Stacked Endoplasmic Reticulum Sheets Are Connected by Helicoidal Membrane Motifs

Abstract

The endoplasmic reticulum (ER) often forms stacked membrane sheets, an arrangement that is likely required to accommodate a maximum of membrane-bound polysomes for secretory protein synthesis. How sheets are stacked is unknown. Here, we used novel staining and automated ultra-thin sectioning electron microscopy methods to analyze stacked ER sheets in neuronal cells and secretory salivary gland cells of mice. Our results show that stacked ER sheets form a continuous membrane system in which the sheets are connected by twisted membrane surfaces with helical edges of left- or right-handedness. The three-dimensional structure of tightly stacked ER sheets resembles a parking garage, in which the different levels are connected by helicoidal ramps. A theoretical model explains the experimental observations and indicates that the structure corresponds to a minimum of elastic energy of sheet edges and surfaces. The structure allows the dense packing of ER sheets in the restricted space of a cell.

Environmental bias and elastic curves on surfaces

“…Whereas a line tension induced on the boundary of a fluid membrane will tend to heal the disruption caused by the edge, [36,37,38] a boundary providing resistance to bending-or selecting some preferred curvature-can provide stable ends to an otherwise unstable membrane preventing its closure. The inner boundary of the recently discovered Terasaki ramps in the rough endoplasmic reticulum are believed to be stabilized by a mechanism of this kind due to the condensation, along it, of reticulons [39]. Unfortunately, as anyone who has taken a moment to ponder these boundary conditions will have noted-even in the apparently simple scenario where the boundary energy is dominated by line tension-getting them right is a challenge.…”

Nup53 interaction with Ndc1 and Nup155 are required for nuclear pore complex assembly

“…This final membrane shape is characterized by the coexistence of a positive and a negative curvature. Because the negative curvature could energetically balance the positive curvature (Terasaki et al, 2013), the final pore membrane structure might be passively adopted and might not require active membrane deformation as induced by Nup53. In this regard, Ndc1 might be the crucial factor regulating the membranedeformation activity of Nup53 in the NPC.…”

Onsager’s Variational Principle in Soft Matter: Introduction and Application to the Dynamics of Adsorption of Proteins onto Fluid Membranes

“…However, we will consider the possibility that the area fraction is finite, and even large. Large area coverage of membrane proteins is common in synthetic systems (Sorre et al, 2012;Zhu et al, 2012) and in cell organelles (Shibata et al, 2009;Terasaki et al, 2013). Molecular crowding of proteins on the membrane can then lead to nonlinear chemical effects as discussed in the introduction.…”