Fish Physiology and Biochemistry vol. 7 nos 1-4 pp 39-48 (1989) Kugler Publications, Amsterdam/Berkeley

Physiology of fish endocrine pancreas Erika M. Plisetskaya Department of Zoology NJ-15, University of Washington, Seattle, WA 98195, USA Keywords: insulin, glucagon, glucagon-like peptide, somatostatin, pancreatic peptide: structure, localization, plasma content, interrelations, metabolic effects

Abstract From the very beginning of physiological studies on the endocine pancreas, fish have been used as experimental subjects. Fish insulin was one of the first vertebrate insulins isolated and one of the first insulins whose primary and then tertiary structures were reported. Before a second pancreatic hormone, glucagon, was characterized, a physiologically active 'impurity', similar to that in mammalian insulin preparations, was found in fish insulins. Fish have become the most widely used model for studies of biosynthesis and processing of the pancreatic hormones. It seems inconceivable, therefore, that until the recent past cod and tuna insulins have been the only purified piscine islet hormones available for physiological experiments. The situation has changed remarkably during the last decade. In this review the contemporary status of physiological studies on the fish pancreas is outlined with an emphasis on the following topics: 1) contents of pancreatic peptides in plasma and in islet tissue; 2) actions of piscine pancreatic hormones in fish; 3) specific metabolic consequences of an acute insufficiency of pancreatic peptides; 4) functional interrelations among pancreatic peptides which differ from those of mammals. The pitfalls, lacunae and the perspectives of contemporary physiological studies on fish endocrine pancreas are outlined.

Introduction From the very beginning of the physiological studies of the endocrine pancreas, fish have been used as experimental subjects. The underlying reason for this probably is the unique structure of the fish islet organ, which in many teleosts is represented by a visible concentration of endocrine cells adjacent to the gall bladder and surrounded by a rim of exocrine tissue, thus forming so called Brockmann body (cf Epple and Brinn 1987). In 1904 Diamare and Kuljabko tested the effects of extracts of anglerfish (Lophius sp.) and scor-

pion fish (Scorpaena sp.) Brockmann bodies on indices of carbohydrate metabolism in fish. Several years later, Diamare unequivocally attributed the hyperglycemia which appeared in Selachians after pancreatectomy to an insufficiency of pancreatic secretion (Diamare 1906, 1908). About the same time, and long before any insulin was isolated, the observation was made that extracts of fish islet tissue temporarily alleviate diabetic symptoms in man (Rennie and Fraser 1906). Immediately after the discovery of insulin, Macleod (1922) compared the effects of extracts of either Brockmann bodies or exocrine pancreatic tissue of anglerfish and sculpin

Correspondenceto: Dr. Erika M. Plisetskaya, Department of Zoology NJ-15, University of Washington Seattle, Washington 98195.

40 (Myoxocephalus sp.) on glycemic levels in rabbits. These experiments confirmed the islet origin of insulin in fish. Fish insulin was one of the first vertebrate insulins isolated (McCormick and Noble 1924; Vincent et al. 1925; Jensen et al. 1929) and sequenced (Reid et al. 1968). Hagfish insulin was one of the first insulins whose tertiary structure was determined (Peterson et al. 1974; Cutfield et al. 1979). Experiments on fish also played a substantial role in identification of a second pancreatic hormone, glucagon. Before the first pure glucagon was isolated by Staub et al. (1953), Audy and Kerly (1952) reported the presence of a glycogenolytic substance in anglerfish islets which was similar to an 'impurity' observed in mammalian insulin preparations. Several decades later, fish islets have become the most widely used model for studies of biosynthesis and processing of pancreatic hormones. It was in the anglerfish Brockmann body that insulin, glucagon and somatostatin biosyntheses were investigated and the processing of glucagon and somatostatin via prohormones was discovered (cf Bauer et al 1965; Noe and Bauer 1971; Noe et al. 1979). It was also in the anglerfish Brockmann body that two forms of somatostatin precursors and two forms of glucagon precursors, each evidently encoded in a different gene, were first reported (Hobart et al. 1980; Goodman et al. 1980; Lund et al. 1981). Considering the multiplicity of studies of the fish endocrine pancreas it is surprising that, until recently, there have been no purified piscine islet hormones available for physiological experiments, other than cod and tuna-bonito insulins. Consequently, mammalian hormones have been employed in a large majority of physiological studies of the fish endocrine pancreas. This situation has changed during recent years. Newly developed techniques of protein chemistry have made possible rapid isolation and purification of pancreatic peptides, as well as their sequencing. As a result, the major pancreatic hormones, insulin, glucagon, somatostatin and pancreatic peptide, were isolated from the islet tissue of representative cyclostomes, elasmobranchs, holostean and teleostean fishes (Conlon 1989; Plisetskaya 1989). However, only the pancreatic hormones of the Pacific

