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TMX4-driven LINC complex disassembly and asymmetric autophagy of the nuclear envelope upon acute ER stress

Author

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  • Marika K. Kucińska

    (Università della Svizzera italiana (USI), Faculty of Biomedical Sciences, Institute for Research in Biomedicine
    Swiss Federal Institute of Technology)

  • Juliette Fedry

    (Utrecht University)

  • Carmela Galli

    (Università della Svizzera italiana (USI), Faculty of Biomedical Sciences, Institute for Research in Biomedicine)

  • Diego Morone

    (Università della Svizzera italiana (USI), Faculty of Biomedical Sciences, Institute for Research in Biomedicine
    University of Bern)

  • Andrea Raimondi

    (Università della Svizzera italiana (USI), Faculty of Biomedical Sciences, Institute for Research in Biomedicine
    San Raffaele Scientific Institute)

  • Tatiana Soldà

    (Università della Svizzera italiana (USI), Faculty of Biomedical Sciences, Institute for Research in Biomedicine)

  • Friedrich Förster

    (Utrecht University)

  • Maurizio Molinari

    (Università della Svizzera italiana (USI), Faculty of Biomedical Sciences, Institute for Research in Biomedicine
    École Polytechnique Fédérale de Lausanne)

Abstract

The endoplasmic reticulum (ER) is an organelle of nucleated cells that produces proteins, lipids and oligosaccharides. ER volume and activity are increased upon induction of unfolded protein responses (UPR) and are reduced upon activation of ER-phagy programs. A specialized domain of the ER, the nuclear envelope (NE), protects the cell genome with two juxtaposed lipid bilayers, the inner and outer nuclear membranes (INM and ONM) separated by the perinuclear space (PNS). Here we report that expansion of the mammalian ER upon homeostatic perturbations results in TMX4 reductase-driven disassembly of the LINC complexes connecting INM and ONM and in ONM swelling. The physiologic distance between ONM and INM is restored, upon resolution of the ER stress, by asymmetric autophagy of the NE, which involves the LC3 lipidation machinery, the autophagy receptor SEC62 and the direct capture of ONM-derived vesicles by degradative LAMP1/RAB7-positive endolysosomes in a catabolic pathway mechanistically defined as micro-ONM-phagy.

Suggested Citation

  • Marika K. Kucińska & Juliette Fedry & Carmela Galli & Diego Morone & Andrea Raimondi & Tatiana Soldà & Friedrich Förster & Maurizio Molinari, 2023. "TMX4-driven LINC complex disassembly and asymmetric autophagy of the nuclear envelope upon acute ER stress," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39172-3
    DOI: 10.1038/s41467-023-39172-3
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    References listed on IDEAS

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    1. John Fielden & Katherine Wiseman & Ignacio Torrecilla & Shudong Li & Samuel Hume & Shih-Chieh Chiang & Annamaria Ruggiano & Abhay Narayan Singh & Raimundo Freire & Sylvana Hassanieh & Enric Domingo & , 2020. "TEX264 coordinates p97- and SPRTN-mediated resolution of topoisomerase 1-DNA adducts," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. Jiajie Diao & Rong Liu & Yueguang Rong & Minglei Zhao & Jing Zhang & Ying Lai & Qiangjun Zhou & Livia M. Wilz & Jianxu Li & Sandro Vivona & Richard A. Pfuetzner & Axel T. Brunger & Qing Zhong, 2015. "ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes," Nature, Nature, vol. 520(7548), pages 563-566, April.
    3. Maurizio Molinari & Ari Helenius, 1999. "Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells," Nature, Nature, vol. 402(6757), pages 90-93, November.
    4. Marisa Loi & Andrea Raimondi & Diego Morone & Maurizio Molinari, 2019. "ESCRT-III-driven piecemeal micro-ER-phagy remodels the ER during recovery from ER stress," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    5. Akiko Kuma & Masahiko Hatano & Makoto Matsui & Akitsugu Yamamoto & Haruaki Nakaya & Tamotsu Yoshimori & Yoshinori Ohsumi & Takeshi Tokuhisa & Noboru Mizushima, 2004. "The role of autophagy during the early neonatal starvation period," Nature, Nature, vol. 432(7020), pages 1032-1036, December.
    6. Aliaksandr Khaminets & Theresa Heinrich & Muriel Mari & Paolo Grumati & Antje K. Huebner & Masato Akutsu & Lutz Liebmann & Alexandra Stolz & Sandor Nietzsche & Nicole Koch & Mario Mauthe & Istvan Kato, 2015. "Regulation of endoplasmic reticulum turnover by selective autophagy," Nature, Nature, vol. 522(7556), pages 354-358, June.
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