The Evolutionarily Conserved LIM Homeodomain Protein LIM-4/LHX6 Specifies the Terminal Identity of a Cholinergic and Peptidergic C. elegans Sensory/Inter/Motor Neuron-Type

PLoS Genet. 2015 Aug 25;11(8):e1005480. doi: 10.1371/journal.pgen.1005480. eCollection 2015 Aug.

Abstract

The expression of specific transcription factors determines the differentiated features of postmitotic neurons. However, the mechanism by which specific molecules determine neuronal cell fate and the extent to which the functions of transcription factors are conserved in evolution are not fully understood. In C. elegans, the cholinergic and peptidergic SMB sensory/inter/motor neurons innervate muscle quadrants in the head and control the amplitude of sinusoidal movement. Here we show that the LIM homeobox protein LIM-4 determines neuronal characteristics of the SMB neurons. In lim-4 mutant animals, expression of terminal differentiation genes, such as the cholinergic gene battery and the flp-12 neuropeptide gene, is completely abolished and thus the function of the SMB neurons is compromised. LIM-4 activity promotes SMB identity by directly regulating the expression of the SMB marker genes via a distinct cis-regulatory motif. Two human LIM-4 orthologs, LHX6 and LHX8, functionally substitute for LIM-4 in C. elegans. Furthermore, C. elegans LIM-4 or human LHX6 can induce cholinergic and peptidergic characteristics in the human neuronal cell lines. Our results indicate that the evolutionarily conserved LIM-4/LHX6 homeodomain proteins function in generation of precise neuronal subtypes.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / physiology*
  • Cell Differentiation
  • Cell Line, Tumor
  • Cholinergic Neurons / metabolism
  • Consensus Sequence
  • Gene Expression Regulation, Developmental
  • Humans
  • Interneurons / physiology*
  • LIM-Homeodomain Proteins / physiology*
  • Motor Neurons / physiology*
  • Nerve Tissue Proteins / physiology
  • Sensory Receptor Cells / physiology*
  • Stress, Physiological
  • Transcription Factors / physiology*
  • Transcriptome

Substances

  • Caenorhabditis elegans Proteins
  • LHX6 protein, human
  • LIM-Homeodomain Proteins
  • Lim-4 protein, C elegans
  • Nerve Tissue Proteins
  • Transcription Factors