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Acute trichinellosis increases susceptibility to Giardia lamblia infection in the mouse model

Published online by Cambridge University Press:  08 May 2006

N. von ALLMEN ,
S. CHRISTEN ,
U. FORSTER ,
B. GOTTSTEIN ,
M. WELLE  and
N. MÜLLER
N. von ALLMEN
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Berne, P.O. Box 8466, CH-3001 Berne, Switzerland
S. CHRISTEN
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Berne, P.O. Box 8466, CH-3001 Berne, Switzerland
U. FORSTER
Affiliation:
Institute of Veterinary Pathology, Vetsuisse Faculty, University of Berne, P.O. Box 8466, CH-3001 Berne, Switzerland
B. GOTTSTEIN
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Berne, P.O. Box 8466, CH-3001 Berne, Switzerland
M. WELLE
Affiliation:
Institute of Veterinary Pathology, Vetsuisse Faculty, University of Berne, P.O. Box 8466, CH-3001 Berne, Switzerland
N. MÜLLER
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Berne, P.O. Box 8466, CH-3001 Berne, Switzerland
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Abstract

The intestinal protozoan parasite Giardia lamblia causes diarrhoea in humans and animals. In the present study, we used the C57BL/6 inbred mouse model to assess the impact of a nematode (Trichinella spiralis) infection on the course of a G. lamblia (clone GS/M-83-H7) infection. Acute trichinellosis coincided with transient intestinal inflammation and generated an intestinal environment that strongly promoted growth of G. lamblia trophozoites although the local anti-Giardia immunoglobulin (Ig) A production was not affected. This increased G. lamblia infection intensity correlated with intestinal mast cell infiltration, mast cell degranulation, and total IgE production. Furthermore, a G. lamblia single-infection investigated in parallel also resulted in intestinal mast cell accumulation but severe infiltration was triggered in the absence of IgE. Recently, intestinal mast cells emerging during a G. lamblia infection were reported to be involved in those immunological mechanisms that control intestinal proliferation of the parasite in mice. This anti-giardial activity was assumed to be related to the capacity of mast cells to produce IL-6. However, this previous assumption was questioned by our present immunohistological findings indicating that murine intestinal mast cells, activated during a G. lamblia infection were IL-6-negative. In the present co-infection experiments, mast cells induced during acute trichinellosis were not able to control a concurrent G. lamblia infection. This observation makes it feasible that the T. spiralis infection created an immunological and physiological environment that superimposed the anti-giardial effect of mast cells and thus favoured intestinal growth of G. lamblia trophozoites in double-infected mice. Furthermore, our findings raise the possibility that intestinal inflammation e.g. as a consequence of a ‘pre-existing’ nematode infection is a factor which contributes to increased susceptibility of a host to a G. lamblia infection. The phenomenon of a ‘pre-existing’ nematode infection prior to a G. lamblia infection is a frequent constellation in endemic areas of giardiasis and may therefore have a direct impact on the epidemiological situation of the disease.

Keywords

Giardia lambliagiardiasisTrichinella spiralistrichinellosisintestinal immune responseintestinal inflammation
Type
Research Article
Information
Parasitology , Volume 133 , Issue 2 , August 2006 , pp. 139 - 149
Copyright
2006 Cambridge University Press