coho salmon (Oncorhynchus kisutch), of the anglerfish (Lophius americanus) and some hormones of the catfish (Ictalurus punctatus), supplemented by several commercial preparations of fish insulins from Japanese and American companies, are now available for experimental use. In this review I will concentrate mostly on results that are derived from our studies on salmonid fishes.

Fish pancreatic peptides Isolation procedures and primary structures of salmon pancreatic hormones have been described in detail in earlier reports (Plisetskaya et al. 1985, 1986a,b; Kimmel et al. 1986). Insulin. Coho salmon insulin is a typical vertebrate insulin. In comparison to mammalian insulin it has 14 substitutions in the A and B chains, all in a variant domaine of the molecule. Remarkably, when insulins of two other species of Pacific salmon 0. keta and 0. gorbuscha were isolated (Rusacov et al. 1987a,b), they appeared to be 1007o identical to each other and to the insulin of the coho salmon (Plisetskaya et al. 1985). Thus, out of six species of Pacific salmon, three species, which have been examined, have at least the same major form of insulin. Before sequencing of any of the insulins isolated from the Pacific salmon was achieved, Sorokin et al. (1982) deduced the sequence of 0. keta insulin from cDNA. The analysis of the nucleotide sequence revealed that two amino acids in the A and B-chains differed from the amino acid sequence actually isolated (Rusacov et al. 1987b). Future investigations should clarify whether salmonids, like some other vertebrates, express multiple generic forms of insulin. Although close to the mammalian hormone structurally, salmon insulin, like other piscine insulins, seems to be very different immunologically; this makes it almost impossible to measure fish insulins by use of mammallian radioimmunoassay systems (Plisetskaya et al. 1986c). Glucagon and glucagon-like peptide. Two peptides belonging to the glucagon family were isolated from coho salmon islet tissue, 29 amino acid residue glucagon and the 31 amino acid residue

41 glucagon-like peptide (GLP), which is encoded at the carboxyl end of the preproglucagon molecule (Plisetskaya et al. 1986b). Fish glucagons are very similar to each other. Mammalian and salmon glucagons differ at 8 amino acid residues (Plisetskaya 1989). In contrast to insulin, fish glucagon can be measured in mammalian RIAs (Gutierrez et al. 1986), because antisera raised against the mammalian peptide crossreact fully with fish glucagons. Nevertheless, we prefer to use a homologous assay for salmon glucagon, starting with precipitation of high molecular forms of peptides, including 'big' immunoreactive glucagons from the plasma (Plisetskaya et al. 1989a). Salmon GLP resembles anglerfish gene II GLP (Plisetskaya et al. 1986b); homologous radioimmune system seems to be most suitable for its assay. Another member of the glucagon family, oxyntomodulin, so far has not been isolated from coho salmon endocrine pancreas, although it has been found in the endocrine pancreas of the shark (Conlon 1989) and of the alligator gar pike (Pollock et al. 1988). Somatostatin. Salmon produce two pancreatic somatostatins (SST) (Plisetskaya et al. 1986a), the smaller one, SST-14, is referred to as the invariant vertebrate peptide. SST-14 has been isolated from the islet tissue of representatives of all vertebrate classes (Andrews et al. 1988; Conlon 1989); the large, and most abundant form is SST-25. It is believed to be a product of a different gene (gene II). Two major forms of SST, invariant SST-14 and either gene II SST-28 or gene II SST-22, were reported also in the anglerfish and in the catfish, respectively (Andrews et al. 1984a,b). Pancreaticpeptide. The latest hormone to be isolated from salmon pancreas, pancreatic peptide (PP), is very similar to analogous peptides from other fishes, as well as to the mammalian neuropeptide Y (NPY): in these two peptides 30 amino acid residues out of 36 are in identical positions. Pancreatic peptides from other fishes investigated so far also show close structural similarity to mammalian NPY (Kimmel et al. 1986). A current question is whether the fish endocrine pancreas produces not only the hormones mentioned above, but also other biologically active peptides like the recently discovered mammalian pan-

creastatin (Tatemoto et al. 1986) or galanin (Ahren et al. 1988).

