Conserved gene regulatory module specifies lateral neural borders across bilaterians

Proc Natl Acad Sci U S A. 2017 Aug 1;114(31):E6352-E6360. doi: 10.1073/pnas.1704194114. Epub 2017 Jul 17.

Abstract

The lateral neural plate border (NPB), the neural part of the vertebrate neural border, is composed of central nervous system (CNS) progenitors and peripheral nervous system (PNS) progenitors. In invertebrates, PNS progenitors are also juxtaposed to the lateral boundary of the CNS. Whether there are conserved molecular mechanisms determining vertebrate and invertebrate lateral neural borders remains unclear. Using single-cell-resolution gene-expression profiling and genetic analysis, we present evidence that orthologs of the NPB specification module specify the invertebrate lateral neural border, which is composed of CNS and PNS progenitors. First, like in vertebrates, the conserved neuroectoderm lateral border specifier Msx/vab-15 specifies lateral neuroblasts in Caenorhabditis elegans Second, orthologs of the vertebrate NPB specification module (Msx/vab-15, Pax3/7/pax-3, and Zic/ref-2) are significantly enriched in worm lateral neuroblasts. In addition, like in other bilaterians, the expression domain of Msx/vab-15 is more lateral than those of Pax3/7/pax-3 and Zic/ref-2 in C. elegans Third, we show that Msx/vab-15 regulates the development of mechanosensory neurons derived from lateral neural progenitors in multiple invertebrate species, including C. elegans, Drosophila melanogaster, and Ciona intestinalis We also identify a novel lateral neural border specifier, ZNF703/tlp-1, which functions synergistically with Msx/vab-15 in both C. elegans and Xenopus laevis These data suggest a common origin of the molecular mechanism specifying lateral neural borders across bilaterians.

Keywords: C. elegans; Msx/vab-15; ZNF703/tlp-1; neural border; neural plate border.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans Proteins / metabolism
  • Carrier Proteins / metabolism
  • Ciona intestinalis / embryology*
  • Drosophila melanogaster / embryology*
  • Gene Expression Regulation, Developmental / physiology*
  • MSX1 Transcription Factor / metabolism
  • Neural Crest / embryology*
  • Neural Plate / embryology*
  • Neural Stem Cells / metabolism*
  • Paired Box Transcription Factors / metabolism
  • Peripheral Nervous System / cytology
  • Peripheral Nervous System / embryology
  • Single-Cell Analysis
  • Xenopus laevis / embryology*

Substances

  • Caenorhabditis elegans Proteins
  • Carrier Proteins
  • MSX1 Transcription Factor
  • PAX-3 protein, C elegans
  • Paired Box Transcription Factors