significantly suppressed this increase in plasma ACTH.
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1 Journal of Physiology (1991), 443, pp With 3 figures Printed in Great Britain ACTH RELEASE INDUCED IN RATS BY NORADRENALINE IS MEDIATED BY PROSTAGLANDIN E2 BY TATSUO WATANABE, AKIO MORIMOTO, KEIKO MORIMOTO, TOMOKI NAKAMORI AND NAOTOSHI MURAKAMI From the Department of Physiology, Yamaguchi University School of Medicine, Ube, Yamaguchi 755, Japan (Received 28 January 1991) SUMMARY 1. We investigated the involvement of prostaglandin E2 in the development of the adrenocorticotrophic hormone (ACTH) response induced by noradrenaline (NA) in rats. 2. Intravenous (i.v.) injection of NA produced dose-dependent increases in the plasma concentration of ACTH and prostaglandin E2. However, pre-treatment with systemic administration of indomethacin, an inhibitor of prostaglandin synthesis, significantly suppressed this increase in plasma ACTH. 3. The i.v. injection of prostaglandin E2 significantly increased the plasma concentration of ACTH in a dose-dependent manner. In contrast, ACTH responses induced by the i.v. injection of prostaglandin E2 were significantly suppressed by systemic pre-treatment with anti-corticotrophin-releasing factor antibody (anti- CRF), although the plasma level of ACTH still increased in comparison to the basal level. 4. These results suggest that NA-stimulated prostaglandin release is involved in the ACTH response induced by NA. In addition, it is likely that CRF may be responsible for a portion of the ACTH response induced by i.v. injection of prostaglandin E2. INTRODUCTION Acute stress has been shown to induce a variety of hormonal responses, including significant increases in the plasma level of catecholamines and adrenocorticotrophic hormone (ACTH). However, still little is known about the trigger(s) that stimulates the release of ACTH during stressful conditions. Recent reports suggest the possibility that the ACTH response during physical or psychological stress is mediated by prostaglandins. Pre-treatment with systemic administration of indomethacin, an inhibitor of prostaglandin synthesis, significantly suppresses the increase in the plasma ACTH induced by swimming (Watanabe, Morimoto, Sakata, Long & Murakami, 1991) or cage-switch stress (Morimoto, Watanabe, Morimoto, Nakamori & Murakami, 1991). In addition, we reported that the intrahypothalamic injection of prostaglandin E2 produced a significant increase in the plasma concentration of ACTH (Morimoto, Murakami, Nakamori, Sakata & Watanabe, MS 9107
2 432 T. WATANABE AND OTHERS 1989; Watanabe, Morimoto, Sakata & Murakami, 1990) and that this ACTH response was completely suppressed by pre-treatment with the intravenous injection of anti-corticotrophin-releasing factor antibody (Watanabe et al. 1990). Therefore, we suggested that prostaglandin E2 induces the ACTH response by acting on the hypothalamus to stimulate corticotrophin-releasing factor (CRF) secretion into the hypophyseal portal vein. CRF subsequently stimulates the pituitary cells to secrete ACTH. At the present time, however, the mechanism by which stress stimulates prostaglandin synthesis is not known. Animals generally respond to stress in a stereotyped manner that includes the activation of the sympathetic nervous system. Sympathetic nerve terminals release noradrenaline (NA), and consequently plasma levels of catecholamines increase. It has been reported that the plasma concentrations of ACTH increase after intravenous injection of catecholamine (Berkenbosch, Vermes, Binnekade & Tilders, 1981; Tilders, Berkenbosch & Smelik, 1982; Hary, Dupouy & Chatelain, 1984). In addition, previous studies have shown that NA stimulates the release of prostaglandin E2 in peripheral tissues (Hedqvist, 1977) and the central nervous system (Busija & Leffler, 1987). Therefore we speculated that during stressful conditions, NA release into the circulation stimulates the prostaglandin synthesis and, consequently, the ACTH response is induced. The present study was carried out to investigate the role of prostaglandins in the NA-induced ACTH response in rats. We found that intravenous injections of NA increased the plasma concentrations of ACTH and prostaglandin E2. In addition, the pre-treatment with systemic administration of indomethacin significantly suppressed the increase in the plasma ACTH induced by intravenous injection of NA. These results suggest that prostaglandins are involved in the NA-induced ACTH response. METHODS Male albino rats (Wistar strain) weighing g were used in this study. The rats were housed in