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Innate immune response mechanisms in the intestinal epithelium: potential roles for mast cells and goblet cells in the expulsion of adult Trichinella spiralis

Published online by Cambridge University Press:  16 April 2008

P. A. KNIGHT ,
J. K. BROWN  and
A. D. PEMBERTON
P. A. KNIGHT*
Affiliation:
Department of Veterinary Clinical Studies, The University of Edinburgh, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, UK
J. K. BROWN
Affiliation:
Department of Veterinary Clinical Studies, The University of Edinburgh, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, UK
A. D. PEMBERTON
Affiliation:
Department of Veterinary Clinical Studies, The University of Edinburgh, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, UK
*
*Corresponding author: Department of Veterinary Clinical Studies, The University of Edinburgh, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, UK. Tel: +0131 650 7348. Fax: +0131 651 3903. E-mail: pam.knight@ed.ac.uk
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Summary

Gastrointestinal infection with the nematode Trichinella spiralis is accompanied by a rapid and reversible expansion of the mucosal mast cell and goblet cell populations in the intestinal epithelium, which is associated with the release of their mediators into the gut lumen. Both goblet cell and mast cell hyperplasia are highly dependent on mucosal T-cells and augmented by the cytokines IL-4 and IL-13. However, the contribution of both mast and goblet cells, and the mediators they produce, to the expulsion of the adults of T. spiralis is only beginning to be elucidated through studies predominantly employing T. spiralis-mouse models. In the present article, we review the factors proposed to control T. spiralis-induced mucosal mast cell (MMC) and goblet cell differentiation in the small intestine, and focus on some key MMC and goblet cell effector molecules which may contribute to the expulsion of adult worms and/or inhibition of larval development.

Keywords

Trichinella spiralisgastrointestinal nematodesmast cellsgoblet cellscytokinesmucusMcpt-1Mcpt-2intelectinRELMβ
Type
Review Article
Information
Parasitology , Volume 135 , Issue 6 , May 2008 , pp. 655 - 670
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Abe, T., Ochiai, H., Minamishima, Y. and Nawa, Y. (1988). Induction of intestinal mastocytosis in nude mice by repeated injection of interleukin-3. International Archives of Allergy and Applied Immunology 86, 356–358.Google Scholar
Annes, J. P., Munger, J. S. and Rifkin, D. B. (2003). Making sense of latent TGFbeta activation. Journal of Cell Science 116, 217–224.Google Scholar
Artis, D. (2006). New weapons in the war on worms: identification of putative mechanisms of immune-mediated expulsion of gastrointestinal nematodes. International Journal for Parasitology 36, 723–733.Google Scholar
Artis, D., Humphreys, N. E., Bancroft, A. J., Rothwell, N. J., Potten, C. S. and Grencis, R. K. (1999). Tumor necrosis factor alpha is a critical component of interleukin 13-mediated protective T helper cell type 2 responses during helminth infection. Journal of Experimental Medicine 190, 953–962.Google Scholar
Artis, D., Mei, L. W., Keilbaugh, S. A., He, W. M., Brenes, M., Swain, G. P., Knight, P. A., Donaldson, D. D., Lazar, M. A., Miller, H. R. P., Schad, G. A., Scott, P. and Wu, G. D. (2004 a). RELM beta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proceedings of the National Academy of Sciences, USA 101, 13596–13600.Google Scholar
Artis, D., Villarino, A., Silverman, M., He, W. M., Thornton, E. M., Mu, S., Summer, S., Covey, T. M., Huang, E., Yoshida, H., Koretzky, G., Goldschmidt, M., Wu, G. D., De Sauvage, F., Miller, H. R. P., Saris, C. J. M., Scott, P. and Hunter, C. A. (2004 b). The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. Journal of Immunology 173, 5626–5634.Google Scholar
Bell, R. G., Adams, L. S. and Ogden, R. W. (1984). Intestinal mucus trapping in the rapid expulsion of Trichinella spiralis by rats – induction and expression analyzed by quantitative worm recovery. Infection and Immunity 45, 267–272.CrossRefGoogle ScholarPubMed
