Calumenin-1 Interacts with Climp63 to Cooperatively Determine the Luminal Width and Distribution of Endoplasmic Reticulum Sheets

Birong Shen; Pengli Zheng; Nannan Qian; Qingzhou Chen; Xin Zhou; Junjie Hu; Jianguo Chen; Junlin Teng

doi:10.1016/j.isci.2019.10.067

Calumenin-1 Interacts with Climp63 to Cooperatively Determine the Luminal Width and Distribution of Endoplasmic Reticulum Sheets

iScience. 2019 Dec 20:22:70-80. doi: 10.1016/j.isci.2019.10.067. Epub 2019 Nov 2.

Authors

Birong Shen¹, Pengli Zheng¹, Nannan Qian², Qingzhou Chen¹, Xin Zhou³, Junjie Hu⁴, Jianguo Chen⁵, Junlin Teng⁶

Affiliations

¹ Key Laboratory of Cell Proliferation and Differentiation of the Ministry of Education, State Key Laboratory of Membrane Biology, College of Life Sciences, Peking University, Beijing 100871, China.
² Key Laboratory of Cell Proliferation and Differentiation of the Ministry of Education, State Key Laboratory of Membrane Biology, College of Life Sciences, Peking University, Beijing 100871, China; College of Life Sciences, Jiangsu Normal University, Xuzhou 221116, China.
³ Department of Genetics and Cell Biology, College of Life Sciences, Nankai University and Tianjin Key Laboratory of Protein Sciences, Tianjin 300071, China.
⁴ National Laboratory of Biomacromolecules and CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China; Department of Genetics and Cell Biology, College of Life Sciences, Nankai University and Tianjin Key Laboratory of Protein Sciences, Tianjin 300071, China.
⁵ Key Laboratory of Cell Proliferation and Differentiation of the Ministry of Education, State Key Laboratory of Membrane Biology, College of Life Sciences, Peking University, Beijing 100871, China; Center for Quantitative Biology, Peking University, Beijing 100871, China. Electronic address: chenjg@pku.edu.cn.
⁶ Key Laboratory of Cell Proliferation and Differentiation of the Ministry of Education, State Key Laboratory of Membrane Biology, College of Life Sciences, Peking University, Beijing 100871, China. Electronic address: junlinteng@pku.edu.cn.

Abstract

The ER is composed of distinct structures like tubules, matrices, and sheets, all of which are important for its various functions. However, how these distinct ER structures, especially the perinuclear ER sheets, are formed remains unclear. We report here that the ER membrane protein Climp63 and the ER luminal protein calumenin-1 (Calu1) collaboratively maintain ER sheet morphology. We show that the luminal length of Climp63 is positively correlated with the luminal width of ER sheets. Moreover, the lumen-only mutant of Climp63 dominant-negatively narrows the lumen of ER sheets, demonstrating that Climp63 acts as an ER luminal bridge. We also reveal that Calu1 specifically interacts with Climp63 and antagonizes Climp63 in terms of both ER sheet distribution and luminal width. Together, our data provide insight into how the structure of ER sheets is maintained and regulated.

Keywords: Cell Biology; Membrane Architecture; Molecular Biology; Molecular Interaction; Organizational Aspects of Cell Biology.