Parasitology Research

, Volume 82, Issue 5, pp 445–453 | Cite as

Irradiated larval vaccination and antibody responses evaluated in relation to the expression of immunity to Heligmosomoides polygyrus

Original Paper

Abstract

Infections induced in NIH mice by irradiated (300 Gy) larvae of Heligmosomoides polygyrus effectively stimulated immunity to challenge, whereas unirra-diated larvae did not. Importantly, this difference was lost by the elimination of the adult worms arising from unirradiated sensitising infections by drug treatment prior to challenge. No difference in the level of parasite-specific serum and mucosal IgG, IgGl, IgG2a or IgA was detected between immune mice sensitised either with drug-abbreviated unirradiated or irradiated larval infections and non-immune mice receiving two superimposed unirradiated infections. An enzyme-linked immu-nosorbent assay (ELISA) and immunoblotting data suggested that parasite-specific IgGl was the predominant antibody class in both serum and intestinal perfusates. IgA exhibited differences in antigen specificity between the serum and the intestine. In serum, IgA responses were directed predominantly to L4 somatic antigens, whereas at the mucosal surface they were biased towards L4 excretory/secretory (ES) antigens. No correlation was found between the intensity of the serum or mucosal antibody responses and the mean worm burdens in groups of immune or non-immune mice. Moreover, no correlation was found between levels of parasite-specific serum or mucosal IgG, IgGl, IgG2a or IgA and the loss of worms in individual mice.

