Progressive sheet-to-tubule transformation is a general mechanism for endoplasmic reticulum partitioning in dividing mammalian cells

Abstract

During mitosis, ER network reorganization can lead to packing of the ER into tight concentric layers at the cell cortex and occurs in tandem with rounding of the cell. Morphometric and 3D EM analysis shows that in addition to reorganization, ER sheets undergo transformation toward more fenestrated and tubular forms before anaphase in mammalian cells.

Endoplasmic Reticulum Structure and Interconnections with Other Organelles

“…Cisternae do have higher concentrations of ribosomes than tubules and also have a larger luminal volume to surface area than tubules, suggesting that they would be the preferred site for luminal processes like protein folding (Fig. 1C) (Shibata et al 2010;West et al 2011;Puhka et al 2012). Consistent with this idea, during the ER stress response yeast peripheral ER shows increased cisternae to accommodate an increase in protein folding (Schuck et al 2009).…”

“…The disparity in conclusions could result from the complexity of ER domains that are reorganized as a result of NE breakdown and relocalization of the mitotic ER toward the cell periphery. Three-dimensional EM tomography reveals domains that appear cisternal by fluorescence microscopy are in fact highly fenestrated and may still contain a high degree of membrane curvature (Puhka et al 2012). It is possible that together these data show that when the NE and ER are redistributed to the periphery during mitosis, the total amount of ER membrane curvature is accommodated through differently shaped mitotic ER domains.…”

“…Analysis of ER structure in HeLa cells and CHO cells, by live 3D confocal fluorescence microscopy and electron microscopy (EM), reveals an interphase ER morphology that is cisternal in the perinuclear region and mostly tubular in the periphery towards the PM, and a mitotic morphology that is almost entirely cisternal (McCullough and Lucocq 2005;Lu et al 2009). In contrast, experiments where ER structure was analyzed by transmission EM and EM tomography of either chemically fixed or highpressure frozen cells, reveal an ER structure that is mostly cisternal in interphase and more fenestrated and tubular in mitosis (Puhka et al 2007(Puhka et al , 2012. The disparity in conclusions could result from the complexity of ER domains that are reorganized as a result of NE breakdown and relocalization of the mitotic ER toward the cell periphery.…”

“…Specifically, the interphase peripheral ER is dispersed throughout the cytoplasm, whereas the mitotic ER is located near the PM and away from the mitotic spindle ( Fig. 2A) (McCullough and Lucocq 2005;Puhka et al 2007Puhka et al , 2012Anderson and Hetzer 2008b;Lu et al 2009;Hetzer 2010;Lu et al 2011;Smyth et al 2012). The mechanism and proteins involved in regulating ER movement during mitosis are not well understood; however, it was recently shown that phosphorylation of STIM1 is required to prevent the ER membrane from associating with the mitotic spindle (Smyth et al 2012).…”

“…ER tubules have lower luminal volume to surface area than cisternae, suggesting that ER tubules could be the preferred site for the accumulation of integral membrane proteins and for processes connected to lipid synthesis . Nevertheless, there are many examples of ER tubules that do have bound ribosomes, just at a lower density than cisternae, which shows that they are not always ribosome excluded Puhka et al 2012).…”