Nodal signaling regulates specification of ascidian peripheral neurons through control of the BMP signal

Development. 2014 Oct;141(20):3889-99. doi: 10.1242/dev.110213. Epub 2014 Sep 17.

Abstract

The neural crest and neurogenic placodes are thought to be a vertebrate innovation that gives rise to much of the peripheral nervous system (PNS). Despite their importance for understanding chordate evolution and vertebrate origins, little is known about the evolutionary origin of these structures. Here, we investigated the mechanisms underlying the development of ascidian trunk epidermal sensory neurons (ESNs), which are thought to function as mechanosensory neurons in the rostral-dorsal trunk epidermis. We found that trunk ESNs are derived from the anterior and lateral neural plate border, as is the case in the vertebrate PNS. Pharmacological experiments indicated that intermediate levels of bone morphogenetic protein (BMP) signal induce formation of ESNs from anterior ectodermal cells. Gene knockdown experiments demonstrated that HrBMPa (60A-subclass BMP) and HrBMPb (dpp-subclass BMP) act to induce trunk ESNs at the tailbud stage and that anterior trunk ESN specification requires Chordin-mediated antagonism of the BMP signal, but posterior trunk ESN specification does not. We also found that Nodal functions as a neural plate border inducer in ascidians. Nodal signaling regulates expression of HrBMPs and HrChordin in the lateral neural plate, and consequently specifies trunk ESNs. Collectively, these findings show that BMP signaling that is regulated spatiotemporally by Nodal signaling is required for trunk ESN specification, which clearly differs from the BMP gradient model proposed for vertebrate neural induction.

Keywords: BMP; Epidermal sensory neuron; Nodal.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Morphogenetic Proteins / metabolism*
  • Cell Lineage
  • Gene Expression Regulation, Developmental*
  • Glycoproteins / metabolism
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Neural Crest / embryology
  • Neurons / metabolism
  • Nodal Protein / physiology*
  • Peripheral Nervous System / physiology*
  • Recombinant Proteins / chemistry
  • Sensory Receptor Cells / metabolism
  • Signal Transduction
  • Urochordata / embryology

Substances

  • Bone Morphogenetic Proteins
  • Glycoproteins
  • Intercellular Signaling Peptides and Proteins
  • Nodal Protein
  • Recombinant Proteins
  • chordin