Co-expression of the transcription factors CEH-14 and TTX-1 regulates AFD neuron-specific genes gcy-8 and gcy-18 in C. elegans

Dev Biol. 2015 Mar 15;399(2):325-36. doi: 10.1016/j.ydbio.2015.01.010. Epub 2015 Jan 19.

Abstract

A wide variety of cells are generated by the expression of characteristic sets of genes, primarily those regulated by cell-specific transcription. To elucidate the mechanism regulating cell-specific gene expression in a highly specialized cell, AFD thermosensory neuron in Caenorhabditis elegans, we analyzed the promoter sequences of guanylyl cyclase genes, gcy-8 and gcy-18, exclusively expressed in AFD. In this study, we showed that AFD-specific expression of gcy-8 and gcy-18 requires the co-expression of homeodomain proteins, CEH-14/LHX3 and TTX-1/OTX1. We observed that mutation of ttx-1 or ceh-14 caused a reduction in the expression of gcy-8 and gcy-18 and that the expression was completely lost in double mutants. This synergy effect was also observed with other AFD marker genes, such as ntc-1, nlp-21and cng-3. Electrophoretic mobility shift assays revealed direct interaction of CEH-14 and TTX-1 proteins with gcy-8 and gcy-18 promoters in vitro. The binding sites of CEH-14 and TTX-1 proteins were confirmed to be essential for AFD-specific expression of gcy-8 and gcy-18 in vivo. We also demonstrated that forced expression of CEH-14 and TTX-1 in AWB chemosensory neurons induced ectopic expression of gcy-8 and gcy-18 reporters in this neuron. Finally, we showed that the regulation of gcy-8 and gcy-18 expression by ceh-14 and ttx-1 is evolutionally conserved in five Caenorhabditis species. Taken together, ceh-14 and ttx-1 expression determines the fate of AFD as terminal selector genes at the final step of cell specification.

Keywords: Differentiation; Nematode; Neuron; Transcription factor.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Differentiation / physiology
  • Computational Biology
  • Electrophoretic Mobility Shift Assay
  • Gene Expression Regulation / physiology*
  • Green Fluorescent Proteins / metabolism
  • Guanylate Cyclase / genetics
  • Guanylate Cyclase / metabolism*
  • Image Processing, Computer-Assisted
  • LIM-Homeodomain Proteins / genetics
  • LIM-Homeodomain Proteins / metabolism*
  • Mutation / genetics
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neurons / metabolism*
  • Neurons / physiology
  • Promoter Regions, Genetic / genetics
  • Species Specificity
  • Thermosensing / physiology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transgenes / genetics

Substances

  • CEH-14 protein, C elegans
  • Caenorhabditis elegans Proteins
  • LIM-Homeodomain Proteins
  • Nerve Tissue Proteins
  • Transcription Factors
  • Ttx-1 protein, C elegans
  • Green Fluorescent Proteins
  • GCY-18 protein, C elegans
  • GCY-8 protein, C elegans
  • Guanylate Cyclase