Hostname: page-component-76d6cb85b7-7262s Total loading time: 0 Render date: 2026-07-21T02:55:13.066Z Has data issue: false hasContentIssue false
  • English
  • Français

Physiological changes in the gastrointestinal tract and host protective immunity: learning from the mouse-Trichinella spiralis model

Published online by Cambridge University Press:  23 May 2008

W. I. Khan
W. I. Khan*
Affiliation:
Intestinal Disease Research Program, Department of Medicine, McMaster University, Hamilton, Ontario, Canada
*
*Corresponding author: Department of Medicine, Room 3N5D, Health Science Center, McMaster University, 1200 Main Street West, Hamilton, Ontario L8N 3Z5, Canada. E-mail: khanwal@mcmaster.ca
Get access Rights & Permissions [Opens in a new window]

Summary

Infection and inflammation in the gastrointestinal (GI) tract induces a number of changes in the GI physiology of the host. Experimental infections with parasites represent valuable models to study the structural and physiological changes in the GI tract. This review addresses research on the interface between the immune system and GI physiology, dealing specifically with 2 major components of intestinal physiology, namely mucin production and muscle function in relation to host defence, primarily based on studies using the mouse-Trichinella spiralis system. These studies demonstrate that the infection-induced T helper 2 type immune response is critical in generating the alterations of infection-induced mucin production and muscle function, and that this immune-mediated alteration in gut physiology is associated with host defence mechanisms. In addition, by manipulating the host immune response, it is possible to modulate the accompanying physiological changes, which may have clinical relevance. In addition to enhancing our understanding of immunological control of GI physiological changes in the context of host defence against enteric infections, the data acquired using the mouse-T. spiralis model provide a basis for understanding the pathophysiology of a wide range of GI disorders associated with altered gut physiology.

Keywords

Trichinella spiralisimmunophysiologyinfectionimmunitymucinmuscle

Information

Type
Review Article
Information
Parasitology , Volume 135 , Issue 6 , May 2008 , pp. 671 - 682
Copyright
Copyright © 2008 Cambridge University Press

