Polymodal Responses in C. elegans Phasmid Neurons Rely on Multiple Intracellular and Intercellular Signaling Pathways

Zou, Wenjuan; Cheng, Hankui; Li, Shitian; Yue, Xiaomin; Xue, Yi; Chen, Sixi; Kang, Lijun

doi:10.1038/srep42295

Cited by 38 publications

(55 citation statements)

References 28 publications

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“…The BP value for most associations was very weak with two exceptions: csGPCR reporters are often coexpressed in the two tail phasmid neuron classes PHA and PHB (AU/BP > 95), and expression in either or both of the phasmid neurons is associated with the expression in the head neuron ASH (AU/BP > 95) ( Fig 4 ). The ASH, PHA and PHB neuron classes are not closely related by lineage but all of these three neuron classes are nociceptive neurons that respond to similar cues and integrate sensory inputs from the head and tail [ 55 , 56 ] and that directly innervate command interneurons involved in reversal behavior [ 9 ]. While csGPCRs expressed in these neurons are likely involved in sensing nociceptive cues, it is notable that these coexpressed csGPCRs came from widely distinct csGPCR families ( Fig 4 ).…”

Section: Resultsmentioning

confidence: 99%

“…The sites of expression of specific csGPCRs point to potential functions of the csGCPRs, guiding the future analysis of csGPCR knockout strains. For example, csGPCRs expressed in the polymodal nociceptive ASH, ADL and phasmid neurons may be mediating the response to a number of distinct sensory cues processed by these neurons [ 56 , 74 ].…”

Section: Discussionmentioning

confidence: 99%

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An atlas of Caenorhabditis elegans chemoreceptor expression

et al. 2018

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One goal of modern day neuroscience is the establishment of molecular maps that assign unique features to individual neuron types. Such maps provide important starting points for neuron classification, for functional analysis, and for developmental studies aimed at defining the molecular mechanisms of neuron identity acquisition and neuron identity diversification. In this resource paper, we describe a nervous system-wide map of the potential expression sites of 244 members of the largest gene family in the C. elegans genome, rhodopsin-like (class A) G-protein-coupled receptor (GPCR) chemoreceptors, using classic gfp reporter gene technology. We cover representatives of all sequence families of chemoreceptor GPCRs, some of which were previously entirely uncharacterized. Most reporters are expressed in a very restricted number of cells, often just in single cells. We assign GPCR reporter expression to all but two of the 37 sensory neuron classes of the sex-shared, core nervous system. Some sensory neurons express a very small number of receptors, while others, particularly nociceptive neurons, coexpress several dozen GPCR reporter genes. GPCR reporters are also expressed in a wide range of inter- and motorneurons, as well as non-neuronal cells, suggesting that GPCRs may constitute receptors not just for environmental signals, but also for internal cues. We observe only one notable, frequent association of coexpression patterns, namely in one nociceptive amphid (ASH) and two nociceptive phasmid sensory neurons (PHA, PHB). We identified GPCRs with sexually dimorphic expression and several GPCR reporters that are expressed in a left/right asymmetric manner. We identified a substantial degree of GPCR expression plasticity; particularly in the context of the environmentally-induced dauer diapause stage when one third of all tested GPCRs alter the cellular specificity of their expression within and outside the nervous system. Intriguingly, in a number of cases, the dauer-specific alterations of GPCR reporter expression in specific neuron classes are maintained during postdauer life and in some case new patterns are induced post-dauer, demonstrating that GPCR gene expression may serve as traits of life history. Taken together, our resource provides an entry point for functional studies and also offers a host of molecular markers for studying molecular patterning and plasticity of the nervous system.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

An atlas of Caenorhabditis elegans chemoreceptor expression

et al. 2018

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“…In our assay, we found that mutants of both these GPCRs associated sensory molecules and also the double mutants with srx-97 showed negative chemotaxis indices towards high concentration of benzaldehyde similar to what was seen with the odr-3 and gpc-1 single mutant animals (Figure 5). OSM-9 is a member of the vanilloid subfamily of Transient Receptor Potential (TRP) channel proteins that regulates avoidance behavior to osmotic strength, nose touch and undiluted benzaldehyde in the ASH neuron (Colbert et al, 1997; Murayama and Maruyama, 2013; Zou et al, 2017). We found that both the single osm-9 mutant and double mutants of osm-9 and srx-97 showed wild type like phenotype to high concentration of benzaldehyde (Figure 5).…”

Section: Resultsmentioning

confidence: 99%

The G-protein coupled receptor SRX-97 is required for concentration dependent sensing of Benzaldehyde inCaenorhabditis elegans

