Hostname: page-component-77c89778f8-vpsfw Total loading time: 0 Render date: 2024-07-18T14:59:04.708Z Has data issue: false hasContentIssue false

The recruitment of mast cells, exclusively of the mucosal phenotype, into granulomatous lesions caused by the pentastomid parasite Porocephalus crotali: recruitment is irrespective of site

Published online by Cambridge University Press:  06 April 2009

P. McHardy
Affiliation:
Department of Biological Sciences, The University of Dundee, Dundee DD1 4HN, Scotland
J. Riley
Affiliation:
Department of Biological Sciences, The University of Dundee, Dundee DD1 4HN, Scotland
J. F. Huntley
Affiliation:
The Moredun Research Institute, 408 Gilmerton Road, Edinburgh EH17 7JH, Scotland

Summary

Adults of the porocephalid pentastomid Porocephalus crotali infect the lung of rattlesnake definitive hosts and larvae develop in rat intermediate hosts. In the latter, nymphs encyst within a variety of tissue sites (commonly abdominal fat bodies and lungs) and each becomes the focus of an eosinophilic granuloma. From an early stage in infections, granulomas become increasingly infiltrated by mast cells which, using conventional histology and paired immunofluorescence against mast cell proteases, appear to be exclusively of the mucosal phenotype. Mucosal mast cells are concentrated along the dorsal region of the parasite and in a plug of tissue containing degenerating cuticles within independent granulomas, which is located between its head and tail. ELISAs against the rat mast cell proteases I and II (RMCP I and II), extracted from abdominal fat, lung, spleen, liver and kidney granulomas at various intervals post-infection, reveal a substantially elevated concentration of RMCP II in all lesions. In fat, concentrations increase up to about 100 days post-infection, at which time moulting ceases and inflammatory responses subside. RMCP II was scarcely detectable in matched control tissues. Unlike infections with certain nematode parasites, where enteric mucosal mast cells secrete RMCP II systemically, concentrations of RMCP II in the serum of infected rats were significantly reduced when compared with age-matched uninfected controls. These results confirm that P. crotali can selectively recruit mucosal mast cells to a variety of tissue sites, most of which are non-mucosal. Possible mechanisms are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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

