Stop or Go? Endosome Positioning in the Establishment of Compartment Architecture, Dynamics, and Function

The endosomal system constitutes a key negotiator between the environment of a cell and its internal affairs. Comprised of a complex membranous network, wherein each vesicle can in principle move autonomously throughout the cell, the endosomal system operates as a coherent unit to optimally face external challenges and maintain homeostasis. Our appreciation of how individual endosomes are controlled in time and space to best serve their collective purpose has evolved dramatically in recent years. In light of these efforts, the endoplasmic reticulum (ER) – with its expanse of membranes permeating the cytoplasmic space – has emerged as a potent spatiotemporal organizer of endosome biology. We review the latest advances in our understanding of the mechanisms underpinning endosomal transport and positioning, with emphasis on the contributions from the ER, and offer a perspective on how the interplay between these aspects shapes the architecture and dynamics of the endosomal system and drives its myriad cellular functions. Endosomal transport and positioning cooperate in the establishment of compartment architecture, dynamics and function. Functional attributes of peripheral endosomes differ from those found in the perinuclear region of the cell. Interactions between the ER and endosomes influence endosome distribution, motility, and fission.