Cellular localization of the pancreatic peptides in fish The next step in our studies was immunohistochemical localization of salmon hormones in the islet tissue, using homologous antibodies. We have found that glucagon and glucagon-like peptide are expressed within the same islet cells (Nozaki et al. 1988b), while SST-14 and SST-25, the products of different genes, are expressed in different cells (Nozaki et al. 1988a). Even more puzzling was the discovery that cells expressing SST-14 are located adjacent to insulin immunoreactive cells, while cells expressing SST-25 are associated topographically with glucagon/GLP-positive cells (Nozaki et al. 1988a). Similar association of SST-28 expressing cells with glucagon cells in anglerfish was reported earlier by McDonald et al. (1987). It is logical to ask whether these consistent cellular associations imply yet unknown functional regulatory relationships. In a pilot experiment (E.M. Plisetskaya and M.G. Bernard 1988, unpublished) juvenile coho salmon were injected with SST-25 or SST-14 and the plasma levels of insulin, glucagon and GLP measured. Indeed, SST-25 lowered plasma insulin titres as well as GLP levels, but the effect of SST-14 on plasma GLP, contrary to what might have been expected, from our immunohistochemical observations, was even more potent, lowering GLP to non-detectable values (Fig. 1). Interrelations among the different SSTs, insulin and glucagonfamily peptides definitely deserve more studies. Immunostaining of salmon and trout neurohypophysis and hypothalamus revealed many SST-14 positive cells but no cells expressing SST-25. (Nozaki et al. 1988a). Conducting tests of the effect of different fish SSTs on growth hormone release from isolated goldfish pituitary, Marchant (1987) failed to observe any action of salmon SST-25 or catfish SST-22, while mammalian SST-14 was a potent inhibitor of growth hormone secretion. Therefore the name 'somatotropin release inhibiting fac-

42 Sline

Dt,9

0.6

Table 1. The yield of purified peptides from coho salmon endocrine pancreas

r-14

(tLg/g islet tissue)

Insulin Somatostatin-25 Somatostatin-14 Glucagon Glucagon-like peptide Pancreatic peptide

a) CD

M -

1.2 1.0 0.08 0.16 0.35 0.004

C D

According to Kimmel et al. 1986; Plisetskaya 1985, 1986a,b.

o

C. _7 W 0 0

3

Hours

Fig. 1. Effect of salmon somatostatin-25 and somatostatin-14 on plasma circulating levels of glucagon-like peptide in juvenile coho salmon; * p < 0.05; ** p < 0.01 (E.M. Plisetskaya and M.G. Bernard, unpublished).

tor' is hardly applicable to these 'big' SSTs, at least in the goldfish. Using antisera raised by P.C. Andrews against anglerfish NPY, M. Nozaki (1988, unpublished) immunostained NPY expressing cells in trout and in salmon endocrine pancreas. These cells were located at the edge of the pancreatic islets (see also Wagner and McKeown 1981). It seems that actively feeding trout have more pancreatic NPY positive cells than coho salmon collected during the spawning period: the difference which might be expected if in fish, as in the rat NPY inhibits sexual behavior and stimulates appetite (Clark et al. 1985).

Contents of the pancreatic peptides in fish It has been known for a long time that the yield of insulin from fish islet tissue can be as much as 75 000 IU/kg, as compared to 10 000 IU/kg from calf pancreas (Humbel et al. 1972). The high yields of pancreatic peptides from coho salmon are in a good agreement with this earlier observation (Table 1).

