Combinatorial control of touch receptor neuron expression in Caenorhabditis elegans

Abstract

Six touch receptor neurons with distinctive morphological features sense gentle touch in Caenorhabditis elegans. Previous studies have identified three genes (lin-32, unc-86 and mec-3) that regulate touch cell development. However, since other cell types also require these genes, we suspected that other genes help restrict the expression of touch cell characteristics to the six neurons seen in the wild type. To identify such genes, we have examined mutants defective in genes required for the development of other C. elegans cells for changes in the pattern of touch cell-specific features. Mutations in seven genes either reduce (lin-14) or increase (lin-4, egl-44, egl-46, sem-4, ced-3 and ced-4) the number of touch receptor-like cells. The combinatorial action of these genes, all of which are required for the production of many cell types, restrict the number of cells expressing touch receptor characteristics in wild-type animals by acting as positive and negative regulators and by removing cells by programmed cell death.

Effects of tap withdrawal response habituation on other withdrawal behaviors: The localization of habituation in the nematode Caenorhabditis elegans.

“…The touch cells are the most likely loci of TWR habituation. These neurons express a well-defined genetic program (Hamelin, Scott, Way, & Culotti, 1992;Mitani, Du, Hall, Driscoll, & Chalfie, 1993;Savage et al, 1989) that has been exploited to efficiently control gene expression exclusively within these neurons (Fire, 1986;Fire, Harrison, & Dixon, 1990). This discovery, in combination with the recent development of reverse genetic technology in the worm (Plasterk, 1992;Zwaal, Brocks, van Meurs, Groenen, & Plasterk, 1993), will make it possible to effectively examine molecular underpinnings of habituation in C. elegans.…”

Piecemeal regulation of convergent neuronal lineages by bHLH transcription factors inCaenorhabditis elegans

“…Our analysis of basic helix-loop-helix (bHLH) transcription factors was originally motivated by our quest to understand how the expression of terminal selector transcription factors is controlled. Terminal selectors have emerged as key regulators of neuronal identity throughout the entire nervous system (Hobert, 2016), yet we understand little about how their expression is induced in the embryo (Baumeister et al, 1996;Bertrand and Hobert, 2009;Christensen et al, 2020;Mitani et al, 1993;Murgan et al, 2015). Based on a previously reported effect of lin-32 on the expression of the terminal selectors unc-86/Brn3 (Baumeister et al, 1996) and mec-3 (Mitani et al, 1993), we sought to investigate the role of lin-32 further.…”

“…Terminal selectors have emerged as key regulators of neuronal identity throughout the entire nervous system (Hobert, 2016), yet we understand little about how their expression is induced in the embryo (Baumeister et al, 1996;Bertrand and Hobert, 2009;Christensen et al, 2020;Mitani et al, 1993;Murgan et al, 2015). Based on a previously reported effect of lin-32 on the expression of the terminal selectors unc-86/Brn3 (Baumeister et al, 1996) and mec-3 (Mitani et al, 1993), we sought to investigate the role of lin-32 further. In a number of different organisms, from flies to worms to vertebrates, Atonal orthologs have mostly been characterized for their proneural activity that imposes neuronal identity on neuroectodermal progenitor cells (Baker and Brown, 2018;Bertrand et al, 2002).…”

“…Cell identity transformations are also evident in a subset of dopaminergic neuron-producing lineages (Doitsidou et al, 2008) as well as in glia cells (Zhang et al, 2020). lin-32 has also been shown to affect the differentiation and/or function of a number of additional neuron types, including oxygen sensory neurons (Rojo Romanos et al, 2017), touch receptor neurons (Mitani et al, 1993), anterior ganglion neurons (Baumeister et al, 1996;Shaham and Bargmann, 2002) and AIB interneurons (Hori et al, 2018). However, it was left unclear whether these defects are proneural lineage defects, cellular differentiation defects, cell identity transformation defects or some combination thereof.…”

Transcription Factors That Control Behavior—Lessons From C. elegans

“…Other transcriptional regulators such as EGL-44, EGL-46, and SEM-4 repress touch receptor identity. For example, removing either egl-44 or egl-46 function results in neurons emerging with touch receptor identity that are absent in the wild-type animals (Mitani et al, 1993). In addition to controlling ets-5 expression in the BAG neurons, VAB-3 also controls other glutamatergic sensory neuron identities.…”