A cisternal maturation mechanism can explain the asymmetry of the Golgi stack

Glick, Benjamin S.; Elston, Timothy C.; Oster, George

doi:10.1016/s0014-5793(97)00984-8

Cited by 154 publications

(50 citation statements)

References 42 publications

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“…Classic models of membrane traffic focus on the generation of stable compartments out of the dynamic process of vesicle exchange (Heinrich and Rapoport, 2005). The few that consider maturation introduce it by hand, and study subsequent features of protein transport (Glick et al, 1997; Weiss and Nilsson, 2000; Dmitrieff et al, 2013; Ispolatov and Müsch, 2013). In contrast, maturation is not built into our framework, it emerges spontaneously.…”

Section: Discussionmentioning

confidence: 99%

“…All earlier mathematical analyses explicitly or implicitly assumed that maturation was driven by retrograde vesicles moving between spatially neighboring compartments (Glick et al, 1997; Weiss and Nilsson, 2000; Dmitrieff et al, 2013; Ispolatov and Müsch, 2013). However, un-stacked Golgi are widespread (Mowbrey and Dacks, 2009); and do have retrograde vesicles (Papanikou et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

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Stacking the odds for Golgi cisternal maturation

Mani

Thattai

2016

eLife

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What is the minimal set of cell-biological ingredients needed to generate a Golgi apparatus? The compositions of eukaryotic organelles arise through a process of molecular exchange via vesicle traffic. Here we statistically sample tens of thousands of homeostatic vesicle traffic networks generated by realistic molecular rules governing vesicle budding and fusion. Remarkably, the plurality of these networks contain chains of compartments that undergo creation, compositional maturation, and dissipation, coupled by molecular recycling along retrograde vesicles. This motif precisely matches the cisternal maturation model of the Golgi, which was developed to explain many observed aspects of the eukaryotic secretory pathway. In our analysis cisternal maturation is a robust consequence of vesicle traffic homeostasis, independent of the underlying details of molecular interactions or spatial stacking. This architecture may have been exapted rather than selected for its role in the secretion of large cargo.DOI: http://dx.doi.org/10.7554/eLife.16231.001

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Stacking the odds for Golgi cisternal maturation

Mani

Thattai

2016

eLife

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“…1). At the carbohydrate synthesis stage, COPIb vesicles are thought to exchange resident Golgi glycosylation enzymes between cisternae, thereby generating gradients of enzyme composition across Golgi stacks [53]. However, fundamental questions remain about intra-Golgi traffic at this stage.…”

Section: Through the Golgi: The Carbohydrate Synthesis Stagementioning

confidence: 99%

“…If these vesicles move one step at a time from older to younger cisternae, the observed gradients of resident Golgi proteins across the stack can be conveniently explained [53]. However, no mechanism for such orderly movement has been described.…”

Section: Through the Golgi: The Carbohydrate Synthesis Stagementioning

confidence: 99%

Golgi compartmentation and identity

Papanikou

Glick

2014

Current Opinion in Cell Biology

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Recent work supports the idea that cisternae of the Golgi apparatus can be assigned to three classes, which correspond to discrete stages of cisternal maturation. Each stage has a unique pattern of membrane traffic. At the first stage, cisternae form in association with the ER at multifunctional membrane assembly stations. At the second stage, cisternae synthesize carbohydrates while exchanging material via COPI vesicles. At the third stage, cisternae of the trans-Golgi network segregate into domains and produce transport carriers with the aid of specific lipids and the actin cytoskeleton. These processes are coordinated by cascades of Rab and Arf/Arl GTPases.

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“…For example, Glick et al . [28] developed a model of sorting in the Golgi based on the postulate that proteins comprise different kin populations that compete with each other for entry into transport vesicles. Their studies showed that different relative affinities of kin groups for potential vesicle types could generate distinct steady-state distributions of the different kin populations across the Golgi compartments.…”

Section: Introductionmentioning

confidence: 99%

Discrete, continuous, and stochastic models of protein sorting in the Golgi apparatus

et al. 2010

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The Golgi apparatus plays a central role in processing and sorting proteins and lipids in eukaryotic cells. Golgi compartments constantly exchange material with each other and with other cellular components, allowing them to maintain and reform distinct identities despite dramatic changes in structure and size during cell division, development, and osmotic stress. We have developed three minimal models of membrane and protein exchange in the Golgi—a discrete, stochastic model, a continuous ordinary differential equation model, and a continuous stochastic differential equation model—each based on two fundamental mechanisms: vesicle-coat-mediated selective concentration of cargoes and soluble N-ethylmaleimide-sensitive factor attachment protein receptor SNARE proteins during vesicle formation and SNARE-mediated selective fusion of vesicles. By exploring where the models differ, we hope to discover whether the discrete, stochastic nature of vesicle-mediated transport is likely to have appreciable functional consequences for the Golgi. All three models show similar ability to restore and maintain distinct identities over broad parameter ranges. They diverge, however, in conditions corresponding to collapse and reassembly of the Golgi. The results suggest that a continuum model provides a good description of Golgi maintenance but that considering the discrete nature of vesicle-based traffic is important to understanding assembly and disassembly of the Golgi. Experimental analysis validates a prediction of the models that altering guanine nucleotide exchange factor expression levels will modulate Golgi size.

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A cisternal maturation mechanism can explain the asymmetry of the Golgi stack

Cited by 154 publications

References 42 publications

Stacking the odds for Golgi cisternal maturation

Stacking the odds for Golgi cisternal maturation

Golgi compartmentation and identity

Discrete, continuous, and stochastic models of protein sorting in the Golgi apparatus

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