Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-23T22:34:32.307Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro metabolism of an insect neuropeptide by homogenates of the nematode Caenorhabditis elegans

Published online by Cambridge University Press:  12 April 2024

E.P. Masler
E.P. Masler*
Affiliation:
Nematology Laboratory, United States Department of Agriculture, Agricultural Research Service, 10300 Baltimore Blvd, R-165B, B-011A, BARC-West, Beltsville, MD 20705, USA
*
*Author for correspondence Fax: 301 504 5589 Email: [email protected] Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture.
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The cytosolic fraction of homogenates from the free-living soil nematode Caenorhabditis elegans is capable of metabolizing the insect neuropeptide adipokinetic hormone, a decapeptide blocked at the N-terminus by a pGlu residue. Analysis of digests by RP-HPLC and LC-MS revealed that an initial endoproteolytic cleavage step produced a heptapeptide with an unblocked N-terminus that can serve as a substrate for aminopeptidases. The aminopeptidase activity is depressed in the presence of the inhibitor amastatin; the initial product of the endoproteolytic step accumulates during incubation, and expected aminopeptidase product peptides are reduced in amount, as assessed by chromatographic peak size. The absence of some expected peptide fragments in the reaction mixtures suggests that multiple proteases contribute to short peptide half-lives. Comparison of the adipokinetic hormone digestion in C. elegans to that reported previously for insects reveals the same general pattern of peptide fragment production.

Type
Review Article
Information
Journal of Helminthology , Volume 77 , Issue 1 , March 2003 , pp. 43 - 48
Copyright
Copyright © Cambridge University Press 2003

