Stay in touch with the endoplasmic reticulum

doi:10.1007/s11427-023-2443-9

Review

. 2024 Feb;67(2):230-257.

doi: 10.1007/s11427-023-2443-9. Epub 2024 Jan 4.

Stay in touch with the endoplasmic reticulum

Sha Sun^#¹, Gan Zhao^#², Mingkang Jia^#², Qing Jiang^#², Shulin Li^#³, Haibin Wang^#¹, Wenjing Li^#⁴, Yunyun Wang^#⁵, Xin Bian⁶, Yan G Zhao⁷, Xun Huang⁸, Ge Yang⁹, Huaqing Cai¹⁰, Jose C Pastor-Pareja^{11

12}, Liang Ge¹³, Chuanmao Zhang¹⁴, Junjie Hu¹⁵

Affiliations

¹ National Laboratory of Biomacromolecules, Institute of Biophysics, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, 100101, China.
² The Ministry of Education Key Laboratory of Cell Proliferation and Differentiation, College of Life Sciences, Peking University, Beijing, 100871, China.
³ State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China.
⁴ Laboratory of Computational Biology & Machine Intelligence, School of Artificial Intelligence, University of Chinese Academy of Sciences, Beijing, 100049, China.
⁵ State Key Laboratory of Medicinal Chemical Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China.
⁶ State Key Laboratory of Medicinal Chemical Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China. xin.bian@nankai.edu.cn.
⁷ Brain Research Center, Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen, 518055, China. zhaoyan@sustech.edu.cn.
⁸ State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing, 100101, China. xhuang@genetics.ac.cn.
⁹ Laboratory of Computational Biology & Machine Intelligence, School of Artificial Intelligence, University of Chinese Academy of Sciences, Beijing, 100049, China. ge.yang@ia.ac.cn.
¹⁰ National Laboratory of Biomacromolecules, Institute of Biophysics, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, 100101, China. huaqingcai@ibp.ac.cn.
¹¹ State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China. josepastor@tsinghua.edu.cn.
¹² Institute of Neurosciences, Consejo Superior de Investigaciones Cientfflcas-Universidad Miguel Hernandez, San Juan de Alicante, 03550, Spain. josepastor@tsinghua.edu.cn.
¹³ State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China. liangge@mail.tsinghua.edu.cn.
¹⁴ The Ministry of Education Key Laboratory of Cell Proliferation and Differentiation, College of Life Sciences, Peking University, Beijing, 100871, China. zhangcm@pku.edu.cn.
¹⁵ National Laboratory of Biomacromolecules, Institute of Biophysics, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, 100101, China. huj@ibp.ac.cn.

^# Contributed equally.

PMID: 38212460
DOI: 10.1007/s11427-023-2443-9

Review

Stay in touch with the endoplasmic reticulum

Sha Sun et al. Sci China Life Sci. 2024 Feb.

. 2024 Feb;67(2):230-257.

doi: 10.1007/s11427-023-2443-9. Epub 2024 Jan 4.

Authors

Affiliations

¹ National Laboratory of Biomacromolecules, Institute of Biophysics, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, 100101, China.
² The Ministry of Education Key Laboratory of Cell Proliferation and Differentiation, College of Life Sciences, Peking University, Beijing, 100871, China.
³ State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China.
⁴ Laboratory of Computational Biology & Machine Intelligence, School of Artificial Intelligence, University of Chinese Academy of Sciences, Beijing, 100049, China.
⁵ State Key Laboratory of Medicinal Chemical Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China.
⁶ State Key Laboratory of Medicinal Chemical Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China. xin.bian@nankai.edu.cn.
⁷ Brain Research Center, Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen, 518055, China. zhaoyan@sustech.edu.cn.
⁸ State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing, 100101, China. xhuang@genetics.ac.cn.
⁹ Laboratory of Computational Biology & Machine Intelligence, School of Artificial Intelligence, University of Chinese Academy of Sciences, Beijing, 100049, China. ge.yang@ia.ac.cn.
¹⁰ National Laboratory of Biomacromolecules, Institute of Biophysics, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, 100101, China. huaqingcai@ibp.ac.cn.
¹¹ State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China. josepastor@tsinghua.edu.cn.
¹² Institute of Neurosciences, Consejo Superior de Investigaciones Cientfflcas-Universidad Miguel Hernandez, San Juan de Alicante, 03550, Spain. josepastor@tsinghua.edu.cn.
¹³ State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China. liangge@mail.tsinghua.edu.cn.
¹⁴ The Ministry of Education Key Laboratory of Cell Proliferation and Differentiation, College of Life Sciences, Peking University, Beijing, 100871, China. zhangcm@pku.edu.cn.
¹⁵ National Laboratory of Biomacromolecules, Institute of Biophysics, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, 100101, China. huj@ibp.ac.cn.

^# Contributed equally.

