BMP and Delta/Notch signaling control the development of amphioxus epidermal sensory neurons: insights into the evolution of the peripheral sensory system

Development. 2012 Jun;139(11):2020-30. doi: 10.1242/dev.073833. Epub 2012 Apr 25.

Abstract

The evolution of the nervous system has been a topic of great interest. To gain more insight into the evolution of the peripheral sensory system, we used the cephalochordate amphioxus. Amphioxus is a basal chordate that has a dorsal central nervous system (CNS) and a peripheral nervous system (PNS) comprising several types of epidermal sensory neurons (ESNs). Here, we show that a proneural basic helix-loop-helix gene (Ash) is co-expressed with the Delta ligand in ESN progenitor cells. Using pharmacological treatments, we demonstrate that Delta/Notch signaling is likely to be involved in the specification of amphioxus ESNs from their neighboring epidermal cells. We also show that BMP signaling functions upstream of Delta/Notch signaling to induce a ventral neurogenic domain. This patterning mechanism is highly similar to that of the peripheral sensory neurons in the protostome and vertebrate model animals, suggesting that they might share the same ancestry. Interestingly, when BMP signaling is globally elevated in amphioxus embryos, the distribution of ESNs expands to the entire epidermal ectoderm. These results suggest that by manipulating BMP signaling levels, a conserved neurogenesis circuit can be initiated at various locations in the epidermal ectoderm to generate peripheral sensory neurons in amphioxus embryos. We hypothesize that during chordate evolution, PNS progenitors might have been polarized to different positions in various chordate lineages owing to differential regulation of BMP signaling in the ectoderm.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Achaete-Scute Complex Genome Region / genetics
  • Animals
  • Biological Evolution*
  • Bone Morphogenetic Proteins / metabolism
  • Chordata, Nonvertebrate / embryology*
  • Cloning, Molecular
  • DNA Primers / genetics
  • Epidermis / embryology
  • Florida
  • Gene Expression Regulation, Developmental / physiology*
  • In Situ Hybridization
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Membrane Proteins / metabolism
  • Neurogenesis / physiology*
  • Peripheral Nervous System / embryology*
  • Peripheral Nervous System / metabolism
  • Receptors, Notch / metabolism
  • Sensory Receptor Cells / metabolism
  • Sensory Receptor Cells / physiology*
  • Signal Transduction / physiology*

Substances

  • Bone Morphogenetic Proteins
  • DNA Primers
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Receptors, Notch
  • delta protein