The cyclooxygenase-2 product prostaglandin E 2 modulates cardiac contractile function in adult rat ventricular cardiomyocytes
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1 Pharmacological Research 49 (2004) The cyclooxygenase-2 product prostaglandin E 2 modulates cardiac contractile function in adult rat ventricular cardiomyocytes Aaron L. Klein, Loren E. Wold, Jun Ren Department of Pharmacology, Physiology and Therapeutics, University of North Dakota School of Medicine and Health Sciences, Grand Forks, ND 58203, USA Accepted 3 September 2003 Abstract Prostaglandin E 2 (PGE 2 ), a product of the cyclooxygenase-2 pathway, has been shown to increase cardiac output and modulate cardiac contractile function. However, whether the cardiac contractile response of PGE 2 is due to its action on single ventricular myocytes has not been elucidated. To assess the mechanical effect of PGE 2 at the cellular level, adult rat ventricular myocytes were isolated and stimulated to contract at 0.5 Hz. Mechanical and intracellular Ca 2+ properties were evaluated using an IonOptix Myocam analog-to-digital optical detection system. Contractile and intracellular Ca 2+ properties were evaluated as peak shortening (PS), time-to-ps (TPS), time-to-90% relengthening (TR 90 ), maximal velocity of shortening or relengthening (±dl/dt) and Ca 2+ -induced intracellular Ca 2+ fluorescence release (CICR), baseline intracellular Ca 2+ levels and intracellular Ca 2+ decay rate (τ). PGE 2 (10 8 to 10 3 M) elicited an augmentation in PS but had no effect on TPS, TR 90, ±dl/dt, CICR and τ. High concentration of PGE 2 (10 5 M or higher) reduced the baseline intracellular Ca 2+ levels. These data indicate that the myocardial contractile response of PGE 2 may be due to its direct cardiac contractile action at the single ventricular myocyte level, probably through a mechanism independent of intracellular Ca 2+ release Elsevier Ltd. All rights reserved. Keywords: Prostaglandin E 2 ; Ventricular myocytes; Shortening; Relengthening; Intracellular Ca Introduction Cyclooxygenase (COX) catalyzes the oxidation and metabolism of arachidonic acid, leading to the formation of prostaglandin H 2 (PGH 2 ) and subsequently other prostaglandins such as PGE 2, PGF 2, PGD 2, PGI 2, and thromboxane A 2 [1,2]. Two COX isoforms, namely COX-1 and COX-2, have been found in mammalian cells with COX-1 being constitutively expressed and COX-2 being normally absent and inducible by various stimuli such as inflammatory cytokines [1,2]. Both prostaglandins and arachidonic acid are believed to participate in multiple physiological as well as pathophysiological responses such as reproductive, immunological, endocrine, tumorigenesis and cardiovascular regulation [1 4]. Arachidonic acid, the precursor for eicosanoid formation, is released in response to receptor activation and pathological stimuli such as my- Corresponding author. Present address: Division of Pharmaceutical Sciences, School of Pharmacy, University of Wyoming College of Health Sciences, P.O. Box 3375, Laramie, WY 82071, USA. Tel.: ; fax: address: jren@uwyo.edu (J. Ren). ocardial ischemia. It has been demonstrated that release of arachidonic acid in response to receptor activation or pathological stimuli elicits a positive cardiac inotropic response probably through modulation of membrane K + and Ca 2+ channel activity [5,6]. Although the precise mechanism(s) behind the positive cardiac inotropic actions of arachidonic acid and inflammatory cytokines (such as tumor necrosis factor- ) is largely undefined, it may be speculated that the COX product PGE 2 plays a major role over other prostaglandins in mediating the cardiac function induced by arachidonic acid and inflammatory cytokines [7]. It was shown that induction of COX-2 by interleukin-1 results in the preferential production of PGE 2 in neonatal ventricular myocytes [8]. This is consistent with the observation that the capacity of PGE 2 production is significantly greater than other prostaglandins in many cell types possibly due to a combined effect of COX-2 and PGE 2 synthase [1,7]. PGE 2 has been shown to play a role in protein synthesis and growth in cardiac myocytes [7]. In vivo administration of PGE 2 significantly improves the cardiac contractility and relaxation rate along with reduced heart rate [9]. However, in vivo action of PGE 2 on cardiac electromechanical function may be affected by non-myocyte /$ see front matter 2003 Elsevier Ltd. All rights reserved. doi: /j.phrs