Blanchard, C., Durual, S., Estienne, M., Bouzakri, K., Heim, M. H., Blin, N. and Cuber, J. C. (2004). IL-4 and IL-13 up-regulate intestinal trefoil factor expression: requirement for STAT6 and de novo protein synthesis. Journal of Immunology 172, 3775–3783.Google Scholar
Brandt, E. B., Strait, R. T., Hershko, D., Wang, Q., Muntel, E. E., Scribner, T. A., Zimmermann, N., Finkelman, F. D. and Rothenberg, M. E. (2003). Mast cells are required for experimental oral allergen-induced diarrhea. Journal of Clinical Investigation 112, 1666–1677.Google Scholar
Breuss, J. M., Gillett, N., Lu, L., Sheppard, D. and Pytela, R. (1993). Restricted distribution of integrin beta-6 messenger RNA in primate epithelial tissues. Journal of Histochemistry & Cytochemistry 41, 1521–1527.Google Scholar
Brown, J. K., Knight, P. A., Pemberton, A. D., Wright, S. H., Pate, J. A., Thornton, E. M. and Miller, H. R. P. (2004). Expression of integrin-alpha (E) by mucosal mast cells in the intestinal epithelium and its absence in nematode-infected mice lacking the transforming growth-factor-beta(1)-activating integrin alpha(v)beta(6). American Journal of Pathology 165, 95–106.Google Scholar
Brown, J. K., Knight, P. A., Thornton, E. M., Pate, J. A., Coonrod, S., Miller, H. R. P. and Pemberton, A. D. (2008). Trichinella spiralis induces de novo expression of group IVC phospholipase A2 in the intestinal epithelium. International Journal for Parasitology 38, 143–147.Google Scholar
Brown, J. K., Knight, P. A., Wright, S. H., Thornton, E. M. and Miller, H. R. (2003). Constitutive secretion of the granule chymase mouse mast cell protease-1 and the chemokine, CCL2, by mucosal mast cell homologues. Clinical and Experimental Allergy: Journal of the British Society For Allergy and Clinical Immunology 33, 132–146.CrossRefGoogle Scholar
Brown, J. K., Mcaleese, S. M., Thornton, E. M., Pate, J. A., Schock, A., Macrae, A., Scott, P. R., Miller, H. R. and Collie, D. S. (2006). Integrin alphaVbeta6, a putative receptor for Foot-and-Mouth disease virus, is constitutively expressed in ruminant airways. Journal of Histochemistry & Cytochemistry 54, 807–816.CrossRefGoogle ScholarPubMed
Cliffe, L. J., Humphreys, N. E., Lane, T. E., Potten, C. S., Booth, C. and Grencis, R. K. (2005). Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308, 1463–1465.Google Scholar
Cunningham, S. A., Awayda, M. S., Bubien, J. K., Ismailov, I., Arrate, M. P., Berdiev, B. K., Benos, D. J. and Fuller, C. M. (1995). Cloning of an epithelial chloride channel from bovine trachea. Journal of Biological Chemistry 270, 31016–31026.CrossRefGoogle ScholarPubMed
Datta, R., Deschoolmeester, M. L., Hedeler, C., Paton, N. W., Brass, A. M. and Else, K. J. (2005). Identification of novel genes in intestinal tissue that are regulated after infection with an intestinal nematode parasite. Infection and Immunity 73, 4025–4033.CrossRefGoogle ScholarPubMed
Dehlawi, M. S., Mahida, Y. R., Hughes, K. and Wakelin, D. (2006). Effects of Trichinella spiralis infection on intestinal pathology in mice lacking interleukin-4 (IL-4) or intestinal trefoil factor (ITF/TFF3). Parasitology International 55, 207–211.Google Scholar
Dehlawi, M. S. and Wakelin, D. (2002). Parameters of intestinal inflammation in mice given graded infections of the nematode Trichinella spiralis. Journal of Helminthology 76, 113–117.CrossRefGoogle ScholarPubMed
Donaldson, L. E., Schmitt, E., Huntley, J. F., Newlands, G. F. J. and 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
Fallon, P. G., Jolin, H. E., Smith, P., Emson, C. L., Townsend, M. J., Fallon, R. and Mckenzie, A. N. (2002). IL-4 induces characteristic Th2 responses even in the combined absence of IL-5, IL-9, and IL-13. Immunity 17, 7–17.Google Scholar
Faulkner, H., Humphreys, N., Renauld, J. C., Van Snick, J. and Grencis, R. (1997). Interleukin-9 is involved in host protective immunity to intestinal nematode infection. European Journal of Immunology 27, 2536–2540.Google Scholar
