Orchestrated Content Release from Drosophila Glue-protein Vesicles by a Contractile Actomyosin Network

Overview

Journal Nat Cell Biol

Specialty Cell Biology

Date 2015 Dec 8

PMID 26641716

Citations 44

Authors

Tal Rousso

Eyal D Schejter

Ben-Zion Shilo

Affiliations

Soon will be listed here.

Abstract

Releasing content from large vesicles measuring several micrometres in diameter poses exceptional challenges to the secretory system. An actomyosin network commonly coats these vesicles, and is thought to provide the necessary force mediating efficient cargo release. Here we describe the spatial and temporal dynamics of the formation of this actomyosin coat around large vesicles and the resulting vesicle collapse, in live Drosophila melanogaster salivary glands. We identify the Formin family protein Diaphanous (Dia) as the main actin nucleator involved in generating this structure, and uncover Rho as an integrator of actin assembly and contractile machinery activation comprising this actomyosin network. High-resolution imaging reveals a unique cage-like organization of myosin II on the actin coat. This myosin arrangement requires branched-actin polymerization, and is critical for exerting a non-isotropic force, mediating efficient vesicle contraction.

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References

Wilson C, Tsuchida M, Allen G, Barnhart E, Applegate K, Yam P . Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature. 2010; 465(7296):373-7. PMC: 3662466. DOI: 10.1038/nature08994. View

Nemoto T, Kojima T, Oshima A, Bito H, Kasai H . Stabilization of exocytosis by dynamic F-actin coating of zymogen granules in pancreatic acini. J Biol Chem. 2004; 279(36):37544-50. DOI: 10.1074/jbc.M403976200. View

Yu H, Bement W . Multiple myosins are required to coordinate actin assembly with coat compression during compensatory endocytosis. Mol Biol Cell. 2007; 18(10):4096-105. PMC: 1995739. DOI: 10.1091/mbc.e06-11-0993. View

Munjal A, Philippe J, Munro E, Lecuit T . A self-organized biomechanical network drives shape changes during tissue morphogenesis. Nature. 2015; 524(7565):351-5. DOI: 10.1038/nature14603. View

Rauzi M, Lenne P, Lecuit T . Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature. 2010; 468(7327):1110-4. DOI: 10.1038/nature09566. View

Masedunskas A, Porat-Shliom N, Weigert R . Linking differences in membrane tension with the requirement for a contractile actomyosin scaffold during exocytosis in salivary glands. Commun Integr Biol. 2012; 5(1):84-7. PMC: 3291323. DOI: 10.4161/cib.18258. View

Medeiros N, Burnette D, Forscher P . Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol. 2006; 8(3):215-26. DOI: 10.1038/ncb1367. View

Sanderson J . Resolving the kinetics of lipid, protein and peptide diffusion in membranes. Mol Membr Biol. 2012; 29(5):118-43. DOI: 10.3109/09687688.2012.678018. View

Biyasheva A, Do T, Lu Y, Vaskova M, Andres A . Glue secretion in the Drosophila salivary gland: a model for steroid-regulated exocytosis. Dev Biol. 2001; 231(1):234-51. DOI: 10.1006/dbio.2000.0126. View

10.

Sokac A, Co C, Taunton J, Bement W . Cdc42-dependent actin polymerization during compensatory endocytosis in Xenopus eggs. Nat Cell Biol. 2003; 5(8):727-32. DOI: 10.1038/ncb1025. View

11.

Dawes-Hoang R, Parmar K, Christiansen A, Phelps C, Brand A, Wieschaus E . folded gastrulation, cell shape change and the control of myosin localization. Development. 2005; 132(18):4165-78. DOI: 10.1242/dev.01938. View

12.

Xu N, Bagumian G, Galiano M, Myat M . Rho GTPase controls Drosophila salivary gland lumen size through regulation of the actin cytoskeleton and Moesin. Development. 2011; 138(24):5415-27. PMC: 3222215. DOI: 10.1242/dev.069831. View

13.

Carvalho K, Lemiere J, Faqir F, Manzi J, Blanchoin L, Plastino J . Actin polymerization or myosin contraction: two ways to build up cortical tension for symmetry breaking. Philos Trans R Soc Lond B Biol Sci. 2013; 368(1629):20130005. PMC: 3785958. DOI: 10.1098/rstb.2013.0005. View

14.

Afshar K, Stuart B, Wasserman S . Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development. 2000; 127(9):1887-97. DOI: 10.1242/dev.127.9.1887. View

15.

Morin X, Daneman R, Zavortink M, Chia W . A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci U S A. 2001; 98(26):15050-5. PMC: 64981. DOI: 10.1073/pnas.261408198. View

16.

Goley E, Welch M . The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol. 2006; 7(10):713-26. DOI: 10.1038/nrm2026. View

17.

Dean S, Rogers S, Stuurman N, Vale R, Spudich J . Distinct pathways control recruitment and maintenance of myosin II at the cleavage furrow during cytokinesis. Proc Natl Acad Sci U S A. 2005; 102(38):13473-8. PMC: 1200093. DOI: 10.1073/pnas.0506810102. View

18.

Masedunskas A, Sramkova M, Parente L, Sales K, Amornphimoltham P, Bugge T . Role for the actomyosin complex in regulated exocytosis revealed by intravital microscopy. Proc Natl Acad Sci U S A. 2011; 108(33):13552-7. PMC: 3158220. DOI: 10.1073/pnas.1016778108. View

19.

Miklavc P, Hecht E, Hobi N, Wittekindt O, Dietl P, Kranz C . Actin coating and compression of fused secretory vesicles are essential for surfactant secretion--a role for Rho, formins and myosin II. J Cell Sci. 2012; 125(Pt 11):2765-74. DOI: 10.1242/jcs.105262. View

20.

Nightingale T, White I, Doyle E, Turmaine M, Harrison-Lavoie K, Webb K . Actomyosin II contractility expels von Willebrand factor from Weibel-Palade bodies during exocytosis. J Cell Biol. 2011; 194(4):613-29. PMC: 3160584. DOI: 10.1083/jcb.201011119. View