A neuronal MAP kinase constrains growth of a Caenorhabditis elegans sensory dendrite throughout the life of the organism

I.G. McLachlan, I. Beets, M. de Bono, M.G. Heiman, PLOS Genetics 14 (2018) e1007435.

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Abstract
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 oxygen-sensing 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 βH-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.
Publishing Year
Date Published
2018-06-07
Journal Title
PLOS Genetics
Volume
14
Issue
6
Article Number
e1007435
ISSN
IST-REx-ID

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McLachlan IG, Beets I, de Bono M, Heiman MG. A neuronal MAP kinase constrains growth of a Caenorhabditis elegans sensory dendrite throughout the life of the organism. PLOS Genetics. 2018;14(6):e1007435. doi:10.1371/journal.pgen.1007435
McLachlan, I. G., Beets, I., de Bono, M., & Heiman, M. G. (2018). A neuronal MAP kinase constrains growth of a Caenorhabditis elegans sensory dendrite throughout the life of the organism. PLOS Genetics, 14(6), e1007435. https://doi.org/10.1371/journal.pgen.1007435
McLachlan, Ian G., Isabel Beets, Mario de Bono, and Maxwell G. Heiman. “A Neuronal MAP Kinase Constrains Growth of a Caenorhabditis Elegans Sensory Dendrite throughout the Life of the Organism.” PLOS Genetics 14, no. 6 (2018): e1007435. https://doi.org/10.1371/journal.pgen.1007435.
I. G. McLachlan, I. Beets, M. de Bono, and M. G. Heiman, “A neuronal MAP kinase constrains growth of a Caenorhabditis elegans sensory dendrite throughout the life of the organism,” PLOS Genetics, vol. 14, no. 6, p. e1007435, 2018.
McLachlan IG, Beets I, de Bono M, Heiman MG. 2018. A neuronal MAP kinase constrains growth of a Caenorhabditis elegans sensory dendrite throughout the life of the organism. PLOS Genetics. 14(6), e1007435.
McLachlan, Ian G., et al. “A Neuronal MAP Kinase Constrains Growth of a Caenorhabditis Elegans Sensory Dendrite throughout the Life of the Organism.” PLOS Genetics, vol. 14, no. 6, Public Library of Science, 2018, p. e1007435, doi:10.1371/journal.pgen.1007435.
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