Field, M. (2003). Intestinal ion transport and the pathophysiology of diarrhea. Journal of Clinical Investigation 111, 931–943.CrossRefGoogle ScholarPubMed
Finkelman, F. D., Shea-Donohue, T., Morris, S. C., Gildea, L., Strait, R., Madden, K. B., Schopf, L. and Urban, J. F. (2004). Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunological Reviews 201, 139–155.CrossRefGoogle ScholarPubMed
Friend, D. S., Ghildyal, N., Austen, K. F., Gurish, M. F., Matsumoto, R. and Stevens, R. L. (1996). Mast cells that reside at different locations in the jejunum of mice infected with Trichinella spiralis exhibit sequential changes in their granule ultrastructure and chymase phenotype. Journal of Cell Biology 135, 279–290.Google Scholar
Friend, D. S., Ghildyal, N., Gurish, M. F., Hunt, J., Hu, X. Z., Austen, K. F. and Stevens, R. L. (1998). Reversible expression of tryptases and chymases in the jejunal mast cells of mice infected with Trichinella spiralis. Journal of Immunology 160, 5537–5545.Google Scholar
Gibson, A., Lewis, A. P., Affleck, K., Aitken, A. J., Meldrum, E. and Thompson, N. (2005). hCLCA1 and mCLCA3 are secreted non-integral membrane proteins and therefore are not ion channels. Journal of Biological Chemistry 280, 27205–27212.Google Scholar
Gilroy, D. W., Newson, J., Sawmynaden, P., Willoughby, D. A. and Croxtall, J. D. (2004). A novel role for phospholipase A2 isoforms in the checkpoint control of acute inflammation. FASEB Journal 18, 489–498.CrossRefGoogle ScholarPubMed
Grencis, R. K., Else, K. J., Huntley, J. F. and 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.Google Scholar
Gustowska, L., Ruitenberg, E. J., Elgersma, A. and Kociecka, W. (1983). Increase of mucosal mast cells in the jejunum of patients infected with Trichinella spiralis. International Archives of Allergy and Applied Immunology 71, 304–308.CrossRefGoogle ScholarPubMed
Ha, T. Y., Reed, N. D. and Crowle, P. K. (1983). Delayed expulsion of adult Trichinella spiralis by mast cell-deficient W/Wv mice. Infection and Immunity 41, 445–447.Google Scholar
He, W. M., Wang, M. L., Jiang, H. Q., Steppan, C. M., Shin, M. E., Thurnheer, M. C., Cebra, J. J., Lazar, M. A. and Wu, G. D. (2003). Bacterial colonization leads to the colonic secretion of RELM beta/FIZZ2, a novel goblet cell-specific protein. Gastroenterology 125, 1388–1397.Google Scholar
Helmby, H. and Grencis, R. K. (2002). IL-18 regulates intestinal mastocytosis and Th2 cytokine production independently of IFN-gamma during Trichinella spiralis infection. Journal of Immunology 169, 2553–2560.Google Scholar
Holcomb, I. N., Kabakoff, R. C., Chan, B., Baker, T. W., Gurney, A., Henzel, W., Nelson, C., Lowman, H. B., Wright, B. D., Skelton, N. J., Frantz, G. D., Tumas, D. B., Peale, F. V., Shelton, D. L. and Hebert, C. C. (2000). FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO Journal 19, 4046–4055.Google Scholar
Horsnell, W. G. C., Cutler, A. J., Hoving, J. C., Mearns, H., Myburgh, E., Arendse, B., Finkelman, F. D., Owens, G. K., Erle, D. and Brombacher, F. (2007). Delayed goblet cell hyperplasia, acetylcholine receptor expression, and worm expulsion in SMC-specific IL-4R alpha-deficient mice. Plos Pathogens 3, 46–53.Google Scholar
Huang, X., Wu, J., Zhu, W., Pytela, R. and Sheppard, D. (1998). Expression of the human integrin beta6 subunit in alveolar type II cells and bronchiolar epithelial cells reverses lung inflammation in beta6 knockout mice. American Journal of Respiratory Cell and Molecular Biology 19, 636–642.Google Scholar
Huang, X. Z., Wu, J. F., Cass, D., Erle, D. J., Corry, D., Young, S. G., Farese, R. V. and Sheppard, D. (1996). Inactivation of the integrin beta 6 subunit gene reveals a role of epithelial integrins in regulating inflammation in the lungs and skin. Journal of Cell Biology 133, 921–928.Google Scholar
Ishikawa, N., Wakelin, D. and Mahida, Y. R. (1997). Role of T helper 2 cells in intestinal goblet cell hyperplasia in mice infected with Trichinella spiralis. Gastroenterology 113, 542–549.Google Scholar
