Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-26T00:53:59.990Z Has data issue: false hasContentIssue false
  • English
  • Français

The immune response to and immunomodulation by Hymenolepis diminuta

Published online by Cambridge University Press:  20 August 2009

DEREK M. McKAY
DEREK M. McKAY*
Affiliation:
Gastrointestinal Research Group, Department of Physiology and Pharmacology, Calvin, Phoebe and Joan Snyder Institute of Infection, Immunity and Inflammation, Univeristy of Calgary, Calgary, Alberta, Canada
*
Corresponding author: Derek M. McKay, PhD., GIRG, HSC 1717, Univeristy of Calgary, 3330 Hospital Drive NW, Calgary, AlbertaCanada, T2N 4N1. Tel: (403)-220-7362. Fax: (403)-283-3028. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Analyses of laboratory-based helminth-rodent model systems have been immensely useful in delineating the workings of the mammalian immune system. Investigations in the 1970s–1980s on the fate of the rat tapeworm, Hymenolepis diminuta, in rats and mice and the systemic and local responses evoked following infection have contributed directly to our knowledge of how permissive and non-permissive hosts respond to the challenge of infection with a helminth parasite. This convenient laboratory model system has, in the authors' opinion, regrettably received considerably less attention in recent years. With the goal of highlighting the utility of this model system, data is presented on: (1) the immune and enteric responses of rats and mice to infection with H. diminuta; (2) the ability of excretory or secretory products derived from H. diminuta to significantly reduce T cell and macrophage activation in vitro; and (3) how assessment of H. diminuta-rodent models can be used to identify immune effector or regulatory mechanisms that can be translated into novel treatments for inflammatory and autoimmune disorders.

Keywords

Intestinal immunitysmall intestinecolonhelminthtapeworm
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 385 - 394
Copyright
Copyright © Cambridge University Press 2009

