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

Cohn, Jesse; Cebul, Elizabeth R.; Valperga, Giulio; Brose, Lotti; Bono, Mario de; Heiman, Maxwell G.; Pierce, Jonathan T.

doi:10.1016/j.ydbio.2020.01.005

Cited by 8 publications

(5 citation statements)

References 48 publications

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“…Interestingly, the URX dendrite is not restricted to growing only by retrograde extension. The dendrite ending continues to grow in adults (Cohn et al, 2020). We previously identified a separate class of dendrite overgrowth mutants in which the URX dendrite forms normally during embryogenesis but then gets longer as the animal ages, ultimately wrapping around the nose and extending posteriorly along the head, up to 150% of its wild-type length (McLachlan et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Dendrites with specialized glial attachments develop by retrograde extension using SAX-7 and GRDN-1

2020

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Dendrites develop elaborate morphologies in concert with surrounding glia, but the molecules that coordinate dendrite and glial morphogenesis are mostly unknown. C. elegans offers a powerful model for identifying such factors. Previous work in this system examined dendrites and glia that develop within epithelia, similar to mammalian sense organs. Here, we focus on the neurons BAG and URX, which are not part of an epithelium but instead form membranous attachments to a single glial cell at the nose, reminiscent of dendrite-glia contacts in the mammalian brain. We show that these dendrites develop by retrograde extension, in which the nascent dendrite endings anchor to the presumptive nose and then extend by stretch during embryo elongation. Using forward genetic screens, we find that dendrite development requires the adhesion protein SAX-7/L1CAM and the cytoplasmic protein GRDN-1/CCDC88C to anchor dendrite endings at the nose. SAX-7 acts in neurons and glia, while GRDN-1 acts in glia to non-autonomously promote dendrite extension. Thus, this work shows how glial factors can help to shape dendrites, and identifies a novel molecular mechanism for dendrite growth by retrograde extension.

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Section: Discussionmentioning

confidence: 99%

Dendrites with specialized glial attachments develop by retrograde extension using SAX-7 and GRDN-1

2020

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“…2021 ). Sensory endings of ciliated dendrites also exhibit age-dependent remodeling, including increased complexity in URX, reduced complexity in AFD, and altered compartmentalization requirements in CEP ( Cohn et al . 2020 ; Huang et al .…”

Section: Ciliated Dendrites Not Ensheathed By Gliamentioning

confidence: 99%

Dendrite morphogenesis in Caenorhabditis elegans

Heiman,

Bülow

2024

Genetics

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Since the days of Ramón y Cajal, the vast diversity of neuronal and particularly dendrite morphology has been used to catalog neurons into different classes. Dendrite morphology varies greatly and reflects the different functions performed by different types of neurons. Significant progress has been made in our understanding of how dendrites form and the molecular factors and forces that shape these often elaborately sculpted structures. Here, we review work in the nematode Caenorhabditis elegans that has shed light on the developmental mechanisms that mediate dendrite morphogenesis with a focus on studies investigating ciliated sensory neurons and the highly elaborated dendritic trees of somatosensory neurons. These studies, which combine time-lapse imaging, genetics, and biochemistry, reveal an intricate network of factors that function both intrinsically in dendrites and extrinsically from surrounding tissues. Therefore, dendrite morphogenesis is the result of multiple tissue interactions, which ultimately determine the shape of dendritic arbors.

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“…The nematode Caenorhabditis elegans has been widely used as a model organism for studying neuron morphology 2,4,14 , connectivity 2,3,15 , plasticity [16][17][18][19][20][21] and activity 15,22,23 . While the majority of the population are hermaphrodites, loss of one X chromosome yields males [24][25][26] , which are sexually dimorphic in anatomy 27 , neuronal connectivity 4 , and behavior 24,28,29 .…”

Section: Introductionmentioning

confidence: 99%

The PVD neuron has male-specific structure and mating function inC. elegans

Iosilevskii,

Podbilewicz

2024

Preprint

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Neurons display unique shapes and establish intricate networks, which may differ between sexes. In complex organisms, studying sex differences in structure and function of individual neurons is difficult. The nematode Caenorhabditis elegans hermaphrodites and males present an exceptional model for studying neuronal morphogenesis in a simple, sexually-dimorphic system. We focus on the polymodal sensory bilateral neuron pair PVD, which forms a complex but stereotypic dendritic tree composed of multiple subunits that resemble candelabra. PVD was previously studied in hermaphrodites, but not in males. We find here that during larval development, male PVDs extend a similar architecture to the hermaphrodite utilizing a sexually-shared patterning mechanism. In early adulthood, however, male PVD develops a unique extension into the copulatory tail structure. This sexually-dimorphic arborization is absent in mutant backgrounds which perturb the sex-shared PVD guidance complex. SAX-7/L1CAM, a hypodermal component of this complex, shows a male-specific expression pattern which precedes PVD extension. Further, our results reveal that genetically altered arborization or ablation of the PVD result in male mating behavioral defects, particularly as males turn around the hermaphrodite. These results uncover an adult-stage sexual dimorphism of dendritic branching and uncover a new function for PVD in male sexual behavior.

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

Cited by 8 publications

References 48 publications

Dendrites with specialized glial attachments develop by retrograde extension using SAX-7 and GRDN-1

Dendrites with specialized glial attachments develop by retrograde extension using SAX-7 and GRDN-1

Dendrite morphogenesis in Caenorhabditis elegans

The PVD neuron has male-specific structure and mating function inC. elegans

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