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© The Rockefeller University Press, 0021-9525/1997//885 $5.00
The Journal of Cell Biology, Volume 139, Number 4, , 1997 885-894

Article

Multiple Forms of Endocytosis In Bovine Adrenal Chromaffin Cells



Corey Smith and Erwin Neher

Department of Membrane Biophysics, Max-Planck-Institute for Biophysical Chemistry, Am Fassberg 11, D-37077 Göttingen, Germany

We studied endocytosis in chromaffin cells with both perforated patch and whole cell configurations of the patch clamp technique using cell capacitance measurements in combination with amperometric catecholamine detection. We found that chromaffin cells exhibit two relatively rapid, kinetically distinct forms of stimulus-coupled endocytosis. A more prevalent "compensatory" retrieval occurs reproducibly after stimulation, recovering an approximately equivalent amount of membrane as added through the immediately preceding exocytosis. Membrane is retrieved through compensatory endocytosis at an initial rate of ~6 fF/s. Compensatory endocytotic activity vanishes within a few minutes in the whole cell configuration. A second form of triggered membrane retrieval, termed "excess" retrieval, occurs only above a certain stimulus threshold and proceeds at a faster initial rate of ~248 fF/s. It typically undershoots the capacitance value preceding the stimulus, and its magnitude has no clear relationship to the amount of membrane added through the immediately preceding exocytotic event. Excess endocytotic activity persists in the whole cell configuration. Thus, two kinetically distinct forms of endocytosis coexist in intact cells during perforated patch recording. Both are fast enough to retrieve membrane after exocytosis within a few seconds. We argue that the slower one, termed compensatory endocytosis, exhibits properties that make it the most likely mechanism for membrane recycling during normal secretory activity.

We would like to gratefully thank Dr. T. Xu for help in the Ca2+ estimation protocol. We would also like to thank Drs. H. von Gersdorff and C. Mathes for helpful discussions of this manuscript. F. Friedlein and M. Pilot furnished invaluable technical assistance. (All acknowledged are affiliated with the Max-Planck Institute for Biophysical Chemistry, Göttingen, Germany.)

Address all correspondence to Corey Smith, Department of Membrane Biophysics, Max-Planck-Institute for Biophysical Chemistry, Am Fassberg 11, D-37077 Göttingen, Germany. Tel.: +49-551-201-1629. Fax: +49-551-201-1688.


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