individual cages in a room maintained at 26±1 C, a temperature within the thermoneutral zone for rats, with a h light-dark cycle, with light on h. Tap water and rodent chow were provided ad libitum. This study consisted of four experiments. In Expt 1, rats were intravenously injected with NA or saline. In Expt 2, rats were intravenously administered indomethacin (INDO) or a control vehicle 15 min before intravenous injection of NA. In Expt 3, rats were intravenously injected with prostaglandin E2 or saline. In Expt 4, rats were intravenously administered anti-crf antibody (anti-crf) or normal rabbit serum (NRS) as a control 15 min before intravenous injection of prostaglandin E2. For blood sampling and intravenous injections, the rats were implanted with intravenous catheters. While the rats were under general anaesthesia (pentobarbitone, 50 mg/kg, i.p.), polyvinyl tubing was inserted from the jugular vein such that the tip of the tubing was located in the superior caval vein (SCV) near the right atrium. The free end of the catheter was passed subcutaneously to the mid-scapular region, where it was exteriorized through the skin on the dorsal side of the neck. The patency of the catheter was maintained by daily flushes with heparinized 0 9 % saline (50 U/ml). In addition, each rat was handled for 10 min every day for at least 5 days prior to the start of the experiments to accustom the animals to the experimenters. For i.v. injection, NA-HCl was dissolved in sterile saline at a concentration of 0 1 or 0 01 mg/ml. Prostaglandin E2 was dissolved in sterile saline containing 0 5 % ethanol at a concentration of 1 or 0 1 mg/ml. We used saline containing 0'5 % ethanol as the control vehicle for prostaglandin E2 solution. Indomethacin was dissolved in sterile saline containing 4 % sodium bicarbonate at a concentration of 1 mg/ml. We used saline containing 4 % sodium bicarbonate as the control vehicle for indomethacin. Anti-corticotrophin-releasing factor antibody (anti-crf, Cambridge Research
3 ACTH AND NORADRENALINE Biomedicals) was also dissolved in sterile saline. Injection doses in each experimental group, including appropriate control injections, are described in the Results. On the day of the experiments, rats were housed in individual cages and were allowed to move freely, with access to food and water ad libitum. The experiments were carried out at an ambient temperature of 'C. i.v. injections of NA, prostaglandin E2 or saline via the SCV cannula were performed at about h. To measure the plasma concentration of ACTH, about 0 5 ml of blood was withdrawn through the cannulae. The blood samples were taken from each rat three times: 30 min before and 20 and 90 min after intravenous injection of NA or prostaglandin E2. Blood was collected into test-tubes containing EDTA (1 mg/ml blood) to measure the ACTH concentration. To measure the plasma concentration of prostaglandin E2, about 1P0 ml of blood was withdrawn. Blood samples were taken twice from each rat, 30 min before and 20 min after intravenous injection of NA and collected into test-tubes containing EDTA (1 mg/ml blood) and indomethacin (0 5 mg/ml blood). The blood was centrifuged at 2000 r.p.m. for 15 min at 4 'C. The plasma was then transferred to new test-tubes and stored at -40 'C until further analysis. The blood cells were resuspended in sterile saline and stored at 4 'C, and returned to each animal after completion of each day of experiments. To determine the ACTH and prostaglandin E2 concentrations, radioimmunoassays were performed, using commercial radioimmunoassay kits (Diagnostic Product Corporation, USA; Amersham, UK). The ACTH or prostaglandin E2 antiserum in the assays exhibited an extremely low cross-reactivity (< 0 5 % for ACTH and < 5 % for prostaglandin E2 antibody) to other compounds. The data were analysed for statistical significance by Student's t test or ANOVA. 433 RESULTS Figure 1A shows the mean change in the plasma concentration of ACTH after intravenous injections of NA (041 or 0-01 mg/kg), or saline. Statistical comparisons were made between the NA-injected group and the saline injected group. As shown in Fig. 1A, the plasma concentration of ACTH increased significantly 20 min after the injection of a low dose of NA and 20 and 90 min after the injection of a high dose of NA. The increased level of ACTH induced by a high dose of NA was significantly (P < 0 01) greater than that induced by a low dose 20 min after injection. Intravenous injection of saline had no effect on plasma concentration of ACTH after injection. Figure lb shows the effect of systemic pre-treatment