Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells

Abstract

Here, we characterize spatial distribution of the Golgi complex in human cells. In contrast to the prevailing view that the Golgi compactly surrounds the centrosome throughout interphase, we observe characteristic differences in the morphology of Golgi ribbons and their association with the centrosome during various periods of the cell cycle. The compact Golgi complex is typical in G1; during S-phase, Golgi ribbons lose their association with the centrosome and extend along the nuclear envelope to largely encircle the nucleus in G2. Interestingly, pre-mitotic separation of duplicated centrosomes always occurs after dissociation from the Golgi. Shortly before the nuclear envelope breakdown, scattered Golgi ribbons reassociate with the separated centrosomes restoring two compact Golgi complexes. Transitions between the compact and distributed Golgi morphologies are microtubule-dependent. However, they occur even in the absence of centrosomes, which implies that Golgi reorganization is not driven by the centrosomal microtubule asters. Cells with different Golgi morphology exhibit distinct differences in the directional persistence and velocity of migration. These data suggest that changes in the radial distribution of the Golgi around the nucleus define the extent of cell polarization and regulate cell motility in a cell cycle-dependent manner.

Endothelial cell polarization and orientation to flow in a novel microfluidic multimodal shear stress generator

“…Analysis of nuclear and Golgi size and position suggested that this increase was likely due to both nuclear and Golgi compaction combined with increased Golgi-nucleus distance, which were similar across all shear stress modalities. Based on reports of compact organellar morphologies in G1-phase hTert-RPE1 cells 56 and reports that flow leads to cell cycle arrest at G1/S transition in HUVECs 57 , we speculate that increased polarization reflects flow-mediated cell cycle arrest.…”

Structural Organization and Function of the Golgi Ribbon During Cell Division

“…As the GC is closely associated with the CEs, a possibility is that Golgi unlinking could be necessary to remove a steric hindrance that could hamper CE separation in G2. However, this is unlikely since the GC is dissociated from the CE during this phase (Frye et al, 2020). Moreover, inhibition of Golgi unlinking does not alter CEs separation (Persico et al, 2010).…”

Emerging roles of centrosome cohesion

“…However, CEP250 KO cells showed defects in the spatial organization of the Golgi apparatus and cell migration [ 33 , 39 ]. It is long known that centrosome derived MTs position the Golgi apparatus of a cell [ 40 , 41 ] and therefore it is easy to envision that the two separated centrosomes in CEP250 KO cells each position spatially distinct Golgi stacks. In addition, in human and rodent cell lines, centrosome orientation was shown to be important to maintain polarization in migrating cells [ 42 , 43 ].…”