Adhesive L1CAM-Robo Signaling Aligns Growth Cone F-Actin Dynamics to Promote Axon-Dendrite Fasciculation in C. elegans

Chen, Chun‐Hao; Hsu, Hao-Wei; Chang, Yun-Hsuan; Pan, Chih-Hong

doi:10.1016/j.devcel.2018.10.028

Cited by 29 publications

(16 citation statements)

References 44 publications

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“…PVD-specific expression of mCherry-tagged UNC-34 protein rescued this Unc-34 mutant phenotype suggesting that unc-34 function is cell-autonomous for the self-avoidance response (Fig 3C). unc-34 mutant 1° and 2° branch defects were not rescued by PVD expression of UNC-34, however, which could be indicative of an additional UNC-34 function in nearby cell types that influence PVD morphogenesis (Fig 3B, S2 Fig) [35,36]. Thus, our results suggest that UNC-34/Ena/VASP is selectively required in PVD neurons for dendrite retraction in the self-avoidance response but not for dendrite outgrowth.…”

Section: Resultsmentioning

confidence: 79%

Actin assembly and non-muscle myosin activity drive dendrite retraction in an UNC-6/Netrin dependent self-avoidance response

et al. 2019

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Dendrite growth is constrained by a self-avoidance response that induces retraction but the downstream pathways that balance these opposing mechanisms are unknown. We have proposed that the diffusible cue UNC-6(Netrin) is captured by UNC-40(DCC) for a short-range interaction with UNC-5 to trigger self-avoidance in the C . elegans PVD neuron. Here we report that the actin-polymerizing proteins UNC-34(Ena/VASP), WSP-1(WASP), UNC-73(Trio), MIG-10(Lamellipodin) and the Arp2/3 complex effect dendrite retraction in the self-avoidance response mediated by UNC-6(Netrin). The paradoxical idea that actin polymerization results in shorter rather than longer dendrites is explained by our finding that NMY-1 (non-muscle myosin II) is necessary for retraction and could therefore mediate this effect in a contractile mechanism. Our results also show that dendrite length is determined by the antagonistic effects on the actin cytoskeleton of separate sets of effectors for retraction mediated by UNC-6(Netrin) versus outgrowth promoted by the DMA-1 receptor. Thus, our findings suggest that the dendrite length depends on an intrinsic mechanism that balances distinct modes of actin assembly for growth versus retraction.

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Section: Resultsmentioning

confidence: 79%

Actin assembly and non-muscle myosin activity drive dendrite retraction in an UNC-6/Netrin dependent self-avoidance response

et al. 2019

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“…The presence of FLP body wall branches that extend from both the lateral and dorso-ventral midlines appears intermediate between the PVD and IL2 branching patterns. Neurite formation has long been known to be shaped by surrounding tissues [ 26 – 28 , 36 , 59 , 60 ]. The primary dendrites of the PVDs fasciculate with the relatively sparsely populated lateral nerve containing only 2–3 other neurons [ 61 ].…”

Section: Discussionmentioning

confidence: 99%

Mutually exclusive dendritic arbors in C. elegans neurons share a common architecture and convergent molecular cues

et al. 2020

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Stress-induced changes to the dendritic architecture of neurons have been demonstrated in numerous mammalian and invertebrate systems. Remodeling of dendrites varies tremendously among neuron types. During the stress-induced dauer stage of Caenorhabditis elegans, the IL2 neurons arborize to cover the anterior body wall. In contrast, the FLP neurons arborize to cover an identical receptive field during reproductive development. Using timecourse imaging, we show that branching between these two neuron types is highly coordinated. Furthermore, we find that the IL2 and FLP arbors have a similar dendritic architecture and use an identical downstream effector complex to control branching; however, regulation of this complex differs between stress-induced IL2 branching and FLP branching during reproductive development. We demonstrate that the unfolded protein response (UPR) sensor IRE-1, required for localization of the complex in FLP branching, is dispensable for IL2 branching at standard cultivation temperatures. Exposure of ire-1 mutants to elevated temperatures results in defective IL2 branching, thereby demonstrating a previously unknown genotype by environment interaction within the UPR. We find that the FOXO homolog, DAF-16, is required cell-autonomously to control arborization during stress-induced arborization. Likewise, several aspects of the dauer formation pathway are necessary for the neuron to remodel, including the phosphatase PTEN/DAF-18 and Cytochrome P450/DAF-9. Finally, we find that the TOR associated protein, RAPTOR/DAF-15 regulates mutually exclusive branching of the IL2 and FLP dendrites. DAF-15 promotes IL2 branching during dauer and inhibits precocious FLP growth. Together, our results shed light on molecular processes that regulate stress-mediated remodeling of dendrites across neuron classes.

