Receptor tyrosine phosphatase CLR-1 acts in skin cells to promote sensory dendrite outgrowth

Liu, Xianzhuang; Wang, Xiangming; Shen, Kang

doi:10.1016/j.ydbio.2016.03.001

Cited by 15 publications

(15 citation statements)

References 23 publications

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“…For example, our sense of touch is mediated by mechanosensory neurons that branch along the basal ("inner") side of the skin epithelium. The skin plays a major role in shaping these sensory neurons, and these epithelia-neuron interactions have been extensively studied in vertebrates (Wang et al, 2013;Zimmerman et al, 2014), Drosophila (Parrish et al, 2009;Han et al, 2012;Kim et al, 2012;Jiang et al, 2014;Tenenbaum et al, 2017), and C. elegans (Dong et al, 2013;Liang et al, 2015;Díaz-Balzac et al, 2016;Liu et al, 2016;Zou et al, 2016;Zhu et al, 2017;Celestrin et al, 2018). Similarly, our senses of hearing and taste are mediated by afferent neurons that are positioned at the basal surfaces of epithelia and receive information from specialized non-neuronal sensory cells (hair cells, taste cells) within these epithelia (Roper, 2013;Frank and Goodrich, 2018).…”

Section: Introductionmentioning

confidence: 99%

Morphogenesis of neurons and glia within an epithelium

Low

Williams

Chong

et al. 2018

Preprint

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To sense the outside world, some neurons protrude across epithelia, the cellular barriers that line every surface of our bodies. To study the morphogenesis of such neurons, we examined the C. elegans amphid, in which dendrites protrude through a glial channel at the nose. During development, amphid dendrites extend by attaching to the nose via DYF-7, a type of protein typically found in epithelial apical ECM. Here, we show that amphid neurons and glia exhibit epithelial properties, including tight junctions and apical-basal polarity, and develop in a manner resembling other epithelia. We find that DYF-7 is a fibril-forming apical ECM component that prevents rupture of the tube-shaped glial channel, reminiscent of roles for apical ECM in other narrow epithelial tubes. We also identify a role for FRM-2, a homolog of EPBL15/moe/Yurt which promote epithelial integrity in other systems. Finally, we show that other environmentally-exposed neurons share a requirement for DYF-7. Together, our results suggest that these neurons and glia can be viewed as part of an epithelium continuous with the skin, and are shaped by mechanisms shared with other epithelia.

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Section: Introductionmentioning

confidence: 99%

Morphogenesis of neurons and glia within an epithelium

Low

Williams

Chong

et al. 2018

Preprint

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“…Fig. 3E-G) (Dong et al, 2013;Islam et al, 2003;Liu et al, 2016;Salzberg et al, 2013). As a further specificity control, we examined a second allele of sax-7, eq1, and observed similar defects to sax-7(ky146) (Supp.…”

Section: Amphid Dendrites In Ptp-3/lar and Sax-7/l1cam Mutants Exhibimentioning

confidence: 86%

Ordered arrangement of dendrites within aC. eleganssensory nerve bundle

Yip

Heiman

2018

Preprint

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Biological systems are organized into well-ordered structures and can evolve new patterns when perturbed. To identify principles underlying biological order, we turned to C. elegans for its simple anatomy and powerful genetics. We developed a method to quantify the arrangement of three dendrites in the main sensory nerve bundle, and found that they exhibit a stereotyped arrangement throughout larval growth. Dendrite order does not require prominent features including sensory cilia and glial junctions. In contrast, loss of the cell adhesion molecule (CAM) CDH-4/Fat-like cadherin causes dendrites to be ordered randomly, despite remaining bundled.Loss of the CAMs PTP-3/LAR or SAX-7/L1CAM causes dendrites to adopt an altered order, which becomes increasingly random as animals grow. Misexpression of SAX-7 leads to subtle but reproducible changes in dendrite order. Our results suggest that differential expression of CAMs allows dendrites to self-organize into a stereotyped arrangement that readily gives rise to new patterns when perturbed.

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“…Dendrite morphogenesis has been studied in C. elegans in the context of branching (PVD, FLP, and IL neurons) and DYF-7-mediated retrograde extension (ciliated sensory neurons of the amphid) [12][13][14][15][16][17][18][19][20][21][22][23]30,63]. Here, we show that URX offers a complementary model of dendrite morphogenesis that provides new mechanistic insights.…”

Section: Age-dependent Dendrite Remodelingmentioning

confidence: 90%

“…While C. elegans has been used extensively as a model for axon development [11], considerably less attention has been paid to its dendrites. Most of the work has focused on interesting sensory neurons with complex branched dendrites, and has revealed mechanisms of dendritic branch formation and spacing [12][13][14][15][16][17][18][19][20][21][22][23], dendritic self-avoidance [24], and even dendrite tiling [25]. By comparison, dendrites with simple unbranched morphologies have been used as a model for understanding axon-dendrite polarity [26,27].…”

Section: Introductionmentioning

confidence: 99%

A neuronal MAP kinase constrains growth of aC. eleganssensory dendrite throughout the life of the organism

McLachlan

Beets

Bono

et al. 2018

Preprint

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Neurons develop elaborate morphologies that provide a model for understanding cellular architecture. By studying C. elegans sensory dendrites, we previously identified genes that act to promote the extension of ciliated sensory dendrites during embryogenesis. Interestingly, the nonciliated dendrite of the oxygensensing neuron URX is not affected by these genes, suggesting it develops through a distinct mechanism.Here, we use a visual forward genetic screen to identify mutants that affect URX dendrite morphogenesis.We find that disruption of the MAP kinase MAPK-15 or the β H -spectrin SMA-1 causes a phenotype opposite to what we had seen before: dendrites extend normally during embryogenesis but begin to overgrow as the animals reach adulthood, ultimately extending up to 150% of their normal length. SMA-1 is broadly expressed and acts non-cell-autonomously, while MAPK-15 is expressed in many sensory neurons including URX and acts cell-autonomously. MAPK-15 acts at the time of overgrowth, localizes at the dendrite ending, and requires its kinase activity, suggesting it acts locally in time and space to constrain dendrite growth. Finally, we find that the oxygen-sensing guanylate cyclase GCY-35, which normally localizes at the dendrite ending, is localized throughout the overgrown region, and that overgrowth can be suppressed by overexpressing GCY-35 or by genetically mimicking elevated cGMP signaling. These results suggest that overgrowth may correspond to expansion of a sensory compartment at the dendrite ending, reminiscent of the remodeling of sensory cilia or dendritic spines. Thus, in contrast to established pathways that promote dendrite growth during early development, our results reveal a distinct mechanism that constrains dendrite growth throughout the life of the animal, possibly by controlling the size of a sensory compartment at the dendrite ending.

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Receptor tyrosine phosphatase CLR-1 acts in skin cells to promote sensory dendrite outgrowth

Cited by 15 publications

References 23 publications

Morphogenesis of neurons and glia within an epithelium

Morphogenesis of neurons and glia within an epithelium

Ordered arrangement of dendrites within aC. eleganssensory nerve bundle

A neuronal MAP kinase constrains growth of aC. eleganssensory dendrite throughout the life of the organism

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