IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39172-3.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39172-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-39172-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Patricia González-Rodríguez & Daniel J. Klionsky & Bertrand Joseph, 2022. "Autophagy regulation by RNA alternative splicing and implications in human diseases," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Shuangcheng Alivia Wu & Chenchen Shen & Xiaoqiong Wei & Xiawei Zhang & Siwen Wang & Xinxin Chen & Mauricio Torres & You Lu & Liangguang Leo Lin & Huilun Helen Wang & Allen H. Hunter & Deyu Fang & Shen, 2023. "The mechanisms to dispose of misfolded proteins in the endoplasmic reticulum of adipocytes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Hong Huang & Qinqin Ouyang & Min Zhu & Haijia Yu & Kunrong Mei & Rong Liu, 2021. "mTOR-mediated phosphorylation of VAMP8 and SCFD1 regulates autophagosome maturation," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Aftab Nadeem & Athar Alam & Eric Toh & Si Lhyam Myint & Zia ur Rehman & Tao Liu & Marta Bally & Anna Arnqvist & Hui Wang & Jun Zhu & Karina Persson & Bernt Eric Uhlin & Sun Nyunt Wai, 2021. "Phosphatidic acid-mediated binding and mammalian cell internalization of the Vibrio cholerae cytotoxin MakA," PLOS Pathogens, Public Library of Science, vol. 17(3), pages 1-34, March.
    5. Yu-Jie Chen & Jeffrey Knupp & Anoop Arunagiri & Leena Haataja & Peter Arvan & Billy Tsai, 2021. "PGRMC1 acts as a size-selective cargo receptor to drive ER-phagic clearance of mutant prohormones," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    6. Catherine J. Greene & Jenny A. Nguyen & Samuel M. Cheung & Corey R. Arnold & Dale R. Balce & Ya Ting Wang & Adrian Soderholm & Neil McKenna & Devin Aggarwal & Rhiannon I. Campden & Benjamin W. Ewanchu, 2022. "Macrophages disseminate pathogen associated molecular patterns through the direct extracellular release of the soluble content of their phagolysosomes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    7. Ryosuke Ishimura & Afnan H. El-Gowily & Daisuke Noshiro & Satoko Komatsu-Hirota & Yasuko Ono & Mayumi Shindo & Tomohisa Hatta & Manabu Abe & Takefumi Uemura & Hyeon-Cheol Lee-Okada & Tarek M. Mohamed , 2022. "The UFM1 system regulates ER-phagy through the ufmylation of CYB5R3," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Zita Fábián & Ellen S. Kakulidis & Ivo A. Hendriks & Ulrike Kühbacher & Nicolai B. Larsen & Marta Oliva-Santiago & Junhui Wang & Xueyuan Leng & A. Barbara Dirac-Svejstrup & Jesper Q. Svejstrup & Micha, 2024. "PARP1-dependent DNA-protein crosslink repair," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Pedro Weickert & Hao-Yi Li & Maximilian J. Götz & Sophie Dürauer & Denitsa Yaneva & Shubo Zhao & Jacqueline Cordes & Aleida C. Acampora & Ignasi Forne & Axel Imhof & Julian Stingele, 2023. "SPRTN patient variants cause global-genome DNA-protein crosslink repair defects," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Linliang Zhang & Hongyun Wang & Chao Han & Qi Dong & Jie Yan & Weiwei Guo & Chao Shan & Wen Zhao & Pu Chen & Rui Huang & Ying Wu & Yu Chen & Yali Qin & Mingzhou Chen, 2024. "AMFR-mediated Flavivirus NS2A ubiquitination subverts ER-phagy to augment viral pathogenicity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Rayene Berkane & Hung Ho-Xuan & Marius Glogger & Pablo Sanz-Martinez & Lorène Brunello & Tristan Glaesner & Santosh Kumar Kuncha & Katharina Holzhüter & Sara Cano-Franco & Viviana Buonomo & Paloma Cab, 2023. "The function of ER-phagy receptors is regulated through phosphorylation-dependent ubiquitination pathways," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Yun Lan & Sophie Wilhelmina Leur & Julia Ayano Fernando & Ho Him Wong & Martin Kampmann & Lewis Siu & Jingshu Zhang & Mingyuan Li & John M. Nicholls & Sumana Sanyal, 2023. "Viral subversion of selective autophagy is critical for biogenesis of virus replication organelles," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    13. Yun Xiang & Rui Lyu & Junjie Hu, 2023. "Oligomeric scaffolding for curvature generation by ER tubule-forming proteins," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    14. Zhen Yuan & Kun Cai & Jiajia Li & Ruifeng Chen & Fuhai Zhang & Xuan Tan & Yaming Jiu & Haishuang Chang & Bing Hu & Weiyi Zhang & Binbin Ding, 2024. "ATG14 targets lipid droplets and acts as an autophagic receptor for syntaxin18-regulated lipid droplet turnover," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Keiji Kajiwara & Hiroshi Osaki & Steffen Greßies & Keiko Kuwata & Ju Hyun Kim & Tobias Gensch & Yoshikatsu Sato & Frank Glorius & Shigehiro Yamaguchi & Masayasu Taki, 2022. "A negative-solvatochromic fluorescent probe for visualizing intracellular distributions of fatty acid metabolites," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    16. Shiyan Liu & Mutian Chen & Yichang Wang & Yuqing Lei & Ting Huang & Yabin Zhang & Sin Man Lam & Huihui Li & Shiqian Qi & Jia Geng & Kefeng Lu, 2023. "The ER calcium channel Csg2 integrates sphingolipid metabolism with autophagy," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    17. Odeta Meçe & Diede Houbaert & Maria-Livia Sassano & Tania Durré & Hannelore Maes & Marco Schaaf & Sanket More & Maarten Ganne & Melissa García-Caballero & Mila Borri & Jelle Verhoeven & Madhur Agrawal, 2022. "Lipid droplet degradation by autophagy connects mitochondria metabolism to Prox1-driven expression of lymphatic genes and lymphangiogenesis," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    18. Yilun Sun & Simone A. Baechler & Xiaohu Zhang & Suresh Kumar & Valentina M. Factor & Yasuhiro Arakawa & Cindy H. Chau & Kanako Okamoto & Anup Parikh & Bob Walker & Yijun P. Su & Jiji Chen & Tabitha Ti, 2023. "Targeting neddylation sensitizes colorectal cancer to topoisomerase I inhibitors by inactivating the DCAF13-CRL4 ubiquitin ligase complex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    19. Xinyu Mei & Yuan Guo & Zhangdan Xie & Yedan Zhong & Xiaofen Wu & Daichao Xu & Ying Li & Nan Liu & Zheng-Jiang Zhu, 2021. "RIPK1 regulates starvation resistance by modulating aspartate catabolism," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    20. Cathena Meiling Li & Jaemin Kang & Jongyeon Baek & Youbin Kim & Heemin Park & Yong-Keun Jung, 2024. "Cytosolic FKBPL and ER-resident CKAP4 co-regulates ER-phagy and protein secretion," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39172-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.