IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-44409-2.html
   My bibliography  Save this article

Longevity interventions modulate mechanotransduction and extracellular matrix homeostasis in C. elegans

Author

Listed:
  • Alina C. Teuscher

    (ETH Zürich)

  • Cyril Statzer

    (ETH Zürich)

  • Anita Goyala

    (ETH Zürich)

  • Seraina A. Domenig

    (ETH Zürich)

  • Ingmar Schoen

    (Irish Centre for Vascular Biology, Royal College of Surgeons in Ireland
    ETH Zürich)

  • Max Hess

    (ETH Zürich)

  • Alexander M. Hofer

    (ETH Zürich)

  • Andrea Fossati

    (ETH Zürich
    University of California San Francisco)

  • Viola Vogel

    (ETH Zürich)

  • Orcun Goksel

    (ETH Zürich
    Uppsala University)

  • Ruedi Aebersold

    (ETH Zürich)

  • Collin Y. Ewald

    (ETH Zürich)

Abstract

Dysfunctional extracellular matrices (ECM) contribute to aging and disease. Repairing dysfunctional ECM could potentially prevent age-related pathologies. Interventions promoting longevity also impact ECM gene expression. However, the role of ECM composition changes in healthy aging remains unclear. Here we perform proteomics and in-vivo monitoring to systematically investigate ECM composition (matreotype) during aging in C. elegans revealing three distinct collagen dynamics. Longevity interventions slow age-related collagen stiffening and prolong the expression of collagens that are turned over. These prolonged collagen dynamics are mediated by a mechanical feedback loop of hemidesmosome-containing structures that span from the exoskeletal ECM through the hypodermis, basement membrane ECM, to the muscles, coupling mechanical forces to adjust ECM gene expression and longevity via the transcriptional co-activator YAP-1 across tissues. Our results provide in-vivo evidence that coordinated ECM remodeling through mechanotransduction is required and sufficient to promote longevity, offering potential avenues for interventions targeting ECM dynamics.