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“…Direct contact-dependent adhesion to an attractive cue was recently demonstrated in C. elegans and underlies the construction of a sensory circuit responding to harsh mechanical stimuli (Chen et al, 2019). Primary dendrites of the enormous PVD neuron adhere to and migrate along axons of the ALA interneuron via adhesive Sax7/L1CAM-Sax3/Robo interactions.…”

Section: Axon Guidance Along Marked Substratesmentioning

confidence: 99%

“…Primary PVD dendrites, on the other hand, express Sax3/Robo and project along ALA axons (Ramirez-Suarez et al, 2019). Sax7/L1CAM co-immunoprecipitated with tagged Sax3/Robo proteins, and mutual recognition in vivo caused morphological changes in PVD dendritic growth cones and re-oriented their actin cytoskeleton (Chen et al, 2019). Substrate adhesion therefore correlated well with structural changes in the underlying cytoskeleton.…”

Section: Axon Guidance Along Marked Substratesmentioning

confidence: 99%

Axon Guidance and Collective Cell Migration by Substrate-Derived Attractants

Aberle

2019

Front. Mol. Neurosci.

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Neurons have evolved specialized growth structures to reach and innervate their target cells. These growth cones express specific receptor molecules that sense environmental cues and transform them into steering decisions. Historically, various concepts of axon guidance have been developed to better understand how axons reach and identify their targets. The essence of these efforts seems to be that growth cones require solid substrates and that major guidance decisions are initiated by extracellular cues. These sometimes highly conserved ligands and receptors have been extensively characterized and mediate four major guidance forces: chemoattraction, chemorepulsion, contact attraction and contact repulsion. However, during development, cells, too, do migrate in order to reach molecularly-defined niches at target locations. In fact, axonal growth could be regarded as a special case of cellular migration, where only a highly polarized portion of the cell is elongating. Here, I combine several examples from genetically tractable model organisms, such as Drosophila or zebrafish, in which cells and axons are guided by attractive cues. Regardless, if these cues are secreted into the extracellular space or exposed on cellular surfaces, migrating cells and axons seem to keep close contact with these attractants and seem to detect them right at their source. Migration towards and along such substrate-derived attractants seem to be particularly robust, as genetic deletion induces obvious searching behaviors and permanent guidance errors. In addition, forced expression of these factors in ectopic tissues is highly distractive too, regardless of the pattern of other endogenous cues. Thus, guidance and migration towards and along attractive tissues is a powerful steering mechanism that exploits affinity differences to the surroundings and, in some instances, determines growth trajectories from source to target region.

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Adhesive L1CAM-Robo Signaling Aligns Growth Cone F-Actin Dynamics to Promote Axon-Dendrite Fasciculation in C. elegans

Cited by 29 publications

References 44 publications

Actin assembly and non-muscle myosin activity drive dendrite retraction in an UNC-6/Netrin dependent self-avoidance response

Actin assembly and non-muscle myosin activity drive dendrite retraction in an UNC-6/Netrin dependent self-avoidance response

Mutually exclusive dendritic arbors in C. elegans neurons share a common architecture and convergent molecular cues

Axon Guidance and Collective Cell Migration by Substrate-Derived Attractants

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