Ethanol Stimulates Locomotion via a Gαs-Signaling Pathway in IL2 Neurons in<i>Caenorhabditis elegans</i>

Johnson, James R.; Edwards, Mark; Davies, Huw C.; Newman, D; Holden, Whitney; Jenkins, Rosalind E.; Burgoyne, Robert D.; Lucas, Robert J.; Barclay, Jeff W.

doi:10.1534/genetics.117.300119

Cited by 15 publications

(13 citation statements)

References 89 publications

(172 reference statements)

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“…Functionally, IL2 cilia are required for the nictation behavior of dauer larvae (Lee et al, 2011). In adult hermaphrodites, IL2 neurons are required and sufficient for stimulatory action of ethanol on locomotion (Johnson et al, 2017). This effect is blocked in several ciliary mutants (Dr. J. Barclay, pers.…”

Section: Discussionmentioning

confidence: 99%

Cell type‐specific structural plasticity of the ciliary transition zone in C. elegans

Akella

Silva

Morsci³

et al. 2019

Biology of the Cell

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Background information The current consensus on cilia development posits that the ciliary transition zone (TZ) is formed via extension of nine centrosomal microtubules. In this model, TZ structure remains unchanged in microtubule number throughout the cilium life cycle. This model does not however explain structural variations of TZ structure seen in nature, and could also lend itself to the misinterpretation that deviations from nine-doublet microtubule ultrastructure represent an abnormal phenotype. Thus, a better understanding of events that occur at the TZ in vivo during metazoan development is required. Results To address this issue, we characterized ultrastructure of two types of sensory cilia in developing Caenorhabditis elegans. We discovered that, in cephalic male (CEM) and inner labial quadrant (IL2Q) sensory neurons, ciliary TZs are structurally plastic and remodel from one structure to another during animal development. The number of microtubules doublets forming the TZ can be increased or decreased over time, depending on cilia type. Both cases result in structural TZ intermediates different from TZ in cilia of adult animals. In CEM cilia, axonemal extension and maturation occurs concurrently with TZ structural maturation. Conclusions and Significance Our work extends the current model to include the structural plasticity of metazoan transition zone, which can be structurally delayed, maintained or remodeled in cell type-specific manner.

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Section: Discussionmentioning

confidence: 99%

Cell type‐specific structural plasticity of the ciliary transition zone in C. elegans

Akella

Silva

Morsci³

et al. 2019

Biology of the Cell

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“…The 27 EVNs regulate behaviors important to mating and potentially survival. CEM neurons sense mating pheromones and are required for male attraction behavior toward adult hermaphrodites (Srinivasan et al, 2008; White et al, 2007); the IL2 neurons are important for locomotion changes in response to ethanol stimulation in adults, and for a dispersal behavior termed nictation in dauer stage larva (Johnson et al., 2017; Lee et al., 2011); the RnB neurons are important for response to hermaphrodites; the HOB neuron is important for location of the hermaphrodite vulva (Barr & Garcia, 2006). Similar to EVNs, environmentally released EVs also regulate mating behaviors.…”

Section: Extracellular Vesicle (Ev) Releasing Abilities Are Limited To a Subset Of Ciliated Neurons And Are An Aspect Of Neuronal Functiomentioning

confidence: 99%

The tubulin code specializes neuronal cilia for extracellular vesicle release

Akella

Barr

2020

Developmental Neurobiology

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Cilia are microtubule‐based organelles that display diversity in morphology, ultrastructure, protein composition, and function. The ciliary microtubules of C. elegans sensory neurons exemplify this diversity and provide a paradigm to understand mechanisms driving ciliary specialization. Only a subset of ciliated neurons in C. elegans are specialized to make and release bioactive extracellular vesicles (EVs) into the environment. The cilia of extracellular vesicle releasing neurons have distinct axonemal features and specialized intraflagellar transport that are important for releasing EVs. In this review, we discuss the role of the tubulin code in the specialization of microtubules in cilia of EV releasing neurons.

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“…Extracellular vesicle releasing neurons (EVNs) are comprised of 21 male-specific and six sex-shared ciliated neurons that possess the remarkable ability to shed and release ciliary extracellular vesicles (EVs) into the environment or extracellular space that are involved in animal-to-animal communication (Figure 1B) (Wang et al, 2014). The six sex-shared inner labial type 2 (IL2) neurons are involved in alcohol sensing, nictation behavior, and sensing blue light (Johnson et al, 2017;Lee et al, 2011;Zaslaver et al, 2015). The IL2 neurons have no known function in mating behavior.…”

Section: A Class Of Neurons With Sex-shared and Sex-specific Implications In Behavior And Physiology: The Ciliary Extracellular Vesicle Rmentioning

confidence: 99%

What about the males? the C. elegans sexually dimorphic nervous system and a CRISPR-based tool to study males in a hermaphroditic species

Walsh

Boivin

Barr

2020

Journal of Neurogenetics

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Sexual dimorphism is a device that supports genetic diversity while providing selective pressure against speciation. This phenomenon is at the core of sexually reproducing organisms. Caenorhabditis elegans provides a unique experimental system where males exist in a primarily hermaphroditic species. Early works of John Sulson, Robert Horvitz, and John White provided a complete map of the hermaphrodite nervous system, and recently the male nervous system was added. This addition completely realized the vision of C. elegans pioneer Sydney Brenner: a model organism with an entirely mapped nervous system. With this 'connectome' of information available, great strides have been made toward understanding concepts such as how a sex-shared nervous system (in hermaphrodites and males) can give rise to sex-specific functions, how neural plasticity plays a role in developing a dimorphic nervous system, and how a shared nervous system receives and processes external cues in a sexually-dimorphic manner to generate sex-specific behaviors. In C. elegans, the intricacies of male-mating behavior have been crucial for studying the function and circuitry of the male-specific nervous system and used as a model for studying human autosomal dominant polycystic kidney disease (ADPKD). With the emergence of CRISPR, a seemingly limitless tool for generating genomic mutations with pinpoint precision, the C. elegans model system will continue to be a useful instrument for pioneering research in the fields of behavior, reproductive biology, and neurogenetics.

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Ethanol Stimulates Locomotion via a Gαs-Signaling Pathway in IL2 Neurons inCaenorhabditis elegans

Abstract: Alcohol abuse is among the top causes of preventable death, generating considerable financial, health, and societal burdens. Paradoxically, alcohol...

Cited by 15 publications

References 89 publications

Cell type‐specific structural plasticity of the ciliary transition zone in C. elegans

Cell type‐specific structural plasticity of the ciliary transition zone in C. elegans

The tubulin code specializes neuronal cilia for extracellular vesicle release

What about the males? the C. elegans sexually dimorphic nervous system and a CRISPR-based tool to study males in a hermaphroditic species

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