with indomethacin (INDO, 1 mg/kg) on the ACTH response induced by intravenous injection of NA (0 1 mg/kg) or saline. INDO or vehicle was intravenously injected 15 min before the injection of NA or saline. Note that the increase in plasma ACTH induced by intravenous injection of NA was significantly suppressed by the pre-treatment with INDO, in comparison to the rats that were injected with vehicle. However, the pre-treatment with INDO 15 min prior to saline injection had no effect on plasma levels of ACTH. Figure 2 shows the mean changes in the plasma concentration of prostaglandin E2 after the intravenous injection of NA (041 and 0 01 mg/kg), or saline. As shown in Fig. 2, the intravenous injection of NA induced significant increases in the plasma concentration of prostaglandin E2 in a dose-dependent manner. No changes in plasma levels of prostaglandin E2 were observed after intravenous injection of saline. Figure 3A shows the mean change in the plasma concentration of ACTH after intravenous injections of prostaglandin E2 (10 and 01 mg/kg) or saline. Prostaglandin E2 produced dose-dependent rises in the plasma concentration of ACTH 20 min after injection, as compared to the rats who received saline. The plasma concentration of ACTH was still significantly elevated 90 min after the
4 434 T. WATANABE AND OTHERS A a 100 < 50 0 B I =I CE :r Fig. 1. A, mean changes (mean+ s.e.m.) in plasma concentration of adrenocorticotrophic hormone (ACTH) in six rats 30 min before, and 20 and 90 min after intravenous injection of noradrenaline (NA: hatched bars, 0 01 mg/kg; filled bars, 0 1 mg/kg) or saline (open bars). Each rat received two doses of NA and saline on separate days. The order of injection was randomized. *P < 0-05, ***P < B, mean changes (mean+s.e.m.) in plasma concentration of ACTH in seven rats 30 min before, and 20 and 90 min after intravenous injection of NA (0-1 mg/kg). Each rat was pre-treated systemically with indomethacin (INDO, 1 mg/kg, hatched bars) or control vehicle (open bars) 15 min before the injection of NA on separate days. The order of injections was randomized. The other group of six rats (filled bars) received intravenous injection of saline following systemic pre-treatment with INDO (1 mg/kg) 15 min before saline injection r 2000 m ** T ma -30 Fig. 2. Mean changes (mean + S.E.M.) in plasma concentration of prostaglandin E2 (PGE2) in six rats 30 min before, and 20 min after intravenous injection of noradrenaline (NA: hatched bars, 0-01 mg/kg; filled bars, 0-1 mg/kg) or saline (open bars). Each rat received two doses of NA and saline on separate days. The order of injection was randomized. **P < 0.01, ***P <
5 ACTH AND NORADRENALINE injection of the higher dose of prostaglandin E2 (10 mg/kg) in comparison to the saline group. Figure 3B shows the mean change in the plasma concentration of ACTH induced by the intravenous injection of prostaglandin E2 (01 mg/kg) in rats that had been A 200 g B 200 P< ] X " P< I- O,I 1E Fig. 3. A, mean changes (mean+s.e.m.) in plasma concentration of adrenocorticotrophic hormone (ACTH) in six rats 30 min before, and 20 and 90 min after intravenous injection of prostaglandin E2 (PGE2) at 0-1 mg/kg (hatched bars) and 10 mg/kg (filled bars), or saline (open bars). Each rat received two doses of PGE2 and saline on separate days. The order of injection was randomized. B, mean changes (mean+s.e.m.) in plasma concentration of adrenocorticotrophic hormone (ACTH) in six rats 30 min before, and 20 and 90 min after intravenous injection of prostaglandin E2 (PGE2, 01 mg/kg). Each rat was pre-treated systemically with anti-crf antibody (anti-crf, filled bars) or normal rabbit serum (NRS, open bars) 15 min before the injection of PGE2 on separate days. The order of injections was randomized. *P < 0-05, **P < 001, ***P < pre-treated with either anti-crf antibody (0-4 ml) or normal rabbit serum (NRS, 04 ml), 15 min before the injection of prostaglandin E2. Note that in this figure, the asterisks refer to comparisons between the ACTH levels at time -30 min and the subsequent time points. The ACTH responses induced by prostaglandin E2 were significantly suppressed by pre-treatment with anti-crf, although the plasma ACTH level 20 min after the intravenous injection of prostaglandin E2 in the 'anti- CRF+PGE2 group' was still significantly greater (***P < 0-001) than that seen 30 min before injection. Figure 3B also shows that the plasma concentration of ACTH is significantly (**P < 0 01) lower 90 min after injection of prostaglandin E2 in the 'anti-crf + PGE2 group', as compared with that 30 min before the injection.