2 100 A.L. Klein et al. / Pharmacological Research 49 (2004) factors such as interstitial connective tissue, fibroblast or nerve terminals. For example, increased ventricular stiffness may reflect a greater amount of interstitial fibrosis and a shift in collagen content rather than a direct effect on the mechanical properties of myocytes themselves. To better understand the effect of PGE 2 on cardiac mechanical function, the aim of the present study was to examine the effect of PGE 2 on cardiac contraction and intracellular Ca 2+ homeostasis in isolated adult rat ventricular myocytes. 2. Materials and methods 2.1. Isolation of adult rat ventricular myocytes The experimental procedures described here were approved by the institutional animal use and care committee of the University of North Dakota (Grand Forks, ND, USA). Ventricular myocytes were isolated from adult male Sprague Dawley rats ( g) as described [10]. Briefly, hearts were rapidly removed and perfused (at 37 C) with oxygenated (5% CO 2 95% O 2 ) Krebs Henseleit bicarbonate (KHB) buffer (118 mm NaCl, 4.7 mm KCl, 1.25 mm CaCl 2, 1.2 mm MgSO 4, 1.2 mm KH 2 PO 4, 25 mm NaHCO 3, 10 mm N-[2-hydro-ethyl]-piperazine-N -[2-ethanesulfonic acid] (HEPES), 11.1 mm glucose, ph 7.4). Hearts were subsequently perfused with a nominally Ca 2+ -free KHB buffer for 2 3 min followed by a 20 min perfusion with Ca 2+ -free KHB containing 223 U/ml collagenase (Worthington Biochemical Corporation, Freehold, NJ, USA) and 0.1 mg/ml hyaluronidase (Sigma, St. Louis, MO, USA). After perfusion, the left ventricle was removed, minced and further digested with trypsin (Sigma) before being filtered through a nylon mesh (300 m) and collected by centrifugation. Cells were initially washed with Ca 2+ -free KHB buffer to remove remnant enzyme and extracellular Ca 2+ was added incrementally back to 1.25 mm Myocyte shortening and relengthening Mechanical properties of ventricular myocytes were assessed by an IonOptix Myocam detection system (IonOptix Incorporation, Milton, MA, USA). Cells were placed in a chamber mounted on the stage of an inverted Olympus IX-70 microscope and superfused (at 25 C) with a buffer containing: 131 mm NaCl, 4 mm KCl, 1 mm CaCl 2,1mM MgCl 2, 10 mm glucose, 10 mm HEPES, at ph 7.4. The cells were field stimulated at a frequency of 0.5 Hz. Cell shortening and relengthening were assessed using the following indices: peak shortening (PS), time-to-ps (TPS) and time-to-90% relengthening (TR 90 ), maximal velocities of shortening (+dl/dt) and relengthening ( dl/dt) [10]. To test the effect of PGE 2 on cardiac contraction, cell shortening and relengthening was recorded before and 5 min after PGE 2 administration Intracellular Ca 2+ fluorescence measurement Myocytes were loaded with fura-2/am (0.5 M) for 10 min and fluorescence measurements were recorded with a dual-excitation fluorescence photomultiplier system (IonOptix Incorporation) as described [10]. Myocytes were plated on glass cover slips on an Olympus IX-70 inverted microscope and imaged through a Fluor 40 oil objective. Cells were exposed to light emitted by a 75 W lamp and passed through either a 360 or 380 nm filter (bandwidths were ±15 nm), while being stimulated to contract at 0.5 Hz. Fluorescence emissions were detected between 480 and 520 nm after first illuminating cells at 360 nm for 0.5 s, then at 380 nm for the duration of the recording protocol (333 Hz sampling rate). The 360 nm excitation scan was repeated at the end of the protocol. Qualitative changes in intracellular Ca 2+ levels were inferred from the ratio of the fluorescence intensity at two wavelengths (360/380 nm) and were used to determine Ca 2+ -induced Ca 2+ release (change of fura-2 fluorescent intensity, CICR). Intracellular Ca 2+ removal was evaluated as the rate of fluorescence decay. To test the effect of PGE 2 on intracellular Ca 2+ properties, fura-2 fluorescent intensity was recorded before and 5 min after PGE 2 administration Data analysis Data were presented as mean ± S.E.M. Statistical significance (P <0.05) for each variable was estimated by analysis of variance (ANOVA). 