The<i>C. elegans</i>Tailless/TLX transcription factor<i>nhr-67</i>controls neuronal identity and left/right asymmetric fate diversification

Sarin, Sumeet; Antonio, Celia; Tursun, Baris; Hobert, Oliver

doi:10.1242/dev.040204

Cited by 46 publications

(63 citation statements)

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“…Taken together, die-1 expression passes through several distinct phases: an early bilateral phase, likely controlled by bilateral ASE fate determinants such as che-1 and nhr-67 (Etchberger et al 2007;Sarin et al 2009); a restriction to ASEL that requires transient activity of the cog-1 homeobox gene; and a maintenance phase that requires ceh-36 and die-1 itself to promote expression in ASEL and fozi-1 to repress expression in ASER.…”

Section: Resultsmentioning

confidence: 99%

Two distinct types of neuronal asymmetries are controlled by the Caenorhabditis elegans zinc finger transcription factor die-1

et al. 2013

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Left/right asymmetric features of animals are either randomly distributed on either the left or right side within a population (''antisymmetries'') or found stereotypically on one particular side of an animal (''directional asymmetries''). Both types of asymmetries can be found in nervous systems, but whether the regulatory programs that establish these asymmetries share any mechanistic features is not known. We describe here an unprecedented molecular link between these two types of asymmetries in Caenorhabditis elegans. The zinc finger transcription factor die-1 is expressed in a directionally asymmetric manner in the gustatory neuron pair ASE left (ASEL) and ASE right (ASER), while it is expressed in an antisymmetric manner in the olfactory neuron pair AWC left (AWCL) and AWC right (AWCR). Asymmetric die-1 expression is controlled in a fundamentally distinct manner in these two neuron pairs. Importantly, asymmetric die-1 expression controls the directionally asymmetric expression of gustatory receptor proteins in the ASE neurons and the antisymmetric expression of olfactory receptor proteins in the AWC neurons. These asymmetries serve to increase the ability of the animal to discriminate distinct chemosensory inputs.

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Section: Resultsmentioning

confidence: 99%

Two distinct types of neuronal asymmetries are controlled by the Caenorhabditis elegans zinc finger transcription factor die-1

et al. 2013

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“…(C) Testing the effect of 39UTR replacement on functional derepression of die-1 and cog-1 gene activity. Based on previous work, derepression of die-1 function in ASER is expected to result in a transformation of ASER to ASEL (Johnston et al 2005), while derepression of cog-1 function in ASEL is expected to result in a transformation of ASEL to ASER (Chang et al 2003;Johnston et al 2005;Sarin et al 2009). Transgenic animals containing reporters with wild-type 39UTRs or replaced 39UTR (as shown in panel A) were assayed for their ability to convert cell fate, as assessed with the ASER fate marker gcy-5Tgfp (ntIs1), which is expressed in ASEL if ASER fate is induced (left table) and repressed in ASER if ASEL fate is induced (right table).…”

Section: Discussionmentioning

confidence: 99%

“…These reporter genes are fully functional and rescue the cog-1 and die-1 mutant phenotypes, respectively (data not shown). The left/right asymmetric regulation of cog-1 and die-1 is functionally relevant since ectopic expression of cog-1 in ASEL converts ASEL into ASER and overexpression of die-1 converts ASER to ASEL (Chang et al 2003;Johnston et al 2005;Sarin et al 2009; data not shown).…”

Section: Sequence Features Of the Three Regulatory Elementsmentioning

confidence: 93%

Neuron-type specific regulation of a 3′UTR through redundant and combinatorially acting cis-regulatory elements

Didiano

Cochella²,

Tursun³

et al. 2009

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ABSTRACT39 Untranslated region (UTR)-dependent post-transcriptional regulation has emerged as a critical mechanism of controlling gene expression in various physiological contexts, including cellular differentiation events. Here, we examine the regulation of the 39UTR of the die-1 transcription factor in a single neuron of the nematode C. elegans. This 39UTR shows the intriguing feature of being differentially regulated across the animal's left/right axis. In the left gustatory neuron, ASEL, in which DIE-1 protein is normally expressed in adult animals, the 39UTR confers no regulatory information, while in the right gustatory neuron, ASER, where DIE-1 is normally not expressed, this 39UTR confers negative regulatory information. Here, we systematically analyze the cis-regulatory architecture of the die-1 39UTR using a transgenic, in vivo assay system. Through extensive mutagenesis and sequence insertions into heterologous 39UTR contexts, we describe three 25-base-pair (bp) sequence elements that are both required and sufficient to mediate the ASER-specific down-regulation of the die-1 39UTR. These three 25-bp sequence elements operate in both a redundant and combinatorial manner. Moreover, there are not only redundant elements within the die-1 39UTR regulating its left/right asymmetric activity but asymmetric 39UTR regulation is itself redundant with other regulatory mechanisms to achieve asymmetric DIE-1 protein expression and function in ASEL versus ASER. The features of 39UTR regulation we describe here may apply to some of the vast number of genes in animal genomes whose expression is predicted to be regulated through their 39UTR.