6 436 T. WATANABE AND OTHERS DISCUSSION It has been demonstrated that the release of prostaglandin E2 is stimulated by NA in peripheral tissues (Hedqvist, 1977) and the central nervous system (Busija & Leffler, 1987). NA is known to be a potent stimulus for the secretion of ACTH, when it is systemically injected (Hary et al. 1984). Recently, we have shown that prostaglandin E2 is involved in the development of the ACTH response induced by physical (Watanabe et al. 1991) and psychological (Morimoto et al. 1991) stresses. During stressful conditions, activation of the sympathetic nervous system stimulates the release of NA. Therefore, we hypothesized that NA-stimulated prostaglandin release is involved in the ACTH response induced by the systemic injection of NA. The present results show that intravenous injections of NA increase the plasma concentrations of ACTH and prostaglandin E2 in a dose-dependent manner. In addition, increases in plasma ACTH induced by intravenous injection of NA are significantly suppressed by pre-treatment with indomethacin, an inhibitor of prostaglandin synthesis. Therefore, prostaglandins may play an important role in the ACTH response induced by NA. This hypothesis is further supported by our results showing that plasma levels of ACTH are elevated after the intravenous injection of prostaglandin E2. The contribution of NA released into the blood stream to hypothalamo-pituitary adrenal response is still controversial (Al-Damluji, 1988). The present results showed that intravenous injection of NA induced significant increases in plasma ACTH levels in rats. However, there are several reports that, in man, increased levels of adrenaline and noradrenaline in the circulation are not responsible for ACTH response (Al- Damluji, Cunnah, Grossman, Perry, Ross, Coy, Rees & Besser, 1987; Al-Damluji, Perry, Tomlin, Bouloux, Grossman, Rees & Besser, 1987). These discrepancies have been well discussed in the review by Al-Damluji (1988). Recently, we have reported that an intrahypothalamic injection of a small dose of prostaglandin E2 (25 ng) significantly increased the plasma concentration of ACTH and that the ACTH response induced by intrahypothalamic prostaglandin E2 was suppressed by pre-treatment with anti-crf antibody (Watanabe et al. 1990). The present results show that a portion of ACTH response induced by intravenous injection of prostaglandin E2 is also mediated by CRF. Since circulating prostaglandin E2 is able to enter into the brain across the blood-brain barrier (Eguchi, Hayashi, Urade, Ito & Hayaishi, 1988), it is likely that circulating prostaglandins released after the intravenous injection of NA cause the ACTH response by their action on the hypothalamic neuroendocrine cells to stimulate the secretion of CRF. CRF subsequently stimulates the pituitary cells to secrete ACTH. However, it has been reported that prostaglandin F2., is the effective secretagogue of CRF, while prostaglandin E2 is without effect in in vitro experiment (Bernardini, Chiarenza, Calogero, Gold & Chrousos, 1989). At the present time, we cannot give a clear explanation for these discrepancies in the results obtained from in vivo and in vitro experiments. In the present study, intravenous injections of prostaglandin E2 into rats were performed at concentrations of 01 or 1 mg/kg. These concentrations seem relatively high. However, it is well known that about 90 % of all prostaglandins are
