The HMX/NKX homeodomain protein MLS-2 specifies the identity of the AWC sensory neuron type via regulation of the ceh-36 Otx gene in C. elegans

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.

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Faculty Opinions recommendation of Glia delimit shape changes of sensory neuron receptive endings in C. elegans.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.10236958.11029057 ◽

2011 ◽

Author(s):

Coleen Murphy ◽

Rachel Kaletsky

Keyword(s):

Sensory Neuron ◽

C Elegans ◽

Shape Changes

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Faculty Opinions recommendation of Neuron type-specific miRNA represses two broadly expressed genes to modulate an avoidance behavior in C. elegans.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.726790125.793525856 ◽

2016 ◽

Author(s):

Thorsten Hoppe ◽

Fabian Finger

Keyword(s):

Avoidance Behavior ◽

Neuron Type ◽

C Elegans

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

Developmental Biology ◽

10.1016/j.ydbio.2020.12.022 ◽

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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C. elegans unc-4 gene encodes a homeodomain protein that determines the pattern of synaptic input to specific motor neurons

Nature ◽

10.1038/355841a0 ◽

1992 ◽

Vol 355 (6363) ◽

pp. 841-845 ◽

Cited By ~ 88

Author(s):

David M. Miller ◽

Michael M. Shen ◽

Caroline E. Shamu ◽

Thomas R. Bürglin ◽

Gary Ruvkun ◽

...

Keyword(s):

Motor Neurons ◽

Synaptic Input ◽

Homeodomain Protein ◽

C Elegans

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Long-term activity drives dendritic branch elaboration of a C. elegans sensory neuron

10.1101/685339 ◽

2019 ◽

Author(s):

Jesse A Cohn ◽

Elizabeth R Cebul ◽

Giulio Valperga ◽

Mario de Bono ◽

Maxwell G Heiman ◽

...

Keyword(s):

Sensory Neuron ◽

Neuronal Activity ◽

Morphological Changes ◽

Model Organism ◽

Neuronal Morphology ◽

Sensory Transduction ◽

Central Component ◽

C Elegans ◽

Activity Dependent

ABSTRACTNeuronal activity often leads to alterations in gene expression and cellular architecture. The nematode Caenorhabditis elegans, owing to its compact translucent nervous system, is a powerful system in which to study conserved aspects of the development and plasticity of neuronal morphology. Here we focus on one sensory neuron in the worm, termed URX, which senses oxygen and signals tonically proportional to environmental oxygen. Previous studies have reported that URX has variable branched endings at its dendritic sensory tip. By controlling oxygen levels and analyzing mutants, we found that these branched endings grow over time as a consequence of neuronal activity. Furthermore, we observed that the branches contain microtubules, but do not appear to harbor the guanylyl cyclase GCY-35, a central component of the oxygen sensory transduction pathway. Interestingly, we found that although URX dendritic tips grow branches in response to long-term activity, the degree of branch elaboration does not correlate with oxygen sensitivity at the cellular or the behavioral level. Given the strengths of C. elegans as a model organism, URX may serve as a potent system for uncovering genes and mechanisms involved in activity-dependent morphological changes in neurons.

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Odor-dependent temporal dynamics in C. elegans odor memory

10.7287/peerj.preprints.26451v1 ◽

2018 ◽

Author(s):

Jae Im Choi ◽

Hee Kyung Lee ◽

Hae Su Kim ◽

So Young Park ◽

Kyoung-hye Yoon ◽

...

Keyword(s):

Sensory Neuron ◽

Temporal Dynamics ◽

Memory Formation ◽

Nuclear Accumulation ◽

C Elegans ◽

Odor Memory ◽

Dependent Protein ◽

Enormous Number ◽

Specific Odor ◽

Over Time

Animals sense an enormous number of cues in their environments, and, over time, can form memories and associations to some of these. The nervous system remarkably maintains the specificity of memory to each of the cues. Here we asked whether the nematode Caenorhabditis elegans adjusts the temporal dynamics of odor memory formation depending on the specific odor sensed. C. elegans senses a multitude of odors, and memory formation to some of these odors requires activity of the cGMP-dependent protein kinase EGL-4 in the AWC sensory neuron. We identified a panel of 17 attractive odors, some of which have not been tested before, and determined that the majority of these odors require the AWC primary sensory neuron for sensation. We then devised a novel assay to assess odor behavior over time for a single population of animals. We used this assay to evaluate the temporal dynamics of memory formation to 13 odors and find that memory formation occurs early in some odors and later in others. We then examined EGL-4 localization in early-trending and late-trending odors over time and found that the timing of memory formation correlated with the timing of nuclear accumulation of EGL-4 in the AWC neuron. We demonstrate that odor memory formation in C. elegans can be used as a model to study the timing of memory formation to different sensory cues.

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xbx-4, a homolog of the Joubert syndrome gene FAM149B1, acts via the CCRK and MAK kinase cascade to regulate cilia morphology

10.1101/2021.05.09.443182 ◽

2021 ◽

Author(s):

Ashish K Maurya ◽

Piali Sengupta

Keyword(s):

Sensory Neuron ◽

Mammalian Cells ◽

Primary Cilia ◽

Cell Types ◽

Joubert Syndrome ◽

C Elegans ◽

Kinase Cascade ◽

Multiple Cell ◽

Kinase Pathway ◽

Sensory Functions

Primary cilia are microtubule (MT)-based organelles that mediate sensory functions in multiple cell types. Disruption of cilia structure or function leads to a diverse collection of diseases termed ciliopathies. Mutations in the DUF3719 domain-containing protein FAM149B1 have recently been shown to elongate cilia via unknown mechanisms and result in the ciliopathy Joubert syndrome. The highly conserved CCRK and MAK/RCK kinases negatively regulate cilia length and structure in Chlamydomonas, C. elegans, and mammalian cells. How the activity of this kinase cascade is tuned to precisely regulate cilia architecture is unclear. Here we identify XBX-4, a DUF3719 domain-containing protein related to human FAM149B1, as a novel regulator of the DYF-18 CCRK and DYF-5 MAK kinase pathway in C. elegans. As in dyf-18 and dyf-5 mutants, sensory neuron cilia are elongated in xbx-4 mutants and exhibit altered axonemal MT stability. XBX-4 promotes DYF-18 CCRK activity to regulate DYF-5 MAK function and localization. We find that Joubert syndrome-associated mutations in the XBX-4 DUF3719 domain also elongate cilia in C. elegans. Our results identify a new metazoan-specific regulator of this highly conserved kinase pathway, and suggest that FAM149B1 may similarly act via the CCRK/MAK kinase pathway to regulate ciliary homeostasis in humans.

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