The Endoplasmic Reticulum Connects to the Nucleus by Constricted Junctions That Mature After Mitosis

Overview

Journal EMBO Rep

Specialty Molecular Biology

Date 2024 Jun 14

PMID 38877171

Authors

Helena Bragulat-Teixidor

Keisuke Ishihara

Greta Martina Szucs

Shotaro Otsuka

Affiliations

Soon will be listed here.

Abstract

Junctions between the endoplasmic reticulum (ER) and the outer membrane of the nuclear envelope (NE) physically connect both organelles. These ER-NE junctions are essential for supplying the NE with lipids and proteins synthesized in the ER. However, little is known about the structure of these ER-NE junctions. Here, we systematically study the ultrastructure of ER-NE junctions in cryo-fixed mammalian cells staged in anaphase, telophase, and interphase by correlating live cell imaging with three-dimensional electron microscopy. Our results show that ER-NE junctions in interphase cells have a pronounced hourglass shape with a constricted neck of 7-20 nm width. This morphology is significantly distinct from that of junctions within the ER network, and their morphology emerges as early as telophase. The highly constricted ER-NE junctions are seen in several mammalian cell types, but not in budding yeast. We speculate that the unique and highly constricted ER-NE junctions are regulated via novel mechanisms that contribute to ER-to-NE lipid and protein traffic in higher eukaryotes.

Citing Articles

Endoplasmic Reticulum Stress in Bronchopulmonary Dysplasia: Contributor or Consequence?.

Wu T, Teng M, Jing X, Pritchard Jr K, Day B, Naylor S Cells. 2024; 13(21.

PMID: 39513884 PMC: 11544778. DOI: 10.3390/cells13211774.

Mechanisms for assembly of the nucleoplasmic reticulum.

McPhee M, Dellaire G, Ridgway N Cell Mol Life Sci. 2024; 81(1):415.

PMID: 39367888 PMC: 11455740. DOI: 10.1007/s00018-024-05437-3.

References

Pawar S, Ungricht R, Tiefenboeck P, Leroux J, Kutay U . Efficient protein targeting to the inner nuclear membrane requires Atlastin-dependent maintenance of ER topology. Elife. 2017; 6. PMC: 5587084. DOI: 10.7554/eLife.28202. View

Albert S, Schaffer M, Beck F, Mosalaganti S, Asano S, Thomas H . Proteasomes tether to two distinct sites at the nuclear pore complex. Proc Natl Acad Sci U S A. 2017; 114(52):13726-13731. PMC: 5748218. DOI: 10.1073/pnas.1716305114. View

Dahl R, Staehelin L . High-pressure freezing for the preservation of biological structure: theory and practice. J Electron Microsc Tech. 1989; 13(3):165-74. DOI: 10.1002/jemt.1060130305. View

Antonny B, Burd C, De Camilli P, Chen E, Daumke O, Faelber K . Membrane fission by dynamin: what we know and what we need to know. EMBO J. 2016; 35(21):2270-2284. PMC: 5090216. DOI: 10.15252/embj.201694613. View

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T . Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012; 9(7):676-82. PMC: 3855844. DOI: 10.1038/nmeth.2019. View

Rossini M, Pizzo P, Filadi R . Better to keep in touch: investigating inter-organelle cross-talk. FEBS J. 2020; 288(3):740-755. DOI: 10.1111/febs.15451. View

Kozlov M, Taraska J . Generation of nanoscopic membrane curvature for membrane trafficking. Nat Rev Mol Cell Biol. 2022; 24(1):63-78. DOI: 10.1038/s41580-022-00511-9. View

Ungricht R, Klann M, Horvath P, Kutay U . Diffusion and retention are major determinants of protein targeting to the inner nuclear membrane. J Cell Biol. 2015; 209(5):687-703. PMC: 4460150. DOI: 10.1083/jcb.201409127. View

Deschuyteneer M, Eckhardt A, Roth J, Hill R . The subcellular localization of apomucin and nonreducing terminal N-acetylgalactosamine in porcine submaxillary glands. J Biol Chem. 1988; 263(5):2452-9. View

10.

Kremer J, Mastronarde D, McIntosh J . Computer visualization of three-dimensional image data using IMOD. J Struct Biol. 1996; 116(1):71-6. DOI: 10.1006/jsbi.1996.0013. View

11.

Bahmanyar S, Schlieker C . Lipid and protein dynamics that shape nuclear envelope identity. Mol Biol Cell. 2020; 31(13):1315-1323. PMC: 7353140. DOI: 10.1091/mbc.E18-10-0636. View

12.

Wang S, Tukachinsky H, Romano F, Rapoport T . Cooperation of the ER-shaping proteins atlastin, lunapark, and reticulons to generate a tubular membrane network. Elife. 2016; 5. PMC: 5021524. DOI: 10.7554/eLife.18605. View

13.

Lee S, Carrasquillo Rodri Guez J, Merta H, Bahmanyar S . A membrane-sensing mechanism links lipid metabolism to protein degradation at the nuclear envelope. J Cell Biol. 2023; 222(9). PMC: 10309186. DOI: 10.1083/jcb.202304026. View

14.

Arslan I, Tong J, Midgley P . Reducing the missing wedge: High-resolution dual axis tomography of inorganic materials. Ultramicroscopy. 2006; 106(11-12):994-1000. DOI: 10.1016/j.ultramic.2006.05.010. View

15.

Nixon-Abell J, Obara C, Weigel A, Li D, Legant W, Xu C . Increased spatiotemporal resolution reveals highly dynamic dense tubular matrices in the peripheral ER. Science. 2016; 354(6311). PMC: 6528812. DOI: 10.1126/science.aaf3928. View

16.

Bragulat-Teixidor H, Otsuka S . Correlative light and electron microscopy at defined cell cycle stages in a controlled environment. Methods Cell Biol. 2024; 187:73-97. DOI: 10.1016/bs.mcb.2024.02.025. View

17.

Peeters B, Piet A, Fornerod M . Generating Membrane Curvature at the Nuclear Pore: A Lipid Point of View. Cells. 2022; 11(3). PMC: 8834089. DOI: 10.3390/cells11030469. View

18.

Preibisch S, Saalfeld S, Tomancak P . Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics. 2009; 25(11):1463-5. PMC: 2682522. DOI: 10.1093/bioinformatics/btp184. View

19.

Craig S, Staehelin L . High pressure freezing of intact plant tissues. Evaluation and characterization of novel features of the endoplasmic reticulum and associated membrane systems. Eur J Cell Biol. 1988; 46(1):81-93. View

20.

Mosalaganti S, Obarska-Kosinska A, Siggel M, Taniguchi R, Turonova B, Zimmerli C . AI-based structure prediction empowers integrative structural analysis of human nuclear pores. Science. 2022; 376(6598):eabm9506. DOI: 10.1126/science.abm9506. View