Gluconeogenesis in Birds
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1 1148 BIOCHEMICAL SOCIETY TRANSACTIONS Gluconeogenesis in Birds DEREK R. LANGSLOW Department of Biochemistry, University of Edinburgh Medical School, Teviot Place, Edinburgh EH8 9AG, Scotland, U.K. It is a characteristic of all avian species that they maintain a plasma glucose concentration between 9 and 15 mm under all physiological circumstances. Even starvation for up to 9 days failed to lower the blood sugar concentration of chickens (Hazelwood & Lorenz, 1959). This concentration is much greater than that found in most mammals and yet, by contrast, the glycogen stores of avian liver are rather lower than those of most mammals. Hence birds require an active gluconeogenic pathway to maintain their plasma glucose concentration during food deprivation and under various forms of stress. The fertile chicken egg contains relatively little carbohydrate, but after 18 days incubation the liver contains 20mg of glycogen/g wet weight and this falls below lomg/g weight at hatching (Gill, 1938; R. S. Campbell & D. R. Langslow, unpublished observations). Most of this glycogen must be derived from the endogenous protein stores of the egg and during the final week of incubation the chick embryo has an extremely active gluconeogenic pathway. Hence, in addition to the usual role of gluconeogenesis in starvation and stress, birds also depend on gluconeogenesis during their embryonic existence. The major pathways of glucose metabolism in birds are similar to those of other animals, except that the pentose phosphate pathway is rather inactive, especially in liver (O Hea & Leveille, 1968; Duncan, 1968), and glucokinase is absent from avian liver (Ureta et a[., 1973; O Neill & Langslow, 1976, ~). The rates of glucose turnover and recycling are substantially higher in chickens than in rats (Brady et al., 1977). Some of the enzymes concerned with glucose metabolism show some important differences between birds and mammals. Both phosphoenolpyruvate carboxykinase (EC ) and alanine aminotransferase (EC ) are almost entirely mitochondria1 in chickens and other birds while less than 10% of their activity is mitochondrial in rat liver (Utter, 1959; Sarker, 1977). The absence of glucokinase poses a problem for the regulation of glucose uptake by avian liver. Glucose uptake is regulated by substrate cycling between glucose and glucose 6-phosphate. Both the activity and K, of glucose 6-phosphatase (EC ) are altered under different conditions. Starvation, for example, increases the activity of the enzyme and lowers the K, (O Neill & Langslow, 1976, a,b). Furthermore, the rapid rate of loss of 3H from [3H]glucose suggests that this cycle occurs twice as fast in chickens as in rats (Brady et al., 1977). Fructose 1,dbisphosphatase (EC ) also differs from the typical mammalian enzyme. Its K, for fructose 1,6-bisphosphate is only lop~ and the enzyme is inhibited by 70% by 200p~-fructose 1,6-bisphosphate (R. S. Campbell & D. R. Langslow, unpublished observations). Substrates for avian gluconeogenesis Gluconeogenesis in avian liver has been studied in a variety of experimental situations. In viuo, different precursors have been injected into starving chickens and the response of the plasma glucose concentration monitored (Sarker, 1971 ; Davison & Langslow, 1975). The efficacy of different precursors in elevating the plasma glucose concentration could be ordered lactate = glycerol > pyruvate > alanine > aspartate > serine. None of these precursors significantly altered the hepatic glycogen content (Davison & Langslow, 1975). In vitro, avian gluconeogenesis has been studied in homogenates of pigeon liver (Krebs & Hems, 1964), perfused pigeon liver (Soling et al., 1973), perfused chicken liver (Bickerstaffe et al., 1970) and isolated chicken hepatocytes (Dickson & Langslow, 1977, ). Glucose production was increased by lactate (20m~) but not by pyruvate (20m~) in perfused pigeon liver (Soling et al., 1973). If ethanol was added to the perfusate, glucose was produced from pyruvate. In isolated chicken hepatocytes derived from both fed and starved chickens, glucose production has been measured from