Itoh, H., Inoue, N. and Podolsky, D. K. (1999). Goblet-cell-specific transcription of mouse intestinal trefoil factor gene results from collaboration of complex series of positive and negative regulatory elements. The Biochemical Journal 341, 461–472.Google Scholar
Iwakiri, D. and Podolsky, D. K. (2001). A silencer inhibitor confers specific expression of intestinal trefoil factor in gobletlike cell lines. American Journal of Physiology-Gastrointestinal and Liver Physiology 280, G1114–G1123.Google Scholar
Kamal, M., Wakelin, D., Ouellette, A. J., Smith, A., Podolsky, D. K. and Mahida, Y. R. (2001). Mucosal T cells regulate Paneth and intermediate cell numbers in the small intestine of T. spiralis-infected mice. Clinical and Experimental Immunology 126, 117–125.Google Scholar
Khan, W. I., Blennerhasset, P., Ma, C., Matthaei, K. I. and Collins, S. M. (2001 a). Stat6 dependent goblet cell hyperplasia during intestinal nematode infection. Parasite Immunology 23, 39–42.Google Scholar
Khan, W. I., Blennerhassett, P. A., Deng, Y. K., Gauldie, J., Vallance, B. A. and Collins, S. M. (2001 b). IL-12 gene transfer alters gut physiology and host immunity in nematode-infected mice. American Journal of Physiology-Gastrointestinal and Liver Physiology 281, G102–G110.CrossRefGoogle ScholarPubMed
Khan, W. I., Vallance, B. A., Blennerhasset, P. A., Deng, Y., Verdu, E. F., Matthaei, K. I. and Collins, S. M. (2001 c). Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infection and Immunity 69, 838–844.CrossRefGoogle ScholarPubMed
Kindon, H., Pothoulakis, C., Thim, L., Lynch_Devaney, K. and Podolsky, D. K. (1995). Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein. Gastroenterology 109, 516–523.Google Scholar
Knight, P. A., Brown, J. K., Wright, S. H., Thornton, E. M., Pate, J. A. and Miller, H. R. P. (2007). Aberrant mucosal mast cell protease expression in the enteric epithelium of nematode-infected mice lacking the Integrin alphaVbeta6 transforming growth factor-beta1 activator. American Journal of Pathology 171, 1237–1248.Google Scholar
Knight, P. A., Pemberton, A. D., Robertson, K. A., Roy, D. J., Wright, S. H. and Miller, H. R. P. (2004). Expression profiling reveals novel innate and inflammatory responses in the jejunal epithelial compartment during infection with Trichinella spiralis. Infection and Immunity 72, 6076–6086.Google Scholar
Knight, P. A., Wright, S. H., Brown, J. K., Huang, X., Sheppard, D. and Miller, H. R. (2002). Enteric expression of the integrin alpha(v)beta(6) 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 Scholar
Knight, P. A., Wright, S. H., Lawrence, C. E., Paterson, Y. Y. and Miller, H. R. (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.Google Scholar
Komiya, T., Tanigawa, Y. and Hirohashi, S. (1998). Cloning of the novel gene intelectin, which is expressed in intestinal paneth cells in mice. Biochemical and Biophysical Research Communications 251, 759–762.Google Scholar
Komiya, T., Tanigawa, Y. and Hirohashi, S. (1999). Cloning and identification of the gene gob-5, which is expressed in intestinal goblet cells in mice. Biochemical and Biophysical Research Communications 255, 347–351.Google Scholar
Kuperman, D. A., Lewis, C. C., Woodruff, P. G., Rodriguez, M. W., Yang, Y. H., Dolganov, G. M., Fahy, J. V. and Erle, D. J. (2005). Dissecting asthma using focused transgenic modeling and functional genomics. Journal of Allergy and Clinical Immunology 116, 305–311.Google Scholar
Lawrence, C. E., Paterson, J. C. M., Higgins, L. M., Macdonald, T. T., Kennedy, M. W. and Garside, P. (1998). IL-4-regulated enteropathy in an intestinal nematode infection. European Journal of Immunology 28, 2672–2684.3.0.CO;2-F>CrossRefGoogle Scholar
Lawrence, C. E., Paterson, J. C. M., Wei, X. Q., Liew, F. Y., Garside, P. and Kennedy, M. W. (2000). Nitric oxide mediates intestinal pathology but not immune expulsion during Trichinella spiralis infection in mice. Journal of Immunology 164, 4229–4234.Google Scholar
Lawrence, C. E., Paterson, Y. Y. W., Wright, S. H., Knight, P. A. and Miller, H. R. P. (2004). Mouse mast cell protease-1 is required for the enteropathy induced by gastrointestinal helminth infection in the mouse. Gastroenterology 127, 155–165.Google Scholar