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References

REFERENCES

Adam, R. D. ( 1991). The biology of Giardia spp. Microbiological Reviews 55, 706–732.Google Scholar
Aggarwal, A., Merritt, J. W. and Nash, T. E. ( 1989). Cysteine-rich variant surface proteins of Giardia lamblia. Molecular and Biochemical Parasitology 32, 39–48.CrossRefGoogle Scholar
Bienz, M., Dai, W. J., Welle, M., Gottstein, B. and Müller, N. ( 2003). Interleukin-6-deficient mice are highly susceptible to Giardia lamblia infections but exhibit normal intestinal IgA responses against the parasite. Infection and Immunity 71, 1569–1573.CrossRefGoogle Scholar
Di Prisco, M. C., Hagel, I., Lynch, N. R., Barrios, R. M., Alvarez, N. and Lopez, R. ( 1993). Possible relationship between allergic disease and infection by Giardia lamblia. Annals of Allergy 70, 210–213.Google Scholar
Donaldson, L. E., Schmitt, E., Huntley, J. F., Newlands, G. F. 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
Eckmann, L. ( 2003). Mucosal defences against Giardia. Parasite Immunology 25, 259–270.CrossRefGoogle Scholar
Erlich, J. H., Anders, R. F., Roberts-Thomson, I. C., Schrader, J. W. and Mitchell, G. F. ( 1983). An examination of differences in serum antibody specificities and hypersensitivity reactions as contributing factors to chronic infection with the intestinal protozoan parasite, Giardia muris, in mice. Australian Journal of Experimental Biology and Medical Sciences 61, 599–615.CrossRefGoogle Scholar
Faubert, G. M. ( 2000). Immune response to Giardia duodenalis. Clinical Microbiology Reviews 13, 35–54.CrossRefGoogle 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.CrossRefGoogle Scholar
Finkelman, F. D., Shea-Donohue, T., Goldhill, J., Sullivan, C. A., Morris, S. C., Madden, K. B., Gause, W. C. and Urban, J. F. Jr. ( 1997). Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annual Review of Immunology 15, 505–533.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Friend, D. S., Gurish, M. F., Austen, K. F., Hunt, J. and Stevens, R. L. ( 2000). Senescent jejunal mast cells and eosinophils in the mouse preferentially translocate to the spleen and draining lymph node, respectively, during the recovery phase of helminth infection. Journal of Immunology 165, 344–352.CrossRefGoogle Scholar
Galli, S. J., Nakae, S. and Tsai, M. ( 2005). Mast cells in the development of adaptive immune responses. Nature Immunology 6, 135–142.CrossRefGoogle Scholar
Garside, P., Kennedy, M. W., Wakelin, D. and Lawrence, C. E. ( 2000). Immunopathology of intestinal helminth infection. Parasite Immunology 22, 605–612.CrossRefGoogle Scholar
Gendrel, D., Treluyer, J. M. and Richard-Lenoble, D. ( 2003). Parasitic diarrhea in normal and malnourished children. Fundamental and Clinical Pharmacology 17, 189–197.CrossRefGoogle Scholar
Ghildyal, N., McNeil, H. P., Stechschulte, S., Austen, K. F., Silberstein, D., Gurish, M. F., Somerville, L. L. and Stevens, R. L. ( 1992). IL-10 induces transcription of the gene for mouse mast cell protease-1, a serine protease preferentially expressed in mucosal mast cells of Trichinella spiralis-infected mice. Journal of Immunology 149, 2123–2129.Google Scholar
Gottstein, B., Deplazes, P. and Tanner, I. ( 1993). In vitro synthesized immunoglobulin A from nu/+ and reconstituted nu/nu mice against a dominant surface antigen of Giardia lamblia. Parasitology Research 79, 644–648.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Gurish, M. F., Bryce, P. J., Tao, H., Kisselgof, A. B., Thornton, E. M., Miller, H. R., Friend, D. S. and Oettgen, H. C. ( 2004). IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. Journal of Immunology 172, 1139–1145.CrossRefGoogle Scholar
Kamiya, M., Oku, Y., Itayama, H. and Ohbayashi, M. ( 1985). Prolonged expulsion of adult Trichinella spiralis and eosinophil infiltration in mast cell-deficient W/Wv mice. Journal of Helminthology 59, 233–239.CrossRefGoogle Scholar
Keister, D. B. ( 1983). Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Transaction of the Royal Society of Tropical Medicine and Hygiene 77, 487–488.CrossRefGoogle Scholar
Khan, W. I. and Collins, S. M. ( 2004). Immune-mediated alteration in gut physiology and its role in host defence in nematode infection. Parasite Immunology 26, 319–326.CrossRefGoogle Scholar
