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The FMRFamide-like neuropeptide AF2 (Ascaris suum) is present in the free-living nematode, Panagrellus redivivus (Nematoda, Rhabditida)

Published online by Cambridge University Press:  06 April 2009

A. G. Maule
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine and Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 INN, Northern Ireland
C. Shaw
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine and Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 INN, Northern Ireland
J. W. Bowman
Affiliation:
The Upjohn Company, Kalamazoo, MI 49001, USA
D. W. Halton
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine and Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 INN, Northern Ireland
D. P. Thompson
Affiliation:
The Upjohn Company, Kalamazoo, MI 49001, USA
T. G. Geary
Affiliation:
The Upjohn Company, Kalamazoo, MI 49001, USA
L. Thim
Affiliation:
Novo Nordisk A/S, 2880 Bagsvaerd, Denmark

Summary

Available primary structural information suggests that the FMRFamide-related peptides (FaRPs) from parasitic and free-living nematodes are different, and that free-living forms may not represent appropriate models for the study of the neurochemistry of parasitic forms in the laboratory. However, here we report the isolation and unequivocal identification of AF2 (originally isolated from the parasite, Ascaris suum) from acidified alcoholic extracts of the free-living species, Panagrellus redivivus. While reverse-phase HPLC analysis of extracts revealed FMRFamide-immunoreactivity to be highly heterogeneous, AF2 was the predominant FMRFamide-immunoreactive peptide present (at least 26 pmol/g wet weight of worms). This peptide was also the major immunoreactant identified by an antiserum raised to the conserved C- terminal hexapeptide amide of mammalian pancreatic polypeptide (PP), which has been used previously to isolate neuropeptide F (NPF). These observations were confirmed by radioimmunoassay and chromatographic fractionation of an acidified alcoholic extract of A. suum heads. The FMRFamide-related peptides present in a nematode extract may be highly dependent on the extraction medium employed, and these data would suggest that this complement of neuropeptides may not be as different between parasitic and free-living nematodes as initial studies have suggested. Finally, all of the evidence suggests that NPF is not present in nematodes and that the PP-immunoreactant previously demonstrated immunochemically is probably AF2.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Brownlee, D. J. A., Fairweather, I., Johnston, C. F., Smart, D., Shaw, C. & Halton, D. W. (1993 a). Immunocytochemical demonstration of neuropeptides in the central nervous system of the roundworm, Ascaris suum (Nematoda, Ascaroidea). Parasitology 106, 305–16.CrossRefGoogle ScholarPubMed
Brownlee, D. J. A., Fairweather, I. & Johnston, C. F. (1993 b). Immunocytochemical demonstration of neuropeptides in the peripheral nervous system of the roundworm Ascaris suum (Nematoda, Ascaroidea). Parasitology Research 79, 302–8.CrossRefGoogle ScholarPubMed
Cowden, C. & Stretton, A. O. W. (1993). AF2, an Ascaris neuropeptide: isolation, sequence and bioactivity. Peptides 14, 423–30.CrossRefGoogle ScholarPubMed
Cowden, C., Stretton, A. O. W. & Davis, A. E. (1989). AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2, 1465–73.CrossRefGoogle ScholarPubMed
Curry, W. J., Shaw, C., Johnston, C. F., Thim, L. & Buchanan, K. D. (1992). Neuropeptide F: Primary structure from the turbellarian, Artioposthia triangulata. Comparative Biochemistry and Physiology 101C, 269–74.Google ScholarPubMed
Ellenby, C. & Smith, L. (1966). Observations on Panagrellus redivivus Goodey, 1945. Journal of Helminthology 40, 323–30.CrossRefGoogle ScholarPubMed