Suggested Citation

  • Alina C. Teuscher & Cyril Statzer & Anita Goyala & Seraina A. Domenig & Ingmar Schoen & Max Hess & Alexander M. Hofer & Andrea Fossati & Viola Vogel & Orcun Goksel & Ruedi Aebersold & Collin Y. Ewald, 2024. "Longevity interventions modulate mechanotransduction and extracellular matrix homeostasis in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44409-2
    DOI: 10.1038/s41467-023-44409-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44409-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-44409-2?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. Su Bin LIM & Swee Jin TAN & Wan-Teck LIM & Chwee Teck LIM, 2017. "An extracellular matrix-related prognostic and predictive indicator for early-stage non-small cell lung cancer," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    2. Seda Koyuncu & Rute Loureiro & Hyun Ju Lee & Prerana Wagle & Marcus Krueger & David Vilchez, 2021. "Rewiring of the ubiquitinated proteome determines ageing in C. elegans," Nature, Nature, vol. 596(7871), pages 285-290, August.
    3. Huimin Zhang & Frédéric Landmann & Hala Zahreddine & David Rodriguez & Marc Koch & Michel Labouesse, 2011. "A tension-induced mechanotransduction pathway promotes epithelial morphogenesis," Nature, Nature, vol. 471(7336), pages 99-103, March.
    4. Collin Y. Ewald & Jess N. Landis & Jess Porter Abate & Coleen T. Murphy & T. Keith Blackwell, 2015. "Dauer-independent insulin/IGF-1-signalling implicates collagen remodelling in longevity," Nature, Nature, vol. 519(7541), pages 97-101, March.
    5. Nan Liu & Hiroyuki Matsumura & Tomoki Kato & Shizuko Ichinose & Aki Takada & Takeshi Namiki & Kyosuke Asakawa & Hironobu Morinaga & Yasuaki Mohri & Adèle Arcangelis & Elisabeth Geroges-Labouesse & Dai, 2019. "Stem cell competition orchestrates skin homeostasis and ageing," Nature, Nature, vol. 568(7752), pages 344-350, April.
    6. Hanna Lucie Sladitschek-Martens & Alberto Guarnieri & Giulia Brumana & Francesca Zanconato & Giusy Battilana & Romy Lucon Xiccato & Tito Panciera & Mattia Forcato & Silvio Bicciato & Vincenza Guzzardo, 2022. "YAP/TAZ activity in stromal cells prevents ageing by controlling cGAS–STING," Nature, Nature, vol. 607(7920), pages 790-798, July.
    7. Ben C. Collins & Christie L. Hunter & Yansheng Liu & Birgit Schilling & George Rosenberger & Samuel L. Bader & Daniel W. Chan & Bradford W. Gibson & Anne-Claude Gingras & Jason M. Held & Mio Hirayama-, 2017. "Multi-laboratory assessment of reproducibility, qualitative and quantitative performance of SWATH-mass spectrometry," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    8. Clara L. Essmann & Daniel Martinez-Martinez & Rosina Pryor & Kit-Yi Leung & Kalaivani Bala Krishnan & Prudence Pokway Lui & Nicholas D. E. Greene & André E. X. Brown & Vijay M. Pawar & Mandayam A. Sri, 2020. "Mechanical properties measured by atomic force microscopy define health biomarkers in ageing C. elegans," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    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. Wenjing Yan & Yongwang Zhong & Xin Hu & Tuan Xu & Yinghua Zhang & Stephen Kales & Yanyan Qu & Daniel C. Talley & Bolormaa Baljinnyam & Christopher A. LeClair & Anton Simeonov & Brian M. Polster & Ruil, 2023. "Auranofin targets UBA1 and enhances UBA1 activity by facilitating ubiquitin trans-thioesterification to E2 ubiquitin-conjugating enzymes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Elle Koren & Alona Feldman & Marianna Yusupova & Avihay Kadosh & Egor Sedov & Roi Ankawa & Yahav Yosefzon & Waseem Nasser & Stefanie Gerstberger & Liam B. Kimel & Noa Priselac & Samara Brown & Sam Sha, 2022. "Thy1 marks a distinct population of slow-cycling stem cells in the mouse epidermis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Xiaofeng Liao & Wenxue Li & Hongyue Zhou & Barani Kumar Rajendran & Ao Li & Jingjing Ren & Yi Luan & David A. Calderwood & Benjamin Turk & Wenwen Tang & Yansheng Liu & Dianqing Wu, 2024. "The CUL5 E3 ligase complex negatively regulates central signaling pathways in CD8+ T cells," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    4. Kenneth A. Wilson & Sudipta Bar & Eric B. Dammer & Enrique M. Carrera & Brian A. Hodge & Tyler A. U. Hilsabeck & Joanna Bons & George W. Brownridge & Jennifer N. Beck & Jacob Rose & Melia Granath-Pane, 2024. "OXR1 maintains the retromer to delay brain aging under dietary restriction," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Sunmin Park & Suna Kang & Woo Jae Lee, 2021. "Menopause, Ultraviolet Exposure, and Low Water Intake Potentially Interact with the Genetic Variants Related to Collagen Metabolism Involved in Skin Wrinkle Risk in Middle-Aged Women," IJERPH, MDPI, vol. 18(4), pages 1-12, February.