Ambrose, N. C. & Riley, J. (1988 a). Light microscope observations of granulomatous reactions against developing Porocephalus crotali (Pentastomida: Porocephalida) in mouse and rat. Parasitology 97, 2742.CrossRefGoogle ScholarPubMed
Ambrose, N. C. & Riley, J. (1988 b). Fine structural aspects of the secretory processes in a pentastomid arthropod parasite in its mouse and rattlesnake hosts. Tissue and Cell 20, 381404.CrossRefGoogle Scholar
Ambrose, N. C. & Riley, J. (1998 c). Studies on the host/parasite interface during the development of a pentastomid arthropod parasite in the rodent intermediate hosts, with observations on protective surface membranes. Tissue and Cell 20, 721–44.CrossRefGoogle Scholar
Ambrose, N. C. & Riley, J. (1989). Further evidence for the protective role of the sub-parietal cell membranous secretory product on the cuticle of a pentastomid arthropod parasite developing in its rodent intermediate host. Tissue and Cell 21, 699722.CrossRefGoogle ScholarPubMed
Chernin, J., Miller, H. R. P., Newlands, G. F. J. & McLaren, D. J.(1988). Proteinase phenotypes and fixation properties of rat mast cells in parasitic lesions caused by Mesocestoides corti: selective and site specific recruitment of mast cell subsets. Parasite Immunology 19, 433–42.CrossRefGoogle Scholar
Claman, H. N. (1985). Mast cells, T cells and abnormal fibrosis. Immunology Today 6, 192–5.CrossRefGoogle ScholarPubMed
Enerback, L. (1966 a). Mast cells in rat gastrointestinal mucosa. 1. Effects of fixation. Acta pathologica et microbiologica scandinavica 66, 289302.CrossRefGoogle Scholar
Enerback, L. (1966 b). Mast cells in the rat gastrointestinal mucosa. 2. Dye binding metachromatic properties. Acta pathologica et microbiologica scandinavica 66, 303–31.CrossRefGoogle ScholarPubMed
Esslinger, J. H. (1962). Development of Porocephalus crotali (Humboldt 1808) (Pentastomidia) in experimental intermediate hosts. Journal of Parasitology 48, 452–6.CrossRefGoogle Scholar
Finkelman, F. D., Pearce, E. J., Urban, J. F. & Sher, A. (1991). In Immunoparasitology Today (ed. Ash, C. and Gallagher, R. B.), pp. A62A66. Cambridge: Elsevier Trends Journals.Google Scholar
Gurish, M. F. & Austen, K. F. (1989). In IgE, Mast Cells and the Allergic Response. Ciba Foundation Symposium 147, pp. 3652. Chichester: Wiley.Google Scholar
Haig, D. M., Jarret, E. E. E. & Tas, J. (1984). In vitro studies on mast cell proliferation in N. brasiliensis infection. Immunology 51, 643–51.Google ScholarPubMed
Huntley, J. F., McGorum, B., Newlands, G. F. J. & Miller, H. R. P. (1984). Granulated intraepithelial lymphocytes: their relationship to mucosal mast cells and globule leucocytes in the rat. Immunology 53, 525–35.Google ScholarPubMed
Huntley, J. G., Newlands, G. F. J., Gibson, S., Ferguson, A. & Miller, H. R. P. (1985). Histochemical demonstration of chymotrypsin like serine esterases in mucosal mast cells in four species including man. Journal of Clinical Pathology 38, 375–84.CrossRefGoogle ScholarPubMed
Huntley, J. F., Mackellar, A., Newlands, G. F. J., Irvine, J. & Miller, H. R. P. (1991). Mapping of rat mast cell granule proteinases RMCP I and II by enzyme-linked immunosorbent assay and paired immunofluorescence. Acta pathologica et microbiologica scandinavica 98, 933–44.CrossRefGoogle Scholar
Irani, A. A. & Schwartz, L. B. (1989). Mast cell heterogeneity: a review. Clinical and Experimental Allergy 19, 143–5.CrossRefGoogle Scholar
Jones, D. A. C. & Riley, J. (1991). An ELISA for the detection of pentastomid infections in the rat. Parasitology 103, 331–7.CrossRefGoogle ScholarPubMed
Jones, D. A. C., Riley, J., Kerby, N. W. & Knox, D. P. (1991). Isolation and preliminary characterisation of a 48 kilodalton metalloproteinase from the excretory/secretory components of the frontal glands of Porocephalus pentastomids. Molecular and Biochemical Parasitology 46, 6172.CrossRefGoogle ScholarPubMed
Jones, D. A. C., Henderson, R. J. & Riley, J. (1992). Preliminary characterization of the lipid and protein components of the surface membranes of a pentastomid Porocephalus crotali. Parasitology 104, 469–78.CrossRefGoogle ScholarPubMed
Kanakura, Y., Thompson, H., Nakano, T., Yamamura, T., Asai, H., Kitamura, Y., Metcalfe, D. & Galli, S. J. (1988). Multiple bidirectional alterations of phenotype and changes in proliferative potential during the in vitro and in vivo passage of clonal mast cell populations derived from mouse peritoneal mast cells. Blood 72, 877–85.CrossRefGoogle ScholarPubMed
Kitamura, Y. & Fujita, J. (1989). Regulation of mast cell differentiation. Bioessays 10, 193–6.CrossRefGoogle ScholarPubMed
Lindsay, M. C. & Williams, J. F. (1985). Hepatic mast cells in rats infected with Taenia taeniaeformis. International Journal for Parasitology 15, 203–9.CrossRefGoogle ScholarPubMed
Marshall, J. S. & Bienenstock, J. (1990). Mast cells. Springer Seminars in Immunopathology 12, 191202.CrossRefGoogle ScholarPubMed
McMenamin, C., Haig, D. M., Gibson, S., Newlands, G. F. J. & Miller, H. R. P. (1987). Phenotypic analysis of mast cell granule proteinases in normal rat bone marrow cultures. Immunology 60, 147–9.Google ScholarPubMed
Miller, H. R. P., Woodbury, R. G., Huntley, J. F., Newlands, G. (1983). Systemic release of mucosal mast cell protease in primed rats challenged with Nippostrongylus brasiliensis. Immunology 49, 471–9.Google ScholarPubMed
Miller, H. R. P. (1987). Immunopathology of nematode infestation and expulsion. In Immunopathology of the Small Intestine (ed. Marsh, M. N.), pp. 177208. New York: John Wiley & Son.Google Scholar
Miller, H. R. P., King, S. J., Gibson, S., Huntley, J. F., Newlands, G. F. J. & Woodbury, R. G. (1986). Intestinal mucosal mast cells in normal and parasitized rats. In Mast Cell Differentiation and Heterogeneity (ed. Befus, et al. ), pp. 239–56. New York: Raven Press.Google Scholar
O'Donnel, M. C., Ackermen, S. J., Gleich, G. J. & Thomas, L. L. (1983). Activation of basophil and mast cell histamine release by eosinophil granule basic protein. Journal of Experimental Medicine 157, 1981–91.CrossRefGoogle Scholar
Riley, J. (1981). An experimental investigation of the development of Porocephalus crotali (Pentastomida: Porocephalida) in the western diamondback rattlesnake (Crotalus atrox). International Journal for Parasitology 11, 127–31.CrossRefGoogle Scholar
Rose, M. E., Ogilvie, B. M. & Bradley, J. W. A. (1980). Intestinal mast cell responses in rats and chickens to coccidiosis with some properties of chicken mast cells. International Archives of Allergy and Applied Immunology 63, 21–9.CrossRefGoogle ScholarPubMed
Ruitenberg, E. J. & Elgersma, A. (1976). Absence of intestinal mast cell response in congenitally athymic mice during Trichinella spiralis infection. Nature, London 264, 258–60.CrossRefGoogle ScholarPubMed
Woodbury, R. G., Gruzenski, G. M. & Lagunoff, D. (1978). Immunofluorescent localisation of a serine protease in rat small intestine. Proceedings of the National Academy of Sciences, USA 75, 2785–9.CrossRefGoogle ScholarPubMed