The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons

PLoS Genet. 2021 Mar 19;17(3):e1009441. doi: 10.1371/journal.pgen.1009441. eCollection 2021 Mar.

Abstract

Biallelic mutations in DONSON, an essential gene encoding for a replication fork protection factor, were linked to skeletal abnormalities and microcephaly. To better understand DONSON function in corticogenesis, we characterized Donson expression and consequences of conditional Donson deletion in the mouse telencephalon. Donson was widely expressed in the proliferation and differentiation zones of the embryonic dorsal and ventral telencephalon, which was followed by a postnatal expression decrease. Emx1-Cre-mediated Donson deletion in progenitors of cortical glutamatergic neurons caused extensive apoptosis in the early dorsomedial neuroepithelium, thus preventing formation of the neocortex and hippocampus. At the place of the missing lateral neocortex, these mutants exhibited a dorsal extension of an early-generated paleocortex. Targeting cortical neurons at the intermediate progenitor stage using Tbr2-Cre evoked no apparent malformations, whereas Nkx2.1-Cre-mediated Donson deletion in subpallial progenitors ablated 75% of Nkx2.1-derived cortical GABAergic neurons. Thus, the early telencephalic neuroepithelium depends critically on Donson function. Our findings help explain why the neocortex is most severely affected in individuals with DONSON mutations and suggest that DONSON-dependent microcephaly might be associated with so far unrecognized defects in cortical GABAergic neurons. Targeting Donson using an appropriate recombinase is proposed as a feasible strategy to ablate proliferating and nascent cells in experimental research.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Cell Cycle Proteins / genetics*
  • Cell Differentiation* / genetics
  • Cerebral Cortex / cytology
  • Cerebral Cortex / metabolism*
  • GABAergic Neurons / cytology
  • GABAergic Neurons / metabolism*
  • Gene Expression Regulation, Developmental*
  • Hippocampus / metabolism
  • Mice
  • Neocortex
  • Neural Stem Cells / cytology
  • Neural Stem Cells / metabolism*
  • Neurogenesis / genetics
  • Neurons / cytology
  • Neurons / metabolism*
  • Nuclear Proteins / genetics*
  • Telencephalon / cytology
  • Telencephalon / metabolism

Substances

  • Cell Cycle Proteins
  • DONSON protein, human
  • Nuclear Proteins

Grants and funding

This work was financed by DFG grant STU295/9-1 to RS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.