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

Andreassen, J., Bennet-Jenkins, E. M. and Bryant, C. (1999). Immunology and biochemistry of Hymenolepis diminuta. Advances in Parasitology 42, 223–275.CrossRefGoogle ScholarPubMed
Andreassen, J., Hindsbo, O. and Vienberg, S. (1982). Responsiveness of congenitally thymus deficient nude mice to the intestinal cestode, Hymenolepis diminuta. International Journal for Parasitology 12, 215–219.CrossRefGoogle Scholar
Andreassen, J. and Hopkins, C. A. (1980). Immunologically mediated rejection of Hymenolepis diminuta by its normal host, the rat. Journal of Parasitology 66, 898–903.CrossRefGoogle ScholarPubMed
Bach, J.-F. (2002). The effect of infections on susceptibility to autoimmune and allergic diseases. New England Journal of Medicine 347, 911–20.CrossRefGoogle ScholarPubMed
Barton-Behravesh, C., Mayberry, L. F., Bristol, J. R., Cardenas, V. M., Mena, K. D., Martíenez-Ocaña, J., Flisser, A. and Snowden, K. F. (2008). Population-based survey of taeniasis along the United States-Mexico border. Annals of Tropical Medicine and Parasitology 102, 325–333.CrossRefGoogle ScholarPubMed
Befus, A. D. and Threadgold, L. T. (1975). Possible immunological damage to the tegument of Hymenolepis diminuta in mice and rats. Parasitology 71, 525–534.CrossRefGoogle Scholar
Cabello, F. C. (2007) Aquaculture and public health. The emergence of diphyllobothriasis in Chile and the world. Reviews in Medicine (Chile) 135, 1064–1071.Google Scholar
Christie, P. R., Wakelin, D. and Wilson, M. M. (1979). The effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in rats. Parasitology 78, 323–330.CrossRefGoogle ScholarPubMed
Collins, S. M., Blennerhassett, P. A., Blennerhassett, M. G. and Vermillion, D. L. (1989). Impaired acetylcholine release from the myenteric plexus of Trichinella-infected rats. American Journal of Physiology Gastrointestinal and Liver Physiology 257, G898–G903.CrossRefGoogle ScholarPubMed
Dwinell, M. B., Bass, P., Schaefer, D. M. and Oaks, J. A. (1997). Tapeworm infection decreases intestinal transit and enteric aerobic bacterial populations. American Journal of Physiology Gastrointestinal and Liver Physiology 273, G480–G485.CrossRefGoogle ScholarPubMed
Elliott, D. E., Setiawan, T., Metwali, A., Blum, A., Urban, J. F. (Jr.) and Weinstock, J. V. (2004). Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. European Journal of Immunology 34, 2690–2698.CrossRefGoogle ScholarPubMed
Elliott, D. E., Summers, R. W. and Weinstock, J. V. (2007). Helminths as governors of immune-mediated inflammation. International Journal for Parasitology 37, 457–464.CrossRefGoogle ScholarPubMed
Fallon, P. G. and Alcami, A. (2006). Pathogen-derived immunomodulatory molecules: future immunotherapeutics? Trends in Immunology 27, 470–476.CrossRefGoogle ScholarPubMed
Fallon, P. G., Ballantyne, S. J., Mangan, N. E., Barlow, J. L., Dasvarma, A., Hewett, D. R., McIlgorm, A., Jolin, H. E. and McKenzie, A. N. (2006). Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. Journal of Experimental Medicine 203, 1105–1116.CrossRefGoogle ScholarPubMed
Goodridge, H. S., Stepek, G., Harnett, W. and Harnett, M. M. (2005). Signaling mechanisms underlying subversion of the immune response by the filarial nematode secreted product ES-62. Immunology 115, 296–304.CrossRefGoogle ScholarPubMed
Harnett, W. and Harnett, M. M. (2006). Filarial nematode secreted product ES-62 is an anti-inflammatory agent: therapeutic potential of small molecule derivatives and ES-62 peptide mimetics. Clinical and Experimental Pharmacology and Physiology 33, 511–518.CrossRefGoogle ScholarPubMed
Harnett, W. and Harnett, M. M. (2008) Therapeutic immunomodulators from nematode parasites. Expert Reviews in Molecular Medicine 10, e18–e25.CrossRefGoogle ScholarPubMed
Hopkins, C. A. (1982). Immunological memory in mice to adult Hymenolepis diminuta (Cestoda). Journal of Parasitology 68, 32–38.CrossRefGoogle ScholarPubMed