Lee, J. K., Schnee, J., Pang, M., Wolfert, M., Baum, L. G., Moremen, K. W. and Pierce, M. (2001). Human homologs of the Xenopus oocyte cortical granule lectin XL35. Glycobiology 11, 65–73.Google Scholar
Leverkoehne, I. and Gruber, A. D. (2002). The murine mCLCA3 (alias gob-5) protein is located in the mucin granule membranes of intestinal, respiratory, and uterine goblet cells. Journal of Histochemistry and Cytochemistry 50, 829–838.Google Scholar
Loewen, M. E. and Forsyth, G. W. (2005). Structure and function of CLCA proteins. Physiological Reviews 85, 1061–1092.CrossRefGoogle ScholarPubMed
Longman, R. J., Douthwaite, J., Sylvester, P. A., Poulsom, R., Corfield, A. P., Thomas, M. G. and Wright, N. A. (2000). Coordinated localisation of mucins and trefoil peptides in the ulcer associated cell lineage and the gastrointestinal mucosa. Gut 47, 792–800.Google Scholar
Ludlow, A., Yee, K. O., Lipman, R., Bronson, R., Weinreb, P., Huang, X. Z., Sheppard, D. and Lawler, J. (2005). Characterization of integrin beta 6 and thrombospondin-1 double-null mice. Journal of Cellular and Molecular Medicine 9, 421–437.Google Scholar
Madden, K. B., Urban, J. F. Jr., Ziltener, H. J., Schrader, J. W., Finkelman, F. D. and Katona, I. M. (1991). Antibodies to IL-3 and IL-4 suppress helminth-induced intestinal mastocytosis. Journal of Immunology 147, 1387–1391.Google Scholar
Madden, K. B., Yeung, K. A., Zhao, A. P., Gause, W. C., Finkelman, F. D., Katona, I. M., Urban, J. F. and Shea-Donohue, T. (2004). Enteric nematodes induce stereotypic STAT6-dependent alterations in intestinal epithelial cell function. Journal of Immunology 172, 5616–5621.Google Scholar
Mancuso, P., Canetti, C., Gottschalk, A., Tithof, P. K. and Peters-Golden, M. (2004). Leptin augments alveolar macrophage leukotriene synthesis by increasing phospholipase activity and enhancing group IVC iPLA2 (cPLA2gamma) protein expression. American Journal of Physiology; Lung, Cell and Molecular Physiology 287, L497–502.CrossRefGoogle ScholarPubMed
Mashimo, H., Wu, D. C., Podolsky, D. K. and Fishman, M. C. (1996). Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science 274, 262–265.CrossRefGoogle ScholarPubMed
McDermott, J. R., Bartram, R. E., Knight, P. A., Miller, H. R. P., Garrod, D. R. and Grencis, R. K. (2003). Mast cells disrupt epithelial barrier function during enteric nematode infection. Proceedings of the National Academy of Sciences, USA 100, 7761–7766.Google Scholar
McDermott, J. R., Humphreys, N. E., Forman, S. P., Donaldson, D. D. and Grencis, R. K. (2005). Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. Journal of Immunology 175, 3207–3213.Google Scholar
Menge, D. M., Behnke, J. M., Lowe, A., Gibson, J. P., Iraqi, F. A., Baker, R. L. and Wakelin, D. (2003). Mapping of chromosomal regions influencing immunological responses to gastrointestinal nematode infections in mice. Parasite Immunology 25, 341–349.Google Scholar
Miller, H. R. (1987). Gastrointestinal mucus, a medium for survival and for elimination of parasitic nematodes and protozoa. Parasitology 94 Suppl, S77–100.Google Scholar
Miller, H. R. (1996). Mucosal mast cells and the allergic response against nematode parasites. Veterinary Immunology and Immunopathology 54, 331–336.CrossRefGoogle ScholarPubMed
Miller, H. R., Huntley, J. F., Newlands, G. F., Mackellar, A., Lammas, D. A. and Wakelin, D. (1988). Granule proteinases define mast cell heterogeneity in the serosa and the gastrointestinal mucosa of the mouse. Immunology 65, 559–566.Google Scholar
Miller, H. R. and Jarrett, W. F. (1971). Immune reactions in mucous membranes. I. Intestinal mast cell response during helminth expulsion in the rat. Immunology 20, 277–288.Google Scholar
Miller, H. R., Wright, S. H., Knight, P. A. and 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.Google Scholar
Miller, H. R. P., Huntley, J. F. and Wallace, G. R. (1981). Immune exclusion and mucus trapping during the rapid expulsion of Nippostrongylus brasiliensis from primed rats. Immunology 44, 419–429.Google Scholar
