Journal Article

Temporal patterning of apical progenitors and their daughter neurons in the developing neocortex

Prados, J., Amberg, N., Bartolini, G., Agirman, G., Dayer, A., Jabaudon, D., Fièvre, S., Hippenmeyer, S., Telley, L., Cadilhac, C., Nguyen, L., Oberst, P., Vitali, I.

2019

Overview

Although the main task of a neuroprogenitor is to produce more cells, it may not always produce the same cells. Some progenitors produce different daughter neurons as an embryo develops. Concurrently, these daughter neurons are also transitioning through states toward maturation. Telley et al. used single-cell RNA sequencing to survey the transcriptional identity of cells early in mouse brain development. As a neuroprogenitor transitioned to new states, it produced daughter neurons that reflect those new states. The neuron's own postmitotic differentiation program is apparently overlaid onto these parentally supplied programs, driving emergence of specialized neuronal cell types in the neocortex. Science , this issue p. eaav2522 During corticogenesis in the brain, temporally dynamic molecular birthmarks in progenitors act as seeds for later neuronal diversity. During corticogenesis, distinct subtypes of neurons are sequentially born from ventricular zone progenitors. How these cells are molecularly temporally patterned is poorly understood. We used single-cell RNA sequencing at high temporal resolution to trace the lineage of the molecular identities of successive generations of apical progenitors (APs) and their daughter neurons in mouse embryos. We identified a core set of evolutionarily conserved, temporally patterned genes that drive APs from internally driven to more exteroceptive states. We found that the Polycomb repressor complex 2 (PRC2) epigenetically regulates AP temporal progression. Embryonic age–dependent AP molecular states are transmitted to their progeny as successive ground states, onto which essentially conserved early postmitotic differentiation programs are applied, and are complemented by later-occurring environment-dependent signals. Thus, epigenetically regulated temporal molecular birthmarks present in progenitors act in their postmitotic progeny to seed adult neuronal diversity.

• Publisher: American Association for the Advancement of Science,The American Association for the Advancement of Science
• Subject: Acceleration / Animals / Brain / Cell cycle / Cerebral cortex / Chromatin / Cognitive ability / Data processing / Daughters / Differentiation / Embryogenesis / Embryonic growth stage / Embryos / Emergence / Environment / Epigenesis, Genetic / Evolution / Excitability / Fruit flies / Gene Expression Regulation, Developmental / Gene sequencing / Genes / Genetic programs / Genetics & genetic processes / Glutamatergic transmission / Ground state / Génétique & processus génétiques / Heterogeneous structure / Individualized Instruction / Information processing / Life sciences / Mice / Neocortex - cytology / Neocortex - embryology / Neoplastic Stem Cells - cytology / Neoplastic Stem Cells - metabolism / Neural stem cells / Neurogenesis / Neurogenesis - genetics / Neurogenesis - physiology / Neurons / Neurons - cytology / Neurons - metabolism / Nuclei (cytology) / Offspring / Pattern formation / Polycomb group proteins / Polycomb Repressive Complex 2 - metabolism / Progeny / Proteins / Receptors / RESEARCH ARTICLE SUMMARY / Ribonucleic acid / RNA / RNA, Messenger - metabolism / Sciences du vivant / Seeds / Sensorimotor system / Sensory Experience / Sequence Analysis, RNA / Signal processing / Single-Cell Analysis / Somatosensory cortex / Synaptogenesis / Temporal lobe / Temporal resolution / Transcription / Transcription, Genetic / Ventricle / Ventricular zone