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“…Hobert , 2003;Johnston et al, 2006;Ortiz et al, 2006;Ortiz et al, 2009; PierceShimomura et al, 2001;Poole and Hobert, 2006;Sarin et al, 2009;Sarin et al, 2007;Uchida et al, 2003;Yu et al, 1997). In both cases, asymmetry contributes to being able to distinguish between attractive chemicals.…”

Section: Development 682mentioning

confidence: 99%

“…In both AWC and ASE neurons, the left and right neurons of a pair are functionally different from each other, with different patterns of gene expression. ASE neurons express multiple genes asymmetrically, including nuclear proteins, transcription factors, guanylyl cyclase sensory receptors and microRNAs (Chang et al, 2004;Chang et al, 2003;Etchberger et al, 2009;Johnston and Hobert, 2003;Johnston et al, 2006;Ortiz et al, 2006;Ortiz et al, 2009;PierceShimomura et al, 2001;Poole and Hobert, 2006;Sarin et al, 2009;Sarin et al, 2007;Uchida et al, 2003;Yu et al, 1997). In both cases, asymmetry contributes to being able to distinguish between attractive chemicals.…”

Section: Types Of Left-right Asymmetry In C Elegans Nervesmentioning

confidence: 99%

Making a difference together: reciprocal interactions in C. elegans and zebrafish asymmetric neural development

et al. 2010

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SummaryBrain asymmetries are thought to increase neural processing capacity and to prevent interhemispheric conflict. In order to develop asymmetrically, neurons must be specified along the left-right axis, assigned left-side versus right-side identities and differentiate appropriately. In C. elegans and zebrafish, the cellular and molecular mechanisms that lead to neural asymmetries have recently come to light. Here, we consider recent insights into the mechanisms involved in asymmetrical neural development in these two species. Although the molecular details are divergent, both organisms use iterative cell-cell communication to establish left-right neuronal identity. Key words: C. elegans, Left-right asymmetry, Zebrafish IntroductionThe phenomenon of left-right asymmetry in biological systems has piqued human curiosity for thousands of years. Brain asymmetry was once thought to be exclusive to humans, partly because two behaviors that we like to consider as typically human, namely hand usage and language, display sidedness. However, this notion has been dispelled over the last century by an accumulation of data that demonstrates asymmetric behaviors in many vertebrates and invertebrates (Sreng, 2003;Vallortigara, 2000), such as handedness in many mammals, task-specific eye use in chickens, fish and toads, sex pheromone perception in cockroaches, olfaction in honeybees and chemosensation in C. elegans. Albeit a blow to human exceptionalism, these discoveries have been a boon to researchers, as they have allowed model organisms to be employed in the investigation of asymmetric brain development. In this review, we highlight recent advances in two species, the nematode C. elegans and the zebrafish D. rerio, that have unveiled genetic pathways required for establishing brain asymmetry. We first discuss the specification of the left and right amphid wing 'C' (AWC) neurons of the C. elegans olfactory system, which is influenced by calcium influx; this, in turn, is regulated by gap junction-and claudin-mediated cell-cell communication. We then discuss the development of asymmetry in the zebrafish epithalamus, where Nodal signaling initiates a series of reciprocal interactions between the left-sided parapineal organ and the left habenular nucleus.Although there is a considerable evolutionary gulf between the 302 neurons of the nematode and the estimated 78,000 neurons of the larval zebrafish (Hill et al., 2003), some common themes arise, in particular the interaction of neurons across the midline during the formation of the lateralized nervous system and the inherently stochastic nature of some developmental pathways. However, the striking differences in the genetic and cellular pathways highlight the improbability that nematode and zebrafish brain asymmetry arose from a shared ancestral event. Rather, the advantages conferred upon neural networks by asymmetry suggest that left-right differences in the worm and zebrafish nervous systems have evolved convergently. Left-right asymmetry in the C. elegans sensory system T...

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TheC. elegansTailless/TLX transcription factornhr-67controls neuronal identity and left/right asymmetric fate diversification

Cited by 46 publications

References 46 publications

Two distinct types of neuronal asymmetries are controlled by the Caenorhabditis elegans zinc finger transcription factor die-1

Two distinct types of neuronal asymmetries are controlled by the Caenorhabditis elegans zinc finger transcription factor die-1

Neuron-type specific regulation of a 3′UTR through redundant and combinatorially acting cis-regulatory elements

Making a difference together: reciprocal interactions in C. elegans and zebrafish asymmetric neural development

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