Miller, H. R. P., Knight, P. A. and Pemberton, A. D. (2006). Mucus; modulation by the TH2 response to enhance an innate defensive barrier against gut nematodes. Parasite Immunology 28, 259–262.Google Scholar
Miller, H. R. P. and Pemberton, A. D. (2002). Tissue-specific expression of mast cell granule serine proteinases and their role in inflammation in the lung and gut. Immunology 105, 375–390.Google Scholar
Mu, D. Z., Cambier, S., Fjellbirkeland, L., Baron, J. L., Munger, J. S., Kawakatsu, H., Sheppard, D., Broaddus, V. C. and Nishimura, S. L. (2002). The integrin alpha v beta 8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta 1. Journal of Cell Biology 157, 493–507.Google Scholar
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. and 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.Google Scholar
Nair, M. G., Gallagher, L. J., Taylor, M. D., Loke, P., Coulson, P. S., Wilson, R. A., Maizels, R. M. and Allen, J. E. (2005). Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and F10.1 by antigen-presenting cells. Infection and Immunity 73, 385–394.Google Scholar
Nakanishi, A., Morita, S., Iwashita, H., Sagiya, Y., Ashida, Y., Shirafuji, H., Fujisawa, Y., Nishimura, O. and Fujino, M. (2001). Role of gob-5 in mucus overproduction and airway hyperresponsiveness in asthma. Proceedings of the National Academy of Sciences, USA 98, 5175–5180.Google Scholar
Nawa, Y., Ishikawa, N., Tsuchiya, K., Horii, Y., Abe, T., Khan, A. I., Bing, S., Itoh, H., Ide, H. and Uchiyama, F. (1994). Selective effector mechanisms for the expulsion of intestinal helminths. Parasite Immunology 16, 333–338.Google Scholar
Nawa, Y. and Miller, H. R. P. (1978). Protection against Nippostrongylus brasiliensis by adoptive immunization with immune thoracic-duct lymphocytes. Cellular Immunology 37, 51–60.Google Scholar
Newlands, G. F. J., Miller, H. R. P. and Jackson, F. (1990). Immune exclusion of Haemonchus contortus larvae in the sheep – effects on gastric mucin of immunization, larval challenge and treatment with dexamethasone. Journal of Comparative Pathology 102, 433–442.Google Scholar
Norkina, O., Burnett, T. G. and De Lisle, R. C. (2004). Bacterial overgrowth in the cystic fibrosis transmembrane conductance regulator null mouse small intestine. Infection and Immunity 72, 6040–6049.Google Scholar
Owyang, A. M., Zaph, C., Wilson, E. H., Guild, K. J., McClanahan, T., Miller, H. R. P., Cua, D. J., Goldschmidt, M., Hunter, C. A., Kastelein, R. A. and Artis, D. (2006). Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. Journal of Experimental Medicine 203, 843–849.Google Scholar
Pemberton, A. D., Brown, J. K., Wright, S. H., Knight, P. A., Mcphee, M. L., McEuen, A. R., Forse, P. A. and Miller, H. R. P. (2003). Purification and characterization of mouse mast cell proteinase-2 and the differential expression and release of mouse mast cell proteinase-1 and -2 in vivo. Clinical and Experimental Allergy 33, 1005–1012.Google Scholar
Pemberton, A. D., Brown, J. K., Wright, S. H., Knight, P. A. and Miller, H. R. P. (2006 a). The proteome of mouse mucosal mast cell homologues: the role of transforming growth factor beta (1). Proteomics 6, 623–631.Google Scholar
Pemberton, A. D., Knight, P. A., Gamble, J., Colledge, W. H., Lee, J. K., Pierce, M. and Miller, H. R. P. (2004 a). Innate BALB/c enteric epithelial responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. Journal of Immunology 173, 1894–1901.Google Scholar
Pemberton, A. D., Knight, P. A., Wright, S. H. and Miller, H. R. P. (2004 b). Proteomic analysis of mouse jejunal epithelium and its response to infection with the intestinal nematode, Trichinella spiralis. Proteomics 4, 1101–1108.Google Scholar
Pemberton, A. D., Wright, S. H., Knight, P. A. and Miller, H. R. P. (2006 b). Anaphylactic release of mucosal mast cell granule proteases: role of serpins in the differential clearance of mouse mast cell proteases-1 and -2. Journal of Immunology 176, 899–904.CrossRefGoogle ScholarPubMed
Pennock, J. L. and Grencis, R. K. (2004). In vivo exit of c-kit(+)/CD49d(hi)/beta 7(+) mucosal mast cell precursors from the bone marrow following infection with the intestinal nematode Trichinella spiralis. Blood 103, 2655–2660.Google Scholar