Hopkins, C. A., Subramanian, G. and Stallard, H. (1972 a). The development of Hymenolepis diminuta in primary and secondary infections in mice. Parasitology 64, 401–412.CrossRefGoogle ScholarPubMed
Hopkins, C. A., Subramanian, G. and Stallard, H. (1972 b). The effect of immunosuppressants on the development of Hymenolepis diminuta in mice. Parasitology 65, 111–120.CrossRefGoogle ScholarPubMed
Hunter, M. M., Wang, A., Hirota, C. L. and McKay, D. M. (2005). Neutralizing anti-IL-10 antibody blocks the protective effect of tapeworm infection in a murine model of chemically-induced colitis. Journal of Immunology 174, 7368–7375.CrossRefGoogle Scholar
Hunter, M. M., Wang, A. and McKay, D. M. (2007). Helminth infection enhances disease in a murine TH2 model of colitis. Gastroenterology 132, 1320–1330.CrossRefGoogle Scholar
Isaak, D. D. (1983). In vitro tapeworm extract-induced proliferative responses of gut-associated lymphoid cells from Hymenolepis diminuta infected mice. Journal of Helminthology 57, 43–50.CrossRefGoogle ScholarPubMed
Isaak, D. D., Jacobson, R. H. and Reed, N. D. (1975). Thymus dependence of tapeworm (Hymenolepis diminuta) elimination from mice. Infection and Immunity 12, 1478–1479.CrossRefGoogle ScholarPubMed
Johnston, M. J. G., MacDonald, J. A. and McKay, D. M. (2009). Parasitic helminths: a pharmacopeia of anti-inflammatory molecules. Parasitology 136, 125–147.CrossRefGoogle ScholarPubMed
Lundgren, O. (1998). 5-hydroxytryptamine, enterotoxins, and intestinal fluid secretion. Gastroenterology 115, 1009–1012.CrossRefGoogle ScholarPubMed
Maizels, R. M. (2005). Infections and allergy – helminths, hygiene and host immune regulation. Current Opinion in Immunology 17, 656–661.CrossRefGoogle ScholarPubMed
McCaigue, M. D. and Halton, D. W. (1987). Immunological damage to Hymenolepis diminuta following a challenge infection in C57 mice. International Journal for Parasitology 17, 795–803.CrossRefGoogle ScholarPubMed
McKay, D. M. (2009) The therapeutic helminth? Trends in Parasitology 25, 109–114.CrossRefGoogle ScholarPubMed
McKay, D. M. and Fairweather, I. (1997). A role for the enteric nervous system in the response to helminth infections. Parasitology Today 13, 63–69.CrossRefGoogle ScholarPubMed
McKay, D. M., Halton, D. W., Johnston, C. F., Fairweather, I. and Shaw, C. (1990 a) Hymenolepis diminuta: changes in intestinal morphology and the enterochromaffin cell population associated with infection in male C57 mice. Parasitology 101, 107–113.CrossRefGoogle ScholarPubMed
McKay, D. M., Halton, D. W., McCaigue, M. D., Johnston, C. F., Fairweather, I. and Shaw, C. (1990 b) Hymenolepis diminuta: Intestinal goblet cell response in male C57 mice. Experimental Parasitology 71, 9–20.CrossRefGoogle ScholarPubMed
McKay, D. M., Halton, D. W., Shaw, C., Johnston, C. F., Fairweather, I. and Buchanan, K. D. (1991) Hymenolepis diminuta: changes in the levels of certain intestinal regulatory peptides in infected C57 mice. Experimental Parasitology 73, 5–26.CrossRefGoogle ScholarPubMed
McKay, D. M. and Khan, W. I. (2003). STAT-6 is an absolute requirement for murine rejection of Hymenolepis diminuta. Journal of Parasitology 89, 188–189.CrossRefGoogle ScholarPubMed
McKay, D. M. and Wallace, J. L. (2009). Acetic acid induced gastric ulceration in rats is not affected by infection with Hymenolepis diminuta. Journal of Parasitology 95, 481–482.CrossRefGoogle Scholar
Moro, P. and Schantz, P. M. (2009). Echinococcosis: a review. International Journal of Infectious Diseases 13, 125–133.CrossRefGoogle ScholarPubMed
Motomura, Y., Ghia, J. E., Wang, H., Akiho, H., El-Sharkawy, R. T., Collins, S. 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 57, 475–481.CrossRefGoogle Scholar
