IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30388-3.html
   My bibliography  Save this article

Shielding of actin by the endoplasmic reticulum impacts nuclear positioning

Author

Listed:
  • Cátia Silva Janota

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa)

  • Andreia Pinto

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Royal Brompton Hospital and Harefield NHS Foundation Trust)

  • Anna Pezzarossa

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Champalimaud Foundation, Champalimaud Centre for the Unknown)

  • Pedro Machado

    (Electron Microscopy Core Facility (EMCF), European Molecular Biology Laboratory
    Centre for Ultrastructural Imaging, King’s College London)

  • Judite Costa

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa)

  • Pedro Campinho

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Champalimaud Foundation, Champalimaud Centre for the Unknown)

  • Cláudio A. Franco

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Instituto de Histologia e Biologia do Desenvolvimento, Faculdade de Medicina, Universidade de Lisboa)

  • Edgar R. Gomes

    (Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa
    Instituto de Histologia e Biologia do Desenvolvimento, Faculdade de Medicina, Universidade de Lisboa)

Abstract

Nuclear position is central to cell polarization, and its disruption is associated with various pathologies. The nucleus is moved away from the leading edge of migrating cells through its connection to moving dorsal actin cables, and the absence of connections to immobile ventral stress fibers. It is unclear how these asymmetric nucleo-cytoskeleton connections are established. Here, using an in vitro wound assay, we find that remodeling of endoplasmic reticulum (ER) impacts nuclear positioning through the formation of a barrier that shields immobile ventral stress fibers. The remodeling of ER and perinuclear ER accumulation is mediated by the ER shaping protein Climp-63. Furthermore, ectopic recruitment of the ER to stress fibers restores nuclear positioning in the absence of Climp-63. Our findings suggest that the ER mediates asymmetric nucleo-cytoskeleton connections to position the nucleus.

