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Unconventional function of an Achaete-Scute homolog as a terminal selector of nociceptive neuron identity

Title
Unconventional function of an Achaete-Scute homolog as a terminal selector of nociceptive neuron identity
Authors
Masoudi, NedaTavazoie, SaeedGlenwinkel, LoriRyu, Lee sunKim, Kyu HyungHobert, Oliver
DGIST Authors
Kim, Kyu Hyung
Issue Date
2018-04
Citation
PLoS Biology, 16(4)
Type
Article
Article Type
Article
Keywords
NEMATODE CAENORHABDITIS-ELEGANSHELIX TRANSCRIPTION FACTORSLIM HOMEOBOX GENEC-ELEGANSNERVOUS-SYSTEMCELL-TYPESCHEMICAL REPELLENTSREGULATORY LOGICPRONEURAL GENEPROTEIN
ISSN
1545-7885
Abstract
Proneural genes are among the most early-acting genes in nervous system development, instructing blast cells to commit to a neuronal fate. Drosophila Atonal and Achaete-Scute complex (AS-C) genes, as well as their vertebrate orthologs, are basic helix-loop-helix (bHLH) transcription factors with such proneural activity. We show here that a C. elegans AS-C homolog, hlh-4, functions in a fundamentally different manner. In the embryonic, larval, and adult nervous systems, hlh-4 is expressed exclusively in a single nociceptive neuron class, ADL, and its expression in ADL is maintained via transcriptional autoregulation throughout the life of the animal. However, in hlh-4 null mutants, the ADL neuron is generated and still appears neuronal in overall morphology and expression of panneuronal and pansensory features. Rather than acting as a proneural gene, we find that hlh-4 is required for the ADL neuron to function properly, to adopt its correct morphology, to express its unusually large repertoire of olfactory receptor–encoding genes, and to express other known features of terminal ADL identity, including neurotransmitter phenotype, neuropeptides, ion channels, and electrical synapse proteins. hlh-4 is sufficient to induce ADL identity features upon ectopic expression in other neuron types. The expression of ADL terminal identity features is directly controlled by HLH-4 via a phylogenetically conserved E-box motif, which, through bioinformatic analysis, we find to constitute a predictive feature of ADL-expressed terminal identity markers. The lineage that produces the ADL neuron was previously shown to require the conventional, transient proneural activity of another AS-C homolog, hlh-14, demonstrating sequential activities of distinct AS-C-type bHLH genes in neuronal specification. Taken together, we have defined here an unconventional function of an AS-C-type bHLH gene as a terminal selector of neuronal identity and we speculate that such function could be reflective of an ancestral function of an “ur-” bHLH gene. © 2018 Masoudi et al.
URI
http://hdl.handle.net/20.500.11750/6394
DOI
10.1371/journal.pbio.2004979
Publisher
PUBLIC LIBRARY SCIENCE
Related Researcher
  • Author Kim, Kyuhyung The K. Kim Lab of Neurobehavior and Neural Circuits
  • Research Interests Neurobehavior; Neural Circuit; Neurodevelopment; 신경회로; 신경행동; 신경발생; 신경유전학
Files:
Collection:
Department of Brain and Cognitive SciencesThe K. Kim Lab of Neurobehavior and Neural Circuits1. Journal Articles


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