Motomura, Y., Wang, H., Deng, Y., El-Sharkawy, R. T., Verdu, E. F. and Khan, W. I. (2009) Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clinical and Experimental Immunology 155, 88–95.CrossRefGoogle Scholar
Palmas, C., Bortoletti, G., Gabriele, F., Wakelin, D. and Conchedda, M. (1997). Cytokine production during infection with Hymenolepis diminuta in Balb/c mice. International Journal for Parasitology 27, 855–859.CrossRefGoogle ScholarPubMed
Persaud, R., Wang, A., Reardon, C. and McKay, D. M. (2007) Characterization of the immuno-regulatory response to the tapeworm Hymenolepis diminuta in the non-permissive mouse host. International Journal for Parasitology 37, 393–403.CrossRefGoogle Scholar
Reardon, C., Sanchez, A., Hogaboam, C. M. and McKay, D. M. (2001). Tapeworm infection reduces the ion transport abnormalities induced by dextran sulphate sodium (DSS) colitis. Infection and Immunity 69, 4417–4423.CrossRefGoogle Scholar
Reyes, J. L. and Terrazas, L. I. (2007). The divergent roles of alternatively activated macrophages in helminthic infections. Parasite Immunology 29, 609–619.CrossRefGoogle ScholarPubMed
Setiawan, T., Metwali, A., Blum, A. M., Ince, M. N., Urban, J. F. (Jr.), Elliott, D. E. and Weinstock, J. V. (2007) Heligmosomoides polygyrus promotes regulatory T-cell cytokine production in the murine normal distal intestine. Infection and Immunity 75, 4655–4663.CrossRefGoogle ScholarPubMed
Silver, B. B., Dick, T. A. and Welch, H. E. (1980). Concurrent infections of Hymenolepis diminuta and Trichinella spiralis in the rat intestine. Journal of Parasitology 66, 786–791.CrossRefGoogle ScholarPubMed
Smith, P., Mangan, N. E. and Fallon, P. G. (2009). Generation of parasite antigens for use in Toll-like receptor research. Methods in Molecular Biology 517, 401–413.CrossRefGoogle ScholarPubMed
Smyth, J. D. (1994). Cestoda: Cyclophyllidea. In An Introduction to Parasitology, 3rd edition, pp. 321–326. Cambridge University Press, Cambridge.Google Scholar
Starke, W. A. and Oaks, J. A. (2001). Ileal mucosal mast cell, eosinophil, and goblet cell populations during Hymenolepis diminuta infection of the rat. Journal of Parasitology 87, 1222–1225.CrossRefGoogle ScholarPubMed
Starke-Buzetti, W. A. and Oaks, J. A. (2008). Increased glial-derived neurotrophic factor in the small intestine of rats infected with the tapeworm, Hymenolepis diminuta. International Journal of Pathology 89, 458–465.Google ScholarPubMed
Summers, R. W., Elliott, D. E., Urban, J. F.(Jr.), Thompson, R. and Weinstock, J. V. (2005). Trichuris suis therapy in Crohn's disease. Gut 54, 87–90.CrossRefGoogle ScholarPubMed
van der Kleij, D., Latz, E., Brouwers, J. F. H. M., Kruize, Y. C. M., Schmitz, M., Kurt-Jones, E. A., Espevik, T., De Jong, E. C., Kapsenberg, M. L., Golenbock, D. T., Tielens, A. G. M. and Yazdanbakhsh, M. (2002). A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. Journal of Biological Chemistry 277, 48122–48129.Google ScholarPubMed
Wang, A. and McKay, D. M. (2005). Immune modulation by a high molecular weight protein from the rat tapeworm Hymenolepis diminuta. Parasitology 130, 575–585.CrossRefGoogle ScholarPubMed
Webb, R. A., Hoque, T. and Dimas, S. (2007). Expulsion of the gastrointestinal cestode, Hymenolepis diminuta by tolerant rats: evidence for mediation by a Th2 type immune enhanced goblet cell hyperplasia, increased mucin production and secretion. Parasite Immunology 29, 11–21.CrossRefGoogle ScholarPubMed
Wilson, M. S. and Maizels, R. M. (2006). Regulatory T cells induced by parasites and the modulation of allergic responses. Chemical Immunology and Allergy 90, 176–195.Google ScholarPubMed
Wood, J. D. (1993). Neuro-immunophysiology of colon function. Pharmacology 47, 7–13.CrossRefGoogle ScholarPubMed
Zimmerman, N. P., Brownfield, M. S., DeVente, J., Bass, P. and Oaks, J. A. (2008). cGMP secreted from the tapeworm Hymenolepis diminuta is a signal molecule to the host intestine. Journal of Parasitology 94, 771–779.CrossRefGoogle Scholar