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Stimulus-Secretion Coupling in Chromaffin Cells Isolated Proc. Natl. Acad. Sci. USA Vol. 74, No. 11, pp. 5036-5040, November 1977 Cell Biology Stimulus-secretion coupling in chromaffin cells isolated from bovine adrenal medulla (catecholamine secretion/acetylcholine receptors/K+ depolarization/calcium requirement/microtubule disruption) ALLAN S. SCHNEIDER*, RUTH HERZ*, AND KURT ROSENHECKt * Sloan-Kettering Institute for Cancer Research, Cornell University Graduate School of Medical Sciences, New York, New York 10021; and tDepartment of Membrane Research, Weizmann Institute of Science, Rehovot, Israel Communicated by Francis 0. Schmitt, August 19,1977 ABSTRACT Bovine adrenal chromaffin cells were isolated membrane fusion and exocytosis, (iii) the possible role of cyclic by removal of the cortex and sequential collagenase digestion nucleotides coupled with ion translocation in mediating hor- of the medulla. The catecholamine secretory function of these cells was characterized with respect to acetylcholine stimula- mone and neurotransmitter synthesis and secretion, and (iv) tion, cation requirements, and cytoskeletal elements. The the role of microfilaments, microtubules, and/or a calcium- dose-response curve for stimulated release had its half-maxi- modulated contractile protein system in bringing secretory mum value at 10-5 M acetylcholine, and maximum secretion granules together with the plasma membrane to facilitate ex- was on the average 7 times that of control basal secretion. The ocytosis. Further advances may be possible on these and related differential release of epinephrine versus norepinephrine after questions through the use of isolated chromaffin cells. stimulation with 0.1 mM acetylcholine occurred in proportion to their distribution in the cell suspension. The cholinergic re- In the present work we provide a functional characterization ceptors were found to be predominantly nicotinic. The kinetics of bovine adrenal chromaffin cells isolated in large quantities of catecholamine release were rapid, with significant secretion (107-108 cells) and essentially free of cortical cells. We report occurring in less than 60 sec and 85% of maximum secretion the dependence of the secretory function of these cells on time, within 5 min. A critical requirement for calcium in the extra- ACh concentration, potassium depolarization, calcium con- cellular medium was demonstrated, and 80% of maximum se- centration, and nicotinic and muscarinic agents. In addition, cretion was achieved at physiologic calcium concentrations. Stimulation by excess potassium (65 mM KCI) also induced data are presented on the differential release of epinephrine catecholamine secretion which differed from acetylcholine and norepinephrine and on the secretory effects of microtubule- stimulation in being less potent, in having a different depen- and microfilament-disrupting agents and of cholinesterase dence on calcium concentration, and in its response to the local inhibitors. anesthetic tetracaine. Tetracaine, which is thought to inhibit Isolated adrenal chromaffin cells were first used by Douglas membrane cation permeability, was able to block acetylcho- and coworkers (5, 6) in mixed tissue culture to study their line-stimulated but not KCI-stimulated secretion. The mi- crotubule disrupting agent vinblastine was able to block cate- electrophysiological properties by microelectrode techniques. cholamine release whereas the microfilament disrupter cyto- More recently, other workers have reported isolation of adrenal chalasin B had little effect. The results show the isolated bovine cells (7-9). Brandt et al. (7) and Biales et al. (8) discovered chromaffin cells to be viable, functioning, and available in large transmembrane action potentials in isolated chromaffin cells quantity. These cells now provide an excellent system for in tissue culture, the former workers using rat and the latter both studying cell surface regulation of hormone and neuro- gerbil and human chromaffin cells. Hochman and Perlman (9) transmitter release. isolated a mixture of chromaffin and cortical cells from whole The term "stimulus-secretion coupling" was originally coined guinea pig adrenal glands and used these to study the conditions by Douglas and Rubin (1, 2) more than a decade ago to describe of catecholamine secretion. In the above studies with rodent the sequence of events initiated by acetylcholine (ACh) stim- adrenal glands, relatively small quantities of chromaffin cells ulation of adrenal chromaffin cells and leading to secretion of were obtained per gland (103-105) due to the small gland catecholamines by exocytosis. They had in mind the close size. similarity to the phenomenon of "excitation-contraction cou- There are several advantages