Kadam

Behera

Kumar³

et al. 2020

Preprint

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32The G-protein (heterotrimeric guanine nucleotide-binding protein)-coupled receptors in 33 the olfactory system function to sense the surroundings and respond to various 34 odorants. The genes encoding for the olfactory receptors in C. elegans are larger in 35 number in comparison to those in mammals, suggesting complexity in the receptor-36 odorant relationships. Recent studies have shown that the same odorant in different 37 concentration could act on multiple receptors in different neurons to induce attractive or 38 repulsive responses. The ASH neuron is known to be responsible for responding to high 39 concentrations of volatile odorants. Here we characterize a new GPCR, SRX-97. We 40 found that the srx-97 promoter shows expression specifically in the head ASH and tail 41 PHB chemosensory neurons of C. elegans. Further, the SRX-97 protein localizes to the 42 ciliary ends of the ASH neurons. Analysis of CRISPR/based deletion mutants of the srx-43 97 gene suggest that this gene is involved in the recognition of high concentrations of 44 benzaldehyde. This was further confirmed through rescue and neuronal ablation 45 experiments. Our work gives insight into concentration dependent receptor function in 46 the olfactory system and provides details of an additional molecule that could help the 47 animal navigate its surroundings. 48 49 50 51 52 53 54Animals sense a wide range of volatile and water-soluble chemicals through their 55 olfactory system. The olfactory system is made up of several neurons that express 56 different sets of seven-transmembrane G-protein coupled receptors (GPCRs). The 57 odorant binds to the GPCRs, activating distinct intracellular signaling pathways and thus 58 directing the animal's response to different external cues (reviewed in (Erlandson et al., 59 2018; Katritch et al., 2013)). 60C. elegans is a soil-dwelling animal that possesses a well-developed chemosensory 61 system for their survival. They perceive their environment through various sensory 62 neurons to find food sources, mates and to escape from dangerous conditions. In C. 63 elegans 13 pairs of chemosensory neurons carry out majority of chemosensation, they 64 express around 1300 functional chemosensory (cs) G-protein coupled receptors 65 (GPCR) (Robertson and Thomas, 2006; Vidal et al., 2018). This diversity of csGPCRs 66 allows the animal to discriminate between different odors. Thus, the specific expression 67 of any GPCR or combined expression of different GPCRs on a specific neuron or 68 different neurons can modulate the animal's perception towards the same odorant. 69The olfactory neurons that are involved in sensing a large number of attractive cues are 70 AWA and AWC. These two pairs of neurons are involved in showing chemotaxis to 71 various chemicals like diacetyl, isoamyl alcohol, pyrazine, benzaldehyde, and butanone 72 (Bargmann et al., 1993; Colbert et al., 1997; Troemel et al., 1995). The avoidance 73 behavior towards the repellents nonanone and 1-octanol is mediated through the 74 sensory neurons AWB...

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“…Day 2 adult worms were glued on the surface of Sylgard-coated coverslips using cyanoacrylate-based glue (Zou et al, 2017), and a dorsolateral incision was made using a sharp glass pipette to expose the body wall muscles for recording. Whole-cell recordings of ventral body wall muscles were carried out by a HEKA EPC10 amplifier using the Patchmaster software.…”

Section: Methodsmentioning

confidence: 99%

A Systematic RNAi Screen Reveals a Novel Role of a Spindle Assembly Checkpoint Protein BuGZ in Synaptic Transmission in C. elegans

Han

Zou

Chang

et al. 2017

Front. Mol. Neurosci.

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Synaptic vesicles (SV) store various neurotransmitters that are released at the synapse. The molecular mechanisms of biogenesis, exocytosis, and endocytosis for SV, however, remain largely elusive. In this study, using Complex Object Parametric Analysis and Sorter (COPAS) to monitor the fluorescence of synapto-pHluorin (SpH), we performed a whole-genome RNAi screen in C. elegans to identify novel genetic modulators in SV cycling. One hundred seventy six genes that up-regulating SpH fluorescence and 96 genes that down-regulating SpH fluorescence were identified after multi-round screen. Among these genes, B0035.1 (bugz-1) encodes ortholog of mammalian C2H2 zinc-finger protein BuGZ/ZNF207, which is a spindle assembly checkpoint protein essential for mitosis in human cells. Combining electrophysiology, imaging and behavioral assays, we reveal that depletion of BuGZ-1 results in defects in locomotion. We further demonstrate that BuGZ-1 promotes SV recycling by regulating the expression levels of endocytosis-related genes such as rab11.1. Therefore, we have identified a bunch of potential genetic modulators in SV cycling, and revealed an unexpected role of BuGZ-1 in regulating synaptic transmission.

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Polymodal Responses in C. elegans Phasmid Neurons Rely on Multiple Intracellular and Intercellular Signaling Pathways

Cited by 38 publications

References 28 publications

An atlas of Caenorhabditis elegans chemoreceptor expression

An atlas of Caenorhabditis elegans chemoreceptor expression

The G-protein coupled receptor SRX-97 is required for concentration dependent sensing of Benzaldehyde inCaenorhabditis elegans

A Systematic RNAi Screen Reveals a Novel Role of a Spindle Assembly Checkpoint Protein BuGZ in Synaptic Transmission in C. elegans

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