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Long-Chain Fatty Acids Activate Calcium Channels in Ventricular Myocytes

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Long-Chain Fatty Acids Activate Calcium Channels in Ventricular Myocytes Proc. Nati. Acad. Sci. USA Vol. 89, pp. 6452-6456, July 1992 Medical Sciences Long-chain fatty acids activate calcium channels in ventricular myocytes (free fatty acids/arachidonic acid/olekic add) JAMES MIN-CHE HUANG, Hu XIAN, AND MARVIN BACANER* Department of Physiology, University of Minnesota, Minneapolis, MN 55455 Communicated by James Serrin, March 30, 1992 (receivedfor review September 15, 1991) ABSTRACT Nonesterified fatty acids accumulate at sites down (>70%o decrease in ICa) during the 10- to 15-min control of tissue injury and necrosis. In cardiac tissue the concentra- period were discarded. Whole-cell voltage-clamp experi- tions of oleic acid, arachidonic acid, leukotrienes, and other ments with myocytes were done at 320C with 2- to 3-MU glass fatty acids increase greatly during ischemia due to receptor or pipettes (Narishige PB 7 puller). Dagan 3900A patch-clamp nonreceptor-mediated activation of phospholipases and/or circuit, axon DMA interface, IBM cloned AT 386 computer, diminished reacylation. In ischemic myocardium, the time and P-CLAMP software were used for command pulses, data course of increase in fatty acids and tissue calcium closely acquisition, and analysis. All lipophilic agents were dissolved parallels irreversible cardiac damage. We postulated that fatty in 95% ethanol to make stock solutions and then diluted to acids released from membrane phospholipids may be involved <0.1% ethanol concentration before being applied by con- in the increase ofintraceilular calcium. We report here that low tinuous bath perfusion. In control studies, 0.1% ethanol in the concentrations (3-30 ,AM) of each long-chain unsaturated buffer solution had no influence on ICa or membrane response (oleic, linoleic, linolenic, and arachidonic) and saturated to fatty acids (see text and Fig. 4). ICa was measured with 2.5 (paimitic, stearic, and arachidic) fatty acid tested induced mM Ba2+ as the charge carrier. From a holding potential of multifold increases in voltage-dependent calcium currents (Ic.) -85 mV, sodium current was inactivated by prepulsing to in cardiac myocytes. In contrast, neither short-chain fatty acids -40 mV for 60 msec. Then a series of depolarization pulses (<12 carbons) or fatty acid esters (oleic and palmitic methyl ranging from -60 to +50 mV in 10-mV increments were sent esters) had any effect on IcS, indicating that activation of at 10-sec intervals. Except where otherwise specified, each calcium channels depended on chain length and required a free family of control ICa pulses was recorded repeatedly with a carboxyl group. Inhibition of protein kinases C and A, G 2-min rest period in between until several sequential families proteins, eicosanoid production, or nonenzymatic oxidation of stable ICa traces were obtained before the bath was did not block the fatty acid-induced increase in Ica. Thus, changed. Potassium currents were blocked with internal Cs long-chain fatty acids appear to directly activate Ica, possibly and external Cs and tetraethylammonium solutions. The bath by acting at some lipid sites near the channels or directly on the solution contained 65 mM NaCl, 2.5 mM BaCl2, 80 mM channel protein itself. We suggest that the combined effects of tetraethylammonium chloride, 5 mM CsCl, 1 mM MgCl2, 5 fatty acids released during ishemla on Ica may contribute to mM Hepes, and 5 mM glucose (pH 7.45). The pipette solution ischemia-induced pathogenic events on the heart that involve contained 145 mM CsCl, 5 mM NaCl, 1 mM MgCl2, 6 mM calcium, such as arrhythmlas, conduction disturbances, and EGTA, 5 mM Hepes, 3 mM Na2ATP, 3 mM creatine phos- myocardial damage due to cytotoxic calcium overload. phate, and 5 mM glucose (pH 7.3). Junction potentials were subtracted by adjusting voltage-offset compensation to zero with pipette in the bath. LaCl3 (0.1 mM), which has no effect Considerable evidence suggests that the accumulation of on sodium current but completely blocks calcium channels, membrane-derived free fatty acids and lysophospholipids are was added as a final step in each study to block ICa for important in the pathogenic events caused by myocardial leakage-current subtraction. Alternatively, nifedipine (3 ,uM) ischemia (1-8). The onset of disturbed membrane function, was used to specifically block L-type calcium channels to proceeding on to irreversible cardiac damage, closely paral- assess the ICa component carried via T-type channels. lels the time course of accumulation of fatty acids and an All chemicals were from Sigma except arachidonic acid associated increase in tissue calcium (3, 8). We postulated (Nu-Chek, Austin, MN), A63162 (Abbott), WY50295 that the increase in fatty acids might be involved in the altered (Wyeth), and U74500A (Upjohn). membrane function that leads to increased tissue calcium. We