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Differential N-glycan- and protein-directed immune responses in Dictyocaulus viviparus-infected and vaccinated calves

Published online by Cambridge University Press:  11 October 2006

F. N. J. KOOYMAN ,
H. W. PLOEGER ,
J. HÖGLUND  and
J. P. M. VAN PUTTEN
F. N. J. KOOYMAN
Affiliation:
Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, The Netherlands
H. W. PLOEGER
Affiliation:
Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, The Netherlands
J. HÖGLUND
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agriculture Sciences, S-751 89 Uppsala, Sweden
J. P. M. VAN PUTTEN
Affiliation:
Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, The Netherlands
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Abstract

Calves with naturally acquired Dictyocaulus viviparus infection mount an effective immune response. In the search for protection-inducing antigens, we found that several D. viviparus third-stage larval (L3) and adult ES products carry N-glycans. Deglycosylation of the worm antigens using PNGase F resulted in reduced IgA, IgE, IgG1 and IgG2 (but not IgM) reactivities in sera of primary infected animals, suggesting that the carbohydrate moieties contained immunodominant epitopes. Challenge infection resulted in increased specific serum antibody levels against ES and L3 in the re-infected and challenge control groups. Testing of sera by enzyme-linked immunosorbent assay (ELISA) demonstrated a significant increase in IgG1 and IgE (but not IgA or IgG2) reactivity against the deglycosylated antigens in the re-infected group compared with the challenge control group. Sera from calves vaccinated with irradiated larvae showed a strong anti-N-glycan response, but no booster response against the protein backbone after challenge infection, consistent with the absence of a memory response. Together, our results suggest that D. viviparus proteins carry immunodominant N-glycan moieties that elicit a strong but short-lived immune response during infection and after vaccination, whereas the protein backbones effectively induce a memory response which results in a long-lasting, potentially protective immune response in re-infected, but not in vaccinated calves.

Keywords

Dictyocaulus viviparusN-glycans, PNGase Fantibody isotypememory response
Type
Research Article
Information
Parasitology , Volume 134 , Issue 2 , February 2007 , pp. 269 - 279
Copyright
2006 Cambridge University Press

