Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-23T11:47:40.743Z Has data issue: false hasContentIssue false
  • English
  • Français

Mucosal mast cells and nematode infection: strain-specific differences in mast cell precursor frequency revisited

Published online by Cambridge University Press:  12 April 2024

J.K. Brown ,
S.H. Wright  and
H.R.P. Miller
J.K. Brown
Affiliation:
Department of Veterinary Clinical Studies and The Wellcome Trust Centre for Research in Comparative Respiratory Medicine, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Veterinary Centre, Easter Bush, Roslin, Midlothian, EH25 9RG, UK.
S.H. Wright
Affiliation:
Department of Veterinary Clinical Studies and The Wellcome Trust Centre for Research in Comparative Respiratory Medicine, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Veterinary Centre, Easter Bush, Roslin, Midlothian, EH25 9RG, UK.
H.R.P. Miller*
Affiliation:
Department of Veterinary Clinical Studies and The Wellcome Trust Centre for Research in Comparative Respiratory Medicine, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Veterinary Centre, Easter Bush, Roslin, Midlothian, EH25 9RG, UK.
*
* Author for correspondence Fax: 44 (0) 131 650 6588 E-mail: [email protected].
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.

Mucosal mast cells (MMC) play an important role in the immune response against selected species of intestinal nematode. The kinetics with which different strains of inbred mice resolve infection with Trichinella spiralis correlates with their ability to mount MMC responses in the intestinal mucosa. Homologues of MMC that express and constitutively secrete abundant amounts of the granule chymase, mouse mast cell protease-1 (mMCP-1), can be generated in vitro from bone marrow cultures supplemented with interleukins-3 and -9, stem cell factor and transforming growth factor-β1. Using the enhanced growth characteristics of these MMC homologues, a novel limiting dilution assay for mast cell precursor (MCp) frequency has been developed. The assay is highly specific, in that cultures containing mast cells are identified with mMCP-1 specific antibody, and almost three-fold more sensitive than previously published systems. MCp frequencies were compared in BALB/c and C57/BL10 strains of mice that, respectively, respond rapidly and slowly to infection with T. spiralis. MCp frequency (1/378 bone marrow cells) was significantly greater (P<0.05) in BALB/c than C57/BL10 mice (frequency: 1/751). Similarly the rate of growth of MMC homologues and the production of mMCP-1 was significantly (P<0.05) greater in BALB/c than in C57/BL10 bone marrow cultures.

Type
Research Article
Information
Journal of Helminthology , Volume 77 , Issue 2 , June 2003 , pp. 155 - 161
Copyright
Copyright © Cambridge University Press 2003

