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The regulation of trehalose metabolism in insects

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Abstract

Trehalose is a non-reducing disaccharide comprising two glucose molecules. It is present in high concentration as the main haemolymph (blood) sugar in insects. The synthesis of trehalose in the fat body (an organ analogous in function to a combination of liver and adipose tissue in vertebrates) is stimulated by neuropeptides (hypertrehalosaemic hormones), released from the corpora cardiaca, a neurohaemal organ associated with the brain. The peptides cause a decrease in the content of fructose 2,6-bisphosphate in fat body cells. Fructose 2,6-bisphosphate, acting synergistically with AMP, is a potent activator of the glycolytic enzyme 6-phosphofructokinase-1 and a strong inhibitor of the gluconeogenic enzyme fructose 1,6-bisphosphatase. This indicates that fructose 2,6-bisphosphate is a key metabolic signal in the regulation of trehalose synthesis in insects. Trehalose is hydrolysed by trehalase (E.C. 3.2.1.28). The activity of this enzyme is regulated in flight muscle, but the mechanism by which this is achieved is unknown. Trehalase from locust, flight muscle is a glycoprotein bound to membranes of the microsomal fraction. The enzyme can be activated by detergents in vitro and by short flight intervals in vivo, which indicates that changes in the membrane environment modulate trehalase activity under physiological conditions.

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References

  1. Azuma, M., and Yamashita, O., Cellular localization and proposed function of midgut trehalase in the silkworm larva,Bombyx mori. Tissue & Cell17 (1985) 539–551.

    Google Scholar 

  2. Azuma, M., and Yamashita, O., Immunohistochemical and biochemical localization of trehalase in developing ovaries of the silkworm,Bombyx mori, Insect Biochem.15 (1985)589–596.

    Article  Google Scholar 

  3. Beenakkers, A. M. Th., Van der Horst, D. J., and Van Marrewijk, W. J. A., Biochemical processes directed to flight muscle metabolism, in: Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol. 10, pp. 451–486. Eds. G. A. Kerkut and L. I. Gilbert. Pergamon Press, Oxford 1984.

    Google Scholar 

  4. Berthelot, M., Sur le tréhalose nouvelle espèce de sucre. C. r. hebd. Séanc. Acad. Sci., Paris46 (1858) 1276–1279.

    Google Scholar 

  5. Bowers, W. S., and Friedman, S., Mobilization of fat body glycogen by an extract of corpus cardiacum. Nature198 (1963) 685.

    PubMed  Google Scholar 

  6. Brandt, N. R., and Huber, R. E., The localization of honey bee thorax trehalase. Can. J. Biochem.57 (1979) 145–154.

    PubMed  Google Scholar 

  7. Cabib, E., and Leloir, L. F., The biosynthesis of trehalose phosphate. J. biol. Chem.231 (1958) 259–275.

    PubMed  Google Scholar 

  8. Candy, D. J., The control of muscle trehalase activity during locust flight. Biochem. Soc. Trans.2 (1974) 1107–1109.

    Google Scholar 

  9. Candy, D. J., and Kilby, B. A., Site and mode of trehalose biosynthesis in the locust. Nature183 (1959) 1594–1595.

    PubMed  Google Scholar 

  10. Candy, D. J., and Kilby, B. A., The biosynthesis of trehalose in the locust fat body. Biochem. J.78 (1961) 531–536.

    PubMed  Google Scholar 

  11. Chino, H., Conversion of glycogen to sorbitol and glycerol in the diapause egg of theBombyx silkworm. Nature180 (1957) 606–607.

    Google Scholar 

  12. Clements, A. N., Page, J., Borck, K., and Van Ooyen, A. J. J., Trehalases from the flesh flySarcophaga barbata. J. Insect Physiol.16 (1970) 1389–1404.

    Article  PubMed  Google Scholar 

  13. Duve, H., Intracellular localization of trehalase in thoracic muscle of the blowfly,Calliphora erythrocephala. Insect Biochem.5 (1975) 299–311.

    Article  Google Scholar 

  14. Gäde, G., The hypertrehalosaemic peptides of cockroaches: a phylogenetic study. Gen. comp. Endocrinol75 (1989) 287–300.

    Article  PubMed  Google Scholar 

  15. Gäde, G., The adipokinetic hormone/red pigment-concentrating hormone peptide family: structures, interrelationships and functions. J. Insect Physiol.36 (1990) 1–12.

    Article  Google Scholar 

  16. Gäde, G., and Rinehart, K. L. Jr., Amino acid sequence of a hypertrehalosaemic neuropeptide from the corpus cardiacum of the cockroachNauphoeta cinerea. Biochem. biophys. Res. Comm.141 (1986) 774–781.

    Article  PubMed  Google Scholar 

  17. Gilby, A. R., Wyatt, S. S., and Wyatt, G. R., Trehalases from the cockroach,Blaberus discoidalis: Activation, solubilization and properties of the muscle enzyme and some properties of the intestinal enzyme. Acta Biochim. Pol.14 (1967) 83–100.

