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The relative involvement of Th1 and Th2 associated immune responses in the expulsion of a primary infection of Heligmosomoides polygyrus in mice of differing response phenotype

  • A. Ben-Smith (a1), D.A. Lammas (a2) and J.M. Behnke (a3)
  • DOI:
  • Published online: 01 February 2007

T helper cell (Th1 and Th2) associated responses were examined following a primary infection with the gastrointestinal nematode Heligmosomoides polygyrus in five inbred strains of mice with different resistance phenotypes. Levels of (i) mast cell protease, (ii) specific IgE, (iii) nitric oxide and (iv) specific IgG2a, as markers of Th2 and Th1 associated responses, respectively, were determined in sera and intestinal fluids and correlated with worm burdens. The ‘fast’ responder (resistant) strains SWR and SJL produced strong Th2 and Th1 associated responses respectively in a mutually exclusive fashion. The F1 hybrid (SWR×SJL) F1, showed rapid expulsion of the parasite and expressed both intense Th1 and Th2 responses, suggesting synergism between Th1 and Th2 activity in these mice. The results indicate that both Th2 and Th1 responses operate in mice following a primary infection with H. polygyrus and that each Th response may be involved to a greater or lesser degree within certain strains. Resistance to H. polygyrus was found to correlate only to the intensity of either the gut-associated mastocytosis or nitric oxide production in these strains but not to either specific IgE or IgG2a titres. Chronic infections in the ‘slow’ response phenotype mouse strains CBA and C57BL/10, were associated with both poor Th2 and poor Th1-associated responses attributed to a general parasite-mediated immunosuppression of the host immune response to infection.

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This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

D. Artis , C.S. Potten , K.J. Else , F.D. Finkleman & R.K. Grencis (1999) Trichuris muris: Host intestinal epithelial cell hyperproliferation during chronic infection is regulated by interferon-γ. Experimental Parasitology 92, 144153.

J.M. Behnke (1987) Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 171.

J.M. Behnke & H.A. Parish (1979) Expulsion of Nematospiroides dubius from the intestine of mice treated with immune serum. Parasite Immunology 1, 2631.

J.M. Behnke & M. Robinson (1985) Genetic control of immunity to Nematospiroides dubius: a 9-day anthelmintic abbreviated immunizing regime which separates weak and strong responder strains of mice. Parasite Immunology 7, 235253.

J.M. Behnke & F.N. Wahid (1991) Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): H-2 linked genes determine worm survival. Parasitology 103, 157164.

R.L. Coffman , B.W.P. Seymour , S. Hudak , J. Jackson & D. Rennick (1989) Antibody to interleukin 5 inhibits helminth-induced eosinophilia in mice. Science 245, 308310.

M.S. Dehlawi & D. Wakelin (1988) Suppression of mucosal mastocytosis by Nematospiroides dubius results from an adult worm-mediated effect upon host lymphocytes. Parasite Immunology 10, 8595.

M.S. Dehlawi , D. Wakelin & J.M. Behnke (1987) Suppression of mucosal mastocytosis by infection with the intestinal nematode Nematospiroides dubius. Parasite Immunology 9, 187194.

C.O. Elson , W. Ealding & J. Lefkowitz (1984) A lavage technique allowing repeated measurement of IgA antibody in mouse intestinal secretions. Journal of Immunological Methods 67, 101108.

F.D. Finkelman , J. Holmes , I.M. Katona , J.F. Urban Jr, M.P. Beckmann , L.S. Park , K.A. Schooley , R.L. Coffman , T.R. Mosmann & W.E. Paul (1990) Lymphokine control of in vivo immunoglobulin isotype selection. Annual Review of Immunology 8, 303333.

F.D. Finkelman , T. Shea-Donohue , J. Goldhill , C.A. Sullivan , S.C. Morris , K.B. Madden , W.C. Gause & J.F. Urban Jr (1997) Cytokine regulation of host defense against parasitic gastrointestinal nematodes. Lessons from studies with rodent models. Annual Review of Immunology 15, 505533.