References

Baset, H.A., Ford-Hutchinson, A.W. & O'Neill, G.P. (1998) Molecular cloning and functional expression of a Caenorhabditis elegans aminopeptidase structurally related to mammalian leukotriene A4 hydrolases. Journal of Biological Chemistry 273, 27978–27987.CrossRefGoogle ScholarPubMed
Brownlee, D.J.A. & Fairweather, I. (1999) Exploring the neurotransmitter labyrinth in nematodes. Trends in Neurosciences 22, 16–24.CrossRefGoogle ScholarPubMed
Chitwood, D.J., Lusby, W.R., Thompson, M.J., Kochansky, J.P. & Howarth, O.W. (1995) The glycosylceramides of the nematode Caenorhabditis elegans contain an unusual, branched-chain sphingoid base. Lipids 30, 567–573.CrossRefGoogle ScholarPubMed
Coates, D., Siviter, R. & Isaac, R.E. (2000) Exploring the Caenorhabditis elegans and Drosophila melanogaster genomes to understand neuropeptide and peptidase function. Biochemical Society Transactions 28, 464–469.CrossRefGoogle ScholarPubMed
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, 419–425.CrossRefGoogle Scholar
Davenport, T.R.B., Eaves, L.A., Hayes, T.K., Lee, D.L. & Isaac, R.E. (1994) The detection of AKH/HrTH-like peptides in Ascaridia galli and Ascaris suum using an insect hyperglycaemic bioassay. Parasitology 108, 479–485.CrossRefGoogle ScholarPubMed
Davis, R.E. & Stretton, A.O.W (1995) Neurotransmitters of helminths. pp. 257–287 in Marr, J.J. & Muller, M. (Eds) Biochemistry and molecular biology of parasites. New York, Academic Press.CrossRefGoogle Scholar
Davis, R.E. & Stretton, A.O.W. (2001) Structure-activity relationships of 18 endogenous neuropeptides on the motonervous system of the nematode Ascaris suum . Peptides 22, 7–23.CrossRefGoogle Scholar
Day, T.A. & Maule, A.G. (1999) Parasitic peptides. The structure and function of neuropeptides in parasitic worms. Peptides 20, 999–1019.CrossRefGoogle ScholarPubMed
Isaac, R.E., Siviter, R.J., Stancombe, P., Coates, D. & Shirras, A.D. (2000) Conserved roles for peptidases in the processing of invertebrate neuropeptides. Biochemical Society Transactions 28, 460–464.CrossRefGoogle ScholarPubMed
Keller, R. (1992) Crustacean neuropeptides: structures, functions and comparative aspects. Experientia 48, 439–448.CrossRefGoogle ScholarPubMed
Kimber, M.J., Fleming, C.C., Bjourson, A.J., Halton, D.W.J. & Maule, A.G. (2001) FMRFamide-related peptides in potato cyst nematodes. Molecular and Biochemical Parasitology 116, 199–208.CrossRefGoogle ScholarPubMed
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, 801–808.CrossRefGoogle ScholarPubMed
Laurent, V., Brooks, D.R., Coates, D. & Isaac, R.E. (2001) Functional expression and characterization of the cytoplasmic aminopeptidase P of Caenorhabditis elegans . European Journal of Biochemistry 20, 5430–5438.CrossRefGoogle Scholar
Masler, E.P. (2002) Aminopeptidases in Caenorhabditis elegans and Panagrellus redivivus: detection using peptide and non-peptide substrates. Journal of Helminthology 76, 45–52.CrossRefGoogle ScholarPubMed
Masler, E.P., Wagner, R.M. & Kovaleva, E.S. (1996) In vitro metabolism of an insect neuropeptide by neural membrane preparations from Lymantria dispar . Peptides 17, 321–326.CrossRefGoogle ScholarPubMed
Masler, E.P., Kovaleva, E.S. & Sardanelli, S.S. (2001) Aminopeptidase-like activities in Caenorhabditis elegans and the soybean cyst nematode, Heterodera glycines . Journal of Helminthology 75, 267–272.Google ScholarPubMed
Muneoka, Y. & Kobayashi, M. (1992) Comparative aspects of structure and action of molluscan neuropeptides. Experientia 48, 448–456.CrossRefGoogle ScholarPubMed
Nassel, D.R. (1993) Neuropeptides in the insect brain: a review. Cell and Tissue Research 273, 1–29.CrossRefGoogle ScholarPubMed
Nelson, L.S., Kim, K., Memmott, J.E. & Li, C. (1998) FMRFamide-related gene family in the nematode, Caenorhabditis elegans . Molecular Brain Research 58, 103–111.CrossRefGoogle ScholarPubMed
Rayne, R.C. & O'Shea, M. (1992) Inactivation of neuropeptide hormones (AKH I and AKH II) studied in vivo and in vitro . Insect Biochemistry and Molecular Biology 22, 25–34.CrossRefGoogle Scholar
Reinitz, C.A., Herfel, H.G., Messinger, L.A. & Stretton, A.O. (2000) Changes in locomotory behavior and cAMP produced in Ascaris suum or Caenorhabditis elegans . Molecular and Biochemical Parasitology 111, 185–197.CrossRefGoogle ScholarPubMed
Sajid, M. & Isaac, R.E. (1995) Identification and properties of a neuropeptide-degrading endopeptidase (neprilysin) of Ascaris suum muscle. Parasitology 111, 599–608.CrossRefGoogle ScholarPubMed
Sajid, M., Keating, C., Holden-Dye, L., Harrow, I.D. & Isaac, R.E. (1996) Metabolism of AF1 (KNEFIRF-NH2) in the nematode, Ascaris suum, by aminopeptidase, endopeptidase and deamidase enzymes. Molecular and Biochemical Parasitology 75, 159–168.CrossRefGoogle ScholarPubMed
Sajid, M., Isaac, R.E. & Harrow, I.D. (1997) Purification and properties of a membrane aminopeptidase from Ascaris suum muscle that degrades neuropeptides AF1 and AF2. Molecular and Biochemical Parasitology 89, 225–234.CrossRefGoogle ScholarPubMed
Shaw, C. (1996) Neuropeptides and their evolution. Parasitology 113, S35–S45.CrossRefGoogle ScholarPubMed
Smart, D., Johnston, C.F., Maule, A.G., Halton, D.W., Hrckova, G., Shaw, C. & Buchanan, K.D. (1995) Localization of Diploptera punctata allatostatin-like immunoreactivity in helminths: an immunocytochemical study. Parasitology 110, 87–96.CrossRefGoogle ScholarPubMed
Turner, A.J., Isaac, R.E. & Coates, D. (2001) The neprilysin (NEP) family of zinc metalloendopeptidases: genomics and function. Bioessays 23, 261–269.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Waggoner, L.E., Hardaker, L.A., Golik, S. & Schafer, W.R. (2000) Effect of a neuropeptide gene on behavioral states in Caenorhabditis elegans egg-laying. Genetics 154, 1181–1192.CrossRefGoogle ScholarPubMed