Geary, T. G., Price, D. A., Bowman, J. W., Winterrowd, C. A., Mackenzie, C. D., Garrison, R. D., Williams, J. F. & Friedman, A. R. (1992). Two FMRFamide-like peptides from the free-living nematode Panagrellus redivivus. Peptides 13, 209–14.CrossRefGoogle ScholarPubMed
Leung, P. S., Shaw, C., Maule, A. G., Thim, L., Johnston, C. F. & Irvine, G. B. (1992). The primary structure of neuropeptide F (NPF) from the garden snail, Helix aspersa. Regulatory Peptides 41, 7181.CrossRefGoogle ScholarPubMed
Linacre, A., Kellet, E., Saunders, S., Bright, K., Benjamin, P. R. & Burke, J. F. (1990). Cardioactive neuropeptide Phe-Met-Arg-Phe-NH2 (FMRFamide) and novel related peptides are encoded in multiple copies by a single gene in the snail, Lymnaea stagnalis. Journal of Neuroscience 10, 412–19.Google Scholar
Maule, A. G., Shaw, C., Halton, D. W., Brennan, G. P., Johnston, C. F. & Moore, S. (1992). Neuropeptide F (Moniezia expansa): localization and characterization using specific antisera. Parasitology 105, 505–12.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Curry, W. J. & Thim, L. (1994). RYIRFamide: a turbellarian FM RFamide-related peptide (FaRP). Regulatory Peptides 50, 3743.CrossRefGoogle Scholar
Maule, A. G., Shaw, C., Halton, D. W. & Thim, L. (1993). GNFFRFamide: a novel FMRFamide-immunoreactive peptide isolated from the sheep tapeworm, Moniezia expansa. Biochemical and Biophysical Research Communications 193, 105–46.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Thim, L., Johnston, C. F., Fairweather, I. & Buchanan, K. D. (1991). Neuropeptide F: a novel parasitic flatworm regulatory peptide from Moniezia expansa (Cestoda: Cyclophyllidea). Parasitology 102, 309–16.CrossRefGoogle Scholar
O'hare, M. M. T., Chen, M. H., Tatemoto, K., Buchanan, K. D., Joffe, S. N. & Murphy, R. F. (1983). Lack of cross-reactivity of peptide YY (PYY) and neuropeptide Y (NPY) with antibodies to pancreatic polypeptide (PP) in radioimmunoassay. Clinical Chemistry 29, 1553–4.CrossRefGoogle Scholar
Rosoff, M. L., Burglin, T. R. & Li, C. (1992). Alternatively spliced transcripts of the flp-1 gene encode distinct FMRFamide-like peptides in Caenorhabditis elegans. Journal of Neuroscience 12, 235–66.Google Scholar
Rosoff, M. L., Doble, K. E., Price, D. A. & Li, C. (1993). The flp-1 propeptide is processed into multiple highly similar FMRFamide-like peptides in Caenorhabditis elegans. Peptides 14, 331–8.CrossRefGoogle ScholarPubMed
Saunders, S. E., Bright, K., Kellet, E., Benjamin, P. R. & Burke, J. F. (1991). Neuropeptides Gly-Asp-Pro-Phe-Leu-Arg-Phe-amide (GDPFLRFamide) and Ser-Asp-Pro-Phe-Leu-Arg-Phe-amide (SDPFLRFamide) are encoded by an exon 3' to Phe-Met-Arg-Phe-NH2 (FMRFamide) in the snail, Lynmea stagnalis. Journal of Neuroscience 11, 740–5.CrossRefGoogle ScholarPubMed
Smart, D., Shaw, C., Johnston, C. F., Halton, D. W., Fairweather, I. & Buchanan, K. D. (1992 a). Chromatographic and immunological characterisation of immunoreactivity towards pancreatic polypeptide and neuropeptide Y in the nematode, Ascaris suum. Comparative Biochemistry and Physiology 102C, 477–81.Google ScholarPubMed
Smart, D., Shaw, C., Johnston, C. F., Thim, L., Halton, D. W. & Buchanan, K. D. (1992 b). Peptide tyrosine phenylalanine (PYF): a novel neuropeptide-F-related nonapeptide from the brain of Loligo vulgaris. Biochemical and Biophysical Research Communications 186, 1323–9.CrossRefGoogle ScholarPubMed
Stretton, A. O. W., Cowden, C., Sithigorngul, P. & Davis, R. E. (1991). Neuropeptides in the nematode Ascaris suum. Parasitology 102, S107–16.CrossRefGoogle ScholarPubMed
Stretton, A. O. W., Donmoyer, J., Davis, R., Meade, J., Cowden, C. & Sithigorngul, P. (1992). Motor activity and motor nervous system function in the nematode Ascaris suum. Journal of Parasitology 78, 206–14.CrossRefGoogle ScholarPubMed
Walker, R. J. (1992). Neuroactive peptides with an RFamide or Famide carboxyl terminal. Comparative Biochemistry and Physiology 102C, 213–22.Google ScholarPubMed