Proteins secreted by the parasitic nematode Nippostrongylus brasiliensis act as adjuvants for Th2 responses

European Journal of Immunology

Volumn 30, Issue 7, 2000, Pages 1977-1987

  Holland, Martin J ^a   Harcus, Yvonne M ^a   Riches, Philip L ^a   Maizels, Rick M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Helminth parasite; Immunomodulator; Th1 Th2

Indexed keywords

FREUND ADJUVANT; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 4; LYSOZYME; PARASITE ANTIGEN; POLYCLONAL ANTIBODY; PROTEINASE K; SECRETORY PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; HEATING; IMMUNIZATION; LYMPHOCYTE PROLIFERATION; MOUSE; NEMATODIASIS; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; TH1 CELL; TH2 CELL;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS, HELMINTH; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; GENOTYPE; HELMINTH PROTEINS; IMMUNIZATION; IMMUNOGLOBULIN E; INTERFERON TYPE II; INTERLEUKIN-4; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED CBA; NIPPOSTRONGYLUS; RATS; RATS, SPRAGUE-DAWLEY; TH2 CELLS;

EID: 0033922732     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/1521-4141(200007)30:7<1977::AID-IMMU1977>3.0.CO;2-3     Document Type: Article

References (65)

1. Abbas, A. K., Murphy, K. M. and Sher, A., Functional diversity of helper T lymphocytes. Nature 1996. 383: 787-793.
2. Mosmann, T. R. and Sad, S., The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol. Today 1996. 17: 138-146.
3. + T cell responses: alternative approaches. Annu. Rev. Immunol. 1997. 15: 297-322.
4. Gause, W. C., Halvorson, M. J., Lu, P., Greenwald, R., Linsley, P., Urban, J. F. and Finkelman, F. D., The function of costimulatory molecules and the development of IL-4-producing T cells. Immunol. Today 1997. 18: 115-120.
5. O'Garra, A., Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 1998. 8: 275-283.
6. Allen, J. E. and Maizels, R. M., Th1-Th2: reliable paradigm or dangerous dogma? Immunol. Today 1997. 18: 387-392.
7. Matsuda, S., Uchikawa, R., Yamada, M. and Arizono, N., Cytokine mRNA expression profiles in rats infected with the intestinal nematode Nippostrongylus brasiliensis. Infect. Immun. 1995. 63: 4653-4660.
8. Lebrun, P. and Spiegelberg, H. L., Concomitant immunoglobulin E and immunoglobulin G1 formation in Nippostrongylus brasiliensis-infected mice. J. Immunol. 1987. 139: 1459-1465.
9. Street, N. E., Schumacher, J. H., Fong, T. A. T., Bass, H., Fiorentino, D. F., Leverah, J. A. and Mosmann, T. R., Heterogeneity of mouse helper T cells. Evidence from bulk cultures and limiting dilution cloning for precursors of Th1 and Th2 cells. J. Immunol. 1990. 144: 1629-1639.
10. Urban, J. F., Madden, K. B., Svetić, A., Cheever, A., Trotta, P. P., Gause, W. C., Katona, I. M. and Finkelman, F. D., The importance of Th2 cytokines in protective immunity to nematodes. Immunol. Rev. 1992. 127: 205-220.
11. Uchikawa, R., Yamada, M., Matsuda, S. and Arizono, N., IgE antibody responses induced by transplantation of the nematode Nippostrongylus brasiliensis in rats: a possible role of nematode excretory-secretory product in IgE production. Immunology 1993. 80: 541-545.
12. Lawrence, R. A., Gray, C., Osborne, J. and Maizels, R. M., Nippostrongylus brasiliensis: Cