Cell cycle regulation of Golgi membrane dynamics

Tang, Danming; Wang, Yanzhuang

doi:10.1016/j.tcb.2013.01.008

Cited by 92 publications

(90 citation statements)

References 81 publications

(142 reference statements)

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“…Thus, reproducing the reassembly process by physical modeling is a promising approach. The Golgi reassembly process in vivo has two phases: formation of initial Golgi ministacks and later Golgi ribbon formation (5). The former process is believed to be independent from the microtubule cytoskeleton and to be reconstituted in vitro (20).…”

Section: Significancementioning

confidence: 99%

“…At the same time, the progression of membrane traffic through the Golgi apparatus is a highly dynamic membrane-reorganizing process that involves formation of new cisternae on the cis face, elongation of membrane tubules for connection of adjacent cisternae, vesicle budding and fusion for retrograde transport of Golgi-resident molecules, and fragmentation of the trans-Golgi network (2). Moreover, the Golgi apparatus in mammalian cells fragments into vesicles at the start of mitosis, and these vesicles reassemble to form Golgi in each daughter cell at the end of mitosis (3)(4)(5). Although chemical and molecular characteristics of the Golgi apparatus are being intensively studied at present, the mechanism underlying the morphology and the above behavior remains unknown.…”

mentioning

confidence: 99%

“…A typical morphological anomaly of the Golgi apparatus is fragmentation, which is observed in Golgi-associated protein deletion mutants, stress-exposed cells, and diseases (5)(6)(7)(8)(9)(10). Via the fragmentation, Golgi components completely decompose and lose their morphological characteristics such as the structural anisotropy and long-range coherence.…”

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confidence: 99%

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Golgi apparatus self-organizes into the characteristic shape via postmitotic reassembly dynamics

Tachikawa

Mochizuki

2017

Proc. Natl. Acad. Sci. U.S.A.

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The Golgi apparatus is a membrane-bounded organelle with the characteristic shape of a series of stacked flat cisternae. During mitosis in mammalian cells, the Golgi apparatus is once fragmented into small vesicles and then reassembled to form the characteristic shape again in each daughter cell. The mechanism and details of the reassembly process remain elusive. Here, by the physical simulation of a coarse-grained membrane model, we reconstructed the threedimensional morphological dynamics of the Golgi reassembly process. Considering the stability of the interphase Golgi shape, we introduce two hypothetical mechanisms-the Golgi rim stabilizer protein and curvature-dependent restriction on membrane fusioninto the general biomembrane model. We show that the characteristic Golgi shape is spontaneously organized from the assembly of vesicles by proper tuning of the two additional mechanisms, i.e., the Golgi reassembly process is modeled as self-organization. We also demonstrate that the fine Golgi shape forms via a balance of three reaction speeds: vesicle aggregation, membrane fusion, and shape relaxation. Moreover, the membrane fusion activity decreases thickness and the number of stacked cisternae of the emerging shapes.Golgi apparatus | self-organization | physical biology modeling | computer simulation

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Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

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Golgi apparatus self-organizes into the characteristic shape via postmitotic reassembly dynamics

Tachikawa

Mochizuki

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…At the onset of mitosis, the Golgi structure is fragmented through ribbon unlinking, cisternae unstacking and vesiculation. In telophase, the Golgi reassembles through reverse processes by membrane fusion to generate new cisternae, cisternal restacking to form stacks, and lateral linking to form a new ribbon in each daughter cell (Tang and Wang, 2013;Wang and Seemann, 2011). A number of factors have been identified that regulate Golgi membrane dynamics during the cell cycle.…”

Section: Introductionmentioning

confidence: 99%

“…Two ATPases associated with diverse cellular activities (AAA) ATPases, the N-ethylmaleimidesensitive fusion protein (NSF) and valosin-containing protein (VCP) p97, together with their adaptors, have been implicated in postmitotic cisternal regrowth from mitotic Golgi fragments Rabouille et al, 1995a). Although the role of NSF and its adaptors a/c-SNAP in Golgi membrane fusion has been well characterized and reviewed (Rabouille et al, 1995a;Shorter and Warren, 2002), p97-mediated membrane fusion has become particularly interesting because of the recent finding of its connection with the ubiquitin system (Meyer et al, 2002;Tang and Wang, 2013;Wang et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Phosphorylation regulates VCIP135 function in Golgi membrane fusion during the cell cycle

Zhang

Wang

2013

Journal of Cell Science

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The Golgi apparatus in mammalian cells consists of stacks that are often laterally linked into a ribbon-like structure. During cell division, the Golgi disassembles into tubulovesicular structures in the early stages of mitosis and reforms in the two daughter cells by the end of mitosis. Valosin-containing protein p97-p47 complex-interacting protein, p135 (VCIP135), an essential factor involved in p97-mediated membrane fusion pathways, is required for postmitotic Golgi cisternae regrowth and Golgi structure maintenance in interphase. However, how VCIP135 function is regulated in the cell cycle remains unclear. Here, we report that VCIP135 depletion by RNA interference results in Golgi fragmentation. VCIP135 function requires membrane association and p97 interaction, both of which are inhibited in mitosis by VCIP135 phosphorylation. We found that wild-type VCIP135, but not its phosphomimetic mutants, rescues Golgi structure in VCIP135-depleted cells. Our results demonstrate that VCIP135 phosphorylation regulates its Golgi membrane association and p97 interaction, and thus contributes to the tight control of the Golgi disassembly and reassembly process during the cell cycle.

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Golgi: Methods for Preparation

Tang

Wang

2013

Encyclopedia of Life Sciences

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The study of Golgi structure and function has been greatly facilitated by the purification of this membrane organelle from cellular homogenates. Purified Golgi membranes have been used in a variety of cell‐free assays to investigate sugar modifications, vesicle transport, Golgi structure formation and Golgi–cytoskeleton interactions. Golgi membranes can be purified from cells and tissues using a number of different methods, with liver as a preferred source. Highly purified Golgi stacks can be obtained after two sequential density gradient centrifugations of rat liver homogenate. The relative purity of the prepared Golgi stacks is assessed by measuring the increase in activity of a Golgi enzyme, β‐1,4‐galactosyltransferase (GalT), over that of the total liver homogenate. A typical preparation can yield milligrams of Golgi membranes that are purified 80‐ to 100‐fold over the homogenate and 60–70% in stacks, which provides abundant material for both structural and functional studies of this organelle. Key Concepts: The Golgi apparatus is an essential membrane‐bound organelle in the centre of the secretory pathway in almost all eukaryotic cells. The primary function of the Golgi is to modify and package proteins and lipids into transport carriers and send them to the proper locations. Golgi can be separated from other membranous organelles by density gradient centrifugation. Glycosyl transferases are used as marker enzymes to monitor the yield and purity of the purified Golgi apparatus during Golgi preparation. Purified Golgi membranes can be used in a variety of cell‐free assays to investigate sugar modifications, vesicle transport, Golgi structure formation and Golgi–cytoskeleton interactions.

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Cell cycle regulation of Golgi membrane dynamics

Cited by 92 publications

References 81 publications

Golgi apparatus self-organizes into the characteristic shape via postmitotic reassembly dynamics

Golgi apparatus self-organizes into the characteristic shape via postmitotic reassembly dynamics

Phosphorylation regulates VCIP135 function in Golgi membrane fusion during the cell cycle

Golgi: Methods for Preparation

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