scholarly journals The lin-11 LIM homeobox gene specifies olfactory and chemosensory neuron fates in C. elegans

Development ◽  
2001 ◽  
Vol 128 (17) ◽  
pp. 3269-3281 ◽  
Author(s):  
Trina R. Sarafi-Reinach ◽  
Tali Melkman ◽  
Oliver Hobert ◽  
Piali Sengupta
Keyword(s):  
Sensory Neuron ◽  
Receptor Gene ◽  
Homeobox Gene ◽  
Nuclear Hormone Receptor ◽  
Olfactory Neuron ◽  
Olfactory Neurons ◽  
Temporal Regulation ◽  
Chemosensory Neurons ◽  
C Elegans ◽  
Chemosensory Neuron

Chemosensory neuron diversity in C. elegans arises from the action of transcription factors that specify different aspects of sensory neuron fate. In the AWB and AWA olfactory neurons, the LIM homeobox gene lim-4 and the nuclear hormone receptor gene odr-7 are required to confer AWB and AWA-specific characteristics respectively, and to repress an AWC olfactory neuron-like default fate. Here, we show that AWA neuron fate is also regulated by a member of the LIM homeobox gene family, lin-11. lin-11 regulates AWA olfactory neuron differentiation by initiating expression of odr-7, which then autoregulates to maintain expression. lin-11 also regulates the fate of the ASG chemosensory neurons, which are the lineal sisters of the AWA neurons. We show that lin-11 is expressed dynamically in the AWA and ASG neurons, and that misexpression of lin-11 is sufficient to promote an ASG, but not an AWA fate, in a subset of neuron types. Our results suggest that differential temporal regulation of lin-11, presumably together with its interaction with asymmetrically segregated factors, results in the generation of the distinct AWA and ASG sensory neuron types. We propose that a LIM code may be an important contributor to the generation of functional diversity in a subset of olfactory and chemosensory neurons in C. elegans.

scholarly journals A natural variant and an engineered mutation in a GPCR promote DEET resistance in C. elegans

2017 ◽  
Author(s):  
Emily J. Dennis ◽  
May Dobosiewicz ◽  
Xin Jin ◽  
Laura B. Duvall ◽  
Philip S. Hartman ◽  
...  
Keyword(s):  
Mechanism Of Action ◽  
The United States ◽  
Single Pair ◽  
United States Department ◽  
Department Of Agriculture ◽  
Chemosensory Neurons ◽  
C Elegans ◽  
Chemosensory Neuron ◽  
Pause Length ◽  
Natural Variant

DEET (N,N-diethyl-meta-toluamide) is a synthetic chemical, identified by the United States Department of Agriculture in 1946 in a screen for repellents to protect soldiers from mosquito-borne diseases1,2. Since its discovery, DEET has become the world’s most widely used arthropod repellent3, and is effective against invertebrates separated by millions of years of evolution, including biting flies4, honeybees5, ticks6, and land leeches4,7. In insects, DEET acts on the olfactory system5,8–14 and requires the olfactory receptor co-receptor orco9,11–13, but its specific mechanism of action remains controversial. Here we show that the nematode Caenorhabditis elegans is sensitive to DEET, and use this genetically-tractable animal to study its mechanism of action. We found that DEET is not a volatile repellent, but interferes selectively with chemotaxis to a variety of attractant and repellent molecules. DEET increases pause lengths to disrupt chemotaxis to some odours but not others. In a forward genetic screen for DEET-resistant animals, we identified a single G protein-coupled receptor, str-217, which is expressed in a single pair of DEET-responsive chemosensory neurons, ADL. Misexpression of str-217 in another chemosensory neuron conferred strong responses to DEET. Both engineered str-217 mutants and a wild isolate of C. elegans carrying a deletion in str-217 are DEET-resistant. We found that DEET can interfere with behaviour by inducing an increase in average pause length during locomotion, and show that this increase in pausing requires both str-217 and ADL neurons. Finally, we demonstrated that ADL neurons are activated by DEET and that optogenetic activation of ADL increased average pause length. This is consistent with the “confusant” hypothesis, in which DEET is not a simple repellent but modulates multiple olfactory pathways to scramble behavioural responses12,13. Our results suggest a consistent motif for the effectiveness of DEET across widely divergent taxa: an effect on multiple chemosensory neurons to disrupt the pairing between odorant stimulus and behavioural response.

scholarly journals Worms get the munchies: the endocannabinoid AEA induces hedonic amplification in C. elegans by modulating the activity of the AWC chemosensory neuron.