After isolation of piscine pancreatic hormones, it became possible for the first time to measure quantitatively their content in islet tissue and their actual plasma levels in salmonids. The results of the assays (Plisetskaya and Sullivan 1989c) of insulin, glucagon and GLP levels in the portal venous blood draining the endocrine pancreas along with other visceral organs nearby, as compared to plasma levels of the same hormones in the heart (conus arteriosus) and in the caudal vein, which drains the bulk of skeletal muscles, are presented in Fig. 2. In this, as well as in many other experiments on fish, the plasma insulin levels are much higher than the levels of glucagon family peptides; also, the levels of insulin and GLP are higher than in mammals (Plisetskaya et al. 1986c; Orskov and Holst 1987). The levels of all three hormones assayed are much higher in the portal vein than in other vessels. There is no statistically significant difference between concentrations of any of the peptides in the caudal vein and in the heart. Nevertheless the average level of GLP (0.22 ± 0.03 ng/ml) in the heart blood is higher than in the blood sampled from the caudal vein (0.15 0.03). These results may imply some functions for GLP in regulation of cardiac metabolism. Moreover, because the liver is evidently experiencing higher levels of pancreatic peptides than the rest of the body, use of higher doses of hormones in in vivo and in vitro experiments on liver may be appropriate. Fish researchers know about difficulties of interpretation of data resulting from variability in reaction to administered hormones during the different stages of piscine life cycle, or during different seasons. It is, therefore, important to evaluate the doses of injected hormones which can be consid-

43

0 Portal vein 0

I

Heart Caudal vein

Insulin

ng/ml

Glucagon

Glucagon-like peptide

Fig. 2. Plasma circulating levels of insulin, glucagon and glucagon-like peptide in different vessels of trout N = 26 (E.M. Plisetskaya and C.V. Sullivan 1989c).

ered to be physiological and appropriate for administration. Evidence is accumulating that pharmacological doses may indeed provide an idea of a potential effect of particular hormone, but may have little relationship to the regulatory events in the living fish. In experiments on juvenile salmon, we have found (Plisetskaya et al. 1989a) that during three hours after injection, 1 ng/g of glucagon or GLP causes a 1.2- 1.6 fold increase in circulating levels of the peptides in the caudal vein' blood, while a 10 ng/g dose causes a 1.7-5.2 increase and a 100 ng/g dose causes 2.0-45.5 fold increase. Therefore, we consider the 10 ng/g dose to be most suitable for our goals. Effects of pancreatic hormones on fish growth and metabolism In our studies on salmon and trout we often have

observed that groups of larger fish have higher average normal levels of insulin than groups of smaller fish (A. Sundby, K. Eliassen, A. Bloom, T. Refsti and E.M. Plisetskaya unpublished). Nevertheless, there is no direct correlation between the weight and insulinemia for individual fish. The relations between fish growth rates and levels of their anabolic and catabolic hormones need further attention, especially in connection with the recent finding of Zapf et al. (1987) that, although both insulin and insulin-growth factor (IGF-I) may exhibit growth-promoting potencies, their appropriate combination with growth hormone seems to be much more powerful in growth stimulation. We do not yet know the structure of fish IGF, therefore one of the most urgent goals at this time is an isolation and purification of piscine IGFs. There are special periods in the fish life cycle (Plisetskaya et al. 1988; Dickhoff et al. 1989, this volume) such as the transitional phase during salmon parr to smolt transformation, or the prespawning phase, which exhibit characteristic elevations of plasma insulin levels. Then, as smoltification or reproduction progresses, insulin levels drop. In previous publications from H.A. Bern's laboratory (referred to in Plisetskaya et al. 1988), it has been reported that the catabolic processes prevail in salmon smolts as compared to parr. In accordance with these findings, we have observed that an abrupt drop in plasma insulin content coincides with an accumulation of insulin in the islet tissue, as well as diminished liver glycogen content and hyperglycemia. A similar metabolic situation can be seen in fish injected with antiinsulin serum. When normoglycemic salmon parr, with abundant liver glycogen stores and high levels of circulating insulin, were injected with anti-insulin serum (AIS), their glycemic levels, liver glycogen content, and liver triacylglycerol lipase activity attained values typical of the smolt's metabolic condition, i.e. with catabolic trends dominating (Plisetskaya et al. 1988). Not only AIS, but other anti-hormonal sera as well, have proved to be useful tools in studies of the regulatory roles of the metabolic hormones, and as such the anti-sera have been used extensively in our experiments. The major effect of anti-glucagon (aGLU) and anti-GLP (aGLP) sera in juvenile salmon appears to be glycogen accumulation in the liver, suggesting that at this season (late summer)

