Essential role for ligand-dependent feedback antagonism of vertebrate hedgehog signaling by PTCH1, PTCH2 and HHIP1 during neural patterning

Development. 2013 Aug;140(16):3423-34. doi: 10.1242/dev.095083.

Abstract

Hedgehog (HH) signaling is essential for vertebrate and invertebrate embryogenesis. In Drosophila, feedback upregulation of the HH receptor Patched (PTC; PTCH in vertebrates), is required to restrict HH signaling during development. By contrast, PTCH1 upregulation is dispensable for early HH-dependent patterning in mice. Unique to vertebrates are two additional HH-binding antagonists that are induced by HH signaling, HHIP1 and the PTCH1 homologue PTCH2. Although HHIP1 functions semi-redundantly with PTCH1 to restrict HH signaling in the developing nervous system, a role for PTCH2 remains unresolved. Data presented here define a novel role for PTCH2 as a ciliary localized HH pathway antagonist. While PTCH2 is dispensable for normal ventral neural patterning, combined removal of PTCH2- and PTCH1-feedback antagonism produces a significant expansion of HH-dependent ventral neural progenitors. Strikingly, complete loss of PTCH2-, HHIP1- and PTCH1-feedback inhibition results in ectopic specification of ventral cell fates throughout the neural tube, reflecting constitutive HH pathway activation. Overall, these data reveal an essential role for ligand-dependent feedback inhibition of vertebrate HH signaling governed collectively by PTCH1, PTCH2 and HHIP1.

Keywords: Hedgehog; Negative feedback; Neural tube.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Animals
  • Body Patterning*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Chick Embryo
  • Embryo, Mammalian / metabolism
  • Feedback, Physiological
  • Female
  • Gene Expression Regulation, Developmental
  • Ligands
  • Male
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neural Tube / metabolism*
  • Patched Receptors
  • Patched-1 Receptor
  • Patched-2 Receptor
  • Protein Binding
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Signal Transduction
  • Transcription, Genetic

Substances

  • Carrier Proteins
  • Hhip protein, mouse
  • Ligands
  • Membrane Glycoproteins
  • Patched Receptors
  • Patched-1 Receptor
  • Patched-2 Receptor
  • Ptch1 protein, mouse
  • Ptch2 protein, mouse
  • Receptors, Cell Surface