Multiscale modeling uncovers 7q11.23 copy number variation-dependent changes in ribosomal biogenesis and neuronal maturation and excitability.


Journal

The Journal of clinical investigation
ISSN: 1558-8238
Titre abrégé: J Clin Invest
Pays: United States
ID NLM: 7802877

Informations de publication

Date de publication:
15 Jul 2024
Historique:
received: 03 02 2023
accepted: 24 05 2024
medline: 15 7 2024
pubmed: 15 7 2024
entrez: 15 7 2024
Statut: epublish

Résumé

Copy number variation (CNV) at 7q11.23 causes Williams-Beuren syndrome (WBS) and 7q microduplication syndrome (7Dup), neurodevelopmental disorders (NDDs) featuring intellectual disability accompanied by symmetrically opposite neurocognitive features. Although significant progress has been made in understanding the molecular mechanisms underlying 7q11.23-related pathophysiology, the propagation of CNV dosage across gene expression layers and their interplay remains elusive. Here we uncovered 7q11.23 dosage-dependent symmetrically opposite dynamics in neuronal differentiation and intrinsic excitability. By integrating transcriptomics, translatomics, and proteomics of patient-derived and isogenic induced neurons, we found that genes related to neuronal transmission follow 7q11.23 dosage and are transcriptionally controlled, while translational factors and ribosomal genes are posttranscriptionally buffered. Consistently, we found phosphorylated RPS6 (p-RPS6) downregulated in WBS and upregulated in 7Dup. Surprisingly, p-4EBP was changed in the opposite direction, reflecting dosage-specific changes in total 4EBP levels. This highlights different dosage-sensitive dyregulations of the mTOR pathway as well as distinct roles of p-RPS6 and p-4EBP during neurogenesis. Our work demonstrates the importance of multiscale disease modeling across molecular and functional layers, uncovers the pathophysiological relevance of ribosomal biogenesis in a paradigmatic pair of NDDs, and uncouples the roles of p-RPS6 and p-4EBP as mechanistically actionable relays in NDDs.

Identifiants

pubmed: 39007270
pii: 168982
doi: 10.1172/JCI168982
doi:
pii:

Substances chimiques

Ribosomal Protein S6 0
TOR Serine-Threonine Kinases EC 2.7.11.1
MTOR protein, human EC 2.7.1.1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Auteurs

Marija Mihailovich (M)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.

Pierre-Luc Germain (PL)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Computational Neurogenomics, D-HEST Institute for Neuroscience, Federal Institute of Technology (ETH) Zürich, Zürich, Switzerland.

Reinald Shyti (R)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.

Davide Pozzi (D)

Department of Biomedical Sciences, Humanitas University, Milan, Italy.
IRCCS Humanitas Research Hospital, Milan, Italy.

Roberta Noberini (R)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.

Yansheng Liu (Y)

Department of Biology, Institute of Molecular Systems Biology, ETH Zürich, Zürich, Switzerland.

Davide Aprile (D)

Human Technopole, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

Erika Tenderini (E)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.

Flavia Troglio (F)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

Sebastiano Trattaro (S)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

Sonia Fabris (S)

Hematology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.

Ummi Ciptasari (U)

Department of Cognitive Neurosciences, RadboudUmc, Donders Institute for Brain Cognition and Behaviour, Nijmegen, Netherlands.

Marco Tullio Rigoli (MT)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

Nicolò Caporale (N)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

Giuseppe D'Agostino (G)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.

Filippo Mirabella (F)

Human Technopole, Milan, Italy.

Alessandro Vitriolo (A)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

Daniele Capocefalo (D)

Human Technopole, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

Adrianos Skaros (A)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.

Agnese Virginia Franchini (AV)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.

Sara Ricciardi (S)

Department of Biosciences, University of Milan, Milan, Italy.
National Institute of Molecular Genetics, Fondazione Romeo ed Enrica Invernizzi, Milan, Italy.

Ida Biunno (I)

Integrated Systems Engineering Srl, c/o OpenZone, Bresso, Milan, Italy.

Antonino Neri (A)

Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.
Hematology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.

Nael Nadif Kasri (N)

Department of Cognitive Neurosciences, RadboudUmc, Donders Institute for Brain Cognition and Behaviour, Nijmegen, Netherlands.

Tiziana Bonaldi (T)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

Rudolf Aebersold (R)

Department of Biology, Institute of Molecular Systems Biology, ETH Zürich, Zürich, Switzerland.

Michela Matteoli (M)

Department of Biomedical Sciences, Humanitas University, Milan, Italy.
IRCCS Humanitas Research Hospital, Milan, Italy.

Giuseppe Testa (G)

European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.
Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

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Classifications MeSH