Cell cycle regulation of Golgi membrane dynamics

Abstract

The Golgi apparatus is a membranous organelle in the cell that plays essential roles in protein and lipid trafficking, sorting, processing and modification. Its basic structure is a stack of closely aligned flattened cisternae. In mammalian cells, dozens of Golgi stacks are often laterally linked into a ribbon-like structure. Biogenesis of the Golgi during cell division occurs through a sophisticated disassembly and reassembly process that can be divided into three distinct but cooperative steps, including the deformation and reformation of the Golgi cisternae, stacks and ribbon. Here, we review our current understanding of the protein machineries that control these three steps in the cycle of mammalian cell division: GRASP65 and GRASP55 in Golgi stack and ribbon formation; ubiquitin and AAA ATPases in post-mitotic Golgi membrane fusion; and golgins and cytoskeleton in Golgi ribbon formation.

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

“…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).…”

“…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.…”

“…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.…”

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

“…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.…”

“…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).…”