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Regulation of Ionic Currents in Pheochromocytoma Cells by Nerve Growth Factor and Dexamethasone

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Regulation of Ionic Currents in Pheochromocytoma Cells by Nerve Growth Factor and Dexamethasone The Journal of Neuroscience, November 1989, 9(11): 3978-3987 Regulation of Ionic Currents in Pheochromocytoma Cells by Nerve Growth Factor and Dexamethasone Sarah S. Garber, Toshinori Hoshi, and Richard W. Aldrich Department of Neurobiology, Stanford University, Stanford, California 94305 Growth factors and hormones induce differentiation of clonal panied by changesin electrical properties (seeSpitzer, 1985, for pheochromocytoma (PC1 2) cells, which are derived from rat review). Many lines of evidence suggestthat the presenceof adrenal medulla chromaffin cells. On application of nerve nerve growth factor (NGF) and glucocorticoids are important growth factor (NGF), PC1 2 cells extend neurites and express to the differentiation of postnatal adrenal medullary cells.Clonal properties characteristic of autonomic ganglion cells. In con- PC12 cells, derived from rat adrenal chromaffin cells, have been trast, incubation of PC12 cells with a corticosteroid, dexa- usedas a model systemfor the study of neuronal differentiation. methasone (DEX), does not induce neurite formation but Rat adrenal chromaffin cellsand rat pheochromocytomasshow causes an increase in tyrosine hydroxylase activity, sug- similar changesin processoutgrowth, catecholaminecontent, gesting that the cells become chromaffin cell-like. The ability and tyrosine hydroxylase activity when treated with NGF or of NGF and DEX to regulate ionic currents has been less glucocorticoids (Tishler et al., 1982b, 1983). well studied. Therefore, we examined how long-term NGF PC 12cells are normally sphericalin shapeand do not generate and DEX treatments affected voltage-dependent Na, Ca, and action potentials. In the presenceof NGF, however, the cells K currents in PC12 cells. Voltage-dependent Na currents develop long, branching processes.This morphological differ- were observed only in a small fraction of the PC12 cells in entiation is accompaniedby increasedsynthesis and storageof the absence of NGF or DEX. Virtually all NGF-treated cells ACh (Greene and Rein, 1977) and development of electrical expressed Na currents within 7 d. DEX increased the number excitability (Dichter et al., 1977), which is, in part, a result of of cells expressing voltage-dependent Na current slowly over the enhanced expressionof Na+ channels (Rudy et al., 1982; 3 weeks, but, unlike NGF, DEX did not change Na current Mandel et al., 1988). PC12 cellshave also beenshown to respond density. Both NGF and DEX also affected the expression of to cortical steroids such as dexamethasone(DEX) by increasing voltage-dependent Ca currents. Most of the untreated cells the activity of tyrosine hydroxylase, an enzyme involved in the had only sustained, high-threshold voltage-dependent Ca synthesisof catecholamines.Glucocorticoids, suchas DEX, also currents. Chronic application of NGF or DEX increased the inhibit neurite outgrowth (Unsicker et al., 1978; Tishler et al., fractions of the cells that showed transient, low-threshold 1982b). It has been suggestedthat NGF causesPC12 cells to T-type Ca currents in addition to the high-threshold currents. develop toward autonomic neurons, whereas glucocorticoids The T-type Ca current density, however, increased signifi- causethem to develop toward a chromaffin cell-like phenotype cantly only in NGF-treated cells. Neither DEX nor NGF af- (Tishler et al., 1982b, 1983). Little is known, however, about fected the voltage-dependent K currents. These results sug- the effect of DEX on the electrophysiologicalproperties of PC12 gest that the expression of voltage-dependent Na and Ca cells. currents are differentially regulated by NGF and DEX. The Several different types of CaZ+channels, such as L-, N-, and distinction between treated and untreated cells decreased T-type Ca2+channels, have been characterized (seeTsien et al., after 3 weeks in culture as older untreated cells showed 1987 for review). High-threshold (L and N) Ca2+channels ac- increases in the fraction of cells expressing both Na and tivate at relatively depolarized voltages (> - 10 mV) and can low-threshold Ca currents. A PC1 2 subline selected for ad- be distinguishedby their slow inactivation and pharmacological herence to uncoated plastic also showed increased fraction properties. Low-threshold, T-type Ca*+ channelsbegin to ac- of cells expressing these currents, suggesting that inter- tivate at more hyperpolarized voltages (< - 70 mV) and inac- actions with substrate may also influence ionic current tivate rapidly with maintaineddepolarization. Each type ofCa2+ expression. channel may serve a different physiological function. The dis- tribution of the types of voltage-dependent Ca2+ channels is Peptide growth factors and steroid hormones play important different among different cell types. Adrenal chromaffin cells, roles in the differentiation of excitable cells such as neuronsand for example, do not expressT-type Ca*+ channels, while cells endocrine cells. Differentiation of excitable