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Published 15 October 2001. doi:10.1083/jcb.200102106
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© The Rockefeller University Press, 0021-9525/2001/10/279 $5.00
The Journal of Cell Biology, Volume 155, Number 2, October 15, 2001 279-290

Article

 Fusion pore expansion is a slow, discontinuous, and Ca2+-dependent process regulating secretion from alveolar type II cells

Thomas Haller1, Paul Dietl1, Kristian Pfaller2, Manfred Frick1, Norbert Mair1, Markus Paulmichl1, Michael W. Hess4, Johannes Fürst1, and Karl Maly3

1 Department of Physiology, University of Innsbruck, A-6020 Innsbruck, Austria
2 Department of Anatomy and Histology, University of Innsbruck, A-6020 Innsbruck, Austria
3 Department of Medical Chemistry and Biochemistry, University of Innsbruck, A-6020 Innsbruck, Austria
4 Institute of Biotechnology, University of Helsinki, FIN 00014 Helsinki, Finland

Address correspondence to Dr. Thomas Haller, Department of Physiology, University of Innsbruck, Fritz-Pregl-Str. 3, A-6020 Innsbruck, Austria. Tel.: 0043-512-507-3770. Fax: 0043-512-507-2853. E-mail: thomas.haller{at}uibk.ac.at

In alveolar type II cells, the release of surfactant is considerably delayed after the formation of exocytotic fusion pores, suggesting that content dispersal may be limited by fusion pore diameter and subject to regulation at a postfusion level. To address this issue, we used confocal FRAP and N-(3-triethylammoniumpropyl)-4-(4-[dibutylamino]styryl) pyridinium dibromide (FM 1-43), a dye yielding intense localized fluorescence of surfactant when entering the vesicle lumen through the fusion pore (Haller, T., J. Ortmayr, F. Friedrich, H. Volkl, and P. Dietl. 1998. Proc. Natl. Acad. Sci. USA. 95:1579–1584). Thus, we have been able to monitor the dynamics of individual fusion pores up to hours in intact cells, and to calculate pore diameters using a diffusion model derived from Fick's law. After formation, fusion pores were arrested in a state impeding the release of vesicle contents, and expanded at irregular times thereafter. The expansion rate of initial pores and the probability of late expansions were increased by elevation of the cytoplasmic Ca2+ concentration. Consistently, content release correlated with the occurrence of Ca2+ oscillations in ATP-treated cells, and expanded fusion pores were detectable by EM. This study supports a new concept in exocytosis, implicating fusion pores in the regulation of content release for extended periods after initial formation.

Key Words: alveolus; exocytosis; lamellar bodies; lung; surfactant secretion

M. Paulmichl's present address is Department of Physiology and Biochemistry, University of Milan, I-20133 Milan, Italy.

* Abbreviations used in this paper: FM 1-43, N-(3-triethylammoniumpropyl)-4-(4-[dibutylamino]styryl) pyridinium dibromide; [Ca2+]i, intracellular Ca2+ concentration; LB, lamellar body; LSM, laser scanning microscopy; SEM, scanning electron microscopy; TEM, transmission electron microscopy.


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