Skin-Derived Cues Control Arborization of Sensory Dendrites in Caenorhabditis elegans

Salzberg, Yehuda; Díaz-Balzac, Carlos A.; Ramírez-Suárez, Nelson J.; Attreed, Matthew; Tecle, Eillen; Desbois, Muriel; Kaprielian, Zaven; Bülow, Hannes E.

doi:10.1016/j.cell.2013.08.058

Cited by 156 publications

(242 citation statements)

References 46 publications

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“…Thus, one plausible model for Raw function in dendrite development is that it interacts with an extracellular signal, which might be a component of the ECM or a cell surface protein on epithelial cells, and signals together with a co-receptor to stimulate downstream pathways for adhesion and cytoskeletal remodeling. Several analogous signaling systems involving interactions with the epidermis that influence terminal dendrite or sensory axon patterning have been described (Chiang et 2012; Salzberg et al, 2013), but how many of these signaling systems are at work in a given neuron, and how Raw interfaces with other signaling pathways, remain to be determined. Although Raw has no obvious vertebrate counterpart, stretches of the ECD bear similarity to mucins and leucine-rich repeat proteins, one of which might serve an analogous function.…”

Section: Discussionmentioning

confidence: 99%

Coordinate control of terminal dendrite patterning and dynamics by the membrane protein Raw

et al. 2015

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The directional flow of information in neurons depends on compartmentalization: dendrites receive inputs whereas axons transmit them. Axons and dendrites likewise contain structurally and functionally distinct subcompartments. Axon/dendrite compartmentalization can be attributed to neuronal polarization, but the developmental origin of subcompartments in axons and dendrites is less well understood. To identify the developmental bases for compartment-specific patterning in dendrites, we screened for mutations that affect discrete dendritic domains in Drosophila sensory neurons. From this screen, we identified mutations that affected distinct aspects of terminal dendrite development with little or no effect on major dendrite patterning. Mutation of one gene, raw, affected multiple aspects of terminal dendrite patterning, suggesting that Raw might coordinate multiple signaling pathways to shape terminal dendrite growth. Consistent with this notion, Raw localizes to branch-points and promotes dendrite stabilization together with the Tricornered (Trc) kinase via effects on cell adhesion. Raw independently influences terminal dendrite elongation through a mechanism that involves modulation of the cytoskeleton, and this pathway is likely to involve the RNA-binding protein Argonaute 1 (AGO1), as raw and AGO1 genetically interact to promote terminal dendrite growth but not adhesion. Thus, Raw defines a potential point of convergence in distinct pathways shaping terminal dendrite patterning.

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Section: Discussionmentioning

confidence: 99%

Coordinate control of terminal dendrite patterning and dynamics by the membrane protein Raw

et al. 2015

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“…Indeed, ectopic expression of lin-29 in the intestine rescues the vitellogenesis defects in the lin-29 mutant, suggesting that LIN-29 may directly activate expression of a soluble intertissue signaling molecule that is perceived by intestinal cells. Interestingly, proper migration of the hermaphrodite-specific neurons and arborization of the sensory dendrites during development are mediated by hypodermal expressed cell surface receptors or adhesion molecules, further underscoring the role of the hypodermis in non-cell-autonomous developmental regulation (Pedersen et al 2013;Salzberg et al 2013).…”

Section: Discussionmentioning

confidence: 99%

A microRNA program in the C. elegans hypodermis couples to intestinal mTORC2/PQM-1 signaling to modulate fat transport

et al. 2016

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Animals integrate metabolic, developmental, and environmental information before committing key resources to reproduction. In Caenorhabditis elegans, adult animals transport fat from intestinal cells to the germline to promote reproduction. We identified a microRNA (miRNA)-regulated developmental timing pathway that functions in the hypodermis to nonautonomously coordinate the mobilization of intestinal fat stores to the germline upon initiation of adulthood. This developmental timing pathway, which is controlled by the lin-4 and let-7 miRNAs, engages mTOR signaling in the intestine. The intestinal signaling component is specific to mTORC2 and functions in parallel to the insulin pathway to modulate the activity of the serum/glucocorticoid-regulated kinase (SGK-1). Surprisingly, SGK-1 functions independently of DAF-16/FoxO; instead, SGK-1 promotes the cytoplasmic localization of the PQM-1 transcription factor, which antagonizes intestinal fat mobilization at the transcriptional level when localized to the nucleus. These results revealed that a non-cell-autonomous developmental input regulates intestinal fat metabolism by engaging mTORC2 signaling to promote the intertissue transport of fat reserves from the soma to the germline.

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“…1A) (Oren-Suissa et al, 2010). These dendritic trees arise and are dynamically maintained through several intrinsic and extrinsic genetic pathways (Chatzigeorgiou et al, 2010;Cohen et al, 2014;Dong et al, 2013Dong et al, , 2015Husson et al, 2012;Liu and Shen, 2011;Maniar et al, 2012;Oren-Suissa et al, 2010;Salzberg et al, 2013;Smith et al, 2010;Wei et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

AFF-1 fusogen can rejuvenate the regenerative potential of adult dendritic trees via self-fusion

2017

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The aging brain undergoes structural changes that affect brain homeostasis, neuronal function and consequently cognition. The complex architecture of dendritic arbors poses a challenge to understanding age-dependent morphological alterations, behavioral plasticity and remodeling following brain injury. Here, we use the PVD polymodal neurons of C. elegans as a model to study how aging affects neuronal plasticity. Using confocal live imaging of C. elegans PVD neurons, we demonstrate age-related progressive morphological alterations of intricate dendritic arbors. We show that mutations in daf-2, which encodes an insulin-like growth factor receptor ortholog, fail to inhibit the progressive morphological aging of dendrites and do not prevent the minor decline in response to harsh touch during aging. We uncovered that PVD aging is characterized by a major decline in the regenerative potential of dendrites following experimental laser dendrotomy. Furthermore, the remodeling of transected dendritic trees by AFF-1-mediated self-fusion can be restored in old animals by daf-2 mutations, and can be differentially re-established by ectopic expression of the fusion protein AFF-1. Thus, ectopic expression of the fusogen AFF-1 in the PVD and mutations in daf-2 differentially rejuvenate some aspects of dendritic regeneration following injury.

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Skin-Derived Cues Control Arborization of Sensory Dendrites in Caenorhabditis elegans

Cited by 156 publications

References 46 publications

Coordinate control of terminal dendrite patterning and dynamics by the membrane protein Raw

Coordinate control of terminal dendrite patterning and dynamics by the membrane protein Raw

A microRNA program in the C. elegans hypodermis couples to intestinal mTORC2/PQM-1 signaling to modulate fat transport

AFF-1 fusogen can rejuvenate the regenerative potential of adult dendritic trees via self-fusion

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