Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFbeta family signaling pathway and a Hox gene

Development. 1999 Dec;126(24):5819-31. doi: 10.1242/dev.126.24.5819.

Abstract

We have investigated the mechanism that patterns dopamine expression among Caenorhabditis elegans male ray sensory neurons. Dopamine is expressed by the A-type sensory neurons in three out of the nine pairs of rays. We used expression of a tyrosine hydroxylase reporter transgene as well as direct assays for dopamine to study the genetic requirements for adoption of the dopaminergic cell fate. In loss-of-function mutants affecting a TGFbeta family signaling pathway, the DBL-1 pathway, dopaminergic identity is adopted irregularly by a wider subset of the rays. Ectopic expression of the pathway ligand, DBL-1, from a heat-shock-driven transgene results in adoption of dopaminergic identity by rays 3-9; rays 1 and 2 are refractory. The rays are therefore prepatterned with respect to their competence to be induced by a DBL-1 pathway signal. Temperature-shift experiments with a temperature-sensitive type II receptor mutant, as well as heat-shock induction experiments, show that the DBL-1 pathway acts during an interval that extends from two to one cell generation before ray neurons are born and begin to differentiate. In a mutant of the AbdominalB class Hox gene egl-5, rays that normally express EGL-5 do not adopt dopaminergic fate and cannot be induced to express DA when DBL-1 is provided by a heat-shock-driven dbl-1 transgene. Therefore, egl-5 is required for making a subset of rays capable of adopting dopaminergic identity, while the function of the DBL-1 pathway signal is to pattern the realization of this capability.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology
  • Caenorhabditis elegans Proteins*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Dopamine / metabolism*
  • GTPase-Activating Proteins
  • Genes, Homeobox*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Intercellular Signaling Peptides and Proteins
  • Ligands
  • Male
  • Neurons, Afferent / physiology*
  • Neuropeptides / metabolism
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Signal Transduction*
  • Transforming Growth Factor beta / metabolism*
  • Tyrosine 3-Monooxygenase / genetics
  • Tyrosine 3-Monooxygenase / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Cell Cycle Proteins
  • Dbl-1 protein, C elegans
  • GTPase-Activating Proteins
  • Git2 protein, mouse
  • Homeodomain Proteins
  • Intercellular Signaling Peptides and Proteins
  • Ligands
  • Neuropeptides
  • Phosphoproteins
  • Transforming Growth Factor beta
  • Tyrosine 3-Monooxygenase
  • Dopamine