Structural Organization and Function of the Golgi Ribbon During Cell Division

Abstract

The Golgi complex has a central role in the secretory traffic. In vertebrate cells it is generally organized in polarized stacks of cisternae that are laterally connected by membranous tubules, forming a structure known as Golgi ribbon. The steady state ribbon arrangement results from a dynamic equilibrium between formation and cleavage of the membrane tubules connecting the stacks. This balance is of great physiological relevance as the unlinking of the ribbon during G2 is required for mitotic entry. A block of this process induces a potent G2 arrest of the cell cycle, indicating that a mitotic “Golgi checkpoint” controls the correct pre-mitotic segregation of the Golgi ribbon. Then, after mitosis onset, the Golgi stacks undergo an extensive disassembly, which is necessary for proper spindle formation. Notably, several Golgi-associated proteins acquire new roles in spindle formation and mitotic progression during mitosis. Here we summarize the current knowledge about the basic principle of the Golgi architecture and its functional relationship with cell division to highlight crucial aspects that need to be addressed to help us understand the physiological significance of the ribbon and the pathological implications of alterations of this organization.

Dominant ARF3 variants disrupt Golgi integrity and cause a neurodevelopmental disorder recapitulated in zebrafish

“…Our cell cycle profiling experiments indicate a possible delay of the mitosis in the early stages and an increased cell death within the developing anterior brain for the majority of the ARF3 fish mutants. A “Golgi checkpoint” sensing Golgi integrity and correct segregation has been suggested as an additional level to control cell cycle progression 116 , whose contribution to the observed brain growth and morphogenesis defects is worth further investigation. On the other hand, our live imaging of the developing fish forebrain determined the occurrence of altered spindle morphology in microcephaly-causing ARF3 mutants, which might ultimately underlie mitotic arrest and cell death.…”

Golgi-Targeting Anticancer Natural Products

“…In response to various perturbations incurred in the Golgi apparatus, its capacity is enhanced to supply the cellular needs, for instance, an increase in the vesicular flux, by upregulating post-translationally modified proteins and transportation of secretory and membrane proteins ( Figure 2 ). To ensure proper functioning of the Golgi apparatus, its structural organization is dynamically regulated [ 1 , 26 , 27 ]. Although much is still not well understood, uncontrolled alteration of the Golgi structure, for example, ribbon disassembly or fragmentation, can lead to disruption in the secretory pathway and a signal that triggers stress responses.…”

“…Various cellular responses, such as inflammation, and many diseases and disorders, from neurodegeneration to cancer, are associated with the loss of Golgi ribbons and the appearance of a dispersed Golgi apparatus [ 8 , 9 , 10 , 11 , 34 , 35 ]. The structural organization of the Golgi apparatus is inherently dynamic and undergoes structural transformation during the cell cycle and under stress conditions through tubule formation, tubular stack assembly and disassembly, fragmentation and vesiculation [ 26 , 27 ]. Under normal cell growth conditions, this transition is highly regulated and the vesiculation of Golgi ribbons is called Golgi haze at the onset of mitosis, which are reorganized into a new set of ribbons assembled at the mitosis exit.…”

Evolution of the ribbon-like organization of the Golgi apparatus in animal cells

“…Indeed, we also observed ribbon-like Golgis in the pluteus of this sea urchin species (Figure S1F). Like the ribbon of mammalian cells, sea urchin's centralized Golgi undergoes disassembly/reassembly cycles during mitosis (Figure S1G) and its maintenance requires an intact microtubule network (Figure S1H-S1I) 2,5,[24][25][26] . All these characteristics strongly indicate that the centralized Golgi complexes of sea urchin cells are indeed ribbons.…”