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Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature.

ABSTRACT: The endosomal pathway is responsible for plasma membrane cargo uptake, sorting, and, in many cases, lysosome targeting. Endosome maturation is complex, requiring proper spatiotemporal recruitment of factors that regulate the size, maturity, and positioning of endosomal compartments. In animal cells, it also requires trafficking of endosomes on microtubules. Recent work has revealed the presence of contact sites between some endosomes and the endoplasmic reticulum (ER). Although these contact sites are believed to have multiple functions, the frequency, dynamics, and physical attributes of these contacts are poorly understood. Here we use high-resolution three-dimensional electron microscopy to reveal that ER tubules wrap around endosomes and find that both organelles contact microtubules at or near membrane contact sites. As endosomes traffic, they remain bound to the ER, which causes the tubular ER to rearrange its structure around dynamic endosomes at contact sites. Finally, as endosomes transition through steps of maturation, they become more tightly associated with the ER. The major implication of these results is that endosomes mature and traffic while coupled to the ER membrane rather than in isolation.

SUBMITTER: Friedman JR

PROVIDER: S-EPMC3608491 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature.

Friedman Jonathan R JR Dibenedetto Jared R JR West Matthew M Rowland Ashley A AA Voeltz Gia K GK

Molecular biology of the cell 20130206 7

The endosomal pathway is responsible for plasma membrane cargo uptake, sorting, and, in many cases, lysosome targeting. Endosome maturation is complex, requiring proper spatiotemporal recruitment of factors that regulate the size, maturity, and positioning of endosomal compartments. In animal cells, it also requires trafficking of endosomes on microtubules. Recent work has revealed the presence of contact sites between some endosomes and the endoplasmic reticulum (ER). Although these contact sit ...[more]

PMID: 23389631

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Project description:The endoplasmic reticulum (ER) forms contact sites with the chloroplast. Exposing contact sites that contain both the chloroplast and the ER to localised high-fluence, wavelength specific, 405 nm violet light, hereinafter referred to as photostimulation, induces multiple, potentially interacting intra- and intercellular responses. The responses vary depending on the tissue type of the cell and the chloroplast. Photostimulating the ER-chloroplast contact sites in growing epidermal cells of the hypocotyl of Arabidopsis thaliana, produces a wave of cytoplasmic ionic calcium that traverses the cell, spreading radially to other cells around the circumference of the hypocotyl. A transient ER stress accompanies the calcium wave. These responses occur in older epidermal cells (5-8 days post-germination) with nonmotile chloroplasts tethered to the ER and the cell cortex but do not occur with motile or dividing chloroplasts. Dividing chloroplasts show a markedly different association with the ER, which forms a ring around the fission plane, similar to that of dividing mitochondria. Inhibition of calcium channels with lanthanum has no effect. Photostimulation of only the ER results in no ER stress and a calcium wave with a different spatiotemporal signature: delayed release and lower magnitude, with no accompanying ER stress response. Likewise, photostimulation of the chloroplast only, without the ER, produces no calcium wave or ER stress. General chloroplast photobleaching or restructuring caused by photostimulation is not the cause of this response; photostimulation with 488 nm of the same intensity and power as 405 nm photostimulation produces no change in cytosolic calcium levels. The pH of the ER decreases, indicating the involvement of ER ion transporters in the response. A wave of increased reactive oxygen species (ROS) in mitochondria and nuclei accompanies photostimulation. Together, these data support a model by which tethered ER-chloroplast contact sites constitute a unique subcellular photosensitive region and are part of an ER-mediated signalling network. Lay Abstract: The endoplasmic reticulum (ER) forms contact sites with the chloroplast. Shining violet (405 nm) light on the chloroplast with its associated ER produces a calcium wave through the cell that is communicated to other cells. This is correlated with a wave of transient denaturation of the luminal proteins of the ER (ER stress) and increased reactive oxygen species (ROS) in mitochondria. The wavelength dependence and precise cellular location of the light stimulation implies a novel way for plants to sense light. The movement of the response through the cell is consistent with the mediation of the response by a subcellular network, such as that formed by the ER.

Dataset Information

Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature.

Publications

Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature.

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