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Molecular mechanics underlying flat-to-round membrane budding in live secretory cells

Author

Listed:
  • Wonchul Shin

    (National Institute of Neurological Disorders and Stroke)

  • Ben Zucker

    (Tel Aviv University)

  • Nidhi Kundu

    (National Institute of Diabetes and Digestive and Kidney Diseases)

  • Sung Hoon Lee

    (Chung-Ang University)

  • Bo Shi

    (National Institute of Neurological Disorders and Stroke)

  • Chung Yu Chan

    (National Institute of Neurological Disorders and Stroke)

  • Xiaoli Guo

    (National Institute of Neurological Disorders and Stroke)

  • Jonathan T. Harrison

    (National Institute of Diabetes and Digestive and Kidney Diseases)

  • Jaymie Moore Turechek

    (National Institute of Neurological Disorders and Stroke)

  • Jenny E. Hinshaw

    (National Institute of Diabetes and Digestive and Kidney Diseases)

  • Michael M. Kozlov

    (Tel Aviv University)

  • Ling-Gang Wu

    (National Institute of Neurological Disorders and Stroke)

Abstract

Membrane budding entails forces to transform flat membrane into vesicles essential for cell survival. Accumulated studies have identified coat-proteins (e.g., clathrin) as potential budding factors. However, forces mediating many non-coated membrane buddings remain unclear. By visualizing proteins in mediating endocytic budding in live neuroendocrine cells, performing in vitro protein reconstitution and physical modeling, we discovered how non-coated-membrane budding is mediated: actin filaments and dynamin generate a pulling force transforming flat membrane into Λ-shape; subsequently, dynamin helices surround and constrict Λ-profile’s base, transforming Λ- to Ω-profile, and then constrict Ω-profile’s pore, converting Ω-profiles to vesicles. These mechanisms control budding speed, vesicle size and number, generating diverse endocytic modes differing in these parameters. Their impact is widespread beyond secretory cells, as the unexpectedly powerful functions of dynamin and actin, previously thought to mediate fission and overcome tension, respectively, may contribute to many dynamin/actin-dependent non-coated-membrane buddings, coated-membrane buddings, and other membrane remodeling processes.

Suggested Citation

  • Wonchul Shin & Ben Zucker & Nidhi Kundu & Sung Hoon Lee & Bo Shi & Chung Yu Chan & Xiaoli Guo & Jonathan T. Harrison & Jaymie Moore Turechek & Jenny E. Hinshaw & Michael M. Kozlov & Ling-Gang Wu, 2022. "Molecular mechanics underlying flat-to-round membrane budding in live secretory cells," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31286-4
    DOI: 10.1038/s41467-022-31286-4
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    1. Emmanuel Boucrot & Antonio P. A. Ferreira & Leonardo Almeida-Souza & Sylvain Debard & Yvonne Vallis & Gillian Howard & Laetitia Bertot & Nathalie Sauvonnet & Harvey T. McMahon, 2015. "Endophilin marks and controls a clathrin-independent endocytic pathway," Nature, Nature, vol. 517(7535), pages 460-465, January.
    2. Shigeki Watanabe & Thorsten Trimbuch & Marcial Camacho-Pérez & Benjamin R. Rost & Bettina Brokowski & Berit Söhl-Kielczynski & Annegret Felies & M. Wayne Davis & Christian Rosenmund & Erik M. Jorgense, 2014. "Clathrin regenerates synaptic vesicles from endosomes," Nature, Nature, vol. 515(7526), pages 228-233, November.
    3. Peter J. Wen & Staffan Grenklo & Gianvito Arpino & Xinyu Tan & Hsien-Shun Liao & Johanna Heureaux & Shi-Yong Peng & Hsueh-Cheng Chiang & Edaeni Hamid & Wei-Dong Zhao & Wonchul Shin & Tuomas Näreoja & , 2016. "Actin dynamics provides membrane tension to merge fusing vesicles into the plasma membrane," Nature Communications, Nature, vol. 7(1), pages 1-14, November.
    4. Shigeki Watanabe & Benjamin R. Rost & Marcial Camacho-Pérez & M. Wayne Davis & Berit Söhl-Kielczynski & Christian Rosenmund & Erik M. Jorgensen, 2013. "Ultrafast endocytosis at mouse hippocampal synapses," Nature, Nature, vol. 504(7479), pages 242-247, December.
    5. Hsueh-Cheng Chiang & Wonchul Shin & Wei-Dong Zhao & Edaeni Hamid & Jiansong Sheng & Maryna Baydyuk & Peter J. Wen & Albert Jin & Fanny Momboisse & Ling-Gang Wu, 2014. "Post-fusion structural changes and their roles in exocytosis and endocytosis of dense-core vesicles," Nature Communications, Nature, vol. 5(1), pages 1-17, May.
    6. Harvey T. McMahon & Jennifer L. Gallop, 2005. "Membrane curvature and mechanisms of dynamic cell membrane remodelling," Nature, Nature, vol. 438(7068), pages 590-596, December.
    7. Leopold Kong & Kem A. Sochacki & Huaibin Wang & Shunming Fang & Bertram Canagarajah & Andrew D. Kehr & William J. Rice & Marie-Paule Strub & Justin W. Taraska & Jenny E. Hinshaw, 2018. "Cryo-EM of the dynamin polymer assembled on lipid membrane," Nature, Nature, vol. 560(7717), pages 258-262, August.
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