44 the glycogen-family peptides, and especially GLP, might stimulate glycogenolysis more than gluconeogenesis (Plisetskaya et al. 1989a,b). During other seasons, and depending on fish species, the prevailing actions of glucagon and GLP might be triggering either glycolysis or gluconeogenesis (Mommsen et al. 1987; Mommsen and Moon 1989). These findings suggest, for the first time, a physiological role for GLP in fish. The search should be continued before a definite conclusion is reached whether the GLP effects on carbohydrate metabolism in liver, and possibly on cardiac muscle, are the major actions or incidental in fish. Salmon SST-25, although ineffective in inhibiting growth hormone release (Marchant 1987), has some metabolic potencies. In in vivo experiments on salmonids, this peptide enhances lipolysis (Sheridan et al. 1987). SST-14 elicit the same response (Sheridan and Bern 1986; M.A. Sheridan and E.M. Plisetskaya, unpublished). The action of SSTs are opposite to those of insulin, which is a lipogenic hormone. In salmon treated with antiSST-25 serum, liver triacylglycerol lipase activity is substantially lowered, while AIS administered in the same experiment elevates lipase activity (Plisetskaya et al. 1989b). At this time, it is difficult to decide whether the metabolic effects of salmon SST-25 are direct or indirect. The effects might be mediated by insulin, since SST-25 inhibits insulin secretion while aSST-25 elevates plasma insulin levels (Plisetskaya et al. 1986c; Sheridan et al. 1987). Evidently the major role of SST-25 in fish remains unresolved. A current question is whether the use of speciesspecific pancreatic hormones in functional tests will alter any of existing concepts in fish endocrinology. Carnivorous fish, such as salmonids, are widely believed to be insulin-deficient, because they are intolerant to carbohydrate intake. However, measurements of plasma insulin titres in fish revealed levels which were much higher than in mammals (Plisetskaya et al. 1986c). We have known for some time (Plisetskaya 1975; Yone 1979) that glucose elevates plasma levels of insulin in fish. Recently, Hilton et al. (1987) demonstrated that a high carbohydrate diet evokes more elevated insulin levels than a low carbohydrate diet (Table 2).

Table 2. Effect of different diets on circulating plasma insulin levels in the rainbow trout

Three hours post-feeding Eighteen hours post-feeding

Low carbohydrate diet

High carbohydrate diet

27.4 ± 1.6

48.2 + 4.0

5.2 ± 1.1

9.5 + 2.9

According to Hilton et al. 1987. Data are shown as mean insulin levels (ng/ml) SEM.

Still the fish remain intolerant to glucose. Rather than insulin-deficiency an impaired hormonereceptor interaction in skeletal muscles may be responsible for this phenomenon. Recently Leibush and Bondareva (1987) and Leibush et al. (1987) reported that, in contrast to the situation in warmblooded animals, neither very high levels of insulin (after injection), nor intermediate or very low levels of insulin (in prespawning autumn and spring seasons, respectively) change the number of insulin receptors in the heart or brain membranes of river lampreys. Ablett et al. (1985) came to a different conclusion about insulin receptors in the membranes of trout hepatocytes. This question needs further investigation. All authors agree that amino acids are the most powerful stimulators of insulin secretion in fish (Epple and Brinn 1987). In our experiments, arginine (6.0 Ctmol/g) appeared as the most potent agent elevating plasma insulin levels from 1.5 + 0.2 to 11.8 2.6 ng/ml two hours after injection. In the same time period, 6.0 Amol/g of lysine elevated insulin levels to 5.2 + 1.2 and of alanine to 2.7 + 0.2 ng/ml. Six mol/g of histidine lowered plasma insulin levels to 0.8 + 0.1 ng/ml. In mammals, the stimulatory action of arginine on insulin secretion is mediated through glucagon (Tan et al. 1985). Therefore, acute glucagon insufficiency, caused by anti-GLU sera, eliminates the arginine effect on insulin. In salmon, this phenomenon seems to be masked or absent. Immunoneutralization of glucagon-family peptides has no significant effect on salmonid plasma insulin levels elevated by arginine. Similarly, immunoneutralization of insulin with AIS has no visible effect on glucagon/

45

311 c

2-

Mc

M~i 0

nJ

ii, |

Dog

Fed [ Fasted overnight * Fasted 2-4 days a

l

v t TV of -

Goose

peptides in trout, however, insulin titres decline more sharply than glucagon or GLP titres. As a result the GLP/insulin molar ratio increases from 0.08 in the fed trout to 0.24 in the trout deprived of food for six weeks, which probably activates gluconeogenic fluxes.