Suggested Citation

  • Cátia Silva Janota & Andreia Pinto & Anna Pezzarossa & Pedro Machado & Judite Costa & Pedro Campinho & Cláudio A. Franco & Edgar R. Gomes, 2022. "Shielding of actin by the endoplasmic reticulum impacts nuclear positioning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30388-3
    DOI: 10.1038/s41467-022-30388-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30388-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-30388-3?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. Francesca Bottanelli & Emil B. Kromann & Edward S. Allgeyer & Roman S. Erdmann & Stephanie Wood Baguley & George Sirinakis & Alanna Schepartz & David Baddeley & Derek K. Toomre & James E. Rothman & Jo, 2016. "Two-colour live-cell nanoscale imaging of intracellular targets," Nature Communications, Nature, vol. 7(1), pages 1-5, April.
    2. Alex M. Valm & Sarah Cohen & Wesley R. Legant & Justin Melunis & Uri Hershberg & Eric Wait & Andrew R. Cohen & Michael W. Davidson & Eric Betzig & Jennifer Lippincott-Schwartz, 2017. "Applying systems-level spectral imaging and analysis to reveal the organelle interactome," Nature, Nature, vol. 546(7656), pages 162-167, June.
    3. Pengli Zheng & Christopher J. Obara & Ewa Szczesna & Jonathon Nixon-Abell & Kishore K. Mahalingan & Antonina Roll-Mecak & Jennifer Lippincott-Schwartz & Craig Blackstone, 2022. "ER proteins decipher the tubulin code to regulate organelle distribution," Nature, Nature, vol. 601(7891), pages 132-138, January.
    4. Thomas Metzger & Vincent Gache & Mu Xu & Bruno Cadot & Eric S. Folker & Brian E. Richardson & Edgar R. Gomes & Mary K. Baylies, 2012. "MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function," Nature, Nature, vol. 484(7392), pages 120-124, April.
    5. Jörg Renkawitz & Aglaja Kopf & Julian Stopp & Ingrid Vries & Meghan K. Driscoll & Jack Merrin & Robert Hauschild & Erik S. Welf & Gaudenz Danuser & Reto Fiolka & Michael Sixt, 2019. "Nuclear positioning facilitates amoeboid migration along the path of least resistance," Nature, Nature, vol. 568(7753), pages 546-550, 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. Katelyn C. Cook & Elene Tsopurashvili & Jason M. Needham & Sunnie R. Thompson & Ileana M. Cristea, 2022. "Restructured membrane contacts rewire organelles for human cytomegalovirus infection," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    2. Ewa Sitarska & Silvia Dias Almeida & Marianne Sandvold Beckwith & Julian Stopp & Jakub Czuchnowski & Marc Siggel & Rita Roessner & Aline Tschanz & Christer Ejsing & Yannick Schwab & Jan Kosinski & Mic, 2023. "Sensing their plasma membrane curvature allows migrating cells to circumvent obstacles," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Noble Kumar Talari & Ushodaya Mattam & Niroj Kumar Meher & Arun Kumar Paripati & Kalyankar Mahadev & Thanuja Krishnamoorthy & Naresh Babu V. Sepuri, 2023. "Lipid-droplet associated mitochondria promote fatty-acid oxidation through a distinct bioenergetic pattern in male Wistar rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Archibald Enninful & Alev Baysoy & Rong Fan, 2022. "Unmixing for ultra-high-plex fluorescence imaging," Nature Communications, Nature, vol. 13(1), pages 1-3, December.
    5. Hannes Gonschior & Christopher Schmied & Rozemarijn Eva Van der Veen & Jenny Eichhorst & Nina Himmerkus & Jörg Piontek & Dorothee Günzel & Markus Bleich & Mikio Furuse & Volker Haucke & Martin Lehmann, 2022. "Nanoscale segregation of channel and barrier claudins enables paracellular ion flux," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    6. Raja Chouket & Agnès Pellissier-Tanon & Aliénor Lahlou & Ruikang Zhang & Diana Kim & Marie-Aude Plamont & Mingshu Zhang & Xi Zhang & Pingyong Xu & Nicolas Desprat & Dominique Bourgeois & Agathe Espagn, 2022. "Extra kinetic dimensions for label discrimination," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    7. Güneş Parlakgül & Song Pang & Leonardo L. Artico & Nina Min & Erika Cagampan & Reyna Villa & Renata L. S. Goncalves & Grace Yankun Lee & C. Shan Xu & Gökhan S. Hotamışlıgil & Ana Paula Arruda, 2024. "Spatial mapping of hepatic ER and mitochondria architecture reveals zonated remodeling in fasting and obesity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Alexandre Santinho & Maxime Carpentier & Julio Lopes Sampaio & Mohyeddine Omrane & Abdou Rachid Thiam, 2024. "Giant organelle vesicles to uncover intracellular membrane mechanics and plasticity," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Patrick A. Sandoz & Robin A. Denhardt-Eriksson & Laurence Abrami & Luciano A. Abriata & Gard Spreemann & Catherine Maclachlan & Sylvia Ho & Béatrice Kunz & Kathryn Hess & Graham Knott & Francisco S. M, 2023. "Dynamics of CLIMP-63 S-acylation control ER morphology," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Agnes Adler & Mamata Bangera & J. Wouter Beugelink & Salima Bahri & Hugo Ingen & Carolyn A. Moores & Marc Baldus, 2024. "A structural and dynamic visualization of the interaction between MAP7 and microtubules," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Jan Kretschmer & Tomáš David & Martin Dračínský & Ondřej Socha & Daniel Jirak & Martin Vít & Radek Jurok & Martin Kuchař & Ivana Císařová & Miloslav Polasek, 2022. "Paramagnetic encoding of molecules," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    12. William Y. C. Huang & Xianrui Cheng & James E. Ferrell, 2022. "Cytoplasmic organization promotes protein diffusion in Xenopus extracts," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    13. Dianne Lumaquin-Yin & Emily Montal & Eleanor Johns & Arianna Baggiolini & Ting-Hsiang Huang & Yilun Ma & Charlotte LaPlante & Shruthy Suresh & Lorenz Studer & Richard M. White, 2023. "Lipid droplets are a metabolic vulnerability in melanoma," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Yong Mi Choi & Dalila Ajjaji & Kaelin D. Fleming & Peter P. Borbat & Meredith L. Jenkins & Brandon E. Moeller & Shaveen Fernando & Surita R. Bhatia & Jack H. Freed & John E. Burke & Abdou Rachid Thiam, 2023. "Structural insights into perilipin 3 membrane association in response to diacylglycerol accumulation," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Junyoung Seo & Yeonbo Sim & Jeewon Kim & Hyunwoo Kim & In Cho & Hoyeon Nam & Young-Gyu Yoon & Jae-Byum Chang, 2022. "PICASSO allows ultra-multiplexed fluorescence imaging of spatially overlapping proteins without reference spectra measurements," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    16. James Burgess & Jeffrey J. Nirschl & Maria-Clara Zanellati & Alejandro Lozano & Sarah Cohen & Serena Yeung-Levy, 2024. "Orientation-invariant autoencoders learn robust representations for shape profiling of cells and organelles," Nature Communications, Nature, vol. 15(1), pages 1-14, 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:13:y:2022:i:1:d:10.1038_s41467-022-30388-3. 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.