Differential adhesion regulates neurite placement via a retrograde zippering mechanism
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 metho...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-11-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/71171 |
| _version_ | 1811203362446639104 |
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| author | Titas Sengupta Noelle L Koonce Nabor Vázquez-Martínez Mark W Moyle Leighton H Duncan Sarah E Emerson Xiaofei Han Lin Shao Yicong Wu Anthony Santella Li Fan Zhirong Bao William A Mohler Hari Shroff Daniel A Colón-Ramos |
| author_facet | Titas Sengupta Noelle L Koonce Nabor Vázquez-Martínez Mark W Moyle Leighton H Duncan Sarah E Emerson Xiaofei Han Lin Shao Yicong Wu Anthony Santella Li Fan Zhirong Bao William A Mohler Hari Shroff Daniel A Colón-Ramos |
| author_sort | Titas Sengupta |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T02:53:25Z |
| format | Article |
| id | doaj.art-e76231349ddb4528bf5399da88172428 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:53:25Z |
| publishDate | 2021-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-e76231349ddb4528bf5399da881724282022-12-22T03:50:54ZengeLife Sciences Publications LtdeLife2050-084X2021-11-011010.7554/eLife.71171Differential adhesion regulates neurite placement via a retrograde zippering mechanismTitas Sengupta0https://orcid.org/0000-0002-7228-719XNoelle L Koonce1Nabor Vázquez-Martínez2Mark W Moyle3Leighton H Duncan4Sarah E Emerson5Xiaofei Han6Lin Shao7Yicong Wu8Anthony Santella9Li Fan10Zhirong Bao11https://orcid.org/0000-0002-2201-2745William A Mohler12Hari Shroff13Daniel A Colón-Ramos14https://orcid.org/0000-0003-0223-7717Department of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United StatesDepartment of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United StatesDepartment of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United StatesDepartment of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United StatesDepartment of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United StatesDepartment of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United StatesLaboratory of High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United StatesDepartment of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United StatesLaboratory of High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United StatesDevelopmental Biology Program, Sloan Kettering Institute, New Haven, United StatesDevelopmental Biology Program, Sloan Kettering Institute, New Haven, United StatesDevelopmental Biology Program, Sloan Kettering Institute, New Haven, United StatesDepartment of Genetics and Genome Sciences and Center for Cell Analysis and Modeling, University of Connecticut Health Center, Farmington, United StatesLaboratory of High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States; MBL Fellows, Marine Biological Laboratory, Woods Hole, United StatesDepartment of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United States; MBL Fellows, Marine Biological Laboratory, Woods Hole, United States; Wu Tsai Institute, Yale University, New Haven, United States; Instituto de Neurobiología, Recinto de Ciencias Médicas, Universidad de Puerto Rico, San Juan, Puerto RicoDuring 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.https://elifesciences.org/articles/71171neurite placementdifferential adhesionIgCAM |
| spellingShingle | Titas Sengupta Noelle L Koonce Nabor Vázquez-Martínez Mark W Moyle Leighton H Duncan Sarah E Emerson Xiaofei Han Lin Shao Yicong Wu Anthony Santella Li Fan Zhirong Bao William A Mohler Hari Shroff Daniel A Colón-Ramos Differential adhesion regulates neurite placement via a retrograde zippering mechanism eLife neurite placement differential adhesion IgCAM |
| title | Differential adhesion regulates neurite placement via a retrograde zippering mechanism |
| title_full | Differential adhesion regulates neurite placement via a retrograde zippering mechanism |
| title_fullStr | Differential adhesion regulates neurite placement via a retrograde zippering mechanism |
| title_full_unstemmed | Differential adhesion regulates neurite placement via a retrograde zippering mechanism |
| title_short | Differential adhesion regulates neurite placement via a retrograde zippering mechanism |
| title_sort | differential adhesion regulates neurite placement via a retrograde zippering mechanism |
| topic | neurite placement differential adhesion IgCAM |
| url | https://elifesciences.org/articles/71171 |
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