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Akiho, H., Blennerhassett, P. A., Deng, Y. and Collins, S. M. (2002). Role of IL-4, IL-13 and Stat6 in inflammation induced hypercontractility of murine smooth muscle cells. American Journal of Physiology – Gastrointestinal and Liver Physiology 282, G226–G233.Google Scholar
Akiho, H., Deng, Y., Blennerhassett, P. A., Pelegrin, P., Grundy, D. and Bardhan, K. D. (2005). Mechanisms underlying the maintenance of muscle hypercontractility in a model of post-infective gut dysfunction. Gastroenterology 129, 131–141.CrossRefGoogle Scholar
Alizadeh, H., Castro, G. A. and Weems, W. A. (1987). Intrinsic jejunal propulsion in the guinea-pig during parasitism with Trichinella spiralis. Gastroenterology 93, 784–790.Google Scholar
Barbara, G., Vallance, B. A. and Collins, S. M. (1997). Persistent intestinal neuromuscular dysfunction after acute nematode infection in mice. Gastroenterology 113, 1224–1232.Google Scholar
Bercik, P., Wang, L., Verdu, E. F., Mao, Y. K., Blennerhassett, P. A., Kean, I., Tougas, G. and Collins, S. M. (2004). Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction. Gastroenterology 127, 179–187.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Blennerhassett, M. G., Vignjevic, P., Vermillion, D. L. and Collins, S. M. (1992). Inflammation causes hyperplasia and hypertrophy in smooth muscle of rat small intestine. American Journal of Physiology 262, G1041–G1046.Google ScholarPubMed
Boland, C. R. and Deshmukh, G. D. (1990). The carbohydrate composition of mucin in colonic cancer. Gastroenterology 98, 1170–1177.CrossRefGoogle ScholarPubMed
Cetin, Y., Kuhn, M., Kulaksiz, H., Adermann, K., Bargsten, G., Grube, D. and Forssmann, W. G. (1994). Enterochromaffin cells of the digestive system: cellular source of guanylin, a guanylate cyclase-activating peptide. Proceedings of the National Academy of Sciences, USA 91, 2935–2939.CrossRefGoogle ScholarPubMed
Chang, S. K., Dohrman, A. F., Basbaum, C. B., Ho, S. B., Tsuda, T., Toribara, N. W., Gum, J. R. and Kim, Y. S. (1994). Localization of mucin (MUC2 and MUC3) messenger RNA and peptide expression in human normal intestine and colon cancer. Gastroenterology 107, 28–36.Google Scholar
Collins, S. M. (1996). The immunomodulation of enteric neuromuscular function: implications for motility and inflammatory disorders. Gastroenterology 111, 1683–1689.Google Scholar
Corfield, A. P., Myerscough, N., Longman, R., Sylvester, P., Arul, S. and Pignatell, M. (2000). Mucins and mucosal protection in the gastrointestinal tract: new prospects for mucins in the pathology of gastrointestinal disease. Gut 47, 589–594.Google Scholar
Crabtree, J. E., Heatley, R. V. and Losowsky, M. S. (1989). Glycoprotein synthesis and secretion by cultured small intestinal mucosa in coeliac disease. Gut 30, 1339–1343.CrossRefGoogle ScholarPubMed
Crabtree, J. E., Heatley, R. V., Trejdosiewicz, L. K. and Losowsky, M. S. (1990). T lymphocyte stimulation of human small intestinal glycoprotein biosynthesis: effects of anti-CD3 antibody on normal and coeliac mucosa. International Archives of Allergy and Applied Immunology 93, 35–40.Google Scholar
Dabbagh, K., Takeyama, K., Lee, H. M., Ueki, I. F., Lausier, J. A. and Nadel, J. A. (1999). IL-4 induces mucin gene expression and goblet cell metaplasia in vitro and in vivo. Journal of Immunology 162, 6233–6237.CrossRefGoogle ScholarPubMed
Der, T., Bercik, P., Donnelly, G., Jackson, T., Berezin, I., Collins, S. M. and Huizinga, J. D. (2000). Interstitial cells of cajal and inflammation-induced motor dysfunction in the mouse small intestine. Gastroenterology 119, 1590–1599.CrossRefGoogle ScholarPubMed
Dignass, A., Lynch-Devaney, K., Kindon, H., Thim, L. and Podolsky, D. K. (1994). Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway. Journal of Clinical Investigation 94, 376–383.Google Scholar
Else, K. J. and Finkelman, F. D. (1998). Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 1145–1158.CrossRefGoogle ScholarPubMed
Farmer, S. G. and Laniyonu, A. A. (1984). Effects of p-chlorophenylalanine on the sensitivity of rat intestine to agonists and on intestinal 5-hydroxytryptamine levels during Nippostrongylus brasiliensis infection. British Journal of Pharmacology 82, 883–889.CrossRefGoogle ScholarPubMed
Garside, P., Grencis, R. K. and Mowat, A. M. (1992). T lymphocyte dependent enteropathy in murine Trichinella spiralis infection. Parasite Immunology 14, 217–225.CrossRefGoogle ScholarPubMed
Gershon, M. D. (1999). Review article: roles played by 5-hydroxytryptamine in the physiology of the bowel. Alimentary Pharmacological Therapeutics 2, 15–30.CrossRefGoogle Scholar