of the isolated bovine chro- pling" in muscle (namely, the key role of calcium in mediating maffin cell system that should prove useful in future studies. both secretion and contraction and a parallel set of electrical First, the system is relatively well defined and available in large and ionic events at the plasma membrane in response to ACh). quantity. Second, the absence of cortical cells should aid future Much progress has been made during the past 2 decades in studies of both the cyclic nucleotide response and differential elucidating the various steps in the mechanism of secretion, with release, because cortical cells are known to have their own cyclic a substantial portion of the data deriving from studies on the nucleotide system and corticosteroids are known to affect the perfused adrenal gland (2-4). There remain, however, many conversion of norepinephrine to epinephrine. Third, the kinetics surface of secretion of coupling between cholinergic stimulation and the secretory important aspects of cell receptor regulation response should be more easily resolved in the isolated cell that are still poorly understood, such as (i) the molecular nature in kinetics of of the calcium permeability sites that are altered by activated suspension than the perfused gland, because the cholinergic receptors and potassium depolarization, (ii) the perfusion and tissue penetration are not complicating factors. which calcium into the cell induces Fourth, isolated cell suspensions offer the possibility of spec- mechanism by entry trofluorometric study of membrane fluidity, ion translocation; receptor topography, etc., by using appropriate fluorescent The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked probes. "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact. Abbreviation: ACh, acetylcholine. 5036 Downloaded by guest on September 27, 2021 Cell Biology: Schneider et al. Proc. Natl. Acad. Sci. USA 74 (1977) 5037 Table 1. Catecholamine' content and differential release 100 0 from isolated chromaffin cells * ACh (10-4M) Total catecholamines, 80/ z nmol/mg of protein % 0 Mean Range epinephrine LUJ 60_ Adrenal medulla* 577 (529-685) 75 LU(0. Cells (day W)t 347 (221-696) 46 U-I) Cells (day 2)t 332 (195-769) 42 40 / ACh (0.1 mM) stimulatedt secretion 72 ( 21-136) 42 20 * Control * Six independent assays on four excised medullas. t Thirteen independent cell preparations. Twenty-seven independent supernatants of stimulated cells at 370, C 20 min, 2 mM CaCl2. Mean (±SD) stimulated release was 7.0 + 3.7 0 4 8 12 16 20 times control basal secretion. TIME (minutes) FIG. 1. Kinetics of catecholamine secretion. Upper curve, 0.1 mM MATERIALS AND METHODS ACh in buffer II; lower curve, control basal secretion in buffer II. Maximum secretion = 74 nmol/mg of protein = 6.4 1.9 (SD) X Cell Preparation. Adrenal glands were removed from bulls control. immediately after slaughter, placed on ice, and delivered to the laboratory within 60-90 min. The chromaffin cell isolation sion intensities of epinephrine and norepinephrine standards procedure was a modification of that reported by Kloppenberg were approximately equal at equal concentrations in the range et al. (10) and Hochman and Perlman (9) for isolation of of 1-10 nmol. For differential determination, oxidations were adrenal cells from whole adrenal glands. In our procedure, the carried out at pH 3.5 (excitation, 410 nm; emission, 520 rm) and cortex, which is easily distinguished from the medulla by the pH 6.0 (excitation, 400 nm; emission, 510 nm). Fluorescence unaided eye, was removed and discarded. The medulla was was monitored with a Perkin-Elmer MPF4 spectrofluorome- then cut into fine pieces (-1 mm) and rinsed thoroughly in cold ter. Ca2+-free Krebs-Ringer bicarbonate glucose buffer, pH 7.2-7.4 We compared the results of the catecholamine assay with and (buffer I, ref. 9). Six to eight medullas were processed at a time without a prior alumina adsorption as described by Anton and (total wet weight, 15-25 g for the cut and washed pieces). The Sayre (14). The effect of alumina adsorption was relatively small cells were separated from the tissue by four or five sequential for medullas (11% increase) and supernatants containing se- collagenase digestions (Type I, Worthington Biochemicals, 0.2% creted catecholamines (6% increase) and slightly larger for cells in buffer 1, 2 ml/g wet weight), each of 30-min duration at 370 (24% increase). Secreted catecholamines were routinely assayed under 95% 02/5% CO2. Cells were harvested after each di- without prior alumina adsorption. gestion by filtration; the first harvest was discarded because it contained damaged cells and erythrocytes. Subsequent cell RESULTS harvests were washed with the same buffer supplemented
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