    PubMed  Google Scholar 

  18. Gussin, A. E. S., and Wyatt, G. R., Membrane-bound trehalase from cecropia silkmoth muscle. Arch. Biochem. Biophys.112 (1965) 626–634.

    Article  PubMed  Google Scholar 

  19. Hasegawa, K., The diapause hormone of the silkworm,Bombyx mori. Nature179 (1957) 1300–1301.

    Google Scholar 

  20. Hasegawa, K., and Yamashita, O., Studies on the mode of action of the diapause hormone in the silkworm,Bombyx mori. VI-The target organ of the diapause hormone. J. exp. Biol.43 (1965) 271–277.

    Google Scholar 

  21. Hayes, T. K., Keeley, L. L., and Knight, D. W., Insect hypertrehalosemic hormone: isolation and primary structure fromBlaberus discoidalis cockroaches. Biochem. biophys. Res. Comm.140 (1986) 674–678.

    Article  PubMed  Google Scholar 

  22. Ikeda, M., Su, Z., Saito, H., Imai, K., Yukihiro, S., Isobe, M., and Yamashita, O., Induction of embryonic diapause and stimulation of ovary trehalase activity in the silkworm,Bombyx mori, by synthetic diapause hormone. J. Insect Physiol.39 (1993) 889–895.

    Article  Google Scholar 

  23. Jutsum, A. R., and Goldsworthy, G. J., Fuels for flight inLocusta. J. Insect Physiol.22 (1976) 243–249.

    Article  Google Scholar 

  24. Kammer, A. E., and Heinrich, B., Insect flight metabolism. Adv. Insect Physiol.13 (1978) 133–228.

    Google Scholar 

  25. Kono, Y., Takahashi, M., Matsushita, K., Nishina, M., Kameda, Y., and Hori, E., Inhibition of flight inPeriplaneta americana (Linn.) by a trehalase inhibitor, Validoxylamine A. J. Insect Physiol.40 (1994) 455–461.

    Article  Google Scholar 

  26. Lee, Y.-H., and Keeley, L. L., Intracellular transduction of trehalose synthesis by hypertrehalosemic hormone in the fat body of the tropical cockroach,Blaberus discoidalis. Insect Biochem. molec. Biol.24 (1994) 473–480.

    Article  Google Scholar 

  27. Mansingh, A., Studies on insect dormancy. II-Relationship of cold-hardiness to diapause and quiescence in the eastern tent caterpillar,Malacosoma americanum (Fab.), (Lasiocampidae: Lepidoptera). Can. J. Zool.52 (1974) 629–637.

    PubMed  Google Scholar 

  28. Mayer, R. J., and Candy, D. J., Changes in energy reserves during flight of the desert locust,Schistocerca gregaria. Comp. Biochem. Physiol.31 (1969) 409–418.

    Article  PubMed  Google Scholar 

  29. McClure, J. B., and Steele, J. E., The role of extracellular calcium in hormonal activation of glycogen phosphorylase in cockroach fat body. Insect Biochem.11 (1981) 605–613.

    Article  Google Scholar 

  30. McDougall, G. E., and Steele, J. E., Free fatty acids as a source of energy for trehalose synthesis in the fat body of the American cockroach (Periplaneta americana). Insect Biochem.18 (1988) 591–597.

    Article  Google Scholar 

  31. Orr, G. L., Gole, J. W. D., Jahagirdar, A. P., Downer, R. G. H., and Steele, J. E., Cyclic AMP does not mediate the action of synthetic hypertrehalosaemic peptides from the corpus cardiacum ofPeriplaneta americana. Insect Biochem.15 (1985) 703–709.

    Article  Google Scholar 

  32. Pilkis, S. J., (Ed.), Fructose-2,6-bisphosphate. CRC Press, Boca Raton, Florida 1990.

    Google Scholar 

  33. Reed, W. D., and Sacktor, B., Localization of trehalase in flight muscle of the blowflyPhormia regina. Arch. Biochem. Biophys.145 (1971) 392–401.

    Article  PubMed  Google Scholar 

  34. Randall, D. D., and Derr, R. F., Trehalose: occurrence and relation to egg diapause and active transport in the differential grasshopper,Melanoplus differentialis. J. Insect Physiol.1 (1965) 329–335.

    Article  Google Scholar 

  35. Scarborough, R. M., Jamieson, G. C., Kalish, F., Kramer, S. J., McEnroe, G. A., Miller, C. A., and Schooley, D. A., Isolation and primary structure of two peptides with cardioacceleratory and hyperglycemic activity from the corpora cardiaca ofPeriplaneta americana. Proc. natl Acad Sci.81 (1984) 5575–5579.

    PubMed  Google Scholar 

  36. Shimada, S., and Yamashita, O., Trehalose absorption related with trehalase in developing ovaries of the silkworm,Bombyx mori. J. comp. Physiol.131 (1979) 333–339.