7 ACTH AND NORADRENALINE metabolized during each pulmonary circulation (Piper, Vane & Wyllie, 1970). Therefore, prostaglandins bolusly injected are thought to be metabolized almost immediately. Furthermore, Eguchi et al. (1988) reported that only 0-13% of the administered dose of prostaglandin E2 was transported into the brain, when prostaglandin E2 was intravenously injected at a concentration of 1 mg/kg. In the present study, we did not determine the origin of circulating prostaglandin E2 released by systemic injection of NA. However, the relationship between the autonomic nervous system and prostaglandin E2, and the role of prostaglandin E2 as modulators of autonomic transmission have been reviewed repeatedly (Brody & Kadowitz, 1974; Hedqvist, 1977; Malik, 1978). The release of prostaglandin E2 is stimulated by sympathetic nerve stimulation or catecholamine injection, and the prostaglandin E2 inhibits NA release from nerve terminals and the response to the secreted transmitter, thus forming a local inhibitory feedback loop system. Therefore, we propose that prostaglandin E2 overflows from sympathetic innervated organs into the circulation after the injection of NA. This speculation is supported by the fact that the release of prostaglandin E2 from the kidney (Cooper & Malik, 1985) or spleen (Hidaka & Malik, 1980) is enhanced, when NA is perfused to these organs in vitro. The possibility remains that circulating prostaglandins act directly on the pituitary cells. Therefore, in order to clarify the role of circulating prostaglandins in the induction of ACTH response, we investigated the effect of anti-crf antibody on the ACTH response induced by intravenous injection of prostaglandin E2. The results show that ACTH responses induced by the injection of prostaglandin E2 were significantly suppressed by systemic pre-treatment with anti-crf antibody. This indicates that CRF is at least in part involved in the ACTH response induced by intravenous prostaglandin E2. However, the plasma concentration of ACTH still increased, even after pre-treatment with anti-crf antibody followed by the injection of prostaglandin E2. The dose of anti-crf antibody used in the present study was sufficient to completely suppress a larger ACTH response induced by intrahypothalamic injection of prostaglandin E2 in a previous experiment (Watanabe et al. 1990). Therefore, our failure to completely block the ACTH response in this experiment may suggest that a portion of this response is not mediated by CRF. These results lead us to speculate that there exist at least two mechanisms by which circulating prostaglandins can induce the ACTH response; indirectly via stimulation of CRF secretion or directly by acting on the pituitary gland. However, Kehrer, Turnhill, Dayer, Muller & Gaillard (1988) reported that prostaglandin E2 did not stimulate the secretion of ACTH from the rat anterior pituitary cell cultures. Moreover, several papers have shown that prostaglandin E2 is inhibitory to ACTH release from the pituitary gland in vitro in response to ACTH secretagogues such as CRF (Sobel, 1987) or arginine vasopressin (AVP) (Knepel & Gotz, 1986; Okajima, Heldt & Hertting, 1986). Therefore, we speculate that circulating prostaglandins may induce the other secretagogues for ACTH secretion such as AVP or angiotensin II, in addition to CRF. Furthermore, it is possible that the peripherally produced prostaglandin E2 exerts peripheral actions which are perceived as 'stressful' by the rat. Consequently, intravenous injection of prostaglandin E2 may lead to the release of ACTH secretagogues other than CRF or to the inhibition of the release of the 437
8 438 T. WATANABE AND OTHERS putative inhibitory factor. Since AVP has been shown to enhance the ACTH response to CRF synergistically, it is possible that a small amount of free CRF which was not neutralized by the anti-crf antibody could induce the ACTH response in the presence of AVP. REFERENCES AL-DAMLUJI, S. (1988). Adrenergic mechanisms in the control of corticotrophin secretion. Journal of Endocrinology 119, AL-DAMLUJI, S., CUNNAH, D., GROSSMAN, A., PERRY, L., Ross, G., Coy, D., REES, L. H. & BESSER, G. M. (1987). Effect of adrenaline on basal and ovine corticotrophin-releasing factor-stimulated ACTH secretion in man. Journal of Endocrinology 112, AL-DAMLUJI, S., PERRY, L., TOMLIN, S., BoULOUX, P., GROSSMAN, A., REES, L. H. & BESSER, G. M. (1987). Alpha-adrenergic stimulation of corticotropin secretion by a specific central mechanism in man. Neuroendocrinology 