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In situ structure of actin remodeling during glucose-stimulated insulin secretion using cryo-electron tomography

Author

Listed:
  • Weimin Li

    (ShanghaiTech University
    ShanghaiTech University)

  • Angdi Li

    (ShanghaiTech University
    ShanghaiTech University)

  • Bing Yu

    (ShanghaiTech University
    ShanghaiTech University)

  • Xiaoxiao Zhang

    (ShanghaiTech University)

  • Xiaoyan Liu

    (ShanghaiTech University)

  • Kate L. White

    (University of Southern California)

  • Raymond C. Stevens

    (ShanghaiTech University
    ShanghaiTech University)

  • Wolfgang Baumeister

    (ShanghaiTech University
    Max Planck Institute of Biochemistry)

  • Andrej Sali

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Marion Jasnin

    (Helmholtz Pioneer Campus, Helmholtz Zentrum München
    Technical University of Munich)

  • Liping Sun

    (ShanghaiTech University)

Abstract

Actin mediates insulin secretion in pancreatic β-cells through remodeling. Hampered by limited resolution, previous studies have offered an ambiguous depiction as depolymerization and repolymerization. We report the in situ structure of actin remodeling in INS-1E β-cells during glucose-stimulated insulin secretion at nanoscale resolution. After remodeling, the actin filament network at the cell periphery exhibits three marked differences: 12% of actin filaments reorient quasi-orthogonally to the ventral membrane; the filament network mainly remains as cell-stabilizing bundles but partially reconfigures into a less compact arrangement; actin filaments anchored to the ventral membrane reorganize from a “netlike” to a “blooming” architecture. Furthermore, the density of actin filaments and microtubules around insulin secretory granules decreases, while actin filaments and microtubules become more densely packed. The actin filament network after remodeling potentially precedes the transport and release of insulin secretory granules. These findings advance our understanding of actin remodeling and its role in glucose-stimulated insulin secretion.

Suggested Citation

  • Weimin Li & Angdi Li & Bing Yu & Xiaoxiao Zhang & Xiaoyan Liu & Kate L. White & Raymond C. Stevens & Wolfgang Baumeister & Andrej Sali & Marion Jasnin & Liping Sun, 2024. "In situ structure of actin remodeling during glucose-stimulated insulin secretion using cryo-electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45648-7
    DOI: 10.1038/s41467-024-45648-7
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    References listed on IDEAS

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    1. Stefan Pfeffer & Johanna Dudek & Miroslava Schaffer & Bobby G. Ng & Sahradha Albert & Jürgen M. Plitzko & Wolfgang Baumeister & Richard Zimmermann & Hudson H. Freeze & Benjamin D. Engel & Friedrich Fö, 2017. "Dissecting the molecular organization of the translocon-associated protein complex," Nature Communications, Nature, vol. 8(1), pages 1-9, April.
    2. Laura Burbaum & Jonathan Schneider & Sarah Scholze & Ralph T. Böttcher & Wolfgang Baumeister & Petra Schwille & Jürgen M. Plitzko & Marion Jasnin, 2021. "Molecular-scale visualization of sarcomere contraction within native cardiomyocytes," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Pakorn Kanchanawong & Gleb Shtengel & Ana M. Pasapera & Ericka B. Ramko & Michael W. Davidson & Harald F. Hess & Clare M. Waterman, 2010. "Nanoscale architecture of integrin-based cell adhesions," Nature, Nature, vol. 468(7323), pages 580-584, November.
    4. Jun Liu & Dianne W. Taylor & Elena B. Krementsova & Kathleen M. Trybus & Kenneth A. Taylor, 2006. "Three-dimensional structure of the myosin V inhibited state by cryoelectron tomography," Nature, Nature, vol. 442(7099), pages 208-211, July.
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