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

J Clin Invest. 2024 Jul 15;134(14):e168982. doi: 10.1172/JCI168982.

Abstract

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.

Keywords: Neurodevelopment; Neuroscience; Psychiatric diseases; Stem cells; Translation.

MeSH terms

  • Cell Differentiation
  • Chromosomes, Human, Pair 7* / genetics
  • DNA Copy Number Variations*
  • Female
  • Humans
  • Male
  • Neurogenesis / genetics
  • Neurons* / metabolism
  • Neurons* / pathology
  • Ribosomal Protein S6 / genetics
  • Ribosomal Protein S6 / metabolism
  • Ribosomes / genetics
  • Ribosomes / metabolism
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / metabolism
  • Williams Syndrome / genetics
  • Williams Syndrome / metabolism
  • Williams Syndrome / pathology
  • Williams Syndrome / physiopathology

Substances

  • Ribosomal Protein S6
  • TOR Serine-Threonine Kinases
  • MTOR protein, human

Grants and funding

ERC DISEASE AVATARS no.616441 and ERC PoC 713652–LSDiASD were granted to Giuseppe Testa