A New Look at the Functional Organization of the Golgi Ribbon

Abstract

A characteristic feature of vertebrate cells is a Golgi ribbon consisting of multiple cisternal stacks connected into a single-copy organelle next to the centrosome. Despite numerous studies, the mechanisms that link the stacks together and the functional significance of ribbon formation remain poorly understood. Nevertheless, these questions are of considerable interest, since there is increasing evidence that Golgi fragmentation – the unlinking of the stacks in the ribbon – is intimately connected not only to normal physiological processes, such as cell division and migration, but also to pathological states, including neurodegeneration and cancer. Challenging a commonly held view that ribbon architecture involves the formation of homotypic tubular bridges between the Golgi stacks, we present an alternative model, based on direct interaction between the biosynthetic (pre-Golgi) and endocytic (post-Golgi) membrane networks and their connection with the centrosome. We propose that the central domains of these permanent pre- and post-Golgi networks function together in the biogenesis and maintenance of the more transient Golgi stacks, and thereby establish “linker compartments” that dynamically join the stacks together. This model provides insight into the reversible fragmentation of the Golgi ribbon that takes place in dividing and migrating cells and its regulation along a cell surface – Golgi – centrosome axis. Moreover, it helps to understand transport pathways that either traverse or bypass the Golgi stacks and the positioning of the Golgi apparatus in differentiated neuronal, epithelial, and muscle cells.

Cytomegalovirus Generates Assembly Compartment in the Early Phase of Infection by Perturbation of Host-Cell Factors Recruitment at the Early Endosome/Endosomal Recycling Compartment/Trans-Golgi Interface

“…This analysis suggests that the unlinking of the Golgi ribbon associated with the reorganization of the post-Golgi linker compartments (Saraste and Prydz, 2019) is the earliest event in the biogenesis of the AC. The basic architecture of the AC is established in the E phase of infection (4-5 hpi), indicating that it is driven by MCMV-encoded E genes and does not require L gene expression, including loading with viral tegument and envelope proteins.…”

“…Altogether, the analysis of the Golgi system demonstrates that oAC is mainly build by the C2-C7 Golgi cisternae, whereas the iAC is composed of membrane intermediates derived at the interface the Golgi and post-Golgi linker compartments (EE-ERC-TGN and cis-Golgi-IC; Saraste and Prydz, 2019 ) that are reoriented toward the cell center.…”

“…2 days after infection (Rebmann et al, 2016;Taisne et al, 2019) and may be an initial step in the formation of the AC, as suggested by Rebmann et al (2016). It may result in unlinking the Golgi non-compact region and dysregulation of linker compartments (the ERC and the IC), as it occurs during mitosis and cell migration (Saraste and Prydz, 2019). Although our study was focused on EE-ERC-TGN interface markers, over-recruitment of Rab41 at membranes of the inner AC, a small GTPase that acts at the IC-Golgi interface (Liu et al, 2016), suggests that both linker compartments could be sequentially reorganized during CMV infection.…”

Plant Golgi ultrastructure

“…In S. cerevisiae there is no Golgi stack, the cis-, median-and trans-cisternae being scattered all over the cytoplasm (Suda & Nakano, 2012). In animal cells the Golgi apparatus is immobile and has a perinuclear distribution either as a ribbon of interconnected Golgi stacks or as a large complex (Lowe, 2011;Saraste & Prydz, 2019). In contrast, the Golgi apparatus of higher plants consists of discrete mobile Golgi stacks (up to several hundred per cell) distributed throughout the cytoplasm (Ito et al, 2014) (see Fig.…”

De Novo and Inherited Variants in GBF1 are Associated with Axonal Neuropathy Caused by Golgi Fragmentation

“… 57 , 58 In general, GA defects are considered as early or preclinical indicators of neuronal loss and range from extensive Golgi unstacking, vesiculation, and ribbon disconnection to generalized Golgi atrophy (loss of Golgi membrane material). Loss of Golgi integrity can have a detrimental effect in cargo transport velocity, 59 mitosis completion, 54 autophagy regulation, 60 cell polarity, and migration. 61 Most precisely, in neurons, the GA is crucial for dendrite formation and growth, axonal polarity, and cell migration during brain development.…”