Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T13:40:04.607Z Has data issue: false hasContentIssue false
  • English
  • Français

The detection of AKH/HrTH-like peptides in Ascaridia galli and Ascaris suum using an insect hyperglycaemic bioassay

Published online by Cambridge University Press:  06 April 2009

T. R. B. Davenport ,
L. A. Eaves ,
T. K. Hayes ,
D. L. Lee  and
R. E. Isaac
T. R. B. Davenport
Affiliation:
Department of Pure and Applied Biology, University of Leeds, Leeds LS2 9JT, UK
L. A. Eaves
Affiliation:
Department of Pure and Applied Biology, University of Leeds, Leeds LS2 9JT, UK
T. K. Hayes
Affiliation:
Department of Entomology, Texas A&M University, College Station, TX 77843-2475, USA
D. L. Lee
Affiliation:
Department of Pure and Applied Biology, University of Leeds, Leeds LS2 9JT, UK
R. E. Isaac
Affiliation:
Department of Pure and Applied Biology, University of Leeds, Leeds LS2 9JT, UK
Get access Rights & Permissions [Opens in a new window]

Summary

Evidence for the presence of adipokinetic hormone/hypertrehalosaemic hormone (AKH/HrTH)-like peptides in the parasitic nematodes Ascaridia galli and Ascaris suum has been obtained using insect bioassays which measure hyperglycaemic responses to peptides belonging to the AKH/HrTH family of insect hormones. A peptide fraction extracted from heads and tails of Ascaridia galli evoked a dose-dependent hyperglycaemic response when injected into the cockroach, Periplaneta americana. Maximal bioactivity was obtained with material that was equivalent to 38 mg (wet weight) of nematode. Bioactivity appeared to be highest in extracts from heads and tails of both male and female worms and could be fractionated into at least three peaks of hyperglycaemic activity by reversed-phase high-performance liquid chromatography. An extract from heads and tails of A. suum also evoked a hyperglycaemic response when injected into the cockroach, Blaberus discoidalis. The bioactivity was inactivated on incubation with pure endopeptidase 24.11, confirming the peptidic nature of the bioactive material. These results provide evidence for the existence of peptides related to the insect AKH/HrTH family of peptides in parasitic nematodes.