3. Results 3.1. Effect of PGE 2 on myocyte shortening (PS) The average cell length was 117 ± 3 m (n = 37) in this study. Acute exposure of PGE 2 did not affect resting myocyte cell length over the range of concentrations tested. At the end of a 5 min exposure, PGE 2 (10 8 to 10 3 M) elicited a concentration-dependent increase of PS, with a maximal augmentation of 33.2%. The threshold of effect was between 10 8 and 10 7 M(Fig. 1). PGE 2 -induced increase on PS was maximal within 4 min of exposure, remained stable for over 20 min and was reversible upon washout (data not shown). PGE 2 had no effect on TPS, TR 90 and ±dl/dt (Table 1) Effect of PGE 2 on intracellular Ca 2+ transients To determine whether the PGE 2 -induced augmentation on PS was due to elevated availability of intracellular Ca 2+, the effect of PGE 2 on intracellular Ca 2+ release in response to electrical stimuli (at 0.5 Hz) was examined. Unlike its effect on cell shortening, PGE 2 (10 8 to 10 4 M) elicited little effect on CICR and intracellular Ca 2+ decay rate (τ). How-
3 A.L. Klein et al. / Pharmacological Research 49 (2004) Table 1 Effect of PGE 2 on duration and maximal velocity of myocyte shortening and relengthening in adult rat ventricular myocytes TPS (ms) TR 90 (ms) +dl/dt ( ms 1 ) dl/dt ( ms 1 ) Control 140 ± ± ± ± 10.9 PGE 2 (10 8 M) 128 ± ± ± ± 20.6 PGE 2 (10 7 M) 146 ± ± ± ± 11.2 PGE 2 (10 6 M) 155 ± ± ± ± 10.2 PGE 2 (10 5 M) 147 ± ± ± ± 9.6 PGE 2 (10 4 M) 148 ± ± ± ± 10.1 PGE 2 (10 3 M) 145 ± ± ± ± 9.9 TPS: time-to-peak shortening; TR 90 : time-to-90% relengthening; ±dl/dt: maximal velocities of shortening and relengthening. Data represent mean±s.e.m., n = cells per group. PS (% Change from Baseline) PGE 2 (M) Ca 2+ -Induced Ca 2+ Release (360/380 ratio) PGE 2 (M) Fig. 1. Concentration-dependent response of PGE 2 (10 8 to 10 3 M) on peak cell shortening. Data are presented as percent change of PS from the baseline value (5.12 ± 0.50% of resting cell length). Data represent mean±s.e.m., n = cells per group. P<0.05 vs. control (without PGE 2 ). ever, PGE 2 significantly reduced the baseline intracellular Ca 2+ at the concentrations of 10 5 and 10 4 M(Fig. 2 and Table 2). A large portion of the fura-2-loaded ventricular myocytes failed to survive the entire PGE 2 concentration response range shown in Fig. 1 (10 8 to 10 3 M) and stopped beating prior to reaching the highest concentration of PGE 2 (10 3 M). This observation may suggest potential interaction between fura-2 and PGE 2. Data from 10 3 MofPGE 2 was thus not available due to this cell variability problem. Table 2 Effect of PGE 2 on baseline intracellular Ca 2+ level and intracellular Ca 2+ decay rate in adult rat ventricular myocytes Baseline (360/380 nm ratio) Ca 2+ decay rate (τ, ms) Control 1.18 ± ± 211 PGE 2 (10 8 M) 1.16 ± ± 293 PGE 2 (10 7 M) 1.14 ± ± 195 PGE 2 (10 6 M) 1.14 ± ± 117 PGE 2 (10 5 M) 1.11 ± ± 162 PGE 2 (10 4 M) 1.09 ± ± 453 Data represent mean ± S.E.M., n = cells per group. P<0.05 vs. control value. Fig. 2. Effect of PGE 2 (10 8 to 10 4 M) on intracellular Ca 2+ -induced Ca 2+ release in adult rat ventricular myocytes. CICR is presented as the difference of peak (electrically stimulated) and basal fura-2 fluorescent intensity (360/380 nm ratio). A control fluorescent CICR value was obtained 5 min prior to PGE 2 addition and is denoted as the 0 concentration of PGE 2. Data represent mean ± S.E.M., n = cells per group. Taken together, the lack of stimulatory effect of PGE 2 on CICR suggests that an increase in intracellular free Ca 2+ is unlikely to be responsible for the PGE 2 -induced stimulatory action on myocyte shortening. 4. Discussion Our study provided evidence that the major COX product PGE 2 directly enhances cardiac contraction in isolated ventricular myocytes, suggesting that the myocardial response of PGE 2 may be attributed, at least in part, to its action in individual myocytes. The PGE 2 -evoked positive cardiac contractile response in isolated ventricular myocytes was not associated with alteration in the duration or maximal velocity of contraction and relaxation. The intracellular Ca 2+ transient recording revealed that the electrically-stimulated Ca 2+ -induced Ca 2+ release and intracellular Ca 2+ clearing (τ) were not affected by PGE 2 with the exception that baseline intracellular Ca 2+ level was reduced by higher concentrations of PGE 2. The discrepancy between myocyte