2 577th MEETING, OXFORD 1149 several precursors. The high endogenous rates of glycogenolysis in fed chicken hepatocytes make it difficult to determine the gluconeogenic flux, even when both the glycogen content of and glucose efflux from the hepatocytes are measured. Hepatocytes from starved chickens overcome the glycogen problem but suffer from the disadvantages that they are more difficult to prepare and less stable than hepatocytes from fed chickens (Dickson et al., ). Optimal concentrations of fructose, lactate, pyruvate and dihydroxyacetone were equally effective in stimulating glucose production from fed chicken hepatocytes, and alanine was half as effective and glycerol had no significant effect (Fig. 1). The fructose effect was only observed after a lag of 15min. The response of cells from starved chickens was similar, except that lactate was more effective than pyruvate. could be made more effective by the addition of ethanol to produce cytoplasmic reducing equivalents (Dickson & Langslow, ). Both glycerol and alanine were poor glucose precursors in hepatocytes from starved chickens. Since gluconeogenesis occurs from a mixture of substrates in vivo, combinations of precursors were also tested, to search for co-operative interactions that might account for some of the differences in precursor effectiveness between situations in vivo and in vitro. and pyruvate gave less than additive effects on glucose production, whereas combinations of glycerol plus pyruvate or alanine mutually stimulated glucose production (Table 1). Glycerol was a much poorer precursor for glucose than was dihydroxyacetone and was much less effective in vitro than in vivo. Glycerol is specifically phosphorylated by i 11 /T A t I Incubation time (min) Fig. 1, Time course of substrate efects on glucose production Hepatocytes were prepared from fed chickens. Substrates were added to give a final concentration of lomm and results were expressed as differences from the control value at each time. Values are means+s.e.m. for the numbers of experiments shown in parentheses. A, (3); A, glycerol (6); 0, pyruvate (4); m, dihydroxyacetone (5); 0, alanine (3); 0, fructose (8). Vol. 6
3 1150 BIOCHEMICAL SOCIETY TRANSACTIONS Table 1. Additive efects of substrates on glucose production Hepatocytes from 24h-starved chickens were incubated for 30min with a single substrate (10 or 2m~) or with mixtures of two substrates (each at 10 or 2m~). Glucose production under each condition was measured and results are expressed as the percentage of the value expected from pure addition of production from each substrate. The results are meansfs.e.m. with the numbers of experiments in parentheses. 1 Fructose Fructose Glycerol Substrate - 2 (8) (4) Fructose (4) Glycerol (4) Dihydroxyacetone (5) Hydroxypyruvate (4) (4) Fructose (3) Glycerol (7) Sorbitol (4) Xylitol (4) Fructose (4) Glycerol (5) Dihydroxyacetone (3) Glycerol (3) Percentage of expected value r 9 10mM-Substrate 2 mm-substrate 31.6f f f f f f f f * f f f f f f f f f f f f 2.8 glycerokinase (EC ), whereas dihdroxyacetone can be phosphorylated by either glycerokinase or triokinase (EC ). Triokinase must be present, since glyceraldehyde is converted into glucose. Glycerokinase activity in chicken liver is low (Dickson, 1977) compared with that in rat liver (Robinson & Newsholme, 1969; Harding et ul., 1975). In addition it may be inhibited by the relatively low ATP content which chicken hepatocytes appear to have (Dickson et al., ). Interactions with other metabolites may also aid glycerol as a precursor. is a good glucose precursor in vivo, but is virtually without effect in hepatocytes. When [I4C]lactate and [I4C]alanine were injected into chickens, they were converted into ['4C]glucose at the same rate (A. J. Dickson, personal communication) and hence the low alanine aminotransferase activity of chicken hepatocytes (Dickson, 1977) was probably rate-limiting in vitro. In uiuo alanine may first be metabolized by tissues such as muscle to lactate and the lactate then converted into glucose by the liver. concentrations above 0.6m~ did not further increase gluconeogenesis in hepatocytes from starved chickens. As ethanol stimulated glucose production from pyruvate, a lack of cytoplasmic NADH was probably rate-limiting for triose phosphate dehydrogenase (EC ). The mitochondria1 location of phosphoenolpyruvate carboxykinase probably causes the lack of NADH supply. The carbon skeleton of pyruvate leaves the mitochondria of chicken liver as phosphoenolpyruvate in exchange for citrate or possible ADP (Robinson, 1971 ; Shrago et ul., 1976; Soling & Kleineke, 1976). By contrast, the carbon skeleton of pyruvate leaves rat liver mitochondria as malate (Berry & Kun, 1972) and reduces NAD+ when it is converted into oxaloacetate. Hence reducing equivalents are not limiting in the cytoplasm of rat liver. The presence of large amounts of cytoplasmic pyruvate in chicken liver will further deplete cytoplasmic NADH.