Goldhill, J., Morris, S. C., Malizewski, C., Urban, J. F. Jr., Finkelman, F. D. and Shea-Donohue, T. (1997). Interleukin-4 modulates cholinergic neural control of mouse small intestinal longitudinal muscle. American Journal of Physiology – Gastrointestinal and Liver Physiology 272, G1135–G1140.Google Scholar
Grencis, R. K. (1997). Th2-mediated host protective immunity to intestinal nematode infections. Philosophical Transactions of the Royal Society, London 352, 1377–1384.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 intestinal nematode Trichinella spiralis in mice. Parasite Immunology 15, 55–59.Google Scholar
Grewal, I. S. and Flavell, R. A. (1996). A central role of CD40 ligand in the regulation of CD4+ T-cell responses. Immunology Today 17, 410–414.Google Scholar
Grossi, L., McHugh, K. and Collins, S. M. (1993). On the specificity of altered muscle function in experimental colitis in rats. Gastroenterology 104, 1049–1056.CrossRefGoogle ScholarPubMed
Ha, T. Y., Reed, N. D. and Croll, P. K. (1983). Delayed expulsion of adult Trichinella spiralis by mast cell-deficient W/Wv mice. Infection and Immunity 41, 445–447.Google Scholar
Ho, S. B., Niehans, G. A., Lyftogt, C., Yan, P. S., Cherwitz, D. L., Gum, E. T., Dahiya, R. and Kim, Y. S. (1993). Heterogeneity of mucin gene expression in normal and neoplastic tissues. Cancer Research 53, 641–651.Google ScholarPubMed
Horsnell, W. G., 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-4Ralpha-deficient mice. PLoS Pathog 3, 0046–0053.Google Scholar
Huizinga, J. D., Thunenberg, L., Kluppel, M., Malysz, J., Mikkelson, H. B. and Bernstein, A. (1995). W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature, London 373, 347–349.Google Scholar
Ishikawa, N., Horii, Y. and Nawa, Y. (1993). Immune-mediated alteration of the terminal sugars of goblet cell mucins in the small intestine of Nippostrongylus brasiliensis-infected rats. Immunology 78, 303–307.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.CrossRefGoogle ScholarPubMed
Iwashita, J., Sato, Y., Sugaya, H., Takahashi, N., Sasaki, H. and Abe, T. (2003). mRNA of MUC2 is stimulated by IL-4, IL-13 or TNF-alpha through a mitogen-activated protein kinase pathway in human colon cancer cells. Immunology and Cell Biology 81: 275–282.CrossRefGoogle ScholarPubMed
Kalia, N., Hardcastle, J., Keating, J. C., Pelegrin, P., Grundy, D. and Bardhan, K. D. (2008). Intestinal secretory and absorptive functions in Trichinella spiralis mouse model of postinfective gut dysfunction: role of bile acids. Gut 57, 41–49.CrossRefGoogle ScholarPubMed
Kamal, M., Wakelin, D., Ouellette, A. J., Smith, A., Podolsky, D. K. and Mahida, Y. R. (1992). 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
Kandori, H., Hirayama, K., Takeda, M. and Doi, K. (1996). Histochemical, lectin-histochemical and morphometrical characteristics of intestinal goblet cells of germfree and conventional mice. Experimental Animals 45, 155–160.CrossRefGoogle ScholarPubMed
Karlsson, N. G., Olson, F. J., Jovall, P. A., Andersch, Y., Enerback, L. and Hansson, G. C. (2000). Identification of transient glycosylation alterations of sialylated mucin oligosaccharides during infection by the rat intestinal parasite Nippostrongylus brasiliensis. The Biochemical Journal 350, 805–814.CrossRefGoogle ScholarPubMed
Khan, W. I., Abe, T., Ishikawa, N., Nawa, Y. and Yoshimura, K. (1995). Reduced amount of intestinal mucus by treatment with anti-CD4 antibody interferes with the spontaneous cure of Nippostrongylus brasiliensis-infection in mice. Parasite Immunology 17, 485–491.CrossRefGoogle ScholarPubMed
Khan, W. I., Blennerhasset, P. A., Ma, C. and Collins, S. M. (2001 a). Stat6 dependent goblet cell hyperplasia during intestinal nematode infection. Parasite Immunology 23, 39–42.CrossRefGoogle ScholarPubMed
Khan, W. I., Blennerhasset, P. A., Deng, Y., 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. and Collins, S. M. (2006). Gut motor function: immunological control in enteric infection and inflammation. Clinical and Experimental Immunology 143, 389–397.CrossRefGoogle ScholarPubMed
Khan, W. I., Motomura, Y., Blennerhassett, P. A., Kanbayashi, H., Varghese, A. K., El-Sharkawy, R. T., Gauldie, J. and Collins, S. M. (2005). Disruption of CD40-CD40 ligand pathway inhibits the development of intestinal muscle hypercontractility and protective immunity in nematode infection. American Journal of Physiology – Gastrointestinal and Liver Physiology 288, G15–G22.CrossRefGoogle ScholarPubMed