2021 ◽  
Author(s):  
Anastasia Levichev ◽  
Serge Faumont ◽  
Rachel Z Berner ◽  
Shawn R Lockery
Keyword(s):  
Calcium Imaging ◽  
Energy State ◽  
Endocannabinoid System ◽  
Olfactory Neuron ◽  
Complete Elimination ◽  
Wild Type ◽  
Food Cues ◽  
Gfp Expression ◽  
C Elegans ◽  
Chemosensory Neuron

The mammalian endocannabinoid system, comprised of the endocannabinoids AEA (N-arachidonoyl-ethanolamine) and 2-AG (2-Arachidonoylglycerol), their receptors, CB1 and CB2, and their metabolic enzymes, is believed to integrate internal energy state and external food cues to modulate feeding. For example, cannabinoids can increase preference for more palatable, calorically dense food: a response called hedonic amplification, colloquially known as "the munchies." In mammals, cannabinoids can increase sensitivity to odors and sweet tastes, which may underlie amplification. We use C. elegans, an omnivorous bacterivore, as a model in which to investigate the neurophysiology of hedonic amplification. We found that exposure to AEA increases the worms' preference for strongly preferred (more palatable) bacteria over weakly preferred (less palatable) bacteria, mimicking hedonic amplification in mammals. Furthermore, AEA acts bidirectionally, increasing consumption of strongly preferred bacteria while decreasing consumption of weakly preferred bacteria. We also found that deletion of the putative CB1 homolog, npr-19, eliminates hedonic amplification, which can be rescued by expression of wild type npr-19 or human CB1, establishing a humanized worm for cannabinoid signaling studies. Deletion of the olfactory neuron AWC, which directs chemotaxis to food, abolishes hedonic amplification. Consistent with this finding, calcium imaging revealed that AEA bidirectionally modulates AWC activity, increasing its responses to strongly preferred food and decreasing its response for weakly preferred food. In a GFP expression analysis, we found that npr-19 is expressed in approximately 21 neuron classes but, surprisingly, not in AWC. Although AEA's effect could be mediated by NPR-19-expressing neurons presynaptic to AWC, nearly complete elimination of fast synaptic transmission, via the mutation unc-13(e51), had no effect on modulation. Instead, it appears that AEA modulates AWC by activating one or more npr-19-expressing neurons that release a diffusible neuromodulator to which AWC is sensitive.

scholarly journals Context-dependent inversion of the response in a single sensory neuron type reverses olfactory preference behavior

2021 ◽  
Author(s):  
Munzareen Khan ◽  
Anna H. Hartmann ◽  
Michael P. O'Donnell ◽  
Madeline Piccione ◽  
Pin-Hao Chao ◽  
...  
Keyword(s):  
Sensory Neuron ◽  
Behavioral Response ◽  
Intracellular Signaling ◽  
Internal State ◽  
Neuron Type ◽  
Olfactory Neurons ◽  
Medium Chain ◽  
C Elegans ◽  
Intracellular Signaling Pathways ◽  
Context Dependent

The valence and salience of individual odorants are modulated by an animals innate preferences, learned associations, and internal state, as well as by the context of odorant presentation. The mechanisms underlying context-dependent flexibility in odor valence are not fully understood. Here we show that the behavioral response of C. elegans to bacterially-produced medium-chain alcohols switches from attraction to avoidance when presented in the background of a subset of additional attractive chemicals. This context-dependent reversal of odorant preference is driven by cell-autonomous inversion of the response to alcohols in the single AWC olfactory neuron pair. We find that while medium-chain alcohols inhibit the AWC olfactory neurons to drive attraction, these alcohols instead activate AWC to promote avoidance when presented in the background of a second AWC-sensed odorant. We show that these opposing responses are driven via engagement of different odorant-directed signal transduction pathways within AWC. Our results indicate that context-dependent recruitment of alternative intracellular signaling pathways within a single sensory neuron type conveys opposite hedonic valences, thereby providing a robust mechanism for odorant encoding and discrimination at the periphery.