4 577th MEETING, OXFORD 1151 stimulates glucose production from chicken hepatocytes immediately without the lag phase characteristic of rat hepatocytes (Johnson et al., 1972; Krebs et al., 1974). In rat hepatocytes, aspartate derived from lactate leaves the mitochondria and amino acids such as glutamate are lost from rat hepatocytes during isolation. Thus the rate of transamination of oxaloacetete to aspartate may be limiting initially. No such problem arises in chickens as the carbon skeleton of lactate leaves as phosphoenolpyruvate. Control of avian gluconeogenesis In the whole animal several different hormones control glucose production from the liver and will exert their action at different places on the gluconeogenic pathway. Glucagon and adrenaline accelerate glucose output from chicken hepatocytes and increase the plasma glucose concentration in vivo (Langslow et al., 1970; Dickson et al., ). Gluconeogenesis from pyruvate, lactate, alanine, glycerol, dihydroxyacetone and fructose is stimulated by glucagon. The percentage stimulation by glucagon over substrate alone is the same for all the substrates (Dickson & Langslow, ). This is unlike rat hepatocytes where the stimulation of glucose production from fructose or dihydroxyacetone is much less than from lactate or pyruvate. It seems likely that regulation between pyruvate and phosphoenolpyruvate is absent from, or much less important in, chickens than rats. Glucagon stimulates cyclic AMP production by chicken hepatocytes, but glucagon stimulates glucose production at concentrations below those at which an increase in cyclic AMP can be detected (D. R. Langslow & K. Siddle, unpublished observations). The mechanism by which gluconeogenesis is stimulated by glucagon remains unknown. Adrenaline and dibutyryl cyclic AMP also stimulate gluconeogenesis in vitro. Gluconeogenesis in avian embryos Gluconeogenesis is an essential process for the avian embryo during the final week of incubation. The glucose produced increases liver glycogen stores and gradually increases the circulating glucose concentration (Daugeras, 1968 ; Langslow, 1975). The increase in gluconeogenic flux in the embryonic liver is mediated by increases in fructose bisphosphatase from day 12 of incubation to day 16, in glucose 6-phosphatase from day 12 to day 20 and in phosphoenolpyruvate carboxykinase up to day 17. Up to about day 18 the glucose units are mainly diverted towards glycogen storage in the liver. On day 19, breathing begins and the glycogen is mobilized. Glucose 6-phosphatase activity increases up to day 20, which is 3 days after other key gluconeogenic enzymes have their maximum activity. In addition to changes in the total activity of glucose 6-phosphatase, which can regulate glucose output from the liver, the K, of the enzyme also changes. The K,,, for glucose 6-phosphate increases from 2.9 mm on day 15 to 4.95 mm on day 18. This is analogous to the change in K, observed between the fed and starved state in 6-week-old chickens. The.K, declines sharply on day 19 at the time the glycogen is mobilized. Insulin modified glucose 6-phosphatase activity by lowering the total activity when injected into embryos over several days and also by raising the K, of the enzyme for glucose 6-phosphate. This effect on glucose 6-phosphatase effectively diverted glucose towards glycogen, and the liver glycogen content was more than doubled by the insulin treatment (Campbell & Langslow, ). Other hormones can alter enzymes in the liver associated with gluconeogenesis in the embryo. Glucagon increased both fructose bisphosphatase and phosphoenolpyruvate carboxykinase activities when injected into chick embryos, whereas insulin decreased fructose bisphosphatase, but was without effect on phosphoenolpyruvate carboxykinase (R. S. Campbell & D. R. Langslow, unpublished observations). Dibutyryl cyclic AMP mimicked the effects of glucagon, and the infusion of anti-insulin serum also increased fructose bisphosphatase. These hormones did not alter the pattern of enzyme activity observed during the development of the embryo and they merely changed the absolute activity. Glucocorticoids caused intense hyperglycaemia and an increase in the liver glycogen content of chick embryos. Glucocorticoids did not alter the activity Vol. 6