Khan, W. I., Motomura, Y., Verdu, E. F., Blennerhasset, P. A., El-Sharkawy, R. T., Verma-Gandhu, M. and Collins, S. M. (2004). Evidence that altered motility contributes in host defence in nematode infection. Gastroenterology 126, A226 (Abstract).Google Scholar
Khan, W. I., Richard, M., Akiho, H., Blennerhasset, P. A., Humphreys, N. E., Grencis, R. K., Van Snick, J. and Collins, S. M. (2003). Modulation of intestinal muscle contraction by interleukin-9 (IL-9) or IL-9 neutralization: correlation with worm expulsion in murine nematode infections. Infection and Immunity 71, 2430–2438.Google Scholar
Khan, W. I., Vallance, B. A., Blennerhasset, P. A., Deng, Y., Verdue, 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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Koninkx, J. F., Mirck, M. H., Hendriks, H. G., Mouwen, J. M. and van Dijk, J. E. (1988). Nippostrongylus brasiliensis: histochemical changes in the composition of mucins in goblet cells during infection in rats. Experimental Parasitology 65, 84–90.Google Scholar
Lawrence, C. E., Paterson, J. C., 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.Google Scholar
Lundgren, O. (2002). Enteric nerves and diarrhoea. Pharmacology and Toxicology 90, 109–120.Google Scholar
Madden, K. B., Young, K. A., Zhao, A., Gause, W. C., Finkelman, F. D., Katona, I. M., Urban, J. F. Jr. and Shea-Donohue, T. (2004). Enteric nematodes induce stereotypic STAT6-dependent alterations in intestinal epithelial cell function. Journal of Immunology 172, 5616–5621.CrossRefGoogle ScholarPubMed
Manetti, R., Parronchi, P., Giudizi, M. G., Piccinni, M. P., Maggi, E., Trinchieri, G. and Romagnani, S. (1993). Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. Journal of Experimental Medicine 177, 1199–1204.Google Scholar
Marzio, L., Blennerhasset, P. A., Chiverton, S., Vermillion, D. L., Langer, J. and Collins, S. M. (1990). Altered smooth muscle function at worm free regions in Trichinella infected rats. American Journal of Physiology 259, G306–G313.Google 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. (2004). Mast cells disrupt epithelial barrier function during enteric nematode infection. Proceedings of the National Academy of Sciences, USA 100, 7761–7766.CrossRefGoogle Scholar
Miller, H. R. P. (1987). Gastrointestinal mucus, a medium for survival and for elimination of parasitic nematodes and protozoa. Parasitology 94, S77–S100.CrossRefGoogle ScholarPubMed
Miller, H. R. and Huntley, J. F. (1982). Protection against nematodes by intestinal mucus. Advances in Experimental Medicine and Biology 144, 243–245.Google Scholar
Miller, H. R. and Nawa, Y. (1979). Nippostrongylus brasiliensis: intestinal goblet-cell response in adoptively immunized rats. Experimental Parasitology 47, 81–90.CrossRefGoogle ScholarPubMed
Mosmann, T. R. and Coffman, R. L. (1989). Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology 7, 145–173.CrossRefGoogle ScholarPubMed
Motomura, Y., Ghia, J.-E., Wang, H., Akiho, H., El-Sharkawy, R. T., Collins, M., Wan, Y., McLaughlin, J. T. and Khan, W. I. (2008). Enterochromaffin cell and 5-hydroxytryptamine responses to the same infectious agent differ in Th1 and Th2 dominant environments. Gut Jan 15 [Epub ahead of print].Google Scholar
Motomura, Y., Verma-Gandhu, M., El-Sharkawy, R. T., McLaughlin, J., Grencis, R. K. and Khan, W. I. (2004). Colonic 5-HT and muscle responses to the same infectious agent differ in Th1 and Th2 dominant environments. Gastroenterology 216, A (Abstract).Google Scholar
Neutra, M. R. and Forstner, J. F. (1987). Gastrointestinal mucus: synthesis, secretion and function. In Physiology of the Gastrointestinal Tract 2nd Edn (ed. Johnson, L. R.), pp. 975–1009. Raven Press, New York.Google Scholar
Olson, F. J., Johansson, M. E., Klinga-Levan, K., Bouhours, D., Enerback, L., Hansson, G. C. and Karlsson, N. G. (2002). Blood group A glycosyltransferase occurring as alleles with high sequence difference is transiently induced during a Nippostrongylus brasiliensis parasite infection. Journal of Biological Chemistry 277, 15044–15052.CrossRefGoogle ScholarPubMed
Ota, H., Nakayama, J., Momose, M., Hayama, M., Akamatsu, T., Katsuyama, T., Graham, D. Y. and Genta, R. M. (1998). Helicobacter pylori infection produces reversible glycosylation changes to gastric mucins. Virchows Archiv 433, 419–426.Google Scholar
Specian, R. D. and Oliver, M. G. (1991). Functional biology of intestinal goblet cells. American Journal of Physiology 260, C183–C193.CrossRefGoogle ScholarPubMed
Perdue, M. H. and McKay, D. M. (1994). Integrative immunophysiology in the intestinal mucosa. American Journal of Physiology – Gastrointestinal and Liver Physiology 267, G151–G165.CrossRefGoogle ScholarPubMed
