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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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