Keywords

Ascaridia galliAscaris suumnematodesadipokinetic hormone/hypertrehalosaemic hormone
Type
Research Article
Information
Parasitology , Volume 108 , Issue 4 , May 1994 , pp. 479 - 485
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Davenport, T. R. B. (1990). Studies on neuropeptides in free-living and animal parasitic nematodes. Ph.D. Thesis, University of Leeds.Google Scholar
Davenport, T. R. B., Isaac, R. E. & Lee, D. L. (1991). The presence of peptides related to the adipokinetic hormone/red pigment-concentrating hormone family in the nematode Panagrellus redivivus. General and Comparative Endocrinology 81, 419–25.CrossRefGoogle Scholar
Ephrussi, B. E. & Beadle, G. W. (1936). Transplantation Technique, Drosophila. Nature, London 70, 218–25.Google Scholar
Fernlund, P. & Josefsson, L. (1972). Crustacean color-change hormone: amino acid sequence and chemical synthesis. Science 177, 173–5.CrossRefGoogle ScholarPubMed
Gade, G. (1980). Further characteristics of adipokinetic and hyperglycaemic factors of stick insects. Journal of Insect Physiology 26, 351–60.CrossRefGoogle Scholar
Gade, G. (1984). Adipokinetic and hyperglycaemic factors of different insect species: separation with high performance liquid chromatography. Journal of Insect Physiology 30, 729–36.CrossRefGoogle Scholar
Gade, G. (1989). The hypertrehalosaemic peptides of cockroaches: A phylogenetic study. General and Comparative Endocrinology 75, 287–300.CrossRefGoogle ScholarPubMed
Gade, G. (1990 a). The adipokinetic hormone/red pigment-concentrating hormone peptide family: Structures, interrelationships and functions. Journal Of Insect Physiology 36, 1–12.CrossRefGoogle Scholar
Gade, G. (1990 b). The putative ancestral peptide of the adipokinetic/red-pigment-concentrating hormone family isolated and sequenced from a dragonfly. Biological Chemistry Hoppe-Seyler 371, 475–83.CrossRefGoogle ScholarPubMed
Gade, G. (1991 a). Hyperglycaemia or hypertrehalosaemia? The effect of insect neuropeptides on haemolymph sugars. Journal of Insect Physiology 37, 483–7.CrossRefGoogle Scholar
Gade, G. (1991 b). A unique charged tyrosine-containing member of the adipokinetic/red-pigment-concentrating hormone peptide family isolated and sequenced from two beetle species. The Biochemical Journal 275, 671–7.CrossRefGoogle Scholar
Gade, G. (1991 c). The adipokinetic neuropeptide of Mantodea: sequence elucidation and evolutionary relationships. Biological Chemistry Hoppe-Seyler 372, 193–201.CrossRefGoogle ScholarPubMed
Gade, G. (1992). Structure-activity relationships for the carbohydrate-mobilising action of further bioanalogues of the adipokinetic hormone/red pigment-concentrating hormone family of peptides. Journal of Insect Physiology 38, 259–66.CrossRefGoogle Scholar
Gade, G. & Rinehart, K. L. (1987 a). Primary sequence analysis by fast atom bombardment mass spectrometry of a peptide with adipokinetic activity from the corpora cardiaca of the cricket Gryllus bimaculatus. Biochemical and Biophysical Research Communications 149, 908–14.CrossRefGoogle ScholarPubMed
Gade, G. & Rinehart, K. L. (1987 b). Primary structure of the hypertrehalosemic factor II from the corpus cardiacum of the Indian stick Insect, Carausius morosus, determined by fast atom bombardment mass spectrometry. Biological Chemistry Hoppe-Seyler 368, 67–75.CrossRefGoogle ScholarPubMed
Gade, G. & Rosinski, G. (1990). The primary structure of the hypertrehalosemic neuropeptide from tenebrionid beetles: a novel member of the AKH/RPCH family. Peptides 11, 455–9.CrossRefGoogle ScholarPubMed
Gade, G. & Kellner, R. (1992). Primary structures of the hypertrehalosemic peptides from corpora cardiaca of the primitive cockroach Polyphaga aegyptiaca. General and Comparative Endocrinology 86, 119–27.CrossRefGoogle ScholarPubMed
Gade, G., Hilbich, C., Beyreuther, K. & Rinehart, K. L. (1988). Sequence analyses of two neuropeptides of the AKH/RPCH-family from the lubber Grasshopper, Romalea microptera. Peptides 9, 681–8.CrossRefGoogle ScholarPubMed
Gade, G., Wilps, H. & Kellner, R. (1990). Isolation and structure of a novel charged member of the red-pigment-concentrating hormone/adipokinetic hormone family of peptides isolated from the corpora cardiaca of the blowfly Phormia terraenovae (Diptera). Biochemical Journal 269, 309–13.CrossRefGoogle ScholarPubMed
Hayes, T. K. & Keeley, L. L. (1985). Properties of an in vitro bioassay for hypertrehalosemic hormone of Blaberus discoidalis cockroaches. General and Comparative Endocrinology 57, 246–56.CrossRefGoogle Scholar
Hayes, T. K. & Keeley, L. L. (1990). Structure-activity relationships on hyperglycemia by representatives of the adipokinetic/hyperglycemic hormone family in Blaberus discoidalis cockroaches. Journal of Comparative Physiology 160, 187–94.CrossRefGoogle ScholarPubMed
Hayes, T. K., Keeley, L. L. & Knight, D. W. (1986). Insect hypertrehalosemic hormone: isolation and primary structure from Blagberus discoidalis cockroaches. Biochemical and Biophysical Research Communications 140, 674–8.CrossRefGoogle ScholarPubMed