PMID: 38212460
DOI: 10.1007/s11427-023-2443-9

Abstract

The endoplasmic reticulum (ER), which is composed of a continuous network of tubules and sheets, forms the most widely distributed membrane system in eukaryotic cells. As a result, it engages a variety of organelles by establishing membrane contact sites (MCSs). These contacts regulate organelle positioning and remodeling, including fusion and fission, facilitate precise lipid exchange, and couple vital signaling events. Here, we systematically review recent advances and converging themes on ER-involved organellar contact. The molecular basis, cellular influence, and potential physiological functions for ER/nuclear envelope contacts with mitochondria, Golgi, endosomes, lysosomes, lipid droplets, autophagosomes, and plasma membrane are summarized.

Keywords: Golgi apparatus; autophagosome; endoplasmic reticulum; endosome; lipid droplets; lysosome; membrane contact site; mitochondria; nuclear envelope; plasma membrane.

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References

1. AhYoung, A.P., Jiang, J., Zhang, J., Khoi Dang, X., Loo, J.A., Zhou, Z.H., and Egea, P.F. (2015). Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc Natl Acad Sci USA 112, E3179–3188. - PubMed - PMC - DOI
1. Allison, R., Edgar, J.R., Pearson, G., Rizo, T., Newton, T., Günther, S., Berner, F., Hague, J., Connell, J.W., Winkler, J., et al. (2017). Defects in ER-endosome contacts impact lysosome function in hereditary spastic paraplegia. J Cell Biol 216, 1337–1355. - PubMed - PMC - DOI
1. Allison, R., Lumb, J.H., Fassier, C., Connell, J.W., Ten Martin, D., Seaman, M.N.J., Hazan, J., and Reid, E. (2013). An ESCRT-spastin interaction promotes fission of recycling tubules from the endosome. J Cell Biol 202, 527–543. - PubMed - PMC - DOI
1. Alpy, F., Rousseau, A., Schwab, Y., Legueux, F., Stoll, I., Wendling, C., Spiegelhalter, C., Kessler, P., Mathelin, C., Rio, M.C., et al. (2013). STARD3/STARD3NL and VAP make a novel molecular tether between late endosomes and the ER. J Cell Sci 126, jcs.139295. - DOI
1. Alpy, F., and Tomasetto, C. (2014). START ships lipids across interorganelle space. Biochimie 96, 85–95. - PubMed - DOI

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[1] AhYoung, A.P., Jiang, J., Zhang, J., Khoi Dang, X., Loo, J.A., Zhou, Z.H., and Egea, P.F. (2015). Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc Natl Acad Sci USA 112, E3179–3188. - PubMed - PMC - DOI

[2] AhYoung, A.P., Jiang, J., Zhang, J., Khoi Dang, X., Loo, J.A., Zhou, Z.H., and Egea, P.F. (2015). Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc Natl Acad Sci USA 112, E3179–3188. - PubMed - PMC - DOI

[3] Allison, R., Edgar, J.R., Pearson, G., Rizo, T., Newton, T., Günther, S., Berner, F., Hague, J., Connell, J.W., Winkler, J., et al. (2017). Defects in ER-endosome contacts impact lysosome function in hereditary spastic paraplegia. J Cell Biol 216, 1337–1355. - PubMed - PMC - DOI

[4] Allison, R., Edgar, J.R., Pearson, G., Rizo, T., Newton, T., Günther, S., Berner, F., Hague, J., Connell, J.W., Winkler, J., et al. (2017). Defects in ER-endosome contacts impact lysosome function in hereditary spastic paraplegia. J Cell Biol 216, 1337–1355. - PubMed - PMC - DOI

[5] Allison, R., Lumb, J.H., Fassier, C., Connell, J.W., Ten Martin, D., Seaman, M.N.J., Hazan, J., and Reid, E. (2013). An ESCRT-spastin interaction promotes fission of recycling tubules from the endosome. J Cell Biol 202, 527–543. - PubMed - PMC - DOI

[6] Allison, R., Lumb, J.H., Fassier, C., Connell, J.W., Ten Martin, D., Seaman, M.N.J., Hazan, J., and Reid, E. (2013). An ESCRT-spastin interaction promotes fission of recycling tubules from the endosome. J Cell Biol 202, 527–543. - PubMed - PMC - DOI

[7] Alpy, F., Rousseau, A., Schwab, Y., Legueux, F., Stoll, I., Wendling, C., Spiegelhalter, C., Kessler, P., Mathelin, C., Rio, M.C., et al. (2013). STARD3/STARD3NL and VAP make a novel molecular tether between late endosomes and the ER. J Cell Sci 126, jcs.139295. - DOI

[8] Alpy, F., Rousseau, A., Schwab, Y., Legueux, F., Stoll, I., Wendling, C., Spiegelhalter, C., Kessler, P., Mathelin, C., Rio, M.C., et al. (2013). STARD3/STARD3NL and VAP make a novel molecular tether between late endosomes and the ER. J Cell Sci 126, jcs.139295. - DOI

[9] Alpy, F., and Tomasetto, C. (2014). START ships lipids across interorganelle space. Biochimie 96, 85–95. - PubMed - DOI

[10] Alpy, F., and Tomasetto, C. (2014). START ships lipids across interorganelle space. Biochimie 96, 85–95. - PubMed - DOI

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Stay in touch with the endoplasmic reticulum

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Stay in touch with the endoplasmic reticulum

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