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References

REFERENCES

Bradford, M. M. ( 1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle Scholar
Britton, C., Canto, G. J., Urquhart, G. M. and Kennedy, M. W. ( 1993). Characterization of excretory-secretory products of adult Dictyocaulus viviparus and the antibody response to them in infection and vaccination. Parasite Immunology 15, 163–174.CrossRefGoogle Scholar
Britton, C., Moore, J., Gilleard, J. S. and Kennedy, M. W. ( 1995). Extensive diversity in repeat unit sequences of the cDNA encoding the polyprotein antigen/allergen from the bovine lungworm Dictyocaulus viviparus. Molecular Biochemical Parasitology 109, 57–67.CrossRefGoogle Scholar
Eberl, M., Langermans, J. A. M., Frost, P. A., Vervenne, R. A., van Dam, G. J., Deelder, A. M., Thomas, A. W., Coulson, P. S. and Wilson, R. A. ( 2001). Cellular and humoral immune responses and protection against schistosomes induced by a radiation-attenuated vaccine in chimpanzees. Infection and Immunity 69, 5352–5362.CrossRefGoogle Scholar
Eysker, M. and Kooyman, F. N. J. ( 1993). Notes on necropsy and herbage processing techniques for gastrointestinal nematodes of ruminants. Veterinary Parasitology 46, 205–213.CrossRefGoogle Scholar
Eysker, M., Boersema, J. H. and Hendrikx, W. M. ( 1990). Recovery of different stages of Dictyocaulus viviparus from cattle lungs by a combination of a perfusion and a Baermann technique. Research in Veterinary Science 49, 373–374.Google Scholar
Haslam, S. M., Coles, G. C., Morris, H. R. and Dell, A. ( 2000). Structural characterization of the N-glycans of Dictyocaulus viviparus: discovery of the Lewis(x) structure in a nematode. Glycobiology 10, 223–229.CrossRefGoogle Scholar
Hein, W. R. and Harrison, G. B. ( 2005). Vaccines against veterinary helminths. Veterinary Parasitology 132, 217–222.CrossRefGoogle Scholar
Höglund, J., Ganheim, C. and Alenius, S. ( 2003). The effect of treatment with eprinomectin on lungworms at early patency on the development of immunity in young cattle. Veterinary Parasitology 114, 205–214.CrossRefGoogle Scholar
Janeway, C. A., Travers, P., Walport, M. and Shlomchik, M. J. ( 2005). Immunobiology. The Immune System in Health and Disease. 6th Edn. Taylor and Francis Group, New York.
Jarrett, W. F., Jennings, F. W., McIntyre, W. I., Mulligan, W. and Urquhart, G. M. ( 1955). Immunological studies on Dictyocaulus viviparus infection. Passive immunisation. Veterinary Record 67, 291–296.Google Scholar
Johnson, D. R., Sales, J. and Matthews, J. B. ( 2005). Local cytokine responses in Dictyocaulus viviparus infection. Veterinary Parasitology 128, 309–318.CrossRefGoogle Scholar
Johnson, M., Labes, R. E., Taylor, M. J. and Mackintosh, C. G. ( 2003). Efficacy trial of an irradiated cattle lungworm vaccine in red deer (Cervus elaphus). Veterinary Parasitology 117, 131–137.CrossRefGoogle Scholar
Khoo, K. H. and Dell, A. ( 2001). Glycoconjugates from parasitic helminths: structure diversity and immunobiological implications. Advances in Experimental Medicine and Biology 491, 185–205.CrossRefGoogle Scholar
Kooyman, F. N. J., Yatsuda, A. P., Ploeger, H. W. and Eysker, M. ( 2002). Serum immunoglobulin E response in calves infected with the lungworm Dictyocaulus viviparus and its correlation with protection. Parasite Immunology 24, 47–56.CrossRefGoogle Scholar
Lazari, O., Selkirk, M. E., Ploeger, H. W. and Matthews, J. B. ( 2004). A putative neuromuscular acetylcholinesterase gene from Dictyocaulus viviparus. Molecular and Biochemical Parasitology 136, 313–317.CrossRefGoogle Scholar
Matthews, J. B., Davidson, A. J., Freeman, K. L. and French, N. P. ( 2001). Immunisation of cattle with recombinant acetylcholinesterase from Dictyocaulus viviparus and with adult worm ES products. International Journal for Parasitology 31, 307–317.CrossRefGoogle Scholar
McKeand, J. B., Knox, D. P., Duncan, J. L. and Kennedy, M. W. ( 1994). The immunogenicity of the acetylcholinesterases of the cattle lungworm Dictyocaulus viviparus. International Journal for Parasitology 4, 501–510.CrossRefGoogle Scholar
McKeand, J. B., Knox, D. P., Duncan, J. L. and Kennedy, M. W. ( 1995). Immunisation of guinea pigs against Dictyocaulus viviparus using adult ES products enriched for acetylcholinesterases. International Journal for Parasitology 25, 829–837.CrossRefGoogle Scholar
McKeand, J. B., Duncan, J. L., Urquhart, G. M. and Kennedy, M. W. ( 1996). Isotype-specific antibody responses to the surface-exposed antigens of adult and larval stages of Dictyocaulus viviparus in infected and vaccinated calves. Veterinary Parasitology 61, 287–295.CrossRefGoogle Scholar
Michel, J. F. ( 1962). Studies on resistance to Dictyocaulus infection. IV. The rate of acquisition of protective immunity in infection of D. viviparus. Journal of Comparative Pathology 72, 281–285.CrossRefGoogle Scholar
Michel, J. F. and Mackenzie, A. ( 1965). Duration of the acquired resistance of calves to infection with Dictyocaulus viviparus. Research in Veterinary Science 64, 344–395.Google Scholar
Nyame, A. K., Leppänen, A. M., Bogitsh, B. J. and Cummings, R. D. ( 2000). Antibody responses to the fucosylated LacdiNAc Glycan antigen in Schistosoma mansoni-infected mice and expression of the glycan among schistosomes. Experimental Parasitology 96, 202–212.CrossRefGoogle Scholar
Richter, D., Incani, R. N. and Harn, D. A. ( 1996). Lacto-N-fucopentaose III (Lewis x), a target of the antibody response in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Infection and Immunity 64, 1826–1831.Google Scholar
Schallig, H. D., van Leeuwen, M. A. and Hendrikx, W. M. ( 1994). Immune responses of Texel sheep to excretory/secretory products of adult Haemonchus contortus. Parasitology 108, 351–357.CrossRefGoogle Scholar
Scott, C. A., McKeand, J. B. and Devaney, E. ( 1996). A longitudinal study of local and peripheral isotype/subclass antibodies in Dictyocaulus viviparus-infected calves. Veterinary Immunology and Immunopathology 53, 235–247.CrossRefGoogle Scholar
Schnieder, T. ( 1993). The diagnostic antigen encoded by gene fragment Dv3-14: a major sperm protein of Dictyocaulus viviparus. International Journal for Parasitology 23, 383–389.CrossRefGoogle Scholar
Thomas, P. G. and Harn, D. A., Jr. ( 2004). Immune biasing by helminth glycans. Cellular Microbiology 6, 13–22.CrossRefGoogle Scholar
Vervelde, L., Bakker, N., Kooyman, F. N. J, Cornelissen, A. W., Bank, C. M., Nyame A. K., Cummings, R. D. and van Die, I. ( 2003). Vaccination-induced protection of lambs against the parasitic nematode Haemonchus contortus correlates with high IgG antibody responses to the LDNF glycan antigen. Glycobiology 13, 795–804.CrossRefGoogle Scholar