TY - JOUR

T1 - Preformed Ω-profile closure and kiss-and-run mediate endocytosis and diverse endocytic modes in neuroendocrine chromaffin cells

AU - Shin, Wonchul

AU - Wei, Lisi

AU - Arpino, Gianvito

AU - Ge, L.

AU - Guo, X.

AU - Hamid, E.

AU - Шупляков, Олег Викторович

AU - Bleck, C.K.E.

AU - Wu, L.G.

N1 - Publisher Copyright: © 2021

PY - 2021/10/1

Y1 - 2021/10/1

N2 - Transformation of flat membrane into round vesicles is generally thought to underlie endocytosis and produce speed-, amount- and vesicle-size-specific endocytic modes. Visualizing depolarization-induced exocytosis and subsequent endocytic transformation in live neuroendocrine chromaffin cells, we found that flat membrane is transformed into Λ-shape, Ω-shape and then O-shape vesicles via membrane invagination, Λ-base constriction and Ω-pore constriction, respectively. Surprisingly, endocytic vesicle formation is predominantly not from flat-membrane-to-round-vesicle transformation, but from calcium-triggered and dynamin-mediated closure of 1) Ω-profiles formed before depolarization and 2) fusion pores (called kiss-and-run). Varying calcium influxes control these pore closures’ speed, number, and vesicle size, resulting in speed-specific slow (>~6-s), fast (<~6-s) or ultrafast (<0.6-s) endocytosis, amount-specific compensatory (endocytosis=exocytosis) or overshoot endocytosis (endocytosis>exocytosis), and size-specific bulk endocytosis. These findings reveal major membrane transformation mechanisms underlying endocytosis, diverse endocytic modes, and exo-endocytosis coupling in neuroendocrine cells, challenging the half-a-century concept that the flat-to-round transformation predominantly mediates endocytosis after physiological stimulation.

AB - Transformation of flat membrane into round vesicles is generally thought to underlie endocytosis and produce speed-, amount- and vesicle-size-specific endocytic modes. Visualizing depolarization-induced exocytosis and subsequent endocytic transformation in live neuroendocrine chromaffin cells, we found that flat membrane is transformed into Λ-shape, Ω-shape and then O-shape vesicles via membrane invagination, Λ-base constriction and Ω-pore constriction, respectively. Surprisingly, endocytic vesicle formation is predominantly not from flat-membrane-to-round-vesicle transformation, but from calcium-triggered and dynamin-mediated closure of 1) Ω-profiles formed before depolarization and 2) fusion pores (called kiss-and-run). Varying calcium influxes control these pore closures’ speed, number, and vesicle size, resulting in speed-specific slow (>~6-s), fast (<~6-s) or ultrafast (<0.6-s) endocytosis, amount-specific compensatory (endocytosis=exocytosis) or overshoot endocytosis (endocytosis>exocytosis), and size-specific bulk endocytosis. These findings reveal major membrane transformation mechanisms underlying endocytosis, diverse endocytic modes, and exo-endocytosis coupling in neuroendocrine cells, challenging the half-a-century concept that the flat-to-round transformation predominantly mediates endocytosis after physiological stimulation.

KW - bulk endocytosis

KW - compensatory endocytosis

KW - endocytosis overshoot

KW - exo-endocytosis coupling

KW - fast endocytosis

KW - kiss-and-run

KW - membrane dynamics

KW - slow endocytosis

KW - super-resolution imaging

KW - ultrafast endocytosis

KW - FUSION

KW - SINGLE

KW - EXOCYTOSIS

KW - SLOW ENDOCYTOSIS

KW - MECHANISMS

KW - MEMBRANE RETRIEVAL

KW - TRANSMITTER RELEASE

KW - SYNAPTIC VESICLE ENDOCYTOSIS

KW - DYNAMIN

KW - PROTEINS

UR - http://www.scopus.com/inward/record.url?scp=85116507277&partnerID=8YFLogxK

UR - https://www.mendeley.com/catalogue/bc8b2586-08a6-3d87-84e0-7deff88dd5d4/

U2 - 10.1016/j.neuron.2021.07.019

DO - 10.1016/j.neuron.2021.07.019

M3 - Article

VL - 109

SP - 3119-3134.e5

JO - Neuron

JF - Neuron

SN - 0896-6273

IS - 19

ER -