Keywords

Adult Worm Immune Mouse Worm Burden Challenge Infection Challenge Control 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bartlett A, Ball PAJ (1974) The immune response of the mouse to larvae and adults of Nematospiroides dubius. Int J Parasitol 4: 463–470PubMedCrossRefGoogle Scholar
  2. Behnke JM (1987) Evasion of immunity by nematode parasites causing chronic infections. Adv Parasitol 26:1–71PubMedCrossRefGoogle Scholar
  3. Behnke JM, Robinson M (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 Immunol 7:235–253PubMedCrossRefGoogle Scholar
  4. Behnke JM, Wakelin D (1977) N. dubius: stimulation of acquired immunity in inbred mice. J Helminthol 51:167–176PubMedGoogle Scholar
  5. Behnke JM, Hannah J, Pritchard DI 81983) Nematospiroides dubius in the mouse: evidence that adult worms depress the expression of homologous immunity. Parasite Immunol 5:397–408Google Scholar
  6. Behnke JM, Williams DJ, Hannah J, Pritchard DI (1987) Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): the capacity of adult worms to survive following transplantation to recipient mice. Parasitology 95:569–581PubMedGoogle Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  8. Brailsford TJ, Behnke JM (1992) The dynamics of trickle infections with Heligmosomoides polygyrus in syngeneic strains of mice. Int J Parasitol 22:651–659CrossRefGoogle Scholar
  9. Cayzer C, Dobson C (1983) Suppression of antibody production in mice given multiple concurrent infections with Nematospiroides dubius. Int J Parasitol 13:61–65PubMedCrossRefGoogle Scholar
  10. Crandall RB, Crandall CA, Franco JA (1974) Heligmosomoides polygyrus: humoral and intestinal immunological responses to infection in mice. Exp Parasitol 35:275–287PubMedCrossRefGoogle Scholar
  11. Cypess RH, Ebersole JL, Molinari JA (1977) Specific antibody levels in the intestinal perfusates of Heligmosomoides polygyrus infected mice. Int Arch Allergy Appl Immunol 55:496–503PubMedGoogle Scholar
  12. DeVos T, Danell G, Dick TA (1992) Trichinella spiralis: dose dependence and kinetics of the mucosal immune response. Exp Parasitol 75:99–111CrossRefGoogle Scholar
  13. Dobson C (1982) Passive transfer of immunity with serum in mice infected with Nematospiroides dubius: influence of quality and quantity of immune serum. Int J Parasitol 12:207–213PubMedCrossRefGoogle Scholar
  14. Elson CO, Ealding W, Lefkowitz J (1984) A lavage technique allowing repeated measurement of IgA antibody in mouse intestinal secretions. J Immunol Methods 67:101–108PubMedCrossRefGoogle Scholar
  15. Enriquez FJ, Boggavarapu J, Bradley-Dunlop D (1993) Presence of non Fab IgE binding molecules in the intestinal nematode parasite of mice, Heligmosomoides polygyrus. Int Arch Allergy Immunol 99:123–126CrossRefGoogle Scholar
  16. Ey PL, Prowse SJ, Jenkins CR (1981) H. polygyrus: simple recovery of postinfective larvae from mouse intestines. Exp Parasitol 52:69–76PubMedCrossRefGoogle Scholar
  17. Hagan P, Behnke JM, Parish HA (1981) Stimulation of immunity to N. dubius in mice using larvae attenuated by cobalt 60 irradiation. Parasite Immunol 3:149–156PubMedCrossRefGoogle Scholar
  18. Jacobsen RH, Brooks BO, Cypess RH (1982) Immunity to Nematospiroides dubius: parasite stages responsible for and subject to resistance in high responder (LAF/J) mice. J Parasitol 68: 1053–1058CrossRefGoogle Scholar
  19. Kerr MA (1990) The structure and function of IgA. Biochem J 271:271–296Google Scholar
  20. Laemmli EK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  21. Larrick KS, Semprevino LH, Maloney MD, Tritschler JP (1991) Immunity to Helimosomoides polygyrus induced by subcutaneous vaccination with postinfective larvae. Int J Parasitol 21: 321–328PubMedCrossRefGoogle Scholar
  22. Lloyd S, Soulsby EJL (1978) The role of IgA immunoglobulin in the passive transfer of protection to Taenia taeniaeformis in the mouse. Immunology 34:939–945PubMedGoogle Scholar
  23. Molinari JA, Ebersole JL, Cypess RH (1978) Specific antibody levels in the serum of Heligmosomoides polygyrus infected mice. J Parasitol 64:233–238PubMedCrossRefGoogle Scholar
  24. Monroy FG, Enriquez FJ (1992) Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitol Today 8:49–54PubMedCrossRefGoogle Scholar
  25. Pleass RJ, Bianco AE (1994) The role of adult worms in suppressing functional protective immunity to Heligmosomoides polygyrus bakeri challenge infections. Parasite Immunol 16:619–628PubMedCrossRefGoogle Scholar
  26. Pleass RJ, Bianco AE (1995) The effects of gamma radiation on the development of Heligmosomoides polygyrus bakeri in mice. Int J Parasitol 25:1099–1109PubMedCrossRefGoogle Scholar
  27. Pritchard DI, Williams DJL, Behnke JM, Lee TDG (1983) The role of IgGl hypergammaglobulinaemia in immunity to the gastrointestinal nematode Nematospiroides dubius. The immu-nochemical purification, antigen specificity and in vivo anti-parasitic effect of IgGl from immune serum. Immunology 49: 353–365PubMedGoogle Scholar
  28. Pritchard DI, Maizels RM, Behnke JM, Appleby P (1984a) Stage-specific antigens of M dubius. Immunology 53:325–335Google Scholar
  29. Pritchard DI, Behnke JM, Williams DJL (1984b) Primary infection sera and IgGl do not block host-protective immunity to Nematospiroides dubius. Immunology 51:73–81Google Scholar
  30. Prowse SJ, Mitchell GF, Ey PL, Jenkin CR (1978) Nematospiroides dubius: susceptibility to infection and development of resistance in hypothalmic (nude) BALB/c mice. Aust J Exp Biol Med Sci 56:561–570PubMedCrossRefGoogle Scholar
  31. Prowse SJ, Mitchell GF, Ey PL, Jenkin CR (1979) The development of resistance in different inbred strains of mice to infection with Nematospiroides dubius. Parasite Immunol 1:277–288PubMedCrossRefGoogle Scholar
  32. Roach TIA, Else KJ, Wakelin D, McLaren DJ, Grencis RK (1991) Trichuris muris: antigen recognition and transfer of immunity in mice by IgA monoclonal antibodies. Parasite Immunol 13:1–12PubMedCrossRefGoogle Scholar
  33. Snapper CM, Mond JJ (1993) Towards a comprehensive view of immunoglobulin class switching. Immunol today 14:15–17PubMedCrossRefGoogle Scholar
  34. Sukhdeo MVK, Croll NA (1981) The location of parasites within their hosts: bile and the site selection behaviour of Nematospiroides dubius. Int J Parasitol 11:157–162PubMedCrossRefGoogle Scholar
  35. Tarleton RL, Kemp WM (1981) Demonstration of IgG-Fc and C3 receptors on adult Schistosoma mansoni. J Immunol 126: 379–384PubMedGoogle Scholar
  36. Torpier G, Capron A, Ouaissi MA (1979) Receptor for IgG(Fc) and human β2-microglobulin on S. mansoni schistosomula. Nature 278:447–449PubMedCrossRefGoogle Scholar
  37. Voller A, Bartlett A, Bidwell DE (1978) Enzyme immunoassays with special reference to ELIS A techniques. J Clin Pathol 31:507–520PubMedCrossRefGoogle Scholar
  38. Wahid FN, Behnke JM (1992) Stimuli for acquired resistance to Heligmosomoides polygyrus from intestinal from intestinal tissue resident L3 and L4 larvae. Int J Parasitol 22:699–710PubMedCrossRefGoogle Scholar
  39. Williams DJ, Behnke JM (1983) Host protective antibodies and serum immunoglobulin isotypes in mice chronically infected or repeatedly immunised with the nematode parasite Nematospiroides dubius. Immunology 48:37–47PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  1. 1.Department of PathologyNinewells HospitalDundeeScotland
  2. 2.Liverpool School of Tropical MedicineLiverpoolUK

Personalised recommendations