4 102 A.L. Klein et al. / Pharmacological Research 49 (2004) shortening (PS) and intracellular Ca 2+ transients (CICR) in response to PGE 2 indicates possible involvement of an intracellular Ca 2+ -independent mechanism(s) in the PGE 2 -induced positive cardiac contractile response. In our current study, PGE 2 directly increases myocyte shortening (PS) in a concentration-dependent manner, revealing its cardiac potentiating property. This cardiac potentiating property of PGE 2 is consistent with those elicited by PGE 2 or its precursor arachidonic acid reported at the whole animal or multicellular myocardial levels [6,9,11]. The PGE 2 -elicited positive cardiac contractile response is expected to counter-balance the vasoconstrictive action of PGE 2 on main arteries such as aorta to facilitate cardiac energy expenditure and ventricular performance [3,12]. The enhanced cardiac contractility in isolated ventricular myocytes is also consistent with the PGE 2 -elicited protection against myocardial dysfunction due to free radical generation [13]. The observation that neither duration nor maximal velocity of contraction and relaxation was affected by PGE 2 may indicate potential selectivity of PGE 2 on certain cardiac contractile elements such that only the peak force determinants such as actin and myosin are affected by the eicosanoid. Nevertheless, further study is warranted to scrutinize the effect of PGE 2 on each individual cardiac contractile element. Although the positive cardiac contractile response for PGE 2 presented in this study confirmed earlier reports of the cardiac effect of PGE 2 at multicellular or whole animal levels, the mechanism(s) of action underneath the enhanced myocyte contraction in response to PGE 2 is not clear at this time. Several speculations may be made at this time. First, the observation that PGE 2 failed to elicit any effect on intracellular Ca 2+ release suggests that PGE 2 may likely elicit its positive cardiac response via a mechanism(s) independent of intracellular Ca 2+ rise such as altered myofilament Ca 2+ sensitivity. PGE 2 has been shown to activate multiple enzymes or protein kinases such as protein kinase C and phospholipase C [14 16]. Activation of these kinases or enzymes may directly affect the actin myosin phosphorylation state although direct evidence is still lacking for PGE 2. Secondly, although the direct action of PGE 2 on cardiac contractile elements such as membrane ion channels, actin, myosin heavy chain, sarcoplasmic Ca 2+ release and Ca 2+ -regulatory proteins or exchanger has not been elucidated in the hearts, PGE 2 has been demonstrated to effectively inhibit certain types of K + channel and stimulate Ca 2+ influx in various cell types such as vascular smooth muscle cells and osteoblasts [15,17]. Modulation of these membrane ion channels may directly modulate myocardial contractile function and may also be responsible for reduced intracellular Ca 2+ levels at higher concentrations of PGE 2. Thirdly, PGE 2 and -adrenergic activation may synergistically stimulate glycolysis and glucose oxidation in the isolated working rat heart and therefore potentiate rather than decrease -adrenergic stimulation of glucose metabolism and promote cardiac contractile function [18]. Last but certainly not the least, PGE 2 has been shown to protect free radical-induced cardiac dysfunction revealing an antioxidant property for PGE 2 [13]. The signaling mechanism involved in the cardiac response of PGE 2 is rather complex and largely unclear. Up to date, the physiological effects of PGE 2 are believed to be carried out through the G protein-coupled E type prostaglandin receptors EP 1,EP 2, EP 3 and EP 4. The cardiac contractile response of PGE 2 in ventricular myocyte is expected to depend on one or more of these receptors with distinct signal transduction pathway(s) associated with each individual receptor subtypes [7]. In conclusion, our study demonstrates a direct cardiac potentiating response of PGE 2 at the ventricular myocyte level, possibly through an intracellular Ca 2+ -independent mechanism(s). The