Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T20:10:52.723Z Has data issue: false hasContentIssue false

Early pulmonary response in rats infected with Trichinella spiralis

Published online by Cambridge University Press:  16 October 2006

S. M. VENTURIELLO
Affiliation:
Chair of Immunology, Faculty of Pharmacy and Biochemistry, University of Buenos Aires, Humoral Immunity Studies Institute CONICET, Junín 956, (1113) Buenos Aires, Argentina
M. L. VERZOLETTI
Affiliation:
Chair of Immunology, Faculty of Pharmacy and Biochemistry, University of Buenos Aires, Humoral Immunity Studies Institute CONICET, Junín 956, (1113) Buenos Aires, Argentina
S. N. COSTANTINO
Affiliation:
Chair of Immunology, Faculty of Pharmacy and Biochemistry, University of Buenos Aires, Humoral Immunity Studies Institute CONICET, Junín 956, (1113) Buenos Aires, Argentina
M. A. FORASTIERO
Affiliation:
Chair of Immunology, Faculty of Pharmacy and Biochemistry, University of Buenos Aires, Humoral Immunity Studies Institute CONICET, Junín 956, (1113) Buenos Aires, Argentina
M. E. ROUX
Affiliation:
Chair of Physiopathology, Faculty of Pharmacy and Biochemistry, University of Buenos Aires, Humoral Immunity Studies Institute CONICET, Junín 956, (1113) Buenos Aires, Argentina

Abstract

The migratory stage of Trichinella spiralis, the newborn larva, travels along the pulmonary microvascular system on its way to the striated muscle cells. In the present study, an important inflammatory reaction was observed on days 5 and 14 post-infection (p.i.) in the lungs of infected rats. This inflammation was characterized by a Th2 cell phenotype of hyperplastic bronchus-associated lymphoid tissue and by goblet cell hyperplasia. Among the inflammatory cells were eosinophils and mast cells scattered over the pulmonary parenchyma. On day 5 p.i. the number of IgE+, CD4+ and CD5+ cells in the bronchus-associated lymphoid tissue were increased and IgE-secreting lung cells were also detected. At the end of the migratory phase of the infection (day 14 p.i.), only IgE+ cells were detected in high numbers and in the bronchoalveolar lavage fluid, an increment in the total IgE levels as well as the presence of IgE and IgA anti-larvae surface were also detected. In cytotoxicity assays, cells from the bronchoalveolar lavage had considerable biological activity since they were able to kill the larvae even in the absence of specific antibodies. These results show that the lung is an organ involved in the immune response developed early during a T. spiralis infection and suggest its importance in the protection of the host.

Type
Research Article
Copyright
2006 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.)

