Summary
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1.
The body tissues of 32-day-old femaleMoniliformis dubius contained substantial levels of reserve carbohydrates. Glycogen accounted for approximately 24% of the tissue solids of worms from normally fed hosts; the non-reducing disaccharide trehalose (α-d-glucopyranosyl-{1→1}-α-d-glycopyranoside) was present at a concentration of 34 μmoles/ml tissue H2O, and tissue levels of free glucose averaged 28 μmoles/ml tissue H2O (Table 1).
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2.
Glycogen was present almost exclusively in the tissues of the body wall (table 2). The ethanol soluble sugars were partitioned between the body wall and the contents of the pseudocoelomic cavity in proportions approximating the percentage of the total body mass associated with each of these compartments (Table 2).
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3.
Exogenous14C-glucose was rapidly phosphorylated and subsequently incorporated into trehalose following its absorption (Table 3); this indicates that newly absorbed glucose did not enter directly into the endogenous glucose pools of the helminth body wall. Incorporation of radioactivity into glycogen was minimal.
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4.
Sequential incubation in3H- and14C-labelled glucose effected a partial separation of the metabolism of newly absorbed glucose from that of endogenous sugars (Tables 4 and 5). Ratios of activity from the two species of radioglucose among the major derivatives of absorbed glucose suggested that the tissue glucose pools derive not from free glucose but from the glucosyl moieties of trehalose (Table 5).
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5.
The data indicate that the glucose pools in the tissues ofM. dubius are physically separated from the tegumental epithelium, and they suggest that the accumulation of hexoses within these pools requires their incorporation into the disaccharide trehalose and its subsequent dismutation into free glucose units. the central role of trehalose in the carbohydrate metabolism ofMoniliformis is discussed, and a possible mechanism for the delivery of glucose moieties from trehalose into the tissue glucose pools by the action of a membrane-traversing “transporting trehalase” is considered.
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References
Branch, S.I.:Moniliformis dubius: Osmotic responses. Exp. Parasit.27, 44–52 (1970)
Bryam, J.E., Fisher, F.M., Jr.: The absorptive surface ofMoniliformis dubius (Acanthocephala). I. Fine structure. Tissue and Cell5, 553–579 (1973)
Crane, R.K.: A digestive-absorptive surface as illustrated by the intestinal cell brush border. Trans. Amer. micros. Soc.94, 529–544 (1975)
Crompton, D.W.T.: An ecological approach to acanthocephalan physiology. Cambridge monographs in experimental biology17, 1–125 (1970)
Crowley, G.J., Moses, V., Ullrich, J.: A versatile solvent to replace phenol for the paper chromatography of radioactive intermediary metabolites. J. Chromatog.12, 219–228 (1963)
Czech, M.P., Lawrence, J.F., Jr., Lynn, W.S.: Hexose transport in isolated brown fat cells. A model system for investigating insulin action on membrane transport. J. biol. Chem.249, 5421–5427 (1974)
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F.: Colorimetric method for determination of sugars and related substances. Analyt. Chem.28, 350–356 (1956)
Elbein, A.D.: The metabolism of α,α-trehalose. Advanc. Carbohyd. Chem. Biochem.30, 227–256 (1974)
Elbrink, J., Bihler, I.: Membrane transport: Its relation to cellular metabolic rates. Science188, 1177–1184 (1975)
Fairbairn, D.: Trehalose and glucose in helminths and other invertebrates. Canad. J. Zool.36, 787–795 (1958)
Graff, D.J.: Metabolism of C14-glucose byMoniliformis dubius (Acanthocephala). J. Parasit.50, 230–234 (1964)
Gray, H.E., Fraenkel, G.: Fructomaltose, a recently discovered trisaccharide isolated from honeydew. Science118, 304–305 (1953)
Kilejian, A.: The effect of carbon dioxide on glycogenesis inMoniliformis dubius (Acanthocephala). J. Parasit.49, 862–863 (1963)
Körting, W., Fairbairn, D.: Anaerobic energy metabolism inMoniliformis dubius (Acanthocephala). J. Parasit.58, 45–50 (1972)
Laurie, J.S.: Aerobic metabolism ofMoniliformis dubius (Acanthocephala) Exp. Parasit.8, 188–197 (1959)
McAlister, R.O., Fisher, F.M., Jr.: The biosynthesis of trehalose inMoniliformis dubius (Acanthocephala). J. Parasit.58, 51–62 (1972)
Pappas, P.W., Read, C.P.: Membrane transport in helminth parasites: A review. Exp. Parasit.37, 469–530 (1975)
Read, C.P., Rothman, A.H.: The carbohydrate requirement ofMoniliformis (Acanthocephala) Exp. Parasit.7, 191–197 (1958)
Read, C.P., Rothman, A.H., Simmons, J.E., Jr.: Studies on membrane transport with special reference to parasite-host integration. Ann. N.Y. Acad. Sci.113, 154–205 (1963)
Schultz, S.G., Curran, P.F.: Coupled transport of sodium and organic solutes. Physiol. Rev.50, 637–718 (1970)
Silverman, M.: Glucose transport in the kidney Biochim. biophys. Acta457, 303–351 (1976)
Starling, J.A.: Tegumental carbohydrate transport in intestinal helminths: correlation between mechanisms of membrane transport and the biochemical environment of absorptive surfaces. Trans. Amer. micros. Soc.94, 508–523 (1975)
Starling, J.A., Fisher, F.M., Jr.: Carbohydrate transport inMoniliformis dubius (Acanthocephala). I. The kinetics and specificity of hexose absorption. J. Parasit.61, 977–990 (1975)
Trevelyan, W.E., Proctor, D.P., Harrison, J.S.: Determination of sugars on paper chromatograms. Nature166, 444–445 (1950)
Wyatt, G.R.: The biochemistry of sugars and polysaccharides in insects. Advanc. Insect Physiol.4, 287–360 (1967)
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This research was sponsored in part by a grant from the Moody Foundation (70-115), Galveston, Texas, and by Grants AI01384 and AI00106 from the NIH, U.S. Public Health Service
Some of the results presented in this paper have been reviewed elsewhere (Starling, 1975)
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Starling, J.A., Fisher, F.M. Carbohydrate transport inMoniliformis dubius (Acanthocephala). J Comp Physiol B 126, 223–231 (1978). https://doi.org/10.1007/BF00688931
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DOI: https://doi.org/10.1007/BF00688931