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Review
. 2022 Apr 28:10:884360.
doi: 10.3389/fcell.2022.884360. eCollection 2022.

The Golgi Apparatus and its Next-Door Neighbors

Akihiko Nakano  1
Affiliations
Review

The Golgi Apparatus and its Next-Door Neighbors

Akihiko Nakano. Front Cell Dev Biol. .

Abstract

The Golgi apparatus represents a central compartment of membrane traffic. Its apparent architecture, however, differs considerably among species, from unstacked and scattered cisternae in the budding yeast Saccharomyces cerevisiae to beautiful ministacks in plants and further to gigantic ribbon structures typically seen in mammals. Considering the well-conserved functions of the Golgi, its fundamental structure must have been optimized despite seemingly different architectures. In addition to the core layers of cisternae, the Golgi is usually accompanied by next-door compartments on its cis and trans sides. The trans-Golgi network (TGN) can be now considered as a compartment independent from the Golgi stack. On the cis side, the intermediate compartment between the ER and the Golgi (ERGIC) has been known in mammalian cells, and its functional equivalent is now suggested for yeast and plant cells. High-resolution live imaging is extremely powerful for elucidating the dynamics of these compartments and has revealed amazing similarities in their behaviors, indicating common mechanisms conserved along the long course of evolution. From these new findings, I would like to propose reconsideration of compartments and suggest a new concept to describe their roles comprehensively around the Golgi and in the post-Golgi trafficking.

Keywords: ERGIC; GECCO; Golgi; SCLIM; live imaging; membrane traffic; recycling endosome; trans-Golgi network.

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Conflict of interest statement

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Spatial organization of the Golgi. The spatial arrangement of the Golgi apparatus looks different among species. (A) In plant cells, Golgi cisternae (cis, medial, and trans) are beautifully layered in single stack units, which are scattered in the cytoplasm. Model animals of invertebrates, Drosophila and C. elegans, show a similar pattern. (B) In vertebrate animals like mammals, Golgi stacks are concentrated at the perinuclear centrosomal region often in an interconnected fashion to form a gigantic Golgi ribbon structure. (C) In the budding yeast S. cerevisiae, Golgi cisternae do not stack and are individually scattered in the cytoplasm. Note that ERES (ER exit sites) are very frequently observed in the very vicinity of the Golgi stack (A) or ERGIC (ER-Golgi intermediate compartment) (B) or cis-Golgi (C) [modified from Kurokawa et al. (2019)].
FIGURE 2
FIGURE 2
Behaviors of Golgi and TGN upon BFA treatment and washout in plant cells. In tobacco BY-2 cells, BFA-treatment gives distinct effects to the cis-most Golgi, the Golgi main body, and TGN (+BFA). The main-body Golgi (with the resident proteins shown by triangles) is completely absorbed into the ER, whereas cis-most Golgi, marked by SYP31 and RER1B (light green stars), remains as punctate structures near the ERES, which we designate GECCO (Golgi entry core compartment). TGN (marked by purple stars; SYP41), on the other hand, gets fragmented into small vesicles and dispersed in the cytoplasm. When BFA is washed out (-BFA), these components regenerate the original structures but their processes are again quite different. The Golgi main body reforms stacks in the cis-to-trans direction using the GECCO as the regeneration scaffold. TGN reassembles by itself independent of the GECCO and the Golgi main body, but finally meets Golgi and starts staying side by side (Ito et al., 2012; Ito et al., 2017; Ito et al., 2018b). GA-TGN, Golgi-associated TGN; GI-TGN, Golgi-independent TGN (see Figure 3).
FIGURE 3
FIGURE 3
Trans-Golgi network of plant cells. In plant cells, TGN (trans-Golgi network) takes two statuses, one being attached to the trans face of the Golgi (Golgi-associated TGN) and the other detached from the Golgi and free in the cytoplasm (Golgi-independent TGN) (Staehelin and Kang, 2008; Uemura et al., 2014). These two statuses are interchangeable; Golgi-independent TGN can dissociate from the Golgi and reassociate with it.
FIGURE 4
FIGURE 4
| Behavior of the Golgi, TGN and RE in Drosophila cells. (A) In Drosophila S2 cells, Golgi stack (cis, medial, and trans) and RE (recycling endosome) show attachment and detachment repeatedly (Fujii et al., 2020a). TGN appears to behave together with RE. Similar behavior of RE is also seen in nocodazole-treated HeLa cells. (B) When S2 cells are treated with BFA, which inhibits Arf GEF Sec71, Golgi, TGN and RE form a large aggregate (BFA body). In the BFA body, RE sits at the center, TGN follows next and Golgi cisternae align from trans to cis toward the periphery. (C) When the other Arf GEF of Drosophila Garz, which is insensitive to BFA, is knocked down, the Golgi main body is mostly absorbed into the ER, while leaving behind a cis component (GM130, red spots) (Fujii et al., 2020b).
FIGURE 5
FIGURE 5
Sorting zones in plant TGN differentiated for secretory and vacuolar trafficking. Cargo sorting events in root epidermal cells of Arabidopsis have been analyzed in detail by state-of-the-art live imaging (SCLIM) (Shimizu et al., 2021). TGN-localized proteins exhibit spatially and temporally distinct distribution. VAMP721 (R-SNARE), AP−1, and clathrin which are involved in secretory trafficking compose an exclusive subregion, whereas VAMP727 (R-SNARE) and AP-4 involved in vacuolar trafficking compose another subregion on the same TGN. These findings indicate that the single TGN has at least two subregions, or “zones”, responsible for distinct cargo sorting: the secretory-trafficking zone destined to the plasma membrane (PM) and the vacuolar-trafficking zone.
FIGURE 6
FIGURE 6
Comprehensive models of trafficking around Golgi and post Golgi. (A) Trafficking pathways around Golgi and its next-door neighbors (GECCO/ERGIC and TGN/RE) as well as post-Golgi trafficking to vacuole (Vac) via prevacuolar compartment (PVC). Arrows are drawn in an attempt to explain the observations described in this review. Note that early TGN, late TGN, and RE can behave together as a mobile unit, which takes Golgi-associated and Golgi-independent statuses. (B) Consideration of conserved Rab GTPases as signboards of compartments, which may be common to yeast, plant, and animal cells. Rab1 (Ypt1 in yeast and RABDs in plants) sits on GECCO/ERGIC, Rab6 (Ypt6 in yeast and RABHs in plants) is probably a good marker of early TGN, and Rab11 (Ypt31/32 in yeast and RABAs in plants) is present in late TGN and RE. The cases of Rab5 (Vps21 in yeast and RABFs in plants) and Rab7 (Ypt7 in yeast and RABGs in plants) are complicated. They mark PVC (MVB) and vacuole, respectively, in yeast and plant cells, but are considered to reside in early and late endosomes, respectively, in mammalian cells (see also Table 1). Blue arrows, i.e., back and forth between plasma membrane and Rab5 compartment and from Rab7 compartment to lysosome (Lys), could be considered inventions in mammals.
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