Convergent genetic programs regulate similarities and differences between related motor neuron classes in Caenorhabditis elegans

Ge Shan, Kyuhyung Kim, Chris Li, W. W. Walthall

Research output: Contribution to journalArticlepeer-review

33 Scopus citations

Abstract

How do genetic programs create features common to a specific cell or tissue type while generating modifications necessary for functional diversification? We have addressed this question using the nematode Caenorhabditis elegans. The dorsal D (DD) and ventral D (VD) motorneurons (mns), referred to collectively as the D mns, compose a cross-inhibitory network that contributes to the animal's sinuous locomotion. The D mns share a number of structural and functional features, but are distinguished from one another by their synaptic patterns and the expression of a neuropeptide gene. Our findings suggest that the similarities and differences are generated at the transcriptional level. UNC-30 contains a homeodomain and activates structural and functional genes expressed in both classes. UNC-55 is a nuclear receptor expressed in the VD mns that is necessary for generating features that distinguish the two classes of D mns from one another. In unc-55 mutants, the VD mns adopt the DD mn synaptic pattern and peptide expression profile. Conversely, ectopic expression of unc-55 in the DD mns causes them to adopt VD mn features. The promoter of the neuropeptide gene expressed in the DD mns contains putative binding sites for both UNC-30 and UNC-55; alteration of these sites suggests that UNC-55 represses the ability of UNC-30 to activate a subset of genes that are expressed in the DD mns but not in the VD mns. Thus UNC-55 acts as a switch for the features that distinguish these two functionally related classes of mns.

Original languageEnglish
Pages (from-to)494-503
Number of pages10
JournalDevelopmental Biology
Volume280
Issue number2
DOIs
StatePublished - 15 Apr 2005

Bibliographical note

Funding Information:
We thank Jung A. Kim, Benton Lawson, Vincent Rehder, Robert Simmons, and H. Mimi Zhou for discussion and comments on previous drafts of this manuscript and Mike Nonet for providing the strain juIs1 containing Punc-25∷snb∷gfp . Some of the strains were obtained from the Caenorhabditis Genetics Center, which is supported by a grant from the National Institutes of Health. Some of this work was supported by NSF Grants IBN-9808861 and IBN-9973581, and NIH Grants K02AG00708 and NS42459 (CL).

Keywords

  • Caenorhabditis elegans
  • GABA
  • Neural differentiation
  • Nuclear hormone receptor
  • Synaptic specificity and rearrangement
  • unc-55 and unc-30

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