A triggered mechanism retrieves membrane in seconds after Ca(2+)- stimulated exocytosis in single pituitary cells

doi:10.1083/jcb.124.5.667

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A triggered mechanism retrieves membrane in seconds after Ca(2+)- stimulated exocytosis in single pituitary cells

P Thomas, AK Lee, JG Wong and W Almers
Department of Physiology and Biophysics, University of Washington, Seattle 98195.

In neuroendocrine cells, cytosolic Ca2+ triggers exocytosis in tens of milliseconds, yet known pathways of endocytic membrane retrieval take minutes. To test for faster retrieval mechanisms, we have triggered short bursts of exocytosis by flash photolysis of caged Ca2+, and have tracked subsequent retrieval by measuring the plasma membrane capacitance. We find that a limited amount of membrane can be retrieved with a time constant of 4 s at 21-26 degrees C, and that this occurs partially via structures larger than coated vesicles. This novel mechanism may be arrested at a late step. Incomplete retrieval structures then remain on the cell surface for minutes until the consequences of a renewed increase in cytosolic [Ca2+] disconnect them from the cell surface in < 1 s. Our results provide evidence for a rapid, triggered membrane retrieval pathway in excitable cells.
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Perrais, D., Kleppe, I. C, Taraska, J. W, Almers, W. (2004). Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J. Physiol. 560: 413-428 [Abstract] [Full Text]
Bauer, R. A., Overlease, R. L., Lieber, J. L., Angleson, J. K. (2004). Retention and stimulus-dependent recycling of dense core vesicle content in neuroendocrine cells. J. Cell Sci. 117: 2193-2202 [Abstract] [Full Text]
Duan, K., Yu, X., Zhang, C., Zhou, Z. (2003). Control of Secretion by Temporal Patterns of Action Potentials in Adrenal Chromaffin Cells. J. Neurosci. 23: 11235-11243 [Abstract] [Full Text]
Kushmerick, C., von Gersdorff, H. (2003). Exo-endocytosis at mossy fiber terminals: Toward capacitance measurements in cells with arbitrary geometry. Proc. Natl. Acad. Sci. USA 100: 8618-8620 [Full Text]
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Burgoyne, R. D., Morgan, A. (2003). Secretory Granule Exocytosis. Physiol. Rev. 83: 581-632 [Abstract] [Full Text]
Graham, M. E., O'Callaghan, D. W., McMahon, H. T., Burgoyne, R. D. (2002). Dynamin-dependent and dynamin-independent processes contribute to the regulation of single vesicle release kinetics and quantal size. Proc. Natl. Acad. Sci. USA 99: 7124-7129 [Abstract] [Full Text]
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Chan, S.-A., Smith, C. (2001). Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells. J. Physiol. 537: 871-885 [Abstract] [Full Text]
Gale, J. E., Marcotti, W., Kennedy, H. J., Kros, C. J., Richardson, G. P. (2001). FM1-43 Dye Behaves as a Permeant Blocker of the Hair-Cell Mechanotransducer Channel. J. Neurosci. 21: 7013-7025 [Abstract] [Full Text]
Heidelberger, R. (2001). ATP Is Required at an Early Step in Compensatory Endocytosis in Synaptic Terminals. J. Neurosci. 21: 6467-6474 [Abstract] [Full Text]
Lee, A. K, Tse, A. (2001). Endocytosis in identified rat corticotrophs. J. Physiol. 533: 389-405 [Abstract] [Full Text]
Kilic, G., Angleson, J. K, Cochilla, A. J, Nussinovitch, I., Betz, W. J (2001). Sustained stimulation of exocytosis triggers continuous membrane retrieval in rat pituitary somatotrophs. J. Physiol. 532: 771-783 [Abstract] [Full Text]
Elhamdani, A., Brown, M. E., Artalejo, C. R., Palfrey, H. C. (2000). Enhancement of the Dense-Core Vesicle Secretory Cycle by Glucocorticoid Differentiation of PC12 Cells: Characteristics of Rapid Exocytosis and Endocytosis. J. Neurosci. 20: 2495-2503 [Abstract] [Full Text]
Parker, D. (2000). Activity and Calcium-Dependent Mechanisms Maintain Reliable Interneuron Synaptic Transmission in a Rhythmic Neural Network. J. Neurosci. 20: 1754-1766 [Abstract] [Full Text]
Cousin, M. A., Robinson, P. J. (2000). Ca2+ Influx Inhibits Dynamin and Arrests Synaptic Vesicle Endocytosis at the Active Zone. J. Neurosci. 20: 949-957 [Abstract] [Full Text]
