Post-fusion structural changes and their roles in exocytosis and endocytosis of dense-core vesicles

Hsueh-Cheng Chiang, Wonchul Shin, Wei-Dong Zhao, Edaeni Hamid, Jiansong Sheng, Maryna Baydyuk, Peter J. Wen, Albert Jin, Fanny Momboisse and Ling-Gang Wu ()
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Hsueh-Cheng Chiang: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012
Wonchul Shin: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012
Wei-Dong Zhao: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012
Edaeni Hamid: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012
Jiansong Sheng: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012
Maryna Baydyuk: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012
Peter J. Wen: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012
Albert Jin: National Institute of Biomedical Imaging and Bioengineering (NIBIB)
Fanny Momboisse: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012
Ling-Gang Wu: National Institute of Neurological Disorders and Stroke, 35 Convent Drive, Building 35, Room 2B-1012

Nature Communications, 2014, vol. 5, issue 1, 1-17

Abstract: Abstract Vesicle fusion with the plasma membrane generates an Ω-shaped membrane profile. Its pore is thought to dilate until flattening (full-collapse), followed by classical endocytosis to retrieve vesicles. Alternatively, the pore may close (kiss-and-run), but the triggering mechanisms and its endocytic roles remain poorly understood. Here, using confocal and stimulated emission depletion microscopy imaging of dense-core vesicles, we find that fusion-generated Ω-profiles may enlarge or shrink while maintaining vesicular membrane proteins. Closure of fusion-generated Ω-profiles, which produces various sizes of vesicles, is the dominant mechanism mediating rapid and slow endocytosis within ~1–30 s. Strong calcium influx triggers dynamin-mediated closure. Weak calcium influx does not promote closure, but facilitates the merging of Ω-profiles with the plasma membrane via shrinking rather than full-collapse. These results establish a model, termed Ω-exo–endocytosis, in which the fusion-generated Ω-profile may shrink to merge with the plasma membrane, change in size or change in size then close in response to calcium, which is the main mechanism to retrieve dense-core vesicles.

Date: 2014
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DOI: 10.1038/ncomms4356

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