3D reconstruction of the mouse cochlea from scRNA-seq data suggests morphogen-based principles in apex-to-base specification

Dev Cell. 2024 Jun 17;59(12):1538-1552.e6. doi: 10.1016/j.devcel.2024.03.028. Epub 2024 Apr 8.

Abstract

In the mammalian auditory system, frequency discrimination depends on numerous morphological and physiological properties of the organ of Corti, which gradually change along the apex-to-base (tonotopic) axis of the organ. For example, the basilar membrane stiffness changes tonotopically, thus affecting the tuning properties of individual hair cells. At the molecular level, those frequency-specific characteristics are mirrored by gene expression gradients; however, the molecular mechanisms controlling tonotopic gene expression in the mouse cochlea remain elusive. Through analyzing single-cell RNA sequencing (scRNA-seq) data from E12.5 and E14.5 time points, we predicted that morphogens, rather than a cell division-associated mechanism, confer spatial identity in the extending cochlea. Subsequently, we reconstructed the developing cochlea in 3D space from scRNA-seq data to investigate the molecular pathways mediating positional information. The retinoic acid (RA) and hedgehog pathways were found to form opposing apex-to-base gradients, and functional interrogation using mouse cochlear explants suggested that both pathways jointly specify the longitudinal axis.

Keywords: 3D reconstruction; organ of corti; retinoic acid; sonic hedgehog; tonotopy.

MeSH terms

  • Animals
  • Cochlea* / metabolism
  • Gene Expression Regulation, Developmental
  • Hair Cells, Auditory / metabolism
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism
  • Imaging, Three-Dimensional / methods
  • Mice
  • Organ of Corti / metabolism
  • RNA-Seq / methods
  • Sequence Analysis, RNA / methods
  • Signal Transduction
  • Single-Cell Analysis / methods
  • Single-Cell Gene Expression Analysis
  • Tretinoin / metabolism
  • Tretinoin / pharmacology

Substances

  • Tretinoin
  • Hedgehog Proteins