Transcriptomic analysis of murine embryos lacking endogenous retinoic acid signaling

PLoS One. 2013 Apr 24;8(4):e62274. doi: 10.1371/journal.pone.0062274. Print 2013.

Abstract

Retinoic acid (RA), an active derivative of the liposoluble vitamin A (retinol), acts as an important signaling molecule during embryonic development, regulating phenomenons as diverse as anterior-posterior axial patterning, forebrain and optic vesicle development, specification of hindbrain rhombomeres, pharyngeal arches and second heart field, somitogenesis, and differentiation of spinal cord neurons. This small molecule directly triggers gene activation by binding to nuclear receptors (RARs), switching them from potential repressors to transcriptional activators. The repertoire of RA-regulated genes in embryonic tissues is poorly characterized. We performed a comparative analysis of the transcriptomes of murine wild-type and Retinaldehyde Dehydrogenase 2 null-mutant (Raldh2 (-/-)) embryos - unable to synthesize RA from maternally-derived retinol - using Affymetrix DNA microarrays. Transcriptomic changes were analyzed in two embryonic regions: anterior tissues including forebrain and optic vesicle, and posterior (trunk) tissues, at early stages preceding the appearance of overt phenotypic abnormalities. Several genes expected to be downregulated under RA deficiency appeared in the transcriptome data (e.g. Emx2, Foxg1 anteriorly, Cdx1, Hoxa1, Rarb posteriorly), whereas reverse-transcriptase-PCR and in situ hybridization performed for additional selected genes validated the changes identified through microarray analysis. Altogether, the affected genes belonged to numerous molecular pathways and cellular/organismal functions, demonstrating the pleiotropic nature of RA-dependent events. In both tissue samples, genes upregulated were more numerous than those downregulated, probably due to feedback regulatory loops. Bioinformatic analyses highlighted groups (clusters) of genes displaying similar behaviors in mutant tissues, and biological functions most significantly affected (e.g. mTOR, VEGF, ILK signaling in forebrain tissues; pyrimidine and purine metabolism, calcium signaling, one carbon metabolism in posterior tissues). Overall, these data give an overview of the gene expression changes resulting from embryonic RA deficiency, and provide new candidate genes and pathways that may help understanding retinoid-dependent molecular events.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aldehyde Oxidoreductases / genetics
  • Animals
  • Cell Lineage / drug effects
  • Cell Lineage / genetics
  • Cluster Analysis
  • Computational Biology
  • Embryo, Mammalian / metabolism*
  • Embryonic Stem Cells / drug effects
  • Embryonic Stem Cells / metabolism
  • Female
  • Gene Expression Profiling*
  • Gene Expression Regulation, Developmental* / drug effects
  • Mice
  • Mice, Knockout
  • Phenotype
  • Pregnancy
  • Regulatory Sequences, Nucleic Acid
  • Reproducibility of Results
  • Signal Transduction*
  • Tretinoin / metabolism*
  • Tretinoin / pharmacology

Substances

  • Tretinoin
  • Aldehyde Oxidoreductases
  • RALDH2 protein, mouse

Grants and funding

This work was supported by grants from the Agence Nationale de la Recherche (ANR Neurosciences 2007, ANR Blanc 2011) and the Fondation pour la Recherche Médicale (Equipe FRM 2007), and by institutional funds from the Centre National de la Recherche Scientifique (CNRS) and Institut National de la Santé et de la Recherche Médicale (INSERM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.