scholarly journals The Divergent Orphan Nuclear Receptor ODR-7 Regulates Olfactory Neuron Gene Expression via Multiple Mechanisms in Caenorhabditis elegans

Genetics ◽  
2003 ◽  
Vol 165 (4) ◽  
pp. 1779-1791
Author(s):  
Marc E Colosimo ◽  
Susan Tran ◽  
Piali Sengupta
Keyword(s):  
Nuclear Receptors ◽  
Nuclear Receptor ◽  
Molecular Mechanisms ◽  
Target Genes ◽  
Receptor Gene ◽  
Biological Processes ◽  
Orphan Nuclear Receptor ◽  
Olfactory Neurons ◽  
C Elegans

Abstract Nuclear receptors regulate numerous critical biological processes. The C. elegans genome is predicted to encode ∼270 nuclear receptors of which >250 are unique to nematodes. ODR-7 is the only member of this large divergent family whose functions have been defined genetically. ODR-7 is expressed in the AWA olfactory neurons and specifies AWA sensory identity by promoting the expression of AWA-specific signaling genes and repressing the expression of an AWC-specific olfactory receptor gene. To elucidate the molecular mechanisms of action of a divergent nuclear receptor, we have identified residues and domains required for different aspects of ODR-7 function in vivo. ODR-7 utilizes an unexpected diversity of mechanisms to regulate the expression of different sets of target genes. Moreover, these mechanisms are distinct in normal and heterologous cellular contexts. The odr-7 ortholog in the closely related nematode C. briggsae can fully substitute for all ODR-7-mediated functions, indicating conservation of function across 25–120 million years of divergence.

The Caenorhabditis elegans odr-2 Gene Encodes a Novel Ly-6-Related Protein Required for Olfaction

Genetics ◽  
2001 ◽  
Vol 157 (1) ◽  
pp. 211-224 ◽  
Author(s):  
Joseph H Chou ◽  
Cornelia I Bargmann ◽  
Piali Sengupta
Keyword(s):  
Caenorhabditis Elegans ◽  
Motor Neurons ◽  
Amino Terminus ◽  
Signaling Proteins ◽  
Related Protein ◽  
Olfactory Neurons ◽  
Unique Role ◽  
C Elegans ◽  
Founding Member ◽  
High Concentrations

Abstract Caenorhabditis elegans odr-2 mutants are defective in the ability to chemotax to odorants that are recognized by the two AWC olfactory neurons. Like many other olfactory mutants, they retain responses to high concentrations of AWC-sensed odors; we show here that these residual responses are caused by the ability of other olfactory neurons (the AWA neurons) to be recruited at high odor concentrations. odr-2 encodes a membrane-associated protein related to the Ly-6 superfamily of GPI-linked signaling proteins and is the founding member of a C. elegans gene family with at least seven other members. Alternative splicing of odr-2 yields three predicted proteins that differ only at the extreme amino terminus. The three isoforms have different promoters, and one isoform may have a unique role in olfaction. An epitope-tagged ODR-2 protein is expressed at high levels in sensory neurons, motor neurons, and interneurons and is enriched in axons. The AWC neurons are superficially normal in their development and structure in odr-2 mutants, but their function is impaired. Our results suggest that ODR-2 may regulate AWC signaling within the neuronal network required for chemotaxis.

scholarly journals GRDN-1/Girdin regulates dendrite morphogenesis and cilium position in two specialized sensory neuron types in C. elegans

2021 ◽  
Vol 472 ◽  
pp. 38-51
Author(s):  
Inna Nechipurenko ◽  
Sofia Lavrentyeva ◽  
Piali Sengupta
Keyword(s):  
Sensory Neuron ◽  
C Elegans ◽  
Dendrite Morphogenesis
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