    6. Ali Akbar Ashkarran & Hassan Gharibi & Elizabeth Voke & Markita P. Landry & Amir Ata Saei & Morteza Mahmoudi, 2022. "Measurements of heterogeneity in proteomics analysis of the nanoparticle protein corona across core facilities," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    7. Cyril Statzer & Jin Meng & Richard Venz & Monet Bland & Stacey Robida-Stubbs & Krina Patel & Dunja Petrovic & Raffaella Emsley & Pengpeng Liu & Ianessa Morantte & Cole Haynes & William B. Mair & Alban, 2022. "ATF-4 and hydrogen sulfide signalling mediate longevity in response to inhibition of translation or mTORC1," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    8. Brian A. Hodge & Geoffrey T. Meyerhof & Subhash D. Katewa & Ting Lian & Charles Lau & Sudipta Bar & Nicole Y. Leung & Menglin Li & David Li-Kroeger & Simon Melov & Birgit Schilling & Craig Montell & P, 2022. "Dietary restriction and the transcription factor clock delay eye aging to extend lifespan in Drosophila Melanogaster," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Yan-Ping Zhang & Wen-Hong Zhang & Pan Zhang & Qi Li & Yue Sun & Jia-Wen Wang & Shaobing O. Zhang & Tao Cai & Cheng Zhan & Meng-Qiu Dong, 2022. "Intestine-specific removal of DAF-2 nearly doubles lifespan in Caenorhabditis elegans with little fitness cost," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    10. Yi Yang & Guoquan Yan & Siyuan Kong & Mengxi Wu & Pengyuan Yang & Weiqian Cao & Liang Qiao, 2021. "GproDIA enables data-independent acquisition glycoproteomics with comprehensive statistical control," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    11. Nanase Igarashi & Kenichi Miyata & Tze Mun Loo & Masatomo Chiba & Aki Hanyu & Mika Nishio & Hiroko Kawasaki & Hao Zheng & Shinya Toyokuni & Shunsuke Kon & Keiji Moriyama & Yasuyuki Fujita & Akiko Taka, 2022. "Hepatocyte growth factor derived from senescent cells attenuates cell competition-induced apical elimination of oncogenic cells," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    12. Jina Yun & Simon Hansen & Otto Morris & David T. Madden & Clare Peters Libeu & Arjun J. Kumar & Cameron Wehrfritz & Aaron H. Nile & Yingnan Zhang & Lijuan Zhou & Yuxin Liang & Zora Modrusan & Michelle, 2023. "Senescent cells perturb intestinal stem cell differentiation through Ptk7 induced noncanonical Wnt and YAP signaling," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    13. Andrea Braeutigam & Ahmet Nihat Simsek & Gerhard Gompper & Benedikt Sabass, 2022. "Generic self-stabilization mechanism for biomolecular adhesions under load," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    14. Hassan Gharibi & Ali Akbar Ashkarran & Maryam Jafari & Elizabeth Voke & Markita P. Landry & Amir Ata Saei & Morteza Mahmoudi, 2024. "A uniform data processing pipeline enables harmonized nanoparticle protein corona analysis across proteomics core facilities," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    15. Fang Ye & Guodong Zhang & Weigao E. & Haide Chen & Chengxuan Yu & Lei Yang & Yuting Fu & Jiaqi Li & Sulei Fu & Zhongyi Sun & Lijiang Fei & Qile Guo & Jingjing Wang & Yanyu Xiao & Xinru Wang & Peijing , 2022. "Construction of the axolotl cell landscape using combinatorial hybridization sequencing at single-cell resolution," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    16. Hirofumi Nagao & Ashok Kumar Jayavelu & Weikang Cai & Hui Pan & Jonathan M. Dreyfuss & Thiago M. Batista & Bruna B. Brandão & Matthias Mann & C. Ronald Kahn, 2023. "Unique ligand and kinase-independent roles of the insulin receptor in regulation of cell cycle, senescence and apoptosis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    17. Marianna Yusupova & Roi Ankawa & Yahav Yosefzon & David Meiri & Ido Bachelet & Yaron Fuchs, 2023. "Apoptotic dysregulation mediates stem cell competition and tissue regeneration," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    18. L. Angela Mihai & Khulud Alayyash & Hayley Wyatt, 2017. "The optimal density of cellular solids in axial tension," Computer Methods in Biomechanics and Biomedical Engineering, Taylor & Francis Journals, vol. 20(7), pages 701-713, May.
    19. Wenping Zhou & Wenxue Li & Shisheng Wang & Barbora Salovska & Zhenyi Hu & Bo Tao & Yi Di & Ujwal Punyamurtula & Benjamin E. Turk & William C. Sessa & Yansheng Liu, 2023. "An optogenetic-phosphoproteomic study reveals dynamic Akt1 signaling profiles in endothelial cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    20. Hisato Nagano & Naoaki Mizuno & Hideyuki Sato & Eiji Mizutani & Ayaka Yanagida & Mayuko Kano & Mariko Kasai & Hiromi Yamamoto & Motoo Watanabe & Fabian Suchy & Hideki Masaki & Hiromitsu Nakauchi, 2024. "Skin graft with dermis and appendages generated in vivo by cell competition," Nature Communications, Nature, vol. 15(1), pages 1-12, 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:15:y:2024:i:1:d:10.1038_s41467-023-44409-2. 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.