Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-27T19:17:05.333Z Has data issue: false hasContentIssue false
  • English
  • Français

Localization of Diploptera punctata allatostatin-like immunoreactivity in helminths: an immunocytochemical study

Published online by Cambridge University Press:  06 April 2009

D. Smart ,
C. F. Johnston ,
A. G. Maule ,
D. W. Halton ,
G. Hrcková ,
C. Shaw  and
K. D. Buchanan
D. Smart
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine, The Queen's University of Belfast, Belfast, Northern Ireland, UK
C. F. Johnston
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine, The Queen's University of Belfast, Belfast, Northern Ireland, UK
A. G. Maule
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine, The Queen's University of Belfast, Belfast, Northern Ireland, UK
D. W. Halton
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of and Biology and Biochemistry, The Queen's University of Belfast, Belfast, Northern Ireland, UK
G. Hrcková
Affiliation:
Parasitological Institute, Slovak Academy of Sciences, 040 01 Kosice, Slovak Republic
C. Shaw
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine, The Queen's University of Belfast, Belfast, Northern Ireland, UK
K. D. Buchanan
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine, The Queen's University of Belfast, Belfast, Northern Ireland, UK
Get access Rights & Permissions [Opens in a new window]

Extract

The nervous systems of helminths are predominantly peptidergic in nature, although it is likely that the full range of regulatory peptides used by these organisms has yet to be elucidated. Attempts to identify novel helminth neuropeptides are being made using immunocytochemistry with antisera raised against peptides isolated originally from insects. One of these antisera was raised against allatostatin III, a peptide isolated originally from the cockroach, Diploptera punctata, and a member of a family of related peptides found in insects. Allatostatin immunoreactivity was found throughout the nervous systems of Mesocestoides corti tetrathyridia, and adult Moniezia expansa, Diclidophora merlangi, Fasciola hepatica, Schistosoma mansoni, Ascaris suum and Panagrellus redivivus. Immunostaining was observed in the nerve cords and anterior ganglia of all the helminths. It was also apparent in the subtegumental nerves and around the reproductive apparatus of the flatworms, in neurones in the pharynx of D. merlangi, F. hepatica, A. suum and P. redivivus, and in fibres innervating the anterior sense organs in the nematodes. Immunostaining in all species was both reproducible and specific in that it could be abolished by pre-absorption of the antiserum with allatostatins I–IV. These results suggest that molecules related to the D. punctata allatostatins are important components in the nervous systems of a number of helminth parasites, and a free-living nematode. Their distribution within the nervous system suggests they function as neurotransmitters/neuromodulators with roles in locomotion, feeding, reproduction and sensory perception.

Keywords

allatostatinneuropeptideMonogenoideaTrematodaCestodaNematodaimmunocytochemistrynervous system
Type
Research Article
Information
Parasitology , Volume 110 , Issue 1 , January 1995 , pp. 87 - 96
Copyright
Copyright © Cambridge University Press 1995

