Semaphorin heterodimerization in cis regulates membrane targeting and neocortical wiring.

Semaphorins / metabolism Animals Neocortex / metabolism Cell Membrane / metabolism Humans Mice Matrix Attachment Region Binding Proteins / metabolism Antigens, CD / metabolism Protein Multimerization Transcription Factors / metabolism Neurons / metabolism Mutation Cell Movement Axons / metabolism Epilepsy / metabolism Corpus Callosum / metabolism HEK293 Cells Glycosylation Male Female Mice, Inbred C57BL

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
16 Aug 2024
Historique:
received: 06 02 2023
accepted: 22 07 2024
medline: 17 8 2024
pubmed: 17 8 2024
entrez: 16 8 2024
Statut: epublish

Résumé

Disruption of neocortical circuitry and architecture in humans causes numerous neurodevelopmental disorders. Neocortical cytoarchitecture is orchestrated by various transcription factors such as Satb2 that control target genes during strict time windows. In humans, mutations of SATB2 cause SATB2 Associated Syndrome (SAS), a multisymptomatic syndrome involving epilepsy, intellectual disability, speech delay, and craniofacial defects. Here we show that Satb2 controls neuronal migration and callosal axonal outgrowth during murine neocortical development by inducing the expression of the GPI-anchored protein, Semaphorin 7A (Sema7A). We find that Sema7A exerts this biological activity by heterodimerizing in cis with the transmembrane semaphorin, Sema4D. We could also observe that heterodimerization with Sema7A promotes targeting of Sema4D to the plasma membrane in vitro. Finally, we report an epilepsy-associated de novo mutation in Sema4D (Q497P) that inhibits normal glycosylation and plasma membrane localization of Sema4D-associated complexes. These results suggest that neuronal use of semaphorins during neocortical development is heteromeric, and a greater signaling complexity exists than was previously thought.

Identifiants

DOI: 10.1038/s41467-024-51009-1 PMID: 39152101
pubmed: 39152101
doi: 10.1038/s41467-024-51009-1
pii: 10.1038/s41467-024-51009-1
doi:

Substances chimiques

Semaphorins 0
Matrix Attachment Region Binding Proteins 0
Antigens, CD 0
Sema7a protein, mouse 0
Transcription Factors 0
SATB2 protein, mouse 0
Sema4d protein, mouse 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

7059

Subventions

Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : 451346372

Informations de copyright

© 2024. The Author(s).

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Auteurs

Paraskevi Bessa (P)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.
ORCID: 0000-0003-1469-5686

Andrew G Newman (AG)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.
ORCID: 0000-0002-0222-9162

Kuo Yan (K)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.

Theres Schaub (T)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.

Rike Dannenberg (R)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.

Denis Lajkó (D)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.

Julia Eilenberger (J)

Department of Pediatrics, Dr. von Hauner Children's Hospital, University Hospital, Ludwig-Maximilians-Universität München, Munich, Germany.

Theresa Brunet (T)

Department of Pediatric Neurology and Developmental Medicine and Ludwig Maximilians University Center for Children with Medical Complexity, Dr. von Hauner Children's Hospital, Ludwig Maximilians University Hospital, Ludwig Maximilians University, Munich, Germany.
Institute of Human Genetics, Klinikum rechts der Isar, School of Medicine, Technical University of Munich, Munich, Germany.
ORCID: 0000-0002-5183-780X

Kathrin Textoris-Taube (K)

Institute of Biochemistry, Charité -Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Philippstrasse 12, 10115, Berlin, Germany.
Core Facility - High-Throughput Mass Spectrometry, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Core Facility - High-Throughput Mass Spectrometry, Am Charitéplatz 1, Berlin, Germany.

Emanuel Kemmler (E)

Institute of Physiology, Charité -Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Philippstrasse 12, 10115, Berlin, Germany.
ORCID: 0009-0008-2046-823X

Penghui Deng (P)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.

Priyanka Banerjee (P)

Institute of Physiology, Charité -Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Philippstrasse 12, 10115, Berlin, Germany.

Ethiraj Ravindran (E)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.

Robert Preissner (R)

Institute of Physiology, Charité -Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Philippstrasse 12, 10115, Berlin, Germany.
ORCID: 0000-0002-2407-1087

Marta Rosário (M)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany.
ORCID: 0000-0003-1101-7177

Victor Tarabykin (V)

Institute of Cell Biology and Neurobiology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117, Berlin, Germany. victor.tarabykin@charite.de.
Institute of Neuroscience, Lobachevsky University of Nizhny Novgorod, Nizhny Novgorod, 603950, Russian Federation. victor.tarabykin@charite.de.
ORCID: 0000-0001-8931-7263

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Classifications MeSH

questionsmedicales.fr › Facteurs biologiques › Protéines et peptides de signalisation intercellulaire › Sémaphorines › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Eucaryotes › Animaux › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Néocortex › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Cellules › Structures cellulaires › Membrane cellulaire › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines de liaison à l'ADN › Protéines de liaison aux séquences d'ADN MAR › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Facteurs biologiques › Marqueurs biologiques › Antigènes de différenciation › Antigènes CD › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Phénomènes chimiques › Phénomènes biochimiques › Multimérisation de protéines › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Cellules › Neurones › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Phénomènes génétiques › Variation génétique › Mutation › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Phénomènes physiologiques › Mouvement cellulaire › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Cellules › Neurones › Neurofibres › Axones › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Maladies du système nerveux › Maladies du système nerveux central › Encéphalopathies › Épilepsie › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Commissures du télencéphale › Corps calleux › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules HEK293 › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Métabolisme › Métabolisme glucidique › Glycosylation › Semaphorin heterodimerization in cis regulates...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Lignées consanguines de souris › Souris de lignée C57BL › Semaphorin heterodimerization in cis regulates...