Holman, G. M., Nachman, R. J., Schoofs, L., Hayes, T. K., Wright, M. S. & Deloof, A. (1991). The Leucophaea maderae hindgut preparation; a rapid and sensitive bioassay tool for the isolation of insect myotropins of other insect species. Insect Biochemistry 21, 107–12.CrossRefGoogle Scholar
Isaac, R. E. (1988). Neuropeptide-degrading endopeptidase activity of locust (Schistocerca gregaria) synaptic membranes. The Biochemical Journal 255, 843–7.CrossRefGoogle ScholarPubMed
Isaac, R. E., Eaves, L., Muimo, R. & Lamango, N. (1991). N-acetylation of biogenic amines in Ascaridia galli. Parasitology 102, 445–50.CrossRefGoogle ScholarPubMed
Jaffe, H., Raina, A. K., Riley, C. T., Fraser, B. A., Bird, T. G., Tseng, C., Zhang, Y. S. & Hayes, D. K. (1988). Isolation and primary structure of a neuropeptide hormone from Heliothis zea with hypertrehalosaemic and adipokinetic activities. Biochemical and Biophysical Research Communications 155, 344–50.CrossRefGoogle Scholar
Jaffe, H., Raina, A. K., Riley, C. T., Fraser, B. A., Nachman, R. J., Vogel, V. W., Zhang, Y. S. & Hayes, D. K. (1989). Primary structure of two neuropeptide hormones with adipokinetic and hypertrehalosaemic Nematode AKH/HrTH-like peptides activity isolated from the corpora cardiaca of horse flies (Diptera). Proceedings of the National Academy of Sciences, USA 86, 8161–4.CrossRefGoogle Scholar
Keeley, L. L., Hayes, T. K., Bradfield, J. Y. & Sowa, S. M. (1991). Physiological actions by hypertrehalosaemic hormone and adipokinetic hormone peptides in adult Blaberus discoidalis cockroaches. Insect Biochemistry 21, 121–9.CrossRefGoogle Scholar
Lamango, N. S. & Isaac, R. E. (1993). Metabolism of insect neuropeptides: properties of a membrane-bound endopeptidase from heads of Musca domestica. Insect Biochemistry and Molecular Biology 23, 801–8.CrossRefGoogle ScholarPubMed
Orchard, I. (1987). Adipokinetic hormones – an update. Journal of Insect Physiology 33, 451–63.CrossRefGoogle Scholar
O'Shea, M. (1986). Insect neuropeptides: pure and applied. In Insect Neurochemistry and Neurophysiology(ed. Borkovek, A. B. & Gelman, D. B.), pp. 3–27. Clifton, New Jersey: Humana Press.Google Scholar
O'Shea, M. & Schaffer, M. (1985). Neuropeptide function: the invertebrate contribution. Annual Reviews in Neuroscience 8, 171–98.CrossRefGoogle ScholarPubMed
Roe, J. H. (1955). The determination of sugar in blood and spinal fluid with anthrone reagent. Journal of Biological Chemistry 212, 335–43.CrossRefGoogle ScholarPubMed
Scarborough, R. M., Jamieson, G. C., Kalish, F., Kramer, S. J., McEnroe, G. A., Miller, C. A. & Schooley, D. A. (1984). Isolation and primary structure of two peptides with cardioacceleratory and hyperglycemic activity from the corpora cardiaca of Periplaneta americana. Proceedings of the National Academy of Sciences, USA 81, 5575–9.CrossRefGoogle ScholarPubMed
Schooneveld, H. (1986). Localisation of AKH/RPCH-related peptides in insects and other invertebrates. In Insect Neurochemistry and Neurophysiology (ed. Borkovek, A. B. & Gelman, D. B.), pp. 443–6. Clifton, New Jersey: Humana Press.Google Scholar
Schooneveld, H., Romberg-Privee, H. M. & Veenstra, J. A. (1985). Adipokinetic hormone-immunoreactive peptide in the endocrine and central nervous system of several insect species: a comparative immunocytochemical approach. General and Comparative Endocrinology 57, 184–94.CrossRefGoogle ScholarPubMed
Schooneveld, H., Van Herp, F. & Van Minnen, J. (1987). Demonstration of substances immunologically related to the identified arthropod neuropeptides AKH/RPCH in the CNS of several invertebrate species. Brain Research 406, 224–32.CrossRefGoogle Scholar
Siegert, K. J., Morgan, P. & Mordue, W. (1985). Primary structures of locust adipokinetic hormones. II. Biological Chemistry Hoppe-Seyler 366, 723–7.CrossRefGoogle ScholarPubMed
Smart, D., Shaw, C., Curry, W. J., Jonston, C. F., Thim, L., Halton, D. W. & Buchanan, K. D. (1992). The primary structure of TE-6: a novel neuropeptide from the nematode Ascaris suum. Biochemical and Biophysical Research Communications 187, 1323–9.CrossRefGoogle ScholarPubMed
Stone, J. V., Mordue, W., Batley, K. E. & Morris, H. R. (1976). Structure of locust adipokinetic Hormone, a neurohormone that regulates lipid utilisation during flight. Nature, London 236, 207–11.CrossRefGoogle Scholar
Stretton, A. O. W. (1992). Chemical intercellular signalling mechanisms in the nervous system of the nematode Ascaris suum; potential sites of action of new generations of anthelmintic drugs. In Neurotox ′91: Molecular Basis of Drug and Pesticide Action (ed. Duce, I. R.), pp. 123–38. London: Elsevier Applied Science.CrossRefGoogle Scholar
Weeda, E. (1981). Hormonal regulation of proline synthesis and glucose release in the fat body of the Colorado potato Beetle, Leptinotarsa decemlineata. Journal of Insect Physiology 27, 411–17.CrossRefGoogle Scholar
Ziegler, R., Kegel, G. & Keller, R. (1984). Isolation and amino acid composition of the adipokinetic hormone of Manduca sexta. Hoppe-Seyler's Zeitschrift für physiologische Chemie 365, 1451–6.CrossRefGoogle ScholarPubMed