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

Angstadt, J. D., Donmoyer, J. E. & Stretton, A. O. W. (1989). Retrovesicular ganglion of the nematode Ascaris. Journal of Comparative Neurology 284, 374–88.CrossRefGoogle ScholarPubMed
Barnes, R. S. K., Calow, P. & Olive, P. J. W. (1993). The Invertebrates: a New Synthesis. Oxford: Blackwell Scientific Publications.Google Scholar
Barrett, J. & Butterworth, P. E. (1984). Acetaldehyde formation by mitochondria from the free-living nematode Panagrellus redivivus. The Biochemical Journal 221, 535–40.CrossRefGoogle ScholarPubMed
Cowden, C., Sithigorngul, P., Brackley, P., Guastella, J. & Stretton, A. O. W. (1993). Localisation and differential expression of FMR Farnide-like immunoreactivity in the nematode Ascaris suum. Journal of Comparative Neurology 333, 455–68.CrossRefGoogle Scholar
Duve, H., Johnsen, A. H., Scott, A. G., Yu, C. G., Yagi, K. J., Tobe, S. S. & Thorpe, A. (1993). Callatostatins–neuropeptides from the blowfly Calliphora vomitoria with sequence homology to cockroach allatostatins. Proceedings of the National Academy of Sciences, USA 90, 2456–60.CrossRefGoogle ScholarPubMed
Geary, T. G., Klein, R. D., Vanover, L., Bowman, J. W. & Thompson, D. P. (1992). The nervous systems of helminths as targets for drugs. Journal of Parasitology 78, 15–230.CrossRefGoogle ScholarPubMed
Halton, D. W., Shaw, C., Maule, A. G., Johnston, C. F. & Fairweather, I. (1992). Peptidergic messengers: A new perspective of the nervous system of parasitic platyhelminths. Journal of Parasitology 78, 179–93.CrossRefGoogle ScholarPubMed
Halton, D. W., Shaw, C., Maule, A. G. & Smart, D. (1994). Regulatory peptides in helminth parasites. Advances in Parasitology 34 (in the Press).CrossRefGoogle ScholarPubMed
Hrcková, G., Halton, D. W., Maule, A. G., Brennan, G. P., Shaw, C. & Johnston, C. F. (1993). Neuropeptide F-immunoreactivity in the tetrathyridium of Mesocestoides corti (Cestoda: Cyclophyllidea). Parasitology Research 79, 690–5.CrossRefGoogle ScholarPubMed
Johnston, C. F., Shaw, C., Halton, D. W. & Fairweather, I. (1990). Confocal scanning laser microscopy and helminth neuroanatomy. Parasitology Today 6, 305–8.CrossRefGoogle ScholarPubMed
Kramer, S. J., Toschi, A., Miller, C. A., Kataoka, H., Quistad, G. B., Li, J. P., Carney, R. L. & Schooley, D. A. (1991). Identification of an allatostatin from the tobacco hornworm, Manduca sexta. Proceedings of the National Academy of Sciences, USA 88, 9458–62.CrossRefGoogle ScholarPubMed
Magee, R. M., Fairweather, I., Johnston, C. F., Halton, D. W. & Shaw, C. (1989). Immunocytochemical demonstration of neuropeptides in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology 98, 227–38.CrossRefGoogle ScholarPubMed
Maule, A. G., Brennan, G. P., Halton, D. W., Shaw, C., Johnston, C. F. & Moore, S. (1992). Neuropeptide F-immunoreactivity in the monogenean parasite Diclidophora merlangi. Parasitology Research 78, 655–60.CrossRefGoogle ScholarPubMed
Maule, A. G., Halton, D. W., Johnston, C. F., Shaw, C. & Fairweather, I. (1990 a). The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite, Diclidophora merlangi: a cytochemical study. Parasitology 100, 255–73.CrossRefGoogle ScholarPubMed
Maule, A. G., Halton, D. W., Johnston, C. F., Shaw, C. & Fairweather, I. (1990 b). A cytochemical study of the serotoninergic, cholinergic and peptidergic components of the reproductive system of the monogenean parasite, Diclidophora merlangi. Parasitology Research 76, 409–19.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
Maule, A. G., Halton, D. W., Shaw, C. & Johnston, C. F. (1993 a). The cholinergic, serotoninergic and peptidergic components of the nervous system of Moniezia expansa (Cestoda, Cyclophyllidea). Parasitology 106, 429–40.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W. & Thim, L.(1993 b). GNFFRFamide: a novel FMRFamide-immunoreactive peptide isolated from the sheep tapeworm, Moniezia expansa. Biochemical and Biophysical Research Communications 193, 1054–60.CrossRefGoogle ScholarPubMed
Pratt, G. E., Farnsworth, D. E., Fok, K. F., Siegel, N. R., McCormack, A. L., Shabanowitz, J., Hunt, D. F. & Feyereisen, R. (1991). Identity of a second type of allatostatin from cockroach brains: An octadecapeptide amide with a tyrosine-rich address sequence. Proceedings of the National Academy of Sciences, USA 88, 2412–16.CrossRefGoogle ScholarPubMed
Sithigorngul, P., Stretton, A. O. W. & Cowden, C. (1990). Neuropeptide diversity in Ascaris: An immunocytochemical study. Journal of Comparative Neurology 294, 362–76.CrossRefGoogle ScholarPubMed
Skuce, P. J., Johnston, C. F., Fairweather, I., Halton, D. W., Shaw, C. & Buchanan, K. D. (1990). Immunoreactivity to the pancreatic polypeptide family in the nervous system of the adult human blood fluke, Schistosoma mansoni. Cell and Tissue Research 261, 573–81.CrossRefGoogle Scholar
Smart, D., Johnston, C. F., Curry, W. J., Shaw, C., Halton, D. W., Fairweather, I. & Buchanan, K. D. (1992). Immunoreactivity to two specific regions of chromogranin A in the nervous system of Ascaris suum: An immunocytochemical study. Parasitology Research 78, 329–35.CrossRefGoogle ScholarPubMed
Smart, D., Johnston, C. F., Curry, W. J., Williamson, R., Maule, A. G., Skuce, P. J., Shaw, C., Halton, D. W. & Buchanan, K. D. (1994). Peptides related to the Diploptera punctata allatostatins in non-arthropod invertebrates: An immunocytochemical survey. Journal of Comparative Neurology (in the Press).CrossRefGoogle Scholar
Smart, D., Johnston, C. F., Shaw, C., Halton, D. W. & Buchanan, K. D. (1993). Use of specific antisera for the localisation and quantitation of leucokinin immunoreactivity in the nematode, Ascaris suum. Comparative Biochemistry and Physiology 106C, 517–22.Google ScholarPubMed
Stretton, A. O. W., Cowden, C., Sithigorngul, P. & Davis, R. E. (1991). Neuropeptides in the nematode Ascaris suum. Parasitology 102, S107–S116.CrossRefGoogle ScholarPubMed
Weaver, R. J., Freeman, Z. A., Pickering, M. G. & Edwards, J. P. (1994). Identification of two allatostatins from the CNS of Periplaneta americana: novel members of a family of neuropeptide inhibitors of insect juvenile hormone biosynthesis. Comparative Biochemistry and Physiology 107C, 119–27.Google Scholar
White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London, Series B 314, 1–340.Google ScholarPubMed
Woodhead, A. P., Stay, B., Seidel, S. L., Khan, M. A. & Tobe, S. S. (1989). Primary structure of four allatostatins: Neuropeptide inhibitors of juvenile hormone synthesis. Proceedings of the National Academy of Sciences, USA 86, 5997–6001.CrossRefGoogle ScholarPubMed
Woodhead, A. P., Stoltzman, C. A. & Stay, B. (1992). Allatostatins in the nerves of the antennal pulsatile organ muscle of the cockroach, Diploptera punctata. Archives of Insect Biochemistry and Physiology 20, 253–63.CrossRefGoogle ScholarPubMed