Rosbottom, A., Knight, P. A., Mclachlan, G., Thornton, E. M., Wright, S. W., Miller, H. R. and Scudamore, C. L. (2002 a). Chemokine and cytokine expression in murine intestinal epithelium following Nippostrongylus brasiliensis infection. Parasite Immunology 24, 67–75.Google Scholar
Rosbottom, A., Scudamore, C. L., von der Mark, H., Thornton, E. M., Wright, S. H. and Miller, H. R. P. (2002 b). TGF-beta 1 regulates adhesion of mucosal mast cell homologues to laminin-1 through expression of integrin alpha(1)(7). Journal of Immunology 169, 5689–5695.Google Scholar
Sandler, N. G., Mentink-Kane, M. M., Cheever, A. W. and Wynn, T. A. (2003). Global gene expression profiles during acute pathogen-induced pulmonary inflammation reveal divergent roles for Th1 and Th2 responses in tissue repair. Journal of Immunology 171, 3655–3667.Google Scholar
Sasaki, Y., Yoshimoto, T., Maruyama, H., Tegoshi, T., Ohta, N., Arizono, N. and Nakanishi, K. (2005). IL-18 with IL-2 protects against Strongyloides venezuelensis infection by activating mucosal mast cell-dependent type 2 innate immunity. Journal of Experimental Medicine 202, 607–616.CrossRefGoogle ScholarPubMed
Scales, H. E., Ierna, M. X. and Lawrence, C. E. (2007). The role of IL-4, IL-13 and IL-4R alpha in the development of protective and pathological responses to Trichinella spiralis. Parasite Immunology 29, 81–91.Google Scholar
Scudamore, C. L., Jepson, M. A., Hirst, B. H. and Miller, H. R. P. (1998). The rat mucosal mast cell chymase, RMCP-II, alters epithelial cell monolayer permeability in association with altered distribution of the tight junction proteins ZO-1 and occludin. European Journal of Cell Biology 75, 321–330.Google Scholar
Scudamore, C. L., McMillan, L., Thornton, E. M., Wright, S. H., Newlands, G. F. J. and 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 Scholar
Scudamore, C. L., Thornton, E. M., McMillan, L., Newlands, G. F. J. and Miller, H. R. P. (1995). Release of the mucosal mast-cell granule chymase, rat mast-cell protease-II, during anaphylaxis is associated with the rapid development of paracellular permeability to macromolecules in rat jejunum. Journal of Experimental Medicine 182, 1871–1881.Google Scholar
Shekels, L. L., Anway, R. E., Lin, J., Kennedy, M. W., Garside, P., Lawrence, C. E. and Ho, S. B. (2001). Coordinated Muc2 and Muc3 mucin gene expression in Trichinella spiralis infection in wild-type and cytokine-deficient mice. Digestive Diseases and Sciences 46, 1757–1764.Google Scholar
Steppan, C. M., Brown, E. J., Wright, C. M., Bhat, S., Banerjee, R. R., Dai, C. Y., Enders, G. H., Silberg, D. G., Wen, X. M., Wu, G. D. and Lazar, M. A. (2001). A family of tissue-specific resistin-like molecules. Proceedings of the National Academy of Sciences, USA 98, 502–506.Google Scholar
Suzuki, Y. A., Shin, K. and Lonnerdal, B. (2001). Molecular cloning and functional expression of a human intestinal lactoferrin receptor. Biochemistry 40, 15771–15779.Google Scholar
Tan, B. L., Yazicioglu, M. N., Ingram, D., McCarthy, J., Borneo, J., Williams, D. A. and Kapur, R. (2003). Genetic evidence for convergence of c-Kit- and alpha(4) integrin-mediated signals on class IAPI-3kinase and the Rac pathway in regulating integrin-directed migration in mast cells. Blood 101, 4725–4732.Google Scholar
Taub, D., Dastych, J., Inamura, N., Upton, J., Kelvin, D., Metcalfe, D. and Oppenheim, J. (1995). Bone-marrow-derived murine mast-cells migrate, but do not degranulate, in response to chemokines. Journal of Immunology 154, 2393–2402.Google Scholar
Theodoropoulos, G., Hicks, S. J., Corfield, A. P., Miller, B. G., Kapel, C. M. O., Trivizaki, M., Balaskas, C., Petrakos, G. and Carrington, S. D. (2005). Trichinella spiralis: enteric mucin-related response to experimental infection in conventional and SPF pigs. Experimental Parasitology 109, 63–71.CrossRefGoogle ScholarPubMed
Thim, L., Madsen, F. and Poulsen, S. S. (2002). Effect of trefoil factors on the viscoelastic properties of mucus gels. European Journal of Clinical Investigation 32, 519–527.Google Scholar
