4.7 Article

Exocytosis by vesicle crumpling maintains apical membrane homeostasis during exocrine secretion

Journal

DEVELOPMENTAL CELL
Volume 56, Issue 11, Pages 1603-+

Publisher

CELL PRESS
DOI: 10.1016/j.devcel.2021.05.004

Keywords

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Funding

  1. Israel Science Foundation [706/20, 557/15]
  2. Minerva Foundation
  3. Federal German Ministry for Education and Research
  4. German-Israeli Foundation [1409-412.13]
  5. Yeda-Sela Center for Basic Research
  6. Ruth and Herman Albert Scholarship Program for New Scientists
  7. Ben B. and Joyce E. Eisenberg Foundation
  8. European Research Council (ERC) under the European Union [851080]
  9. David Barton Center for Research on the Chemistry of Life
  10. Jeanne and Joseph Nissim Center for Life Sciences Research
  11. European Research Council (ERC) [851080] Funding Source: European Research Council (ERC)

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This study found that vesicular membranes prevent fusion with the apical surface through actomyosin-mediated folding and retention, and isolate the membranes by crumpling to limit protein and lipid diffusion. Actomyosin contraction and membrane crumpling play key roles in recruiting endocytosis.
Exocrine secretion commonly employs micron-scale vesicles that fuse to a limited apical surface, presenting an extreme challenge for maintaining membrane homeostasis. Using Drosophila melanogaster larval salivary glands, we show that the membranes of fused vesicles undergo actomyosin-mediated folding and retention, which prevents them from incorporating into the apical surface. In addition, the diffusion of proteins and lipids between the fused vesicle and the apical surface is limited. Actomyosin contraction and membrane crumpling are essential for recruiting clathrin-mediated endocytosis to clear the retained vesicular membrane. Finally, we also observe membrane crumpling in secretory vesicles of the mouse exocrine pancreas. We conclude that membrane sequestration by crumpling followed by targeted endocytosis of the vesicular membrane, represents a general mechanism of exocytosis that maintains membrane homeostasis in exocrine tissues that employ large secretory vesicles.

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