    Google Scholar 

  37. Steele, J. E., Occurrence of a hyperglycemic factor in the corpus cardiacum of an insect. Nature192 (1961) 680–681.

    Google Scholar 

  38. Steele, J. E., McDougall, G. E., and Shadwick, R., Trehalose efflux from cockroach fat bodyin vitro: paradoxical effects of the corpus cardiacum and methylxanthines. Insect Biochem.18 (1988) 585–590.

    Article  Google Scholar 

  39. Su, Z., Ikeda, M., Sato, Y., Saito, H., Imai, K., Isobe, M., and Yamashita, O., Molecular characterization of ovary trehalase of the silkworm,Bombyx mori and its transcriptional activation by diapause hormone. Biochim. biophys. Acta1218 (1994) 366–374.

    PubMed  Google Scholar 

  40. Takesue, Y., Yokota, K., Nishi, Y., Taguchi, R., and Ikezawa, H., Solubilization of trehalase from rabbit renal and intestinal burshborder membranes by a phosphatidylinositolspecific phospholipase C. FEBS Lett.201 (1986) 5–8.

    Article  PubMed  Google Scholar 

  41. Terra, W. R., and Ferreira, C., Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol.109B (1994) 1–62.

    Google Scholar 

  42. Vaandrager, S. H., Haller, T. B., Van Marrewijk, W. J. A., and Beenakkers, A. M. Th., Fractionation and kinetic properties of trehalase from flight muscles and haemolymph of the locust,Locusta migratoria. Insect Biochem.19 (1989) 89–94.

    Article  Google Scholar 

  43. Van der Horst, D. J., Van Doorn, J. M., and Beenakkers, A. M. Th., Dynamics in the haemolymph trehalose pool during flight of the locustLocusta migratoria. Insect Biochem.8 (1978) 413–416.

    Article  Google Scholar 

  44. Van Laere, A., Trehalose, reserve and/or stress metabolite? FEMS Microbiol. Rev.63 (1989) 201–210.

    Google Scholar 

  45. Van Schaftingen, E., Role of fructose-2,6-bisphosphate in the regulation of hepatic carbohydrate metabolism, in: Fructose-2,6-bisphosphate, pp. 65–85. Ed. S. J. Pilkis. CRC Press, Boca Raton, Florida 1990.

    Google Scholar 

  46. Van Schaftingen, E., Hue, L., and Hers, H.-G., Fructose 2,6-bisphosphate, the probable structure of the glucose- and glucagon-sensitive stimulator of phosphofructokinase. Biochem. J.192 (1980) 897–901.

    PubMed  Google Scholar 

  47. Wegener, G., Elite invertebrate athletes: flight in insects its metabolic requirements and regulation and its effects on life span, in: International Perspectives in Exercise Physiology, pp. 83–87. Eds. K. Nazar, R. L. Terjung, H. Kaciuba-Uscilko and L. Budhoski. Human Kinetics Books, Champaign, Illinois 1990.

    Google Scholar 

  48. Weis-Fogh, T., Fat combustion and metabolic rate of flying locusts (Schistocerca gregaria Forskal), Phil. Trans. Roy. Soc. Lond.B237 (1952) 1–36.

    Google Scholar 

  49. Wiens, A. W., and Gilbert, L. I., Regulation of cockroach fat body metabolism by the corpus cardiacumin vitro. Science150 (1965) 614–616.

    PubMed  Google Scholar 

  50. Wiens, A. W., and Gilbert, L. I., Regulation of carbohydrate mobilization and utilization inLeucophaea maderae. J. Insect Physiol.13 (1967) 779–794.

    Article  PubMed  Google Scholar 

  51. Worm, R. A. A., Characterization of trehalase from locust flight muscle. Comp. biochem. Physiol.70B (1981) 509–514.

    Google Scholar 

  52. Wyatt, G. R., The biochemistry of sugars and polysaccharides in insects. Adv. Insect. Physiol.4 (1967) 287–360.

    Google Scholar 

  53. Yamashita, O., and Suzuki, K., Roles of morphogenetic hormones in embryonic diapause, in: Morphogenic Hormones in Arthropods pp. 82–128. Ed. A. P. Gupta. Rutgers University Press, New Brunswick 1991.

    Google Scholar 

  54. Zebe, E. C., and McShan, W. H., Trehalase in the thoracic muscles of the woodroach,Leucophaea maderae. J. cell. comp. Physiol.53 (1959) 21–29.

    Article  PubMed  Google Scholar 

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Author notes

  1. J. E. Steele

    Present address: Department of Zoology, University of Western Ontario, N6A 5B7, London, Ontario, Canada

Authors and Affiliations

  1. Institut für Zoologie, Johannes-Gutenberg-Universität, Saarstrasse 21, D-55099, Mainz, (Germany)

    A. Becker, P. Schlöder, J. E. Steele & G. Wegener

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Becker, A., Schlöder, P., Steele, J.E. et al. The regulation of trehalose metabolism in insects. Experientia 52, 433–439 (1996). https://doi.org/10.1007/BF01919312

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