Trout

Fig. 3. Comparison of the glucagon/insulin ratios in fed and fasted dog, (Unger and Lefrbvre 1972), goose (Sitbon 1976), and trout. (Plisetskaya et al. 1987).

GLP levels elevated by arginine. It would be important to repeat these experiments in vitro, using perifused pancreatic islets. So far, it seems that in salmonids circulating plasma insulin and glucagon levels are regulated independently (Plisetskaya et al. 1989a).

Interrelations among the pancreatic hormones: adaptation to feeding-fasting conditions Fish are becoming valuable models for studies of metabolic processes in the fasting vertebrates, because many fish species, including salmonids, normally experience long nontrophic periods. During a short period (up to 3-4 days) of fasting the plasma molar glucagon/insulin (G/I) ratio in fish increases, as it does in mammals and birds (Miahle 1976); in fish this change in ratio is mostly due to a lowering of insulin levels, whereas in warmblooded vertebrates this increase in G/I ratio is a result of simultaneous elevation of glucagon levels. As a consequence, in mammals, and especially in birds, after several days of starvation the molar G/I ratio exceeds 2.0. In fish it remains below 0.2. (Fig. 3). In their review of physiology and biochemistry of long-term fasting (for months) in birds, Cherel et al. (1988) do not report the plasma levels of metabolic hormones. It would be interesting to compare these levels especially in carnivorous birds, such a penguins, with their counterparts in salmonids. According to our observations (T.W. Moon, G.D. Foster and E.M. Plisetskaya, unpublished), a starvation period of six weeks results in a decline of the plasma titres of all three

Some selected questions to be addressed: 1. Does the fish endocrine pancreas produce not only insulin, glucagon, GLP, somatostatins and NPY but also some other biologically active peptides as well? 2. Is there any physiological significance to the abundance of islet cells producing 'big' somatostatins and their localization adjacent to the glucagon/GLP producing cells? 3. How does insulin interact with various growth factors in promoting fish growth? 4. Which mechanisms are involved in glucose intolerance in carnivorous fish? 5. What is the role, if any, of insulin in fish reproduction? 6. What is the major physiological role of 'big' somatostatins? 7. What is the major physiological role of glucagon-like peptide? Might the GLP operate outside the liver? 8. Does pancreatic NPY have any role in regulation of the release of fish pancreatic hormones, control of metabolic events, or regulation of the appetite and sexual behavior? 9. What interaction between pancreatic hormones exists in the fish endocrine pancreas? 10. Are pancreatic hormone-receptor interactions in fish similar to, or different from those in higher vertebrates? 11. Is there any difference in hormonal regulation of metabolism in carnivorous and omnivorous fish? Space does not permit an elaboration on other aspects of the physiology of the fish endocrine pancreas, such as the regulation of synthesis and secretion of pancreatic hormones, the nervous regulation of islet function, or the interactions of endocrine and exocrine components of the pancreas.

46 Fortunately, we now have an excellent monograph available (Epple and Brinn 1987) which thoroughly covers all of these, as well as many other, topics. As recently as four years ago, I was aware that most of my peer scientists, who were engaged in physiological studies of the fish pancreas, when I started my own research career, had already left the field. However now, when new enthusiastic and ambitious younger researchers are entering the field we can reasonably hope that important and still puzzling questions concerning the fish endocrine pancreas will continue to be pursued.

Acknowledgements The author was supported by a grant from the National Science Foundation DCB 8615551. The cooperation of Drs. T.P. Mommsen, T.W. Moon and C.V. Sullivan, who gave their permission to cite unpublished results from experiments, carried out in collaboration, are acknowledged with gratitude. The critical reading of the manuscript by Drs. A. Gorbman, R.E. Peter and C.V. Sullivan is highly appreciated.

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Physiology of fish endocrine pancreas.

From the very beginning of physiological studies on the endocine pancreas, fish have been used as experimental subjects. Fish insulin was one of the f...
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