Neale, E. A., Bowers, L. M., Jia, M., Bateman, K. E., Williamson, L. C. (1999). Botulinum Neurotoxin a Blocks Synaptic Vesicle Exocytosis but Not Endocytosis at the Nerve Terminal. JCB 147: 1249-1260 [Abstract] [Full Text]
Vogel, S. S., Smith, R. M., Baibakov, B., Ikebuchi, Y., Lambert, N. A. (1999). Calcium influx is required for endocytotic membrane retrieval. Proc. Natl. Acad. Sci. USA 96: 5019-5024 [Abstract] [Full Text]
Neves, G., Lagnado, L. (1999). The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J. Physiol. 515: 181-202 [Abstract] [Full Text]
Roberts, R., Barbieri, M., Pryse, K., Chua, M, Morisaki, J., Stahl, P. (1999). Endosome fusion in living cells overexpressing GFP-rab5. J. Cell Sci. 112: 3667-3675 [Abstract]
Becker, K., Hart, N. (1999). Reorganization of filamentous actin and myosin-II in zebrafish eggs correlates temporally and spatially with cortical granule exocytosis. J. Cell Sci. 112: 97-110 [Abstract]
Takei, T., Yasufuku-Takano, J., Takano, K., Fujita, T., Yamashita, N. (1998). Effect of Ca2+ and cAMP on capacitance-measured hormone secretion in human GH-secreting adenoma cells. Am. J. Physiol. Endocrinol. Metab. 275: E649-E654 [Abstract] [Full Text]
Giovannucci, D. R., Yule, D. I., Stuenkel, E. L. (1998). Optical measurement of stimulus-evoked membrane dynamics in single pancreatic acinar cells. Am. J. Physiol. Cell Physiol. 275: C732-C739 [Abstract] [Full Text]
Nucifora, P. G P, Fox, A. P (1998). Barium triggers rapid endocytosis in calf adrenal chromaffin cells. J. Physiol. 508: 483-494 [Abstract] [Full Text]
Burgoyne, R. D (1998). Two forms of triggered endocytosis in regulated secretory cells. J. Physiol. 506: 589-589 [Full Text]
Engisch, K. L, Nowycky, M. C (1998). Compensatory and excess retrieval: two types of endocytosis following single step depolarizations in bovine adrenal chromaffin cells. J. Physiol. 506: 591-608 [Abstract] [Full Text]
Ohya, T., Sasaki, T., Kato, M., Takai, Y. (1998). Involvement of Rabphilin3 in Endocytosis through Interaction with Rabaptin5. J. Biol. Chem. 273: 613-617 [Abstract] [Full Text]
Mansvelder, H. D., Kits, K. S. (1998). The Relation of Exocytosis and Rapid Endocytosis to Calcium Entry Evoked by Short Repetitive Depolarizing Pulses in Rat Melanotropic Cells. J. Neurosci. 18: 81-92 [Abstract] [Full Text]
Smith, C., Neher, E. (1997). Multiple Forms of Endocytosis In Bovine Adrenal Chromaffin Cells. JCB 139: 885-894 [Abstract] [Full Text]
Takahashi, N., Kadowaki, T., Yazaki, Y., Miyashita, Y., Kasai, H. (1997). Multiple Exocytotic Pathways in Pancreatic {beta} Cells. JCB 138: 55-64 [Abstract] [Full Text]
Dai, J., Ting-Beall, H. P., Sheetz, M. P. (1997). The Secretion-coupled Endocytosis Correlates with Membrane Tension Changes in RBL 2H3 Cells. JGP 110: 1-10 [Abstract] [Full Text]
Lindgren, C. A., Emery, D. G., Haydon, P. G. (1997). Intracellular Acidification Reversibly Reduces Endocytosis at the Neuromuscular Junction. J. Neurosci. 17: 3074-3084 [Abstract] [Full Text]
Urrutia, R., Henley, J.�R., Cook, T., McNiven, M.�A. (1997). The dynamins: Redundant or distinct functions for an expanding family of�related�GTPases?. Proc. Natl. Acad. Sci. USA 94: 377-384 [Abstract] [Full Text]
Ninomiya, Y., Kishimoto, T., Miyashita, Y., Kasai, H. (1996). Ca2+-dependent Exocytotic Pathways in Chinese Hamster Ovary Fibroblasts Revealed by a Caged-Ca2+ Compound. J. Biol. Chem. 271: 17751-17754 [Abstract] [Full Text]
Parsons, T.D., Coorssen, J.R., Hortmann, H., Lee, A.K., Tse, F.W., Almers, W. (1995). The Last Seconds in the Life of a Secretory Vesicle. Cold Spring Harb Symp Quant Biol 60: 389-396 [Abstract]
Dai, J., Sheetz, M.P. (1995). Regulation of Endocytosis, Exocytosis, and Shape by Membrane Tension. Cold Spring Harb Symp Quant Biol 60: 567-571 [Abstract]
Keller, J. E., Neale, E. A. (2001). The Role of the Synaptic Protein SNAP-25 in the Potency of Botulinum Neurotoxin Type A. J. Biol. Chem. 276: 13476-13482 [Abstract] [Full Text]
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Rupnik, M., Kreft, M., Sikdar, S. K., Grilc, S., Romih, R., Zupancic, G., Martin, T. F. J., Zorec, R. (2000). Rapid regulated dense-core vesicle exocytosis requires the CAPS protein. Proc. Natl. Acad. Sci. USA 97: 5627-5632 [Abstract] [Full Text]