precise nature of cardiac contractile effects of PGE 2 under both physiological and pathophysiological conditions (e.g., myocardial inflammation, myocardial infarction and ischemia reperfusion injury) is still far from being clear. Future studies should focus on the action of PGE 2 on cardiac oxidation and antioxidant defense, receptor/g-protein-coupled signal transduction and certain membrane elements of excitation-contraction coupling such as ion channels. These investigations are essential to the better understanding of the cellular effects and pharmacological profiles for PGE 2 in the heart so that optimal management of cardiac function may be achieved. Acknowledgements This work was supported in part by Max Baer Heart Fund and NASA Grant # NCC5-582 to JR. We sincerely thank Dr. James Haselton for serving as the work-study faculty mentor for ALK at University of North Dakota. References [1] Vane JR, Bakhle YS, Botting RM. Cyclooxygenases 1 and 2. Annu Rev Pharmacol Toxicol 1998;38: [2] Tapiero H, Ba GN, Couvreur P, Tew KD. Polyunsaturated fatty acids (PUFA) and eicosanoids in human health and pathologies. Biomed Pharmacother 2002;56: [3] Ren J, Karpinski E, Benishin CG. Prostaglandin E 2 contracts vascular smooth muscle and inhibits potassium currents in vascular smooth muscle cells of rat tail artery. J Pharmacol Exp Ther 1995;275: [4] Amadou A, Nawrocki A, Best-Belpomme M, Pavoine C, Pecker F. Arachidonic acid mediates dual effect of TNF-alpha on Ca 2+ transients and contraction of adult rat cardiomyocytes. Am J Physiol Cell Physiol 2002;282:C [5] Otani H, Otani H, Das DK. Positive inotropic effect and phosphoinositide breakdown mediated by arachidonic acid and prostaglandin F2 alpha. J Pharmacol Exp Ther 1988;244: [6] Damron DS, Summers BA. Arachidonic acid enhances contraction and intracellular Ca 2+ transients in individual rat ventricular myocytes. Am J Physiol 1997;272:H [7] Mendez M, LaPointe MC. Trophic effects of the cyclooxygenase-2 product prostaglandin E 2 in cardiac myocytes. Hypertension 2002;39:382 8.
5 A.L. Klein et al. / Pharmacological Research 49 (2004) [8] LaPointe MC, Isenovic E. Interleukin-1 regulation of inducible nitric oxide synthase and cyclooxygenase-2 involves the p42/44 and p38 MAPK signaling pathways in cardiac myocytes. Hypertension 1999;33: [9] Schutte PJ, du Plooy WJ, Hay L. Some adverse cardiodynamic effects of prostaglandin E 2 in congestive heart failure. Prostaglandins Leukot Essent Fatty Acids 1996;54: [10] Ren J, Duan J, Hintz KK, Ren BH. High glucose induces cardiac insulin-like growth factor I resistance in ventricular myocytes: role of Akt and ERK activation. Cardiovasc Res 2003;57: [11] Canga L, Sterin-Borda L. Increase in atrial contractility induced by PGE2 in diabetic rats. Pharmacol Res Commun 1986;18: [12] Mobert J, Becker BF, Zahler S, Gerlach E. Hemodynamic effects of isoprostanes (8-iso-prostaglandin F2alpha and E2) in isolated guinea pig hearts. J Cardiovasc Pharmacol 1997;29: [13] Zimmer KM, Karmazyn M. Prostaglandins attenuate cardiac contractile dysfunction produced by free radical generation but not by hydrogen peroxide. Mol Cell Biochem 1997;176: [14] Asboth G, Phaneuf S, Europe-Finner GN, Toth M, Bernal AL. Prostaglandin E2 activates phospholipase C and elevates intracellular calcium in cultured myometrial cells: involvement of EP1 and EP3 receptor subtypes. Endocrinology 1996;137: [15] Ren J, Karpinski E, Benishin CG. The actions of prostaglandin E 2 on potassium currents in rat tail artery vascular smooth muscle cells: regulation by protein kinase A and protein kinase C. J Pharmacol Exp Ther 1996;277: [16] Church DJ, Van der Bent V, Vallotton MB, Lang U. Role of prostaglandin-mediated cyclic AMP formation in protein kinase C-dependent secretion of atrial natriuretic peptide in rat cardiomyocytes. Biochem J 1994;303: [17] Tokuda H, Miwa M, Oiso Y, Kozawa O. Autoregulation of prostaglandin E 2 -induced Ca 2+ influx in osteoblast-like cells: inhibition by self-induced activation of protein kinase C. Cell Signal 1992;4: [18] Olley PM, Kasserra J, Kozak R, Lopaschuk GD. Synergism between prostaglandin E 2 and isoproterenol in stimulating glucose oxidation in the heart. Can J Physiol Pharmacol 1996;74:590 7.
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