Medical Genetics and Applied Genomics, University of Tübingen, Tübingen, Germany.
³⁴ Department of Human Genetics, Amsterdam University Medical Center (UMC), University of Amsterdam, Amsterdam, the Netherlands.
³⁵ Emma Center for Personalized Medicine, Amsterdam University Medical Center (UMC), University of Amsterdam, Amsterdam, the Netherlands.
³⁶ University Children's Hospital, Paracelsus Medical University, Salzburg, Austria.
³⁷ Department of Neurology, Erasmus Medical Center (MC) Sophia Children's Hospital, Rotterdam, the Netherlands.
³⁸ Erfelijke Neuro-Cognitieve Ontwikkelingsstoornissen, Rotterdam, Erasmus Medical Center (ENCORE)-GRIN Expertise Center, Rotterdam, the Netherlands.
³⁹ Department of Development and Regeneration, Section Paediatric Neurology, member of the European Reference Network EpiCARE, University Hospitals Leuven, Leuven, Belgium.
⁴⁰ Genetic Services, Kaiser Permanente of Washington, Seattle, Washington, USA.
⁴¹ Department of Medicine, Surgery, and Neurosciences, University of Siena, Siena, Italy.
⁴² Molecular Medicine for Neurodegenerative and Neuromuscular Diseases Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Stella Maris Foundation, Pisa, Italy.
⁴³ Division of Neurology, Epilepsy Neurogenetics Initiative, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
⁴⁴ Research Institute, Children's Hospital of Eastern Ontario, Ottawa, Ontario, Canada.
⁴⁵ Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada.
⁴⁶ Division of Clinical Genetics, Department of Pediatrics, Columbia University Vagelos College of Physicians and Surgeons and New York-Presbyterian Morgan Stanley Children's Hospital, New York, New York, USA.
⁴⁷ Institute of Human Genetics, University of Leipzig Medical Center, Leipzig, Germany.
⁴⁸ Department of Medical Genetics, CHU de Rennes, Rennes, France.
⁴⁹ Institute for Genomic Medicine, Columbia University Irving Medical Center, New York, New York, USA.
⁵⁰ Department of Functional Neurology and Epileptology, member of the European Reference Network EpiCARE, Hospices Civils de Lyon and Lyon 1 University, Lyon, France.
⁵¹ Paediatric Neurology Unit, Department of Pediatrics, Hospital Universitari Germans Trias i Pujol, Universitat Autònoma de Barcelona, Barcelona, Spain.
⁵² Grupo de Investigación Biomédica en Red de Enfermedades Raras, Instituto de Salud Carlos III, Madrid, Spain.
⁵³ Department of Pediatric Neurology, Neuroscience Center, Joe DiMaggio Children's Hospital, Hollywood, Florida, USA.
⁵⁴ Division of Neurology, Children's Hospital of Eastern Ontario, Ottawa, Ontario, Canada.
⁵⁵ Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
⁵⁶ Center of Excellence for Rare and Undiagnosed Diseases, Medical University of Warsaw, Warsaw, Poland.
⁵⁷ Department of Neurology, Neurointensive Care and Neurorehabilitation, Christian Doppler University Hospital, member of the European Reference Network EpiCARE, Paracelsus Medical University, Center for Cognitive Neuroscience, Salzburg, Austria.
⁵⁸ Neuroscience Institute, Christian Doppler University Hospital, member of the European Reference Network EpiCARE, Paracelsus Medical University, Center for Cognitive Neuroscience, Salzburg, Austria.
⁵⁹ Medical Genomics Research Department, King Abdullah International Medical Research Center, King Saud Bin Abdulaziz University for Health Sciences, Ministry of National Guard Health Affairs, Riyadh, Saudi Arabia.
⁶⁰ Department of Life Sciences, School of Science, University of Management and Technology, Lahore, Pakistan.
⁶¹ Center for Human Genetics, University Hospitals Leuven, Leuven, Belgium.
⁶² Department of Pediatrics, Erasmus Medical Center (MC)-Sophia Hospital, Rotterdam, the Netherlands.
⁶³ Service de Génétique, Centre Hospitalier Universitaire (CHU) de Caen-Normandie, Caen, France.
⁶⁴ Service de Neurologie, Centre Hospitalier Universitaire (CHU) de Caen-Normandie, Caen, France.
⁶⁵ Applied and Translational Neurogenomics Group, Vlaams Instituut voor Biotechnologie (VIB) Center for Molecular Neurology, Antwerp, Belgium.
⁶⁶ Department of Neurology, Antwerp University Hospital, Antwerp, Belgium.
⁶⁷ Center for Adults with Disability (MZEB), Epilepsy Center Kleinwachau, Radeberg, Germany.
⁶⁸ Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

^# Contributed equally.

PMID: 38135915
DOI: 10.1111/epi.17876

Abstract

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.

Keywords: DEE‐SWAS; ESES; PSD‐95; SHINE syndrome; epilepsy.

PubMed Disclaimer

References

REFERENCES

1. Sheng M. The postsynaptic NMDA‐receptor‐PSD‐95 signaling complex in excitatory synapses of the brain. J Cell Sci. 2001;114. www.biologists.com/jcs:1251–1252.
1. Sheng M, Kim E. The postsynaptic organization of synapses. Cold Spring Harb Perspect Biol. 2011;3(12):a005678.
1. Levy AM, Gomez‐Puertas P, Tümer Z. Neurodevelopmental disorders associated with PSD‐95 and its interaction partners. Int J Mol Sci. 2022;23(8):4390.
1. Curran OE, Qiu Z, Smith C, Grant SGN. A single‐synapse resolution survey of PSD95‐positive synapses in twenty human brain regions. Eur J Neurosci. 2021;54(8):6864–6881.
1. Zhu J, Shang Y, Zhang M. Mechanistic basis of MAGUK‐organized complexes in synaptic development and signalling. Nat Rev Neurosci. 2016;17:209–223.

Publication types

Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions
Actions

Grants and funding

LinkOut - more resources

Full Text Sources
- Ovid Technologies, Inc.
- Wiley
Medical
- MedlinePlus Consumer Health Information
- MedlinePlus Health Information

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Developmental epileptic encephalopathy in DLG4-related synaptopathy

Affiliations

Developmental epileptic encephalopathy in DLG4-related synaptopathy

Authors

Affiliations

Abstract

References

REFERENCES

Publication types

MeSH terms

Substances

Grants and funding

LinkOut - more resources

Full Text Sources

Medical