report that fatty acids have powerful effects on voltage- dependent calcium currents (ICa) in cardiac cells, which could RESULTS AND DISCUSSION trigger ischemia-induced pathogenic actions on the heart that The -10 mV traces shown in Fig. 1 (Left) indicate that involve calcium-such as arrhythmias, coronary vasocon- perfusion of myocytes with 10 ,uM arachidonic acid, 10 gM striction, and cytotoxic calcium overload. oleic acid, or 30 uM stearic acid caused a large increase in Ica. The respective current-voltage relationships (Fig. ld) show MATERIALS AND METHODS an increase in ICa with no shift in activation or maximal peak current potential. Nor was there a significant potential shift The effect of fatty acids on calcium currents was studied in in steady-state activation and inactivation curves (Fig. 2). single guinea pig ventricular myocytes using a standard The current was completely blocked by LaCl3, which blocks whole-cell voltage-clamp technique. Ventricular myocytes both L- and T-type channels. Blockade of L-type channels were isolated as described (9). Only calcium-tolerant myo- with nifedipine suppressed 95-98% of the current, indicating cytes with clear striations were used. Cells with rapid run- Abbreviations: Ica. voltage-dependent calcium currents; PKA and The publication costs ofthis article were defrayed in part by page charge PKC, protein kinase A and C, respectively; NDGA, nordihydrogua- payment. This article must therefore be hereby marked "advertisement" iaretic acid; GDP[,6S], guanosine 5'-[-thio]diphosphate. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 6452 Downloaded by guest on September 26, 2021 Medical Sciences: Huang et al. Proc. Natl. Acad. Sci. USA 89 (1992) 6453 a d (nA) 0.8 uof 0.6- at C._N - C 0.4 CZ 0 z 0.2 - C .- -100 -80 -60 -40 -20 0 20 SA 4ms -5.0 Em (mV) FIG. 1. acid oleic acid (OA), and stearic acid FIG. 2. Steady-state activation and inactivation curves of cal- Arachidonic (AA), cium channels in control and after application of fatty acid (linole- (SA) increase calcium currents in guinea pig ventricular myo- (IC.) laidic acid, 30 MM). Both activation and steady-state inactivation cytes. (a-c) ICa (before leakage-current subtraction) during - 10-mV curves were from the same representative cell. The steady-state test pulse before (middle traces) and after (lower traces), showing a multifold increase in ICa after perfusion with arachidonic acid (10 inactivation curves were obtained with a double-pulse protocol. From a holding potential of -85 mV, a prepulse (-100 to +20 mV) 16 oleic acid 14 or stearic acid AM, min) (a), (10MAM, min) (b), (30MuM, of 5-sec duration was followed by a test pulse at 0 mV. Sodium 17 min) (c). Upper trace in a-c shows that lanthanum (0.1 mM) added after the fatty acids completely suppressed the calcium current. (d) current was blocked by 30 MM tetrodotoxin. Peak amplitudes of ICa Respective current-voltage relationships after subtraction ofleakage of the test pulses were normalized to the amplitude of the test pulse with the -100-mV prepulse and plotted as a function of prepulse current. Open symbols are controls. After addition of arachidonic potential. Activation curves were obtained by normalizing conduc- acid (e), oleic acid (U), or stearic acid (A), ICa increased significantly tances (g) to the value at 0 mV (g max). Current amplitudes at 0-mV with no shift in activation or maximal peak currents. Em, membrane potential. test pulses in control and after application of 30 AM linolelaidic acid were 664 pA and 1250 pA, respectively. Em, membrane potential; I, current; hoc, steady-state inactivation; moo, steady-state activation. that not more than 5% was carried via T channels. After nifedipine blockade, fatty acids increased ICa up to 5%, and linolenic acids. Oleic acid produced maximal increases in indicating a small component was carried via T-type chan- at nels. The increase in peak ICa induced by fatty acids was ICa 10 uM concentration, whereas arachidonic, linoleic, associated with accelerated inactivation. In the control and linolenic acids (3-50 uM) increased ICa in a dose- concen- -10-mV trace (Fig. la) ICa inactivation fit a single exponen- dependent manner (Table 1). In contrast, at 100 MLM the relative increases in ICa by oleic acid and tial (Trs0w = 264 msec), whereas after arachidonic acid there trations, were + = was a fast component (Tfast = 24 msec) as well as a slow arachidonic acid decreased to 446 207% (n 3) and ± = the component (Trjow = 278 msec) in the -10-mV trace. The 213 117% (n 4), respectively. Palmitic acid (30 MkM), effect offatty acids on ICa was similar to the kinetics seen with most potent saturated fatty acid, increased ICa 6-fold, fol- the calcium-channel agonist Bay K 8644 and may be similarly lowed by stearic and arachidic acids. Fatty acids applied related to altered channel gating and a partial antagonist internally had an identical effect on 'Ca, but the effects were effect on inactivation attributed to Bay K 8644 (10, 11).
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