Preformed Ω-profile closure and kiss-and-run mediate endocytosis and diverse endocytic modes in neuroendocrine chromaffin cells

Shin, Wonchul; Wei, Lisi; Arpino, Gianvito; Ge, Lihao; Guo, Xiaoli; Chan, Collin; Hamid, Edaeni; Shupliakov, Oleg; Bleck, Christopher K. E.; Wu, Ling−Gang

doi:10.1016/j.neuron.2021.07.019

Cited by 27 publications

(127 citation statements)

References 63 publications

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“…Calcium influx, but not the exocytosis amount triggers bulk endocytosis at synapses ( Morton et al., 2015 ; Wu et al., 2009 , 2014a ). Recently, bulk membrane invaginations have been observed directly in real time in live cells after just a 1-s depolarization, and it is also triggered by calcium influx in chromaffin cells ( Shin et al., 2021 ). Thus, calcium-triggered bulk endocytosis is a major endocytic mechanism in neurons and endocrine cells in both mild and strong stimulation conditions.…”

Section: Discussionmentioning

confidence: 99%

Clathrin-mediated endocytosis cooperates with bulk endocytosis to generate vesicles

et al. 2022

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Section: Discussionmentioning

confidence: 99%

Clathrin-mediated endocytosis cooperates with bulk endocytosis to generate vesicles

et al. 2022

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“…Recent studies reveal an essential role of F-actin in mediating all kinetically distinguishable forms of endocytosis, including ultrafast, fast, slow, bulk, and overshoot endocytosis (Figure 5). Ultrastructural examination and real-time imaging suggest that F-actin is involved in pit formation, a critical step of endocytosis that has just been visualized in real time in live cells (Shin et al, 2021(Shin et al, , 2022. The essential role of F-actin in mediating endocytosis may facilitate active zone clearance that may in turn promote RRP replenishment (Figure 5).…”

Section: Conclusion and Future Research Questionsmentioning

confidence: 99%

“…The other limits release by closing a narrow fusion pore, called kiss-and-run or close-fusion (Ceccarelli et al, 1973;Chiang et al, 2014;Zhao et al, 2016). With super-resolution STED microscopy to visualize fusion modes of dense-core vesicles in neuroendocrine cells, it has been found, surprisingly, that facilitation of release is not mediated by full-collapse, but rather shrink fusion, in which the -profile generated by vesicle fusion shrinks, but maintains a large non-dilating pore until the -profile is undetectable (Figure 4A; Chiang et al, 2014;Wen et al, 2016;Shin et al, 2018Shin et al, , 2021. Inhibition of F-actin polymerization by Lat A, cytochalasin D, or β-actin knockout significantly reduces plasma membrane tension (Figure 3G) and shrink fusion percentage (Figures 4B,C; Wen et al, 2016;Shin et al, 2020).…”

Section: Filamentous Actin Promotes Shrink Fusionmentioning

confidence: 99%

Multiple Roles of Actin in Exo- and Endocytosis

Chan

2022

Front. Synaptic Neurosci.

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Cytoskeletal filamentous actin (F-actin) has long been considered a molecule that may regulate exo- and endocytosis. However, its exact roles remained elusive. Recent studies shed new light on many crucial roles of F-actin in regulating exo- and endocytosis. Here, this progress is reviewed from studies of secretory cells, particularly neurons and endocrine cells. These studies reveal that F-actin is involved in mediating all kinetically distinguishable forms of endocytosis, including ultrafast, fast, slow, bulk, and overshoot endocytosis, likely via membrane pit formation. F-actin promotes vesicle replenishment to the readily releasable pool most likely via active zone clearance, which may sustain synaptic transmission and overcome short-term depression of synaptic transmission during repetitive firing. By enhancing plasma membrane tension, F-actin promotes fusion pore expansion, vesicular content release, and a fusion mode called shrink fusion involving fusing vesicle shrinking. Not only F-actin, but also the F-actin assembly pathway, including ATP hydrolysis, N-WASH, and formin, are involved in mediating these roles of exo- and endocytosis. Neurological disorders, including spinocerebellar ataxia 13 caused by Kv3.3 channel mutation, may involve impairment of F-actin and its assembly pathway, leading in turn to impairment of exo- and endocytosis at synapses that may contribute to neurological disorders.

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“…4a) and pre-O (Fig. 6a) (fordetail,seeRef. 12 ). These transitions reflect three modular transitions, including Flat,  and O, which mediate the Flat-to-O transition.…”

Section: Experimental Setting For Observing Flato In Real Timementioning

confidence: 99%

“…After depol1s formed by Flat and pre- underwent  at a probability [Prob(  ] of 0.12±0.01 (from513cells;Fig.4a,b) 12 . This transition was due to constriction of ~300-1000nm -base at a rate of 160±28nm/s (20-80%,n=37;Fig.4a,b) 12 . The resulting  with a visible pore (p,>~60nm,ourSTEDresolution) sometimes continued to constrict its pore until it became a non-visible pore (np,<~60nm,Fig.4a) 12 .…”

Section: Dynamin Helices Surround and Constrict 'S Base To Mediate mentioning

confidence: 99%

Molecular mechanics underlying flat-to-round membrane budding in live secretory cells

Shin

Zucker

Kundu

et al. 2022

Preprint

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Membrane budding entails forces to transform flat membrane into vesicles essential for cell survival. Accumulated studies have identified coat-proteins (e.g., clathrin) as potential budding factors. However, forces mediating many non-coated membrane buddings remain unclear. By visualizing proteins in mediating endocytic budding in live neuroendocrine cells, performing in vitro protein reconstitution and physical modelling, we discovered how non-coated-membrane budding is mediated: actin filaments and dynamin generate a pulling force transforming flat membrane into Λ-shape; subsequently, dynamin helices surround and constrict Λ-profile’s base, transforming Λ- to Ω-profile, and then constrict Ω-profile’s pore, converting Ω-profiles to vesicles. These mechanisms control budding speed, vesicle size and number, generating diverse endocytic modes differing in these parameters. Their impact is widespread beyond secretory cells, as the unexpectedly powerful functions of dynamin and actin, previously thought to mediate fission and overcome tension, respectively, may contribute to many dynamin/actin-dependent non- coated-membrane buddings, coated-membrane buddings, and other membrane remodelling processes.

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Preformed Ω-profile closure and kiss-and-run mediate endocytosis and diverse endocytic modes in neuroendocrine chromaffin cells

Cited by 27 publications

References 63 publications

Clathrin-mediated endocytosis cooperates with bulk endocytosis to generate vesicles

Clathrin-mediated endocytosis cooperates with bulk endocytosis to generate vesicles

Multiple Roles of Actin in Exo- and Endocytosis

Molecular mechanics underlying flat-to-round membrane budding in live secretory cells

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