References

Artis, D., Humphreys, N.E., Potten, C.S., Wagner, N., Muller, W., McDermott, J.R., Grencis, R.K. & Else, K.J. (2000) Beta7 integrin-deficient mice: delayed leukocyte recruitment and attenuated protective immunity in the small intestine during enteric helminth infection. European Journal of Immunology 30, 1656–1664.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Ashman, R.I., Jarboe, D.L., Conrad, D.H. & Huff, T.F. (1991) The mast cell-committed progenitor In vitro generation of committed progenitors from bone marrow. Journal of Immunology 146, 211–216.CrossRefGoogle ScholarPubMed
Dillon, S.B. & MacDonald, T.T. (1986) Limit dilution analysis of mast cell precursor frequency in the gut epithelium of normal and Trichinella spiralis infected mice. Parasite Immunology 8, 503–511.CrossRefGoogle ScholarPubMed
Donaldson, L.E., Schmitt, E., Huntley, J.F., Newlands, G.F. & Grencis, R.K. (1996) A critical role for stem cell factor and c-kit in host protective immunity to an intestinal helminth. International Immunology 8, 559–567.CrossRefGoogle Scholar
Galli, S.J. (1993) New concepts about the mast cell. New England Journal of Medicine 328, 257–265.Google ScholarPubMed
Grencis, R.K., Else, K.J., Huntley, J.F. & Nishikawa, S.I. (1993) The in vivo role of stem cell factor (c-kit ligand) on mastocytosis and host protective immunity to the intestinal nematode Trichinella spiralis in mice. Parasite Immunology 15, 55–59.CrossRefGoogle Scholar
Gurish, M.F., Tao, H., Abonia, J.P., Arya, A., Friend, D.S., Parker, C.M. & Austen, K.F. (2001) Intestinal mast cell progenitors require CD49dbeta7 (alpha4beta7 integrin) for tissue-specific homing. Journal of Experimental Medicine 194, 1243–1252.CrossRefGoogle ScholarPubMed
Kasugai, T., Tei, H., Okada, M., Hirota, S., Morimoto, M., Yamada, M., Nakama, A., Arizono, N. & Kitamura, Y. (1995) Infection with Nippostrongylus brasiliensis induces invasion of mast cell precursors from peripheral blood to small intestine. Blood 85, 1334–1340.CrossRefGoogle ScholarPubMed
Kitamura, Y., Shimada, M., Go, S., Matsuda, H., Hatanaka, K. & Seki, M. (1979) Distribution of mast-cell precursors in haematopoietic and lymphopoietic tissues of mice. Journal of Experimental Medicine 150, 482–490.CrossRefGoogle ScholarPubMed
Knight, P.A., Wright, S.H., Brown, J.K., Huang, X., Sheppard, D. & Miller, H.R.P. (2002) Enteric expression of the integrin αvβ6 is essential for nematode-induced mucosal mast cell hyperplasia and expression of the granule chymase, mouse mast cell protease-1. American Journal of Pathology; 161, 771–779.CrossRefGoogle ScholarPubMed
Knight, P.A., Wright, S.H., Lawrence, C.E., Paterson, Y.Y. & Miller, H.R.P. (2000) Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cell-specific granule chymase, mouse mast cell protease-1. Journal of Experimental Medicine 192, 1849–1856.CrossRefGoogle ScholarPubMed
Lantz, C.S. & Huff, T.F. (1995) Murine KIT+ lineage- bone marrow progenitors express Fc gamma-RII but do not express Fc epsilon-RI until mast cell granule formation. Journal of Immunology 154, 355–362.CrossRefGoogle Scholar
Metcalfe, D.D., Baram, D. & Mekori, Y.A. (1997) Mast cells. Physiological Reviews 77, 1033–1079.CrossRefGoogle ScholarPubMed
Miller, H.R.P. (1996) Mucosal mast cells and the allergic response against nematode parasites. Veterinary Immunology and Immunopathology 54, 331–336.CrossRefGoogle ScholarPubMed
Miller, H.R.P., Wright, S.H., Knight, P.A. & Thornton, E.M. (1999) A novel function for transforming growth factor-beta1: upregulation of the expression and the IgE-independent extracellular release of a mucosal mast cell granule-specific beta-chymase, mouse mast cell protease-1. Blood 93, 3473–3486.CrossRefGoogle ScholarPubMed
Munger, J.S., Huang, X., Kawakatsu, H., Griffiths, M.J., Dalton, S.L., Wu, J., Pittet, J.F., Kaminski, N., Garat, C., Matthay, M.A., Rifkin, D.B. & Sheppard, D. (1999) The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96, 319–328.CrossRefGoogle ScholarPubMed
Nawa, Y. & Miller, H.R.P. (1979) Adoptive transfer of the intestinal mast cell response in rats infected with Nippostrongylus brasiliensis . Cellular Immunology 42, 225–239.CrossRefGoogle ScholarPubMed
Nawa, Y., Parish, C.R. & Miller, H.R.P. (1978) The protective capacities of fractionated immune thoracic duct lymphocytes against Nippostrongylus brasiliensis . Cellular Immunology 37, 41–50.CrossRefGoogle ScholarPubMed
Reed, N.D., Wakelin, D., Lammas, D.A. & Grencis, R.K. (1988) Genetic control of mast cell development in bone marrow cultures. Strain-dependent variation in cultures from inbred mice. Clinical and Experimental Immunology 73, 510–515.Google ScholarPubMed
Scudamore, C.L., McMillan, L., Thornton, E.M., Wright, S.H., Newlands, G.F. & Miller, H.R.P. (1997) Mast cell heterogeneity in the gastrointestinal tract: variable expression of mouse mast cell protease-1 (mMCP-1) in intraepithelial mucosal mast cells in nematode-infected and normal BALB/c mice. American Journal of Pathology 150, 1661–1672.Google ScholarPubMed
Tegoshi, T., Okada, M., Nishida, M. & Arizono, N. (1997) Early increase of gut intraepithelial mast cell precursors following Strongyloides venezuelensis infection in mice. Parasitology 114, 181–187.CrossRefGoogle ScholarPubMed
Tuohy, M., Lammas, D.A., Wakelin, D., Huntley, J.F., Newlands, G.F. & Miller, H.R.P. (1990) Functional correlations between mucosal mast cell activity and immunity to Trichinella spiralis in high and low responder mice. Parasite Immunology 12, 675–685.CrossRefGoogle ScholarPubMed
Wakelin, D. (1978) Immunity to intestinal parasites. Nature 273, 617–620.CrossRefGoogle ScholarPubMed
Wakelin, D. (1986) Genetic and other constraints on resistance to infection with gastrointestinal nematodes. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 742–747.CrossRefGoogle ScholarPubMed
Wakelin, D. & Donachie, A.M. (1981) Genetic control of immunity to Trichinella spiralis. Donor bone marrow cells determine responses to infection in mouse radiation chimaeras. Immunology 43, 787–792.Google ScholarPubMed
Wakelin, D. & Wilson, M.M. (1979) T and B cells in the transfer of immunity against Trichinella spiralis in mice. Immunology 37, 103–109.Google Scholar
Wastling, J.M., Scudamore, C.L., Thornton, E.M., Newlands, G.F. & Miller, H.R.P. (1997) Constitutive expression of mouse mast cell protease-1 in normal BALB/c mice and its up-regulation during intestinal nematode infection. Immunology 90, 308–313.CrossRefGoogle ScholarPubMed
Wright, S.H., Brown, J., Knight, P.A., Thornton, E.M., Kilshaw, P.J. & Miller, H.R.P. (2002) Transforming growth factor-β1 mediates coexpression of the integrin subunit αE and the chymase mouse mast cell protease-1 during the early differentiation of bone marrow-derived mucosal mast cell homologues. Clinical and Experimental Allergy 31, 315–324.CrossRefGoogle Scholar