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Am J Physiol Cell Physiol 288: C46-C56, 2005. First published September 1, 2004; doi:10.1152/ajpcell.00397.2004
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PROTEIN AND VESICLE TRAFFICKING, CYTOSKELETON

Barrier role of actin filaments in regulated mucin secretion from airway goblet cells

Camille Ehre,1 Andrea H. Rossi,2 Lubna H. Abdullah,1 Kathleen De Pestel,3 Sandra Hill,4 John C. Olsen,1 and C. William Davis1,2

1Cystic Fibrosis/Pulmonary Research and Treatment Center and 2Department of Cell and Molecular Physiology, University of North Carolina, Chapel Hill, North Carolina; 3Department of Biochemistry, Faculty of Medicine and Health Sciences, University of Ghent and Flanders Interuniversity Institute for Biotechnology (VIB09), Ghent, Belgium; and 4Novartis Respiratory Research Centre, Horsham, United Kingdom

Submitted 13 August 2004 ; accepted in final form 30 August 2004

Airway goblet cells secrete mucin onto mucosal surfaces under the regulation of an apical, phospholipase C/Gq-coupled P2Y2 receptor. We tested whether cortical actin filaments negatively regulate exocytosis in goblet cells by forming a barrier between secretory granules and plasma membrane docking sites as postulated for other secretory cells. Immunostaining of human lung tissues and SPOC1 cells (an epithelial, mucin-secreting cell line) revealed an apical distribution of {beta}- and {gamma}-actin in ciliated and goblet cells. In goblet cells, actin appeared as a prominent subplasmalemmal sheet lying between granules and the apical membrane, and it disappeared from SPOC1 cells activated by purinergic agonist. Disruption of actin filaments with latrunculin A stimulated SPOC1 cell mucin secretion under basal and agonist-activated conditions, whereas stabilization with jasplakinolide or overexpression of {beta}- or {gamma}-actin conjugated to yellow fluorescent protein (YFP) inhibited secretion. Myristoylated alanine-rich C kinase substrate, a PKC-activated actin-plasma membrane tethering protein, was phosphorylated after agonist stimulation, suggesting a translocation to the cytosol. Scinderin (or adseverin), a Ca2+-activated actin filament severing and capping protein was cloned from human airway and SPOC1 cells, and synthetic peptides corresponding to its actin-binding domains inhibited mucin secretion. We conclude that actin filaments negatively regulate mucin secretion basally in airway goblet cells and are dynamically remodeled in agonist-stimulated cells to promote exocytosis.

lung; mucus; exocytosis


Address for reprint requests and other correspondence: C. W. Davis, Cystic Fibrosis/Pulmonary Research and Treatment Center, 6009 Thurston Bowles, CB 7248, Univ. of North Carolina, Chapel Hill, NC 27599-7248 (E-mail: cwdavis{at}med.unc.edu)




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