XStacked endoplasmic reticulum sheets are connected by helicoidal membrane motifs

Mark Terasaki; Tom Shemesh; Narayanan Kasthuri; Robin W. Klemm; Richard Schalek; Kenneth J. Hayworth; Arthur R. Hand; Maya Yankova; Greg Huber; Jeff W. Lichtman; Tom A. Rapoport; Michael M. Kozlov

doi:10.1016/j.cell.2013.06.031

XStacked endoplasmic reticulum sheets are connected by helicoidal membrane motifs

Mark Terasaki^*, Tom Shemesh, Narayanan Kasthuri, Robin W. Klemm, Richard Schalek, Kenneth J. Hayworth, Arthur R. Hand, Maya Yankova, Greg Huber, Jeff W. Lichtman, Tom A. Rapoport, Michael M. Kozlov

^*Corresponding author for this work

Physiology Pharmacology

Research output: Contribution to journal › Article › peer-review

189 Scopus citations

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 improved staining and automated ultrathin 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.

Original language	English
Pages (from-to)	285
Number of pages	1
Journal	Cell
Volume	154
Issue number	2
DOIs	https://doi.org/10.1016/j.cell.2013.06.031
State	Published - 18 Jul 2013

Funding

Funders	Funder number
Joseph Klafter Chair in Biophysics
Marie Curie Network
National Science Foundation	NSF PHY11-25915
National Institute of Biomedical Imaging and Bioengineering	R01EB016411
Israel Science Foundation

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10.1016/j.cell.2013.06.031

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title = "XStacked 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 improved staining and automated ultrathin 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.",

author = "Mark Terasaki and Tom Shemesh and Narayanan Kasthuri and Klemm, {Robin W.} and Richard Schalek and Hayworth, {Kenneth J.} and Hand, {Arthur R.} and Maya Yankova and Greg Huber and Lichtman, {Jeff W.} and Rapoport, {Tom A.} and Kozlov, {Michael M.}",

note = "Funding Information: We thank Shigeki Watanabe for providing his unpublished freeze substitution protocol and Yoko Shibata, Rindy Jaffe, and Adrian Salic for critical reading of the manuscript. We thank Sid Tamm for pointing out the parking garage analogy. M.M.K. is supported by the Israel Science Foundation (ISF) and the Marie Curie network “Virus Entry” and holds the Joseph Klafter Chair in Biophysics. T.A.R. is a Howard Hughes Medical Institute Investigator. G.H. acknowledges support from the National Science Foundation under grant NSF PHY11-25915 and from the Richard Berlin Center for Cell Analysis and Modeling. ",

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AU - Terasaki, Mark

AU - Shemesh, Tom

AU - Kasthuri, Narayanan

AU - Klemm, Robin W.

AU - Schalek, Richard

AU - Hayworth, Kenneth J.

AU - Hand, Arthur R.

AU - Yankova, Maya

AU - Huber, Greg

AU - Lichtman, Jeff W.

AU - Rapoport, Tom A.

AU - Kozlov, Michael M.

N1 - Funding Information: We thank Shigeki Watanabe for providing his unpublished freeze substitution protocol and Yoko Shibata, Rindy Jaffe, and Adrian Salic for critical reading of the manuscript. We thank Sid Tamm for pointing out the parking garage analogy. M.M.K. is supported by the Israel Science Foundation (ISF) and the Marie Curie network “Virus Entry” and holds the Joseph Klafter Chair in Biophysics. T.A.R. is a Howard Hughes Medical Institute Investigator. G.H. acknowledges support from the National Science Foundation under grant NSF PHY11-25915 and from the Richard Berlin Center for Cell Analysis and Modeling.

PY - 2013/7/18

Y1 - 2013/7/18

N2 - 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 improved staining and automated ultrathin 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.

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XStacked endoplasmic reticulum sheets are connected by helicoidal membrane motifs

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