Extracellular LGALS3BP regulates neural progenitor position and relates to human cortical complexity

Christina Kyrousi, Adam C. O’Neill, Agnieska Brazovskaja, Zhisong He, Pavel Kielkowski, Laure Coquand, Rossella Giaimo, Pierpaolo D’ Andrea, Alexander Belka, Andrea Forero Echeverry, Davide Mei, Matteo Lenge, Cristiana Cruceanu, Isabel Y. Buchsbaum, Shahryar Khattak, Guimiot Fabien, Elisabeth Binder, Frances Elmslie, Renzo Guerrini, Alexandre D. Baffet, Stephan A. Sieber, Barbara Treutlein, Stephen P. Robertson () and Silvia Cappello ()
Additional contact information
Christina Kyrousi: Max Planck Institute of Psychiatry
Adam C. O’Neill: University of Otago
Agnieska Brazovskaja: Max Planck Institute for Evolutionary Anthropology
Zhisong He: Max Planck Institute for Evolutionary Anthropology
Pavel Kielkowski: Technische Universität München
Laure Coquand: CNRS, UMR 144, 26 rue d’Ulm
Rossella Giaimo: Max Planck Institute of Psychiatry
Pierpaolo D’ Andrea: Max Planck Institute of Psychiatry
Alexander Belka: Max Planck Institute of Psychiatry
Andrea Forero Echeverry: Max Planck Institute of Psychiatry
Davide Mei: Children’s Hospital A. Meyer-University of Florence
Matteo Lenge: Children’s Hospital A. Meyer-University of Florence
Cristiana Cruceanu: Max Planck Institute of Psychiatry
Isabel Y. Buchsbaum: Max Planck Institute of Psychiatry
Shahryar Khattak: School of Medicine, Technical University Dresden
Guimiot Fabien: Unité de Foetopathologie, Assistance Publique-Hôpitaux de Paris, CHU Robert Debré
Elisabeth Binder: Max Planck Institute of Psychiatry
Frances Elmslie: University of London
Renzo Guerrini: Children’s Hospital A. Meyer-University of Florence
Alexandre D. Baffet: CNRS, UMR 144, 26 rue d’Ulm
Stephan A. Sieber: Technische Universität München
Barbara Treutlein: Max Planck Institute for Evolutionary Anthropology
Stephen P. Robertson: University of Otago
Silvia Cappello: Max Planck Institute of Psychiatry

Nature Communications, 2021, vol. 12, issue 1, 1-22

Abstract: Abstract Basal progenitors (BPs), including intermediate progenitors and basal radial glia, are generated from apical radial glia and are enriched in gyrencephalic species like humans, contributing to neuronal expansion. Shortly after generation, BPs delaminate towards the subventricular zone, where they further proliferate before differentiation. Gene expression alterations involved in BP delamination and function in humans are poorly understood. Here, we study the role of LGALS3BP, so far known as a cancer biomarker, which is a secreted protein enriched in human neural progenitors (NPCs). We show that individuals with LGALS3BP de novo variants exhibit altered local gyrification, sulcal depth, surface area and thickness in their cortex. Additionally, using cerebral organoids, human fetal tissues and mice, we show that LGALS3BP regulates the position of NPCs. Single-cell RNA-sequencing and proteomics reveal that LGALS3BP-mediated mechanisms involve the extracellular matrix in NPCs’ anchoring and migration within the human brain. We propose that its temporal expression influences NPCs’ delamination, corticogenesis and gyrification extrinsically.

Date: 2021
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DOI: 10.1038/s41467-021-26447-w

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