Dynamic polyhedral actomyosin lattices remodel micron-scale curved membranes during exocytosis in live mice

Seham Ebrahim, Desu Chen, Max Weiss, Lenka Malec, Yeap Ng, Ivan Rebustini, Evan Krystofiak, Longhua Hu, Jian Liu, Andrius Masedunskas, Edna Hardeman, Peter Gunning, Bechara Kachar, Roberto Weigert

Research output: Contribution to journalLetter

Abstract

Actomyosin networks, the cell’s major force production machineries, remodel cellular membranes during myriad dynamic processes1,2 by assembling into various architectures with distinct force generation properties3,4. While linear and branched actomyosin architectures are well characterized in cell-culture and cell-free systems3, it is not known how actin and myosin networks form and function to remodel membranes in complex three-dimensional mammalian tissues. Here, we use four-dimensional spinning-disc confocal microscopy with image deconvolution to acquire macromolecular-scale detail of dynamic actomyosin networks in exocrine glands of live mice. We address how actin and myosin organize around large membrane-bound secretory vesicles and generate the forces required to complete exocytosis5–7. We find that actin and non-muscle myosin II (NMII) assemble into previously undescribed polyhedral-like lattices around the vesicle membrane. The NMII lattice comprises bipolar minifilaments8–10 as well as non-canonical three-legged configurations. Using photobleaching and pharmacological perturbations in vivo, we show that actomyosin contractility and actin polymerization together push on the underlying vesicle membrane to overcome the energy barrier and complete exocytosis7. Our imaging approach thus unveils a force-generating actomyosin lattice that regulates secretion in the exocrine organs of live animals.

Original languageEnglish (US)
Pages (from-to)933-939
Number of pages7
JournalNature cell biology
Volume21
Issue number8
DOIs
StatePublished - Aug 1 2019

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Actomyosin
Exocytosis
Actins
Membranes
Myosin Type II
Myosins
Exocrine Glands
Photobleaching
Animal Structures
Secretory Vesicles
Confocal Microscopy
Polymerization
Cell Culture Techniques
Pharmacology

ASJC Scopus subject areas

  • Cell Biology

Cite this

Ebrahim, S., Chen, D., Weiss, M., Malec, L., Ng, Y., Rebustini, I., ... Weigert, R. (2019). Dynamic polyhedral actomyosin lattices remodel micron-scale curved membranes during exocytosis in live mice. Nature cell biology, 21(8), 933-939. https://doi.org/10.1038/s41556-019-0365-7

Dynamic polyhedral actomyosin lattices remodel micron-scale curved membranes during exocytosis in live mice. / Ebrahim, Seham; Chen, Desu; Weiss, Max; Malec, Lenka; Ng, Yeap; Rebustini, Ivan; Krystofiak, Evan; Hu, Longhua; Liu, Jian; Masedunskas, Andrius; Hardeman, Edna; Gunning, Peter; Kachar, Bechara; Weigert, Roberto.

In: Nature cell biology, Vol. 21, No. 8, 01.08.2019, p. 933-939.

Research output: Contribution to journalLetter

Ebrahim, S, Chen, D, Weiss, M, Malec, L, Ng, Y, Rebustini, I, Krystofiak, E, Hu, L, Liu, J, Masedunskas, A, Hardeman, E, Gunning, P, Kachar, B & Weigert, R 2019, 'Dynamic polyhedral actomyosin lattices remodel micron-scale curved membranes during exocytosis in live mice', Nature cell biology, vol. 21, no. 8, pp. 933-939. https://doi.org/10.1038/s41556-019-0365-7
Ebrahim, Seham ; Chen, Desu ; Weiss, Max ; Malec, Lenka ; Ng, Yeap ; Rebustini, Ivan ; Krystofiak, Evan ; Hu, Longhua ; Liu, Jian ; Masedunskas, Andrius ; Hardeman, Edna ; Gunning, Peter ; Kachar, Bechara ; Weigert, Roberto. / Dynamic polyhedral actomyosin lattices remodel micron-scale curved membranes during exocytosis in live mice. In: Nature cell biology. 2019 ; Vol. 21, No. 8. pp. 933-939.
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