Sexual Dimorphism and Sex Differences in <i>Caenorhabditis elegans</i> Neuronal Development and Behavior

Barr, Maureen M.; García, L. René; Portman, Douglas S.

doi:10.1534/genetics.117.300294

Cited by 72 publications

(87 citation statements)

References 228 publications

(305 reference statements)

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“…C. elegans male mating involves stereotyped behavior steps including response to hermaphrodite contact, location of the hermaphrodite's vulva, spicule insertion, and sperm transfer to the hermaphrodite's uterus [7]. To examine male-hermaphrodite EV interactions during mating, we paired fluorescently labeled transgenic adult males with unlabeled adult hermaphrodites ( Figure 1A).…”

Section: Resultsmentioning

confidence: 99%

“…The mechanoresponsive nature of the EV release suggests a similar cue may function during male-hermaphrodite mating in vivo. The success of vulva location depends on proper localization of PKD-2 to the sensory cilia of male-specific EV-releasing neurons [7,9]. Transcriptional profiling of these EVreleasing neurons revealed enrichment with transcripts encoding a large variety of adhesive membrane proteins [10].…”

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confidence: 99%

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Polycystin-2 ciliary extracellular vesicle release and targeting

Wang¹,

Nikonorova²,

Gu³

et al. 2020

Preprint

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Extracellular vesicles (EVs) are emerging as a universal means of cell-to-cell communication and hold great potential in diagnostics and regenerative therapies [1]. The urgent need of the field is precise understanding of physiological mechanisms driving EV generation and function. Ciliary EVs act as signaling devices in Chlamydomonas and C. elegans [2][3][4]. Mammalian cilia shed EVs to eliminate unwanted receptors [5] or in the process of cilia retraction when cultured cells enter the cell cycle [6]. Here we used our established C. elegans model to study sensory-evoked ciliary EV release and targeting using a fluorescently labeled EV cargo polycystin-2 (PKD-2). In C. elegans and mammals, the Autosomal Dominant Polycystic Kidney Disease (ADPKD) gene products polycystin-1 and polycystin-2 localize to both cilia and EVs, act in the same genetic pathway, and function in a sensory capacity, suggesting ancient conservation. We find that males deposit PKD-2::GFP-carrying EVs onto the vulva of the hermaphrodite during mating. We also show that mechanical stimulation triggers release of PKD-2::GFP-carrying EVs from cilia. To our knowledge this is the first report of mechanoresponsive nature of the ciliary EV release and of ciliary EV directional transfer from one animal to another animal. Since the polycystins are evolutionary conserved ciliary EV cargoes, our findings suggest that similar mechanisms for EV release and targeting may occur in other animals. ResultsC. elegans male mating involves stereotyped behavior steps including response to hermaphrodite contact, location of the hermaphrodite's vulva, spicule insertion, and sperm transfer to the hermaphrodite's uterus [7]. To examine male-hermaphrodite EV interactions during mating, we paired fluorescently labeled transgenic adult males with unlabeled adult hermaphrodites ( Figure 1A). Male sperm transfer was visualized with MitoTracker dye and ciliary EVs were tracked via the PKD-2::GFP EV cargo protein. After mating, we scored the hermaphrodite uterus for the presence of MitoTracker labeled male sperm. In all inseminated hermaphrodites, we observed highly localized deposition of the male-specific PKD-2-carrying EVs along the hermaphrodite vulva ( Figure 1B-C). These data demonstrate that the male directly transferred PKD-2::GFP-carrying EVs to the hermaphrodite during mating. The location of the male-deposited EVs at the hermaphrodite's vulva is consistent with the position of male

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Polycystin-2 ciliary extracellular vesicle release and targeting

Wang¹,

Nikonorova²,

Gu³

et al. 2020

Preprint

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“…The coordinated execution of innate, stereotyped sexual behaviours, such as courtship and mating, requires sexually dimorphic sensory-motor circuits that are genetically specified during development (reviewed in [1][2][3]. Studies in the nematode Caenorhabditis elegans, in which the development and function of neural circuits can be interrogated with single cell resolution, have revealed two general developmental mechanisms underlying sexual dimorphism in the nervous system.…”

Section: Introductionmentioning

confidence: 99%

“…Sex-specific neurons are primarily involved in controlling distinct aspects of reproductive behaviours, such as egg-laying in the hermaphrodite and mating in the male (reviewed in 15 ). Generation of sex-specific neurons requires sex-specific cell death 16 or neurogenesis events resulting from sex differences in the cell division patterns and neurodevelopmental programmes of post-embryonic cell lineages (reviewed in 3 ). Here we identify a third, novel way to generate sexual dimorphism in the nervous system.…”

Section: Introductionmentioning

confidence: 99%

A direct glia-to-neuron natural transdifferentiation ensures nimble sensory-motor coordination of male mating behaviour

García

Kim²,

Cook

et al. 2018

Preprint

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Sexually dimorphic behaviours require underlying differences in the nervous system between males and females. The extent to which nervous systems are sexually dimorphic and the cellular and molecular mechanisms that regulate these differences are only beginning to be understood. We reveal here a novel mechanism to generate male-specific neurons in Caenorhabditis elegans, through the direct transdifferentiation of sex-shared glial cells. This glia-to-neuron cell fate switch occurs during male sexual maturation under the cell-autonomous control of the sex-determination pathway. We show that the neurons generated are cholinergic, peptidergic and ciliated putative proprioceptors which integrate into male-specific circuits for copulation. These neurons ensure coordinated backward movement along the mate's body during mating. One step of the mating sequence regulated by these neurons is an alternative readjustment movement performed when intromission becomes difficult to achieve. Our findings reveal programmed transdifferentiation as a developmental mechanism underlying flexibility in innate behaviour.

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“…Consistent with their non-volatile nature, ascarosides are not sensed by the olfactory neurons AWA, but by a distinct set of chemosensory neurons with exposed sensory endings, including the male-specific CEM neurons and the sex-shared ADL, ASK, and ADF neurons [5,10]. Responses to ascarosides often depend on sex-specific perception (e.g., by the male-specific CEM neurons or by the sex-specific activation of a sex-shared neuron), but there are also downstream, circuit-based mechanisms that control the sex-specificity of behavioral responses [5,10]. Taken together, worms generate sexspecific pheromone responses through a number of distinct mechanisms, ranging from sex-specific sensory neuron activation Only wild-type C. elegans males but not hermaphrodites get attracted to volatile sex pheromones (VSP) derived from self sperm-depleted hermaphrodite C. elegans or female Caenorhabditis remanei.…”

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confidence: 99%

Sex‐specific pheromone responses in Caenorhabditis elegans

Wang

Hobert

2019

EMBO Reports

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The characterization of receptors for sex pheromones provides important clues for understanding the mechanisms controlling animal mating and reproduction. In this issue, Wan et al identify a putative sex pheromone receptor, the G protein‐coupled receptor SRD‐1, acting in a single Caenorhabditis elegans olfactory neuron class, called AWA, to mediate male attraction to volatile sex pheromones. Like in other systems, C. elegans sex pheromone elicits sex‐specific responses even though sex pheromone activates sensory neurons of both sexes.

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Sexual Dimorphism and Sex Differences in Caenorhabditis elegans Neuronal Development and Behavior

Cited by 72 publications

References 228 publications

Polycystin-2 ciliary extracellular vesicle release and targeting

Polycystin-2 ciliary extracellular vesicle release and targeting

A direct glia-to-neuron natural transdifferentiation ensures nimble sensory-motor coordination of male mating behaviour

Sex‐specific pheromone responses in Caenorhabditis elegans

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