Podolsky, D. K. and Isselbacher, K. J. (1983). Composition of human colonic mucin. Selective alteration in inflammatory bowel disease. Journal of Clinical Investigation 72, 142–153.CrossRefGoogle ScholarPubMed
Podolsky, D. K., Lynch-Devaney, K., Stow, J. L., Oates, P., Murgue, B., De-Beaumont, M., Sand, B. E. and Mahida, Y. R. (1993). Identification of human intestinal trefoil factor. Goblet cell-specific expression of a peptide targeted for apical secretion. Journal of Biological Chemistry 268, 6694–6702.Google Scholar
Reinecker, H. C. and Podolsky, D. K. (1995). Human intestinal epithelial cells express functional cytokine receptors sharing the common gamma c chain of the interleukin 2 receptor. Proceedings of the National Academy of Sciences, USA 92, 8353–8357.CrossRefGoogle Scholar
Rothwell, T. L. (1989). Immune expulsion of parasitic nematodes from the alimentary tract. International Journal for Parasitology 19, 139–168.Google Scholar
Sagar, M., Padol, I., Khan, W. I., Bonin, R. P., Blennerhassett, P. A. and Hunt, R. H. (2004). Establishment of T-Helper-2 immune response based gerbil model of enteric infection. Scandinavian Journal of Gastroenterology 39, 668–673.Google Scholar
Sands, B. E. and Podolsky, D. K. (1996). The trefoil peptide family. Annual Review of Physiology 58, 253–273.CrossRefGoogle ScholarPubMed
Sharkey, K. A. and Mawe, G. M. (2002). Neuroimmune and epithelial interactions in intestinal inflammation. Current Opinion in Pharmacology 2, 669–677.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Smith, J. W. and Castro, G. A. (1978). Relation of peroxidase activity in gut mucosa to inflammation. The American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 235, R72–R79.Google Scholar
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
Urban, J. F. Jr, 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
Vallance, B. A., Blennerhassett, P. A. and Collins, S. M. (1997). Increased intestinal muscle contractility and worm expulsion in nematode infected mice. American Journal of Physiology – Gastrointestinal and Liver Physiology 272, G321–G327.Google Scholar
Vallance, B. A., Blennerhassett, P. A., Deng, Y., Matthaei, K. I., Young, I. G. and Collins, S. M. (1999 a). IL-5 contributes to worm expulsion and muscle hypercontractility in a primary T. spiralis infection. American Journal of Physiology 277, G400–G408.Google Scholar
Vallance, B. A., Blennerhassett, P. A., Huizinga, J. D. and Collins, S. M. (2001). Mast cell-independent impairment of host defense and muscle contraction in T. spiralis-infected W/W(V) mice. American Journal of Physiology – Gastrointestinal and Liver Physiology 280, G640–G648.Google Scholar
Vallance, B. A., Croitoru, K. and Collins, S. M. (1998). T lymphocyte-dependent and -independent intestinal smooth muscle dysfunction in the T. spiralis-infected mouse. American Journal of Physiology 275, G1157–G1165.Google Scholar
Vallance, B. A., Galeazzi, F., Collins, S. M. and Snider, D. P. (1999 b). CD4 T cells and major histocompatibility complex class II expression influence worm expulsion and increased intestinal muscle contraction during Trichinella spiralis infection. Infection and Immunity 67, 6090–6097.CrossRefGoogle ScholarPubMed
Vermillion, D. L. and Collins, S. M. (1988). Increased responsiveness of jejunal longitudinal muscle in Trichinella-infected rats. American Journal of Physiology – Gastrointestinal and Liver Physiology 254, G124–G129.CrossRefGoogle ScholarPubMed
Wang, H., Steeds, J., Motomura, Y., Deng, Y., Verma-Gandhu, M., El-Sharkawy, R., McLaughlin, J., Grencis, R. K. and Khan, W. I. (2007). CD4+ T cell-mediated immunological control of enterochromaffin cell hyperplasia and 5-hydroxytryptamine production in enteric infection. Gut 56, 949–957.CrossRefGoogle ScholarPubMed
Wheatcroft, J., Wakelin, D., Smith, A., Mahoney, C. R., Mawe, G. and Spiller, R. (2005). Enterochromaffin cell hyperplasia and decreased serotonin transporter in a mouse model of postinfectious bowel dysfunction. Neurogastroenterology and Motility 17, 863–870.CrossRefGoogle Scholar
Zhao, A., McDermott, J., Urban, J. F. Jr., Gause, W., Madden, K. B., Yeung, K. A., Morris, S. C., Finkelman, F. D. and Shea-Donohue, T. (2003). Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. Journal of Immunology 171, 948–954.Google Scholar
Zhao, A., Urban, J. F. Jr., Morimoto, M., Elfrey, J. E., Madden, K. B., Finkelman, F. D. and Shea-Donohue, T. (2006). Contribution of 5-HT2A receptor in nematode infection-induced murine intestinal smooth muscle hypercontractility. Gastroenterology 131, 568–578.Google Scholar