Literature DB >> 22482019

Linking differences in membrane tension with the requirement for a contractile actomyosin scaffold during exocytosis in salivary glands.

Andrius Masedunskas, Natalie Porat-Shliom, Roberto Weigert.   

Abstract

In all the major secretory organs regulated exocytosis is a fundamental process that is used for releasing molecules in the extracellular space. Molecules destined for secretion are packaged into secretory vesicles that fuse with the plasma membrane upon the appropriate stimulus. In exocrine glands, large secretory vesicles fuse with specialized domains of the plasma membrane, which form ductal structures that are in direct continuity with the external environment and exhibit various architectures and diameters. In a recent study, we used intravital microscopy to analyze in detail the dynamics of exocytic events in the salivary glands of live rodents under conditions that cannot be reproduced in in vitro or ex vivo model systems. We found that after the opening of the fusion pore large secretory vesicles gradually collapse with their limiting membranes being completely absorbed into the apical plasma membrane canaliculi within 40-60 sec. Moreover, we observed that this controlled collapse requires the contractile activity of actin and its motor myosin II, which are recruited onto the large secretory vesicles immediately after their fusion with the plasma membrane. Here we suggest that the actomyosin complex may be required to facilitate exocytosis in those systems, such as the salivary glands, in which the full collapse of the vesicles is not energetically favorable due to a difference in membrane tension between the large secretory vesicles and the canaliculi.

Keywords:  Secretion; actin; cytoskeleton; exocrine glands; exocytosis; intravital microscopy; membrane tension; myosin; salivary glands

Year:  2012        PMID: 22482019      PMCID: PMC3291323          DOI: 10.4161/cib.18258

Source DB:  PubMed          Journal:  Commun Integr Biol        ISSN: 1942-0889


  30 in total

1.  Actin coating of secretory granules during regulated exocytosis correlates with the release of rab3D.

Authors:  J A Valentijn; K Valentijn; L M Pastore; J D Jamieson
Journal:  Proc Natl Acad Sci U S A       Date:  2000-02-01       Impact factor: 11.205

2.  Dynamics of fusion pores connecting membranes of different tensions.

Authors:  Y A Chizmadzhev; P I Kuzmin; D A Kumenko; J Zimmerberg; F S Cohen
Journal:  Biophys J       Date:  2000-05       Impact factor: 4.033

Review 3.  Secretory granule exocytosis.

Authors:  Robert D Burgoyne; Alan Morgan
Journal:  Physiol Rev       Date:  2003-04       Impact factor: 37.312

4.  Regulation of fusion pore closure and compound exocytosis in neuroendocrine PC12 cells by SCAMP1.

Authors:  Jie Zhang; David Castle
Journal:  Traffic       Date:  2011-02-25       Impact factor: 6.215

Review 5.  Exocytosis in neuroendocrine cells: new tasks for actin.

Authors:  Magali Malacombe; Marie-France Bader; Stéphane Gasman
Journal:  Biochim Biophys Acta       Date:  2006-09-14

Review 6.  Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells.

Authors:  J-M Trifaró; S Gasman; L M Gutiérrez
Journal:  Acta Physiol (Oxf)       Date:  2007-11-16       Impact factor: 6.311

Review 7.  Lamellar body exocytosis by cell stretch or purinergic stimulation: possible physiological roles, messengers and mechanisms.

Authors:  Paul Dietl; Birgit Liss; Edward Felder; Pika Miklavc; Hubert Wirtz
Journal:  Cell Physiol Biochem       Date:  2009-12-22

8.  Actin and non-muscle myosin II facilitate apical exocytosis of tear proteins in rabbit lacrimal acinar epithelial cells.

Authors:  Galina V Jerdeva; Kaijin Wu; Francie A Yarber; Christopher J Rhodes; Daniel Kalman; Joel E Schechter; Sarah F Hamm-Alvarez
Journal:  J Cell Sci       Date:  2005-10-15       Impact factor: 5.285

Review 9.  Kiss-and-run, collapse and 'readily retrievable' vesicles.

Authors:  Silvio O Rizzoli; Reinhard Jahn
Journal:  Traffic       Date:  2007-07-20       Impact factor: 6.215

10.  Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines.

Authors:  John C Castle; Chaolin Zhang; Jyoti K Shah; Amit V Kulkarni; Auinash Kalsotra; Thomas A Cooper; Jason M Johnson
Journal:  Nat Genet       Date:  2008-11-02       Impact factor: 38.330

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  9 in total

Review 1.  Intravital microscopy in mammalian multicellular organisms.

Authors:  Seham Ebrahim; Roberto Weigert
Journal:  Curr Opin Cell Biol       Date:  2019-05-21       Impact factor: 8.382

Review 2.  Imaging membrane remodeling during regulated exocytosis in live mice.

Authors:  Akiko Shitara; Roberto Weigert
Journal:  Exp Cell Res       Date:  2015-07-06       Impact factor: 3.905

Review 3.  Unresolved issues in theories of autoimmune disease using myocarditis as a framework.

Authors:  Robert Root-Bernstein; DeLisa Fairweather
Journal:  J Theor Biol       Date:  2014-12-04       Impact factor: 2.691

Review 4.  Multiple roles for the actin cytoskeleton during regulated exocytosis.

Authors:  Natalie Porat-Shliom; Oleg Milberg; Andrius Masedunskas; Roberto Weigert
Journal:  Cell Mol Life Sci       Date:  2012-09-18       Impact factor: 9.261

5.  Orchestrated content release from Drosophila glue-protein vesicles by a contractile actomyosin network.

Authors:  Tal Rousso; Eyal D Schejter; Ben-Zion Shilo
Journal:  Nat Cell Biol       Date:  2015-12-07       Impact factor: 28.824

Review 6.  Imaging cell biology in live animals: ready for prime time.

Authors:  Roberto Weigert; Natalie Porat-Shliom; Panomwat Amornphimoltham
Journal:  J Cell Biol       Date:  2013-06-24       Impact factor: 10.539

Review 7.  Intravital microscopy: a practical guide on imaging intracellular structures in live animals.

Authors:  Andrius Masedunskas; Oleg Milberg; Natalie Porat-Shliom; Monika Sramkova; Tim Wigand; Panomwat Amornphimoltham; Roberto Weigert
Journal:  Bioarchitecture       Date:  2012-09-01

8.  Homeostasis of the apical plasma membrane during regulated exocytosis in the salivary glands of live rodents.

Authors:  Andrius Masedunskas; Monika Sramkova; Roberto Weigert
Journal:  Bioarchitecture       Date:  2011-09-01

9.  Concerted actions of distinct nonmuscle myosin II isoforms drive intracellular membrane remodeling in live animals.

Authors:  Oleg Milberg; Akiko Shitara; Seham Ebrahim; Andrius Masedunskas; Muhibullah Tora; Duy T Tran; Yun Chen; Mary Anne Conti; Robert S Adelstein; Kelly G Ten Hagen; Roberto Weigert
Journal:  J Cell Biol       Date:  2017-06-09       Impact factor: 10.539

  9 in total

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