Langford, T. D., Housley, M. P., Boes, M., Chen, J., Kagnoff, M. F., Gillin, F. D. and Eckmann, L. ( 2002). Central importance of immunoglobulin A in host defense against Giardia spp. Infection and Immunity 70, 11–18.CrossRefGoogle Scholar
Lawrence, C. E. ( 2003). Is there a common mechanism of gastrointestinal nematode expulsion? Parasite Immunology 25, 271–281.Google Scholar
Li, E., Zhou, P., Petrin, Z. and Singer, S. ( 2004). Mast cell-dependent control of Giardia lamblia infections in mice. Infection and Immunity 72, 6642–6649.CrossRefGoogle Scholar
Li, E., Zhou, P. and Singer, S. ( 2006). Neuronal nitric oxide synthetase is necessary for elimination of Giardia lamblia infections in mice. Journal of Immunology 176, 516–521.CrossRefGoogle Scholar
Maizels, R. M., Balic, A., Gomez-Excobar, N., Nair, M., Taylor, M. D. and Allen, J. E. ( 2004). Helminth parasites-masters of regulation. Immunological Reviews 201, 89–116.CrossRefGoogle Scholar
Matossian, R. M., Salti, I. and Stephan, E. ( 1977). Variation in serum immunoglobulin levels in acute trichinosis. Journal of Helminthology 51, 1–4.CrossRefGoogle Scholar
McGee, D. W., Elson, C. O. and McGee, J. R. ( 1993). Enhancing effect of cholera toxin on interleukin-6 secretion by IEC-6 intestinal epithelial cells: mode of action and augmentation effect of inflammatory cytokines. Infection and Immunity 61, 970–978.Google Scholar
Mitchell, G. F., Anders, R. F., Brown, G. V., Handman, E., Roberts-Thompson, I. C., Chapman, C. B., Forsyth, K. P., Kahl, L. P. and Cruise, K. M. ( 1982). Analysis of infection characteristics and antiparasite immune responses in resistant compared with susceptible hosts. Immunological Reviews 61, 137–188.CrossRefGoogle Scholar
Morakote, N., Sukhavat, K., Khamboonruang, C., Siriprasert, V., Suphawitayanukul, S. and Thamasonthi, W. ( 1992). Persistence of IgG, IgM, and IgE antibodies in human trichinosis. Tropical Medicine and Parasitology 43, 167–169.Google Scholar
Müller, N. and von Allmen, N. ( 2005). Recent insights into the mucosal reactions associated with Giardia lamblia infections. International Journal for Parasitology 35, 1339–1347.CrossRefGoogle Scholar
Owen, I. L. ( 2005). Parasitic zoonoses in Papua New Guinea. Journal of Helminthology 79, 1–14.CrossRefGoogle Scholar
Prophet, E. D., Mills, B., Arrington, J. B. and Sobin, L. H. ( 1994). Laboratory Methods in Histotechnology of the Armed Forces Institute of Pathology2nd Edn. American Registry of Pathology, Washington, D.C., USA.
Roberts-Thompson, I. C., Grove, D. I., Stevens, D. P. and Warren, K. S. ( 1976). Suppression of giardiasis during the intestinal phase of trichinosis in the mouse. Gut 17, 953–958.CrossRefGoogle Scholar
Rosenberg, E. B., Polmar, S. H. and Whalen, G. E. ( 1971). Increased circulating IgE in trichinosis. Annals of Internal Medicine 75, 575–578.CrossRefGoogle Scholar
Singer, S. M. and Nash, T. E. ( 2000). T-cell-dependent control of acute Giardia lamblia infections in mice. Infection and Immunity 68, 170–175.CrossRefGoogle Scholar
Stäger, S., Gottstein, B. and Müller, N. ( 1997). Systemic and local antibody response in mice induced by a recombinant peptide fragment from Giardia lamblia variant surface protein (VSP) H7 produced by a Salmonella typhimurium vaccine strain. International Journal for Parasitology 27, 965–971.CrossRefGoogle Scholar
Stäger, S. and Müller, N. ( 1997). Giardia lamblia infections in B-cell-deficient transgenic mice. Infection and Immunity 65, 3944–3946.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 15, 2046–2052.CrossRefGoogle Scholar
Venkatesan, P., Finch, R. G. and Wakelin, D. ( 1997). A comparison of mucosal inflammatory responses to Giardia muris in resistant B10 and susceptible BALB/c mice. Parasite Immunology 19, 137–143.CrossRefGoogle Scholar
Watanabe, N., Bruschi, F. and Korenaga, M. ( 2005). IgE: a question of protective immunity in Trichinellaspiralis infection. Trends in Parasitology 21, 175–178.CrossRefGoogle Scholar
Zhou, P., Li, E., Zhu, N., Robertson, J., Nash, T. and Singer, S. M. ( 2003). Role of interleukin-6 in the control of acute and chronic Giardia lamblia infections in mice. Infection and Immunity 71, 1566–1568.CrossRefGoogle Scholar