Membrane traffic within the Golgi apparatus

Abstract

Newly synthesized secretory cargo molecules pass through the Golgi apparatus while resident Golgi proteins remain in the organelle. However, the pathways of membrane traffic within the Golgi are still uncertain. Most of the available data can be accommodated by the cisternal maturation model, which postulates that Golgi cisternae form de novo, carry secretory cargoes forward and ultimately disappear. The entry face of the Golgi receives material that has been exported from transitional endoplasmic reticulum sites, and the exit face of the Golgi is intimately connected with endocytic compartments. These conserved features are enhanced by cell-type-specific elaborations such as tubular connections between mammalian Golgi cisternae. Key mechanistic questions remain about the formation and maturation of Golgi cisternae, the recycling of resident Golgi proteins, the origins of Golgi compartmental identity, the establishment of Golgi architecture, and the roles of Golgi structural elements in membrane traffic.

Figure 1. Two models for membrane traffic through the Golgi

(a) Stable compartments model. According to this view, cis-, medial-, and trans-Golgi cisternae as well as the trans-Golgi network (TGN) are long-lived entities that retain distinct sets of resident Golgi proteins. Secretory cargoes travel from one Golgi compartment to the next in anterograde COPI vesicles, and then exit the TGN in clathrin-coated vesicles (CCV) or secretory carriers. ER-to-Golgi transport is regarded as a donor-acceptor pathway connected by COPII vesicles. (b) Cisternal maturation model. According to this view, Golgi cisternae are transient structures that form de novo by the coalescence of COPII vesicles. A new cisterna matures from cis to trans, and then breaks down into transport carriers at the TGN stage. Cargoes are transported through the Golgi by cisternal progression. Maturation is driven by the retrograde transport of resident Golgi proteins. This retrograde transport involves COPI vesicles within the Golgi, and may also involve clathrin-mediated recycling from a maturing TGN compartment.

Figure 2. Possible roles of tubules that connect heterologous Golgi cisternae

(a) Tubules might transport small soluble secretory cargoes (red) in an anterograde fashion. Large secretory cargoes (blue) cannot follow this path and thus move forward exclusively by cisternal progression. (b) Tubules might facilitate cisternal maturation by allowing the retrograde diffusion of resident Golgi proteins (pink and purple). These two possibilities are not mutually exclusive.

Figure 3. Tubules may give rise to cisternal fenestrations

We speculate that fenestrations are formed at the periphery of a cisterna when tubules fuse homotypically with the originating cisterna.

Figure 4. A model for post-Golgi membrane traffic

This model incorporates existing evidence to depict trafficking steps between exocytic, endocytic, and lysosomal/vacuolar compartments. Transport from the TGN to late endosomes (LE) and the lysosome/vacuole (Lys/Vac) is mediated by vesicles, some of which are coated with clathrin (gray). Transport from the TGN to the plasma membrane (PM) can be either direct, or indirect via fusion of TGN-derived carriers with recycling endosomes (RE). Recycling endosomes also receive material that was previously endocytosed to early endosomes (EE). The dashed line from the PM to the TGN is based on recent tentative findings in plant cells.

Figure 5. Comparison of secretory pathway organization in mammalian and plant cells

(a) In mammalian cells, Golgi stacks form an interconnected Golgi ribbon in the perinuclear centrosomal region. Pre-Golgi ERGIC (ER-Golgi intermediate compartment) elements form in the cell periphery and then undergo dynein-dependent transport along microtubules (arrows) to the Golgi ribbon. (b) In plant cells, the ER is often connected to the actin cable network, and individual Golgi stacks move along actin cables (arrows) by the action of myosin motors.