References

REFERENCES

Bienenstock, J. and Clancy, R. L. ( 2005). Bronchus-associated lymphoid tissues. In Mucosal Immunology ( ed. Mestecky, J., Lamm, M. E., Strober, W., Bienenstock, J., McGhee, J. R. and Mayer, L.), pp. 375384. Elsevier Academic Press, New York.CrossRef
Bruschi, F., Solfanelli, S. and Binaghi, R. A. ( 1992). Trichinella spiralis: modifications of the cuticle of the newborn larva during passage through the lung. Experimental Parasitology 75, 19.CrossRefGoogle Scholar
Capron, M. and Capron, A. ( 1994). Immunoglobulin E and effector cells in schistosomiasis. Science 264, 18761877.CrossRefGoogle Scholar
Culley, F. J., Brown, A., Girod, N., Pritchard, D. I. and Williams, T. J. ( 2002). Innate and cognate mechanisms of pulmonary eosinophilia in helminth infection. European Journal of Immunology 32, 13761385.3.0.CO;2-8>CrossRefGoogle Scholar
Czerkinsky, C. C., Nilsson, L. A., Nygren, H., Ouchterlony, O. and Tarkowski, A. ( 1983). A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. Journal of Immunological Methods 65, 109121.CrossRefGoogle Scholar
Dennis, D., Despommier, D. D. and David, N. ( 1970). Infectivity of newborn larvae of Trichinella spiralis in the rat. Journal of Parasitology 56, 974977.CrossRefGoogle Scholar
Despommier, D. D. ( 1983). Biology. In Trichinella and Trichinosis ( ed. Campbell, W. C.), pp. 75151. Plenum Press, New York.CrossRef
Egwang, T. G., Gauldie, J. and Befus, D. ( 1984). Broncho-alveolar leukocyte responses during primary and secondary Nippostrongylus brasiliensis infection in the rat. Parasite Immunology 6, 191201.CrossRefGoogle Scholar
Gansmüller, A., Anteunis, A., Venturiello, S. M., Bruschi, F. and Binaghi, R. A. ( 1987). Antibody-dependent in vitro cytotoxicity of newborn Trichinella spiralis: Nature of the cells involved. Parasite Immunology 9, 281292.CrossRefGoogle Scholar
Garside, P., Kennedy, M., Wakelin, D. and Lawrence, C. ( 2000). Immunopathology of intestinal helminth infection. Parasite Immunology 22, 605612.CrossRefGoogle Scholar
Holmgren, J. and Czerkinsky, C. ( 2005). Mucosal immunity and vaccines. Nature Medicine 11, 545553.CrossRefGoogle Scholar
Jungery, M., Clark, N. W. T. and Parkhouse, M. ( 1983). A major change in surface antigens during the maturation of newborn larvae of Trichinella spiralis. Molecular and Biochemical Parasitology 7, 101109.CrossRefGoogle Scholar
Kazura, J. W. ( 1981). Host defense mechanisms against nematode parasites: destruction of newborn Trichinella spiralis larvae by human antibodies and granulocytes. Journal of Infectious Diseases 143, 712718.CrossRefGoogle Scholar
Lamm, M. E. and Phillips-Quagliata, J. M. ( 2002). Origin and homing of intestinal IgA antibody-secreting cells. Journal of Experimental Medicine 195, 58.CrossRefGoogle Scholar
Larsh, J. E. and Kent, D. E. ( 1949). The effect of alcohol on natural and acquired immunity of mice infected with Trichinella spiralis. American Journal of Tropical Medicine and Hygiene 16, 4553.Google Scholar
Laycock, S. M., Smith, H. and Spicer, B. A. ( 1986). Airway hyper-reactivity and blood, lung and airway eosinophilia in rats treated with Sephadex particles. International Archives of Allergy and Applied Immunology 81, 363367.CrossRefGoogle Scholar
Manson-Smith, D. F., Bruce, R. and Parrott, D. M. V. ( 1979). Villus atrophy and expulsion of intestinal Trichinella spiralis are mediated by T cells. Cellular Immunology 47, 285292.CrossRefGoogle Scholar
Negrão Corrêa, D., Adams, L. S. and Bell, R. G. ( 1999). Variability of the intestinal immunoglobulin E response of rats to infection with Trichinella spiralis, Heligmosomoides polygyrus or Nippostrongylus brasiliensis. Parasite Immunology 21, 287297.CrossRefGoogle Scholar
Nuñez, G. G., Costantino, S. N. and Venturiello, S. M. ( 2003). Immunoparasitological parameters of the intestinal phase of trichinellosis in rats. Parasitology 126, 321325.CrossRefGoogle Scholar
Roux, M. E., Marquez, M. G., Olmos, S., Frecha, C. A. and Florin-Christensen, A. ( 2003). Compartmentalization between gut and lung mucosae in a model of secondary immunodeficiency: effect of thymomodulin. International Journal of Immunopathology and Pharmacology 16, 151156.CrossRefGoogle Scholar
Sainte-Marie, G. ( 1961). A paraffin-embedding technique for studies employing immunofluorescence. The Journal of Histochemistry and Cytochemistry 10, 250256.Google Scholar
Silveira, M. R., Nunes, K. P., Cara, D. C., Souza, D. G., Corrêa, A., Texeira, M. M. and Negrão-Corrêa, D. ( 2002). Infection with Strongyloides venezuelensis induces transient airway eosinophilic inflammation, an increase in immunoglobulin E, and hyperresponsiveness in rats. Infection and Immunity 70, 62636272.CrossRefGoogle Scholar
Soulé, C. ( 1991). Cycle biologique. In La Trichinellose: une Zoonose en Évolution ( ed. Soulé, C. and Dupouy-Camet, J.), pp. 1524. Office International des Epizooties, Centre National d'Etudes Vétérinaires et Alimentaires, Paris.
Scicchitano, R., Husband, A. J. and Clancy, R. L. ( 1984). Contribution of intraperitoneal immunization to the local immune response in the respiratory tract of sheep. Immunology 53, 375384.Google Scholar
Venturiello, S. M., Giambartolomei, G. G. and Costantino, S. N. ( 1993). Immune killing of newborn Trichinella spiralis larvae by human leukocytes. Parasite Immunology 15, 559564.CrossRefGoogle Scholar
Vermeer, L. A., de Boer, N. K., Bucci, C., Bos, N. A., Kroese, F. G. and Alberti, S. ( 1994). MRC OX19 recognizes the rat CD5 surface glycoprotein, but does not provide evidence for a population of CD 5bright B cells. European Journal of Immunology 24, 585592.CrossRefGoogle Scholar
Wakelin, D. ( 1997). Immune response to intestinal parasites: protection, pathology and prophylaxis. Parassitologia 39, 269274.Google Scholar
Wang, C. H. and Bell, R. G. ( 1986). Trichinella spiralis: vascular recirculation and organ retention of newborn larvae in rats. Experimental Parasitology 62, 430441.CrossRefGoogle Scholar
Wang, C. H. and Bell, R. G. ( 1992). Characterization of cellular and molecular immune effectors against Trichinella spiralis newborn larvae in vivo. Cellular and Molecular Biology 38, 311325.Google Scholar
Wilkinson, M. J., Wells, C. and Behnke, J. M. ( 1990). Necator americanus in the mouse: histopathological changes associated with the passage of larvae through the lung of mice exposed to primary and secondary infection. Parasitology Research 76, 386392.CrossRefGoogle Scholar
Wranicz, M. J., Cabaj, W. and Moskwa, B. ( 1999). Trichinella spiralis: the infectivity of synchronous newborn larvae of different ages inoculated intraocularly. Parasitology Research 85, 290292.CrossRefGoogle Scholar