cells is often accom- from many other tissuesexpress both T-type and L-type CaZ+ channels(Tsien et al., 1987). Both L- and N-type channelshave Received Mar. 22, 1989; revised June 1, 1989; accepted June 8, 1989. beenimplicated in the control of neurotransmitter release(Rane We thank Drs. C. Bitler, R. Maue, M. P. Nusbaum, and D. Shelton for critical et al., 1987; Hirning et al., 1988). reading of this manuscript, Dr. R. Tsien for helpful discussion, and Drs. M. Morganfield and C. Burnett for their constant support and encouragement. We Pharmacological evidence has suggestedthat undifferentia- are indebted to Drs. D. L. Shelton and E. Shooter for making clone B and PC12 ted PC12 cells, like chromaffin cells, expressprimarily a dihy- cell lines available to us. Supported by NS07 158 to S.S.G., NIH and American Heart (CA affilate) postdoctoral fellowships to T.H., and NS23294 to R.W.A. dropyridine-sensitive, high-threshold voltage-dependent Ca Correspondence should be addressed to Sarah S. Garber at the above address. current (Kongsamut and Miller, 1986). A minor dihydropyri- Copyright 0 1989 Society for Neuroscience 0270-6474/89/l 13976-12$02.00/O dine-insensitive Ca2+component which increasesafter the ap- The Journal of Neuroscience, November 1989, 9(11) 3977 plication of NGF has also been observed (Takahashi et al., 1985; currents primarily from the cell body. There were no marked qualitative Kongsamut and Miller, 1986; Streit and Lux, 1987). These ob- differences in the capacitance measurements or the current recordings obtained from the cells using either of these 2 methods or those made servations are consistent with the development of a neuronal from intact cells with neurites. phenotype in the presence of NGF. The cell capacitance was determined from the capacitative transient The amount and temporal pattern of Ca influx can be regu- current in response to a 20 mV voltage step. The whole-cell results lated by voltage-dependent Na, Ca, and K channels. Because presented are based on recordings from >900 cells. Single-channel re- cordings were made from 25 cells. the regulation ofintracellular levels ofCa2+ is important to many Solutions. Whole-cell Ca currents were recorded with external solu- cellular processes, including the differentiation of excitable cells tions containing (in mM) 10 CaCl,; 130 tetraethylammonium (TEA); 2 (see Kater et al., 1988, and Miller, 1988), we hypothesized that MgCl,; 10 HEPES; 5 4-aminopyridine; internal solutions contained (in DEX or NGF would differentially affect the expression of these mM) 120 CsCl; 20 TEA, 2 MgCl,; 11 EGTA, 1 CaCl,; 10 HEPES; 10 ion channels. Although the effects of NGF on voltage-dependent nM free Ca2+. Whole-cell Na and K currents were recorded with external solutions with 140 NaCl; 2.8 KCl; 2 MgCl,; 1 CaCl,; 10 HEPES (so- Na currents of PC12 cells have been studied (e.g., Mandel et lutions contained up to 40 mM sucrose); internal solutions normally al., 1988) neither the effects of NGF on other ion currents nor contained (in mM) 140 KCl; 2 MgCl,; 11 EGTA, 1 CaCl,; 10 HEPES; the effects of DEX on the electrical properties of PC 12 cells have 10 nM free Ca2+. All solutions were brought to pH 7.2 with N-meth- been systematically examined. We show here that chronic in- ylglucamine (NMG). Single-channel recordings were made in the cell- attached configuration. The pipette was filled with (in mM) 105 BaCl,; cubation of PC 12 cells with DEX and/or NGF induces distinct 10 HEPES: pH 7.2 with TEAOH. The bath solution contained (in mM) changes in cellular morphologies and changes in voltage-depen- 140 K-g&&rate; 3 MgCl,; 1 EGTA, 10 HEPES; pH 7.2 with NMG. dent Na and Ca currents, but not in voltage-dependent K cur- Other solutions used are described in the figure legends. Salts and DEX rents (cell culture grade) were obtained from Sigma Chemical Co. (St. Louis, -‘--I.MO\ Statistical analysis. Recordings from cells were scored on the absence Materials and Methods or presence of transient T-type Ca current, Na current, or transient K current. Recordings made from cells within each treatment group were Cell culture. PC12 cells were obtained from the laboratory of Dr. E. M. distributed over 30 d after plating. Data from each group, at each time Shooter (Department of Neurobiology, Stanford University, CA). The point, were pooled for statistical comparison. We found that changes cells were maintained in plastic Lux tissue culture dishes (Miles Lab- in the numbers of cells expressing the ionic current in question and oratories, Naperville, IL). with Dulbecco’s modified Eagle’s medium current densities occurred gradually. These changes could be summa- with or without 25 mM HEPES (GIBCO. Grand Island, NY). supnle- rized by pooling the data into groups which were treated up to (and mented with 5% horse- and 5%-supplemented calf sera (Hyclone-Lab- inclusive of) 2 1 d, over 2 1 d, or up to 30 d. Percentages of cells expressing oratories, Logan, UT). Two different lots of each sera type produced either T-type Ca current or Na current weredetermined as a simple indistinguishable results. Levels of glucocorticoids in the media were average of cells within a treatment group over an indicated time period.
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