45, BERKENBOSCH, F., VERMES, I., BINNEKADE, R. & TILDERS, F. J. H. (1981). Beta-adrenergic stimulation induces an increase of the plasma levels of immunoreactive a-msh, /3-endorphin, ACTH and of corticosterone. Life Sciences 29, BERNARDINI, R., CHIARENZA, A., CALOGERO, A. E., GOLD, P. W. & CHROu'SOS, G. P. (1989). Arachidonic acid metabolites modulate rat hypothalamic corticotropin-releasing hormone secretion in vitro. NVeuroendocrinology 50, BRODY, M. J. & KADOWITZ, P. J. (1974). Prostaglandins as modulators of the autonomic nervous system. Federation Proceedings 33, BUSIJA, D. W. & LEFFLER, C. W. (1987). Eicosanoid synthesis elicited by norepinephrine in piglet parietal cortex. Brain Research 403, COOPER, C. L. & MALIK, K. U. (1985). Prostaglandin synthesis and renal vasoconstriction elicited by adrenergic stimuli are linked to activation of alpha-1 adrenergic receptors in the isolated rat kidney. Journal of Pharmacology and Experimental Therapeutics 233, EGUCHI, N., HAYASHI, H., URADE, Y., ITO, S. & HAYAISHI, 0. (1988). Central action of prostaglandin E2 and its methyl ester in the induction of hyperthermia after their systemic administration in urethane-anesthetized rats. Journal of Pharmacology and Experimental Therapeutics 247, HARY, L., DuPouy, J. P. & CHATELAIN, A. (1984). Effect of norepinephrine on the pituitary adrenocorticotrophic activation by ether stress and on the in v,itro release of ACTH by the adenohypophysis of male and female newborn rats. Neuroendocrinology 39, HEDQVIST, P. (1977). Basic mechanisms of prostaglandin action on autonomic neurotransmission. Annual Review of Pharmacology and Toxicology 17, HIDAKA, T. & MALIK, K. U. (1980). Release of prostaglandins evoked by neurohormonal stimuli in the isolated spleen of rabbit. European Journal of Pharmacology 62, KEHRER, P., TURNILL, D., DAYER, J., MULLER, A. F. & GAILLARD, R. C. (1988). Human recombinant interleukin-1 beta and -alpha, but not recombinant tumor necrosis factor alpha stimulate ACTH release from rat anterior pituitary cells in vitro in a prostaglandin E2 and camp independent manner. Neuroendocrinology 48, KNEPEL, W. & GOTZ, D. (1986). Effect of prostaglandin E2 on ACTH and /l-endorphin release from rat adenohypophysis in vitro after secretagogues which can mimic various first or second messengers. Naunyn Schmiedeberg's Archives of Pharmacology 333, MALIK, K. U. (1978). Prostaglandins - modulation of adrenergic nervous system. Federation Proceedings 37, MORIMOTO, A., MURAKAMI, N., NAKAMORI, T., SAKATA, Y. & WATANABE, T. (1989). Possible involvement of prostaglandin E in development of ACTH response in rats induced by human recombinant interleukin-1. Journal of Physiology 411, MORIMOTO, A., WATANABE, T., MORIMOTO, K., NAKAMORI, T. & MURAKAMI, N. (1991). Possible involvement of prostaglandins in psychological stress-induced responses in rats. Journal of Physiology 443, OKAJIMA, T., HELDT, R. & HERTTING, G. (1986). Functional compartmentalization of argininevasopressin-activated cyclic AMP in anterior pituitary gland: the presence of a compartment activated by prostaglandin E2. Life Sciences 38,
9 ACTH AND NORADRENALINE 439 PIPER, P. J., VANE, J. R. & WYLLIE, J. H. (1970). Inactivation of prostaglandins by the lungs. Nature 225, SOBEL, D. 0. (1987). Characterization of PGE2 inhibition of corticotropin releasing factormediated ACTH release. Brain Research 411, TILDERS, F. J. H., BERKENBOSCH, F. & SMELIK, P. G. (1982). Adrenergic mechanisms involved in the control of pituitary-adrenal activity in the rat: A,-adrenergic stimulatory mechanism. Endocrinology 110, WATANABE, T., MORIMOTO, A., SAKATA, Y., LONG, N. C. & MURAKAMI, N. (1991). Prostaglandin E2 is involved in adrenocorticotrophic hormone release during swimming exercise in rats. Journal of Physiology 433, WATANABE, T., MORIMOTO, A., SAKATA, Y. & MURAKAMI, N. (1990). ACTH response induced by interleukin-1 is mediated by CRF secretion stimulated by hypothalamic PGE. Experientia 46,
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