Thim, L. and May, F. E. B. (2005). Structure of mammalian trefoil factors and functional insights. Cellular and Molecular Life Sciences 62, 2956–2973.CrossRefGoogle ScholarPubMed
Townsend, M. J., Fallon, P. G., Matthews, D. J., Smith, P., Jolin, H. E. and McKenzie, A. N. J. (2000). IL-9-deficient mice establish fundamental roles for IL-9 in pulmonary mastocytosis and goblet cell hyperplasia but not T cell development. Immunity 13, 573–583.Google Scholar
Tsuji, K., Zsebo, K. M. and Ogawa, M. (1991). Murine mast-cell colony formation supported by IL-3, IL-4, and recombinant rat stem-cell factor, ligand for c-Kit. Journal of Cellular Physiology 148, 362–369.CrossRefGoogle ScholarPubMed
Tsuji, S., Uehori, J., Matsumoto, M., Suzuki, Y., Matsuhisa, A., Toyoshima, K. and Seya, T. (2001). Human intelectin is a novel soluble lectin that recognizes galactofuranose in carbohydrate chains of bacterial cell wall. Journal of Biological Chemistry 276, 23456–23463.Google Scholar
Urban, J. F., Noben-Trauth, N., Schopf, L., Madden, K. B. and Finkelman, F. D. (2001). Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. Journal of Immunology 167, 6078–6081.Google Scholar
Urban, J. F., Schopf, L., Morris, S. C., Orekhova, T., Madden, K. B., Betts, C. J., Gamble, H. R., Byrd, C., Donaldson, D., Else, K. and Finkelman, F. D. (2000). Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. Journal of Immunology 164, 2046–2052.CrossRefGoogle ScholarPubMed
Vliagoftis, H. and Befus, A. D. (2005). Rapidly changing perspectives about mast cells at mucosal surfaces. Immunological Reviews 206, 190–203.Google Scholar
Wang, M. L., Shin, M. E., Knight, P. A., Artis, D., Silberg, D. G., Suh, E. and Wu, G. D. (2005). Regulation of RELM/FIZZ isoform expression by Cdx2 in response to innate and adaptive immune stimulation in the intestine. American Journal of Physiology – Gastrointestinal and Liver Physiology 288, G1074–G1083.Google Scholar
Wastling, J. M., Knight, P., Ure, J., Wright, S., Thornton, E. M., Scudamore, C. L., Mason, J., Smith, A. and Miller, H. R. P. (1998). Histochemical and ultrastructural modification of mucosal mast cell granules in parasitized mice lacking the beta-chymase, mouse mast cell protease-1. American Journal of Pathology 153, 491–504.CrossRefGoogle ScholarPubMed
Wastling, J. M., Scudamore, C. L., Thornton, E. M., Newlands, G. F. J. and 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
Weller, C. L., Collington, S. J., Brown, J. K., Miller, H. R., Al-Kashi, A., Clark, P., Jose, P. J., Hartnell, A. and Williams, T. J. (2005). Leukotriene B4, an activation product of mast cells, is a chemoattractant for their progenitors. Journal of Experimental Medicine 201, 1961–1971.Google Scholar
Weller, C. L., Collington, S. J., Hartnell, A., Conroy, D. M., Kaise, T., Barker, J. E., Wilson, M. S., Taylor, G. W., Jose, P. J. and Williams, T. J. (2007). Chemotactic action of prostaglandin E2 on mouse mast cells acting via the PGE2 receptor 3. Proceedings of the National Academy of Sciences, USA. 104, 11712–11717.Google Scholar
Wright, S. H., Brown, J., Knight, P. A., Thornton, E. M., Kilshaw, P. J. and Miller, H. R. (2002). Transforming growth factor-beta1 mediates coexpression of the integrin subunit alphaE and the chymase mouse mast cell protease-1 during the early differentiation of bone marrow-derived mucosal mast cell homologues. Clinical and Experimental Allergy 32, 315–324.Google Scholar
Yamauchi, J., Kawai, Y., Yamada, M., Uchikawa, R., Tegoshi, T. and Arizono, N. (2006). Altered expression of goblet cell- and mucin glycosylation-related genes in the intestinal epithelium during infection with the nematode Nippostrongylus brasiliensis in rat. Apmis 114, 270–278.Google Scholar
Zimmermann, N., Mishra, A., King, N. E., Fulkerson, P. C., Doepker, M. P., Nikolaidis, N. M., Kindinger, L. E., Moulton, E. A., Aronow, B. J. and Rothenberg, M. E. (2004). Transcript signatures in experimental asthma: identification of STAT6-dependent and -independent pathways. Journal of Immunology 172, 1815–1824.Google Scholar