5 1152 BIOCHEMICAL SOCIETY TRANSACTIONS of fructose bisphosphatase, glucose 6-phosphatase or phosphoenolpyruvate car boxykinase when expressed per g wet wt. of liver, but they significantly increased the liver weight of the embryos and hence the total gluconeogenic capacity of the individual embryo (R. S. Campbell & D. R. Langslow, unpublished observations). Hence several different hormones can modify the activities of gluconeogenic enzymes in chickembryo liver. I am grateful to the Medical Research Council and the British Egg Marketing Board Trust for grants that supported part of this work. Berry, M. N. & Kun, E. (1972) Eur. J. Biochem. 27, Bickerstaffe, R., West, C. E. & Annison, E. F. (1970) Biochem. J. 118, Brady, K. J., Romas, D. R. & Leveille, G. A. (1977) Comp. Biochem. Physiol Campbell, R. S. & Langslow, D. R. () Biochem. SOC. Trans. 6, Daugeras, N. (1968) C.R. Hebd. SPances Acad. Sci. Ser. D 267, Davison, T. F. & Langslow, D. R. (1975) Comp. Biochem. Physiol. 52A, Dickson, A. J. (197) Ph.D. Thesis, University of Edinburgh Dickson, A. J. & Langslow, D. R. (1977) Biochem. Soc. Trans. 5, Dickson, A. J. & Langslow, D. R. () Mol. Cell Biochem. in the press Dickson, A. J., Anderson, C. E. & Langslow, D. R. () Mol. Cell. Biochem. 19,81-92 Duncan, H. J. (1968) Can. J. Biochem. 46, Gill, P. M. (1938) Biochem. J. 32, Harding, J. W., Pyeritz, E. A., Copeland, E. S. &White, H. B. (1975) Biochem. J. 146, Hazelwood, R. L. & Lorenz, F. W. (1959) Am. J. Physiol. 197, Johnson, M. E. M.,Das, M. N.,Butcher, F. R. &Fain, J. N. (1972)J. Biol. Chern. 247, Krebs, H. A. & Hems, R. (1964) Biochem. J. 93, Krebs, H. A., Cornell, N. W., Lund, P. & Hems, R. (1974) Arfred Benzon Symp. 6, Langslow, D. R. (1975) Br. Poult. Sci. 16, Langslow, D. R.,Butler, E. J., Hales, C. N. &Pearson, A. W. (1970)J. Endocrinol. 46, O Hea, E. K. & Leveille, G. A. (1968) Comp. Biochem. Physiol. 26, O Neill, I. E. & Langslow, D. R. (1976) Biochem. Soc. Trans. 4, O Neill, I. E. & Langslow, D. R. (~) Comp. Biochem. Physiol. 59B, O Neill, I. E. & Langslow, D. R. (6) Gen. Comp. Endocrinol. 34, Robinson, B. H. (1971) FEBS Lett. 14, Robinson, J. & Newsholme, E. A. (1969) Biochem. J. 112, Sarker, N. K. (1971) Life Sci. 10, Sarker, N. K. (1977) Inf. J. Biochem. 8, Shrago, E., Shug, A. & Elson, C. (1976) in Gluconeogenesis: its Regulation in Mammalian Species (Hanson, R. W. & Mehlman, M. A.,eds.), pp , Wiley, New York and London Soling, H. D. & Kleineke, J. (1976) in Gluconeogenesis: its Regulation in Mammalian Species (Hanson, R. W. & Mehlman, M. A., eds.), pp , Wiley, New York and London Soling, H. D., Kleineke, J., Willus,B., Janson, G. &Kuhn, A. (1973) Eur. J. Biochem. 37, Ureta, T., Reichberg, S. B., Radojkovic, J. & Slebe, J. C. (1973) Comp. Biochem. Physiol. 45B, Utter, M. F. (1959) Ann. N. Y. Acad. Sci. 72, Gluconeogenesis in Ruminants D. B. LINDSAY Department of Biochemistry, A.R.C. Institute of Animal Physiology, Babraham, Cambridge CB2 4AT, U.K. Ruminants are characterized by having their gluconeogenic pathway more or less permanently switched on. Indeed the rate of gluconeogenesis is greatest after a meal, and slowly declines during starvation. There are several reasons for believing that little dietary glucose is available. (1) Most of the dietary carbohydrate can be accounted for by the amounts of volatile fatty acids, methane and C02 produced
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