A molecular analysis of neurogenic placode and cranial sensory ganglion development in the shark, Scyliorhinus canicula

Dev Biol. 2007 Apr 1;304(1):156-81. doi: 10.1016/j.ydbio.2006.12.029. Epub 2006 Dec 19.

Abstract

In order to gain insight into the evolution of the genetic control of the development of cranial neurogenic placodes and cranial sensory ganglia in vertebrates, we cloned and analysed the spatiotemporal expression pattern of six transcription factor genes in a chondrichthyan, the shark Scyliorhinus canicula (lesser-spotted dogfish/catshark). As in other vertebrates, NeuroD is expressed in all cranial sensory ganglia. We show that Pax3 is expressed in the profundal placode and ganglion, strongly supporting homology between the separate profundal ganglion of elasmobranchs and basal actinopterygians and the ophthalmic trigeminal placode-derived neurons of the fused amniote trigeminal ganglion. We show that Pax2 is a conserved pan-gnathostome marker for epibranchial and otic placodes, and confirm that Phox2b is a conserved pan-gnathostome marker for epibranchial placode-derived neurons. We identify Eya4 as a novel marker for the lateral line system throughout its development, expressed in lateral line placodes, sensory ridges and migrating primordia, neuromasts and electroreceptors. We also identify Tbx3 as a specific marker for lateral line ganglia in shark embryos. We use the spatiotemporal expression pattern of these genes to characterise the development of neurogenic placodes and cranial sensory ganglia in the dogfish, with a focus on the epibranchial and lateral line placodes. Our findings demonstrate the evolutionary conservation across all gnathostomes of at least some of the transcription factor networks underlying neurogenic placode development.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Brain / embryology*
  • Brain / metabolism
  • Cluster Analysis
  • Computational Biology
  • DNA Primers
  • Evolution, Molecular
  • Ganglia, Sensory / embryology*
  • Gene Expression Regulation, Developmental*
  • Immunohistochemistry
  • In Situ Hybridization
  • Molecular Sequence Data
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Phylogeny*
  • Sensory Receptor Cells / metabolism*
  • Sequence Analysis, DNA
  • Sharks / embryology*
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism*

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • DNA Primers
  • Nerve Tissue Proteins
  • Transcription Factors
  • Neurogenic differentiation factor 1