P. Garside , M.W. Kennedy , D. Wakelin & C. Lawrence (2000) Immunopathology of intestinal helminth infection. Parasite Immunology 22, 605612.

L.C. Green , D.A. Wagner , J. Glogowski , P.L. Skipper , J.S. Wishnok ]#x0026; S.R. Tannenbaum (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Analytical Biochemistry 126, 131138.

R.K. Grencis , K.J. Else , J.F. Huntley & S.I. Nishikawa (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, 5559.

J.F. Huntley , C. Gooden , G.F. Newlands , A. Mackellar , D.A. Lammas , M. Tuohy , R.G. Woodbury & H.R.P. Miller (1990) Distribution of intestinal mast cell protease in blood and tissues of normal and Trichinella infected mice. Parasite Immunology 12, 8595.

S.N. Jenkins & J.M. Behnke (1977) Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75, 7178.

F.Y. Liew , S. Milliott , Y. Li , R. Lelchuk , R. Chan & H. Ziltener (1989) Macrophage activation by interferon-gamma from host-protective T cells is inhibited by interleukin (IL) 3 and IL4 produced by disease-promoting T cells in leishmaniasis. European Journal of Immunology 19, 12271232.

T.R. Mossman & R.L. Coffman (1989) Heterogeneity of cytokine secretion patterns and function of helper T cells. Advances in Immunology 46, 111147.

T.R. Mossman & K.W. Moore (1991) The role of IL-10 in crossregulation of Th1 and Th2 responses. Immunology Today 12, A49A53.

Y. Nawa & H.R.P. Miller (1979) Adoptive transfer of intestinal mast cell response in rats infected with Nippostrongylus brasiliensis. Cellular Immunology 42, 225239.

D. Negrao-Correa (2001) Importance of immunoglobulin E (IgE) in the protective mechanism against gastrointestinal nematode infection: looking at the intestinal mucosae. Revista do Instituto de Medicina Tropical Sao Paulo 43, 291299.

D.N. Onah & Y. Nawa (2000) Mucosal immunity against parasitic gastrointestinal nematodes. Korean Journal of Parasitology 38, 209236.

S. Romagnani (1992) Induction of Th1 and Th2 responses: a key role for the ‘natural’ immune response? Immunology Today 13, 379381.

T.L.W. Rothwell (1989) Immune expulsion of parasitic nematodes from the alimentary tract. International Journal for Parasitology 19, 139168.

T. Shea-Donohue , C. Sullivan , F.D. Finkelman , K.B. Madden , S.C. Morris , J. Goldhill , V. Pineiro-Carrero & J.F. Urban Jr (2001) The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. Journal of Immunology 167, 22342239.

M.B. Tuohy , D.A. Lammas , D. Wakelin , J.F. Huntley , G.F. Newlands & H.R.P. Miller (1990) Functional correlations between mucosal mast cell activity and immunity to Trichinella spiralis in high and low responder mice. Parasite Immunology 12, 675685.

J.F. Urban , I.M. Katona , W.E. Paul & F.D. Finkelman (1991) Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proceedings of the National Academy of Sciences, USA 88, 55135517.

J.F. Urban , K.B. Madden , A. Svetic , A. Cheever , P.P. Trotta , W.C. Guuse , I.M. Katona & F.D. Finkelman (1992) The importance of Th2 cytokines in protective immunity to nematodes. Immunological Reviews 127, 205219.

F.N. Wahid & J.M. Behnke (1993) Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): parasite specific IgG1 antibody responses and primary response phenotype. Parasite Immunology 15, 401413.

F.N. Wahid , M. Robinson & J.M. Behnke (1989) Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): expulsion of adult worms from fast responder syngeneic and hybrid strains of mice. Parasitology 98, 459469.

D. Wakelin (1993) Allergic inflammation as a hypothesis for the expulsion of worms from tissues. Parasitology Today 9, 115116.

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Journal of Helminthology
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