Authors: | Sengupta, T.; Koonce, N. L.; Vázquez-Martínez, N.; Moyle, M. W.; Duncan, L. H.; Emerson, S. E.; Han, X.; Shao, L.; Wu, Y.; Santella, A.; Fan, L.; Bao, Z.; Mohler, W. A.; Shroff, H.; Colón-Ramos, D. A. |
Article Title: | Differential adhesion regulates neurite placement via a retrograde zippering mechanism |
Abstract: | During development, neurites and synapses segregate into specific neighborhoods or layers within nerve bundles. The developmental programs guiding placement of neurites in specific layers, and hence their incorporation into specific circuits, are not well understood. We implement novel imaging methods and quantitative models to document the embryonic development of the C. elegans brain neuropil, and discover that differential adhesion mechanisms control precise placement of single neurites onto specific layers. Differential adhesion is orchestrated via developmentally-regulated expression of the IgCAM SYG-1, and its partner ligand SYG-2. Changes in SYG-1 expression across neuropil layers result in changes in adhesive forces, which sort SYG-2-expressing neurons. Sorting to layers occurs, not via outgrowth from the neurite tip, but via an alternate mechanism of retrograde zippering, involving interactions between neurite shafts. Our study indicates that biophysical principles from differential adhesion govern neurite placement and synaptic specificity in vivo in developing neuropil bundles. © 2021, eLife Sciences Publications Ltd. All rights reserved. |
Keywords: | controlled study; unclassified drug; single nucleotide polymorphism; microscopy; nonhuman; neuroimaging; cell structure; gene overexpression; gene expression; confocal microscopy; image analysis; green fluorescent protein; embryo development; caspase 3; cell lineage; regulatory mechanism; caenorhabditis elegans; cell adhesion; nerve cell differentiation; cell adhesion molecule; synapse; levamisole; brain slice; protein p17; light sheet microscopy; differential adhesion; neurite; gain of function mutation; article; whole genome sequencing; synaptogenesis protein 1; synaptogenesis protein 2; retrograde zippering mechanism |
Journal Title: | eLife |
Volume: | 10 |
ISSN: | 2050-084X |
Publisher: | eLife Sciences Publications Ltd. |
Date Published: | 2021-11-16 |
Start Page: | e71171 |
Language: | English |
DOI: | 10.7554/eLife.71171 |
PROVIDER: | scopus |
PUBMED: | 34783657 |
PMCID: | PMC8843091 |
DOI/URL: | |
Notes: | Article -- Export Date: 3 January 2022 -- Source: Scopus |