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Age-progressive interplay of HSP-proteostasis, ECM-cell junctions and biomechanics ensures C. elegans astroglial architecture

Author

Listed:
  • Francesca Coraggio

    (European Molecular Biology Laboratory)

  • Mahak Bhushan

    (European Molecular Biology Laboratory)

  • Spyridon Roumeliotis

    (European Molecular Biology Laboratory)

  • Francesca Caroti

    (European Molecular Biology Laboratory)

  • Carlo Bevilacqua

    (European Molecular Biology Laboratory)

  • Robert Prevedel

    (European Molecular Biology Laboratory
    European Molecular Biology Laboratory
    European Molecular Biology Laboratory
    Heidelberg University)

  • Georgia Rapti

    (European Molecular Biology Laboratory
    European Molecular Biology Laboratory
    Heidelberg University)

Abstract

Tissue integrity is sensitive to temperature, tension, age, and is sustained throughout life by adaptive cell-autonomous or extrinsic mechanisms. Safeguarding the remarkably-complex architectures of neurons and glia ensures age-dependent integrity of functional circuits. Here, we report mechanisms sustaining the integrity of C. elegans CEPsh astrocyte-like glia. We combine large-scale genetics with manipulation of genes, cells, and their environment, quantitative imaging of cellular/ subcellular features, tissue material properties and extracellular matrix (ECM). We identify mutants with age-progressive, environment-dependent defects in glial architecture, consequent disruption of neuronal architecture, and abnormal aging. Functional loss of epithelial Hsp70/Hsc70-cochaperone BAG2 causes ECM disruption, altered tissue biomechanics, and hypersensitivity of glia to environmental temperature and mechanics. Glial-cell junctions ensure epithelia-ECM-CEPsh glia association. Modifying glial junctions or ECM mechanics safeguards glial integrity against disrupted BAG2-proteostasis. Overall, we present a finely-regulated interplay of proteostasis-ECM and cell junctions with conserved components that ensures age-progressive robustness of glial architecture.

Suggested Citation

  • Francesca Coraggio & Mahak Bhushan & Spyridon Roumeliotis & Francesca Caroti & Carlo Bevilacqua & Robert Prevedel & Georgia Rapti, 2024. "Age-progressive interplay of HSP-proteostasis, ECM-cell junctions and biomechanics ensures C. elegans astroglial architecture," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46827-2
    DOI: 10.1038/s41467-024-46827-2
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    References listed on IDEAS

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    1. Menachem Katz & Francis Corson & Wolfgang Keil & Anupriya Singhal & Andrea Bae & Yun Lu & Yupu Liang & Shai Shaham, 2019. "Glutamate spillover in C. elegans triggers repetitive behavior through presynaptic activation of MGL-2/mGluR5," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Daniel Witvliet & Ben Mulcahy & James K. Mitchell & Yaron Meirovitch & Daniel R. Berger & Yuelong Wu & Yufang Liu & Wan Xian Koh & Rajeev Parvathala & Douglas Holmyard & Richard L. Schalek & Nir Shavi, 2021. "Connectomes across development reveal principles of brain maturation," Nature, Nature, vol. 596(7871), pages 257-261, August.
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