The epithelial Na+ channel UNC-8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neurons
Summary: Circuit refinement involves the formation of new presynaptic boutons as others are dismantled. Nascent presynaptic sites can incorporate material from recently eliminated synapses, but the recycling mechanisms remain elusive. In early-stage C. elegans larvae, the presynaptic boutons of GABA...
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| Format: | Article |
| Language: | English |
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Elsevier
2023-11-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124723013396 |
| _version_ | 1797448035055173632 |
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| author | Andrea Cuentas-Condori Siqi Chen Mia Krout Kristin L. Gallik John Tipps Casey Gailey Leah Flautt Hongkyun Kim Ben Mulcahy Mei Zhen Janet E. Richmond David M. Miller, III |
| author_facet | Andrea Cuentas-Condori Siqi Chen Mia Krout Kristin L. Gallik John Tipps Casey Gailey Leah Flautt Hongkyun Kim Ben Mulcahy Mei Zhen Janet E. Richmond David M. Miller, III |
| author_sort | Andrea Cuentas-Condori |
| collection | DOAJ |
| description | Summary: Circuit refinement involves the formation of new presynaptic boutons as others are dismantled. Nascent presynaptic sites can incorporate material from recently eliminated synapses, but the recycling mechanisms remain elusive. In early-stage C. elegans larvae, the presynaptic boutons of GABAergic DD neurons are removed and new outputs established at alternative sites. Here, we show that developmentally regulated expression of the epithelial Na+ channel (ENaC) UNC-8 in remodeling DD neurons promotes a Ca2+ and actin-dependent mechanism, involving activity-dependent bulk endocytosis (ADBE), that recycles presynaptic material for reassembly at nascent DD synapses. ADBE normally functions in highly active neurons to accelerate local recycling of synaptic vesicles. In contrast, we find that an ADBE-like mechanism results in the distal recycling of synaptic material from old to new synapses. Thus, our findings suggest that a native mechanism (ADBE) can be repurposed to dismantle presynaptic terminals for reassembly at new, distant locations. |
| first_indexed | 2024-03-09T14:05:33Z |
| format | Article |
| id | doaj.art-26ea0a70ac5f4aa09bcf619ad2cc3d89 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-03-09T14:05:33Z |
| publishDate | 2023-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-26ea0a70ac5f4aa09bcf619ad2cc3d892023-11-30T05:06:48ZengElsevierCell Reports2211-12472023-11-014211113327The epithelial Na+ channel UNC-8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neuronsAndrea Cuentas-Condori0Siqi Chen1Mia Krout2Kristin L. Gallik3John Tipps4Casey Gailey5Leah Flautt6Hongkyun Kim7Ben Mulcahy8Mei Zhen9Janet E. Richmond10David M. Miller, III11Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37240, USADepartment of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37240, USADepartment of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607, USADepartment of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607, USADepartment of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37240, USADepartment of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37240, USADepartment of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37240, USADepartment of Cell Biology and Anatomy, Chicago Medical School, Rosalind Franklin University of Medicine and Science, North Chicago, IL 60064, USALunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON M5G 1X5, CanadaLunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON M5G 1X5, CanadaDepartment of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607, USADepartment of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37240, USA; Neurosience Program, Vanderbilt University, Nashville, TN 37240, USA; Corresponding authorSummary: Circuit refinement involves the formation of new presynaptic boutons as others are dismantled. Nascent presynaptic sites can incorporate material from recently eliminated synapses, but the recycling mechanisms remain elusive. In early-stage C. elegans larvae, the presynaptic boutons of GABAergic DD neurons are removed and new outputs established at alternative sites. Here, we show that developmentally regulated expression of the epithelial Na+ channel (ENaC) UNC-8 in remodeling DD neurons promotes a Ca2+ and actin-dependent mechanism, involving activity-dependent bulk endocytosis (ADBE), that recycles presynaptic material for reassembly at nascent DD synapses. ADBE normally functions in highly active neurons to accelerate local recycling of synaptic vesicles. In contrast, we find that an ADBE-like mechanism results in the distal recycling of synaptic material from old to new synapses. Thus, our findings suggest that a native mechanism (ADBE) can be repurposed to dismantle presynaptic terminals for reassembly at new, distant locations.http://www.sciencedirect.com/science/article/pii/S2211124723013396CP: NeuroscienceCP: Cell biology |
| spellingShingle | Andrea Cuentas-Condori Siqi Chen Mia Krout Kristin L. Gallik John Tipps Casey Gailey Leah Flautt Hongkyun Kim Ben Mulcahy Mei Zhen Janet E. Richmond David M. Miller, III The epithelial Na+ channel UNC-8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neurons Cell Reports CP: Neuroscience CP: Cell biology |
| title | The epithelial Na+ channel UNC-8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neurons |
| title_full | The epithelial Na+ channel UNC-8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neurons |
| title_fullStr | The epithelial Na+ channel UNC-8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neurons |
| title_full_unstemmed | The epithelial Na+ channel UNC-8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neurons |
| title_short | The epithelial Na+ channel UNC-8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neurons |
| title_sort | epithelial na channel unc 8 promotes an endocytic mechanism that recycles presynaptic components to new boutons in remodeling neurons |
| topic | CP: Neuroscience CP: Cell biology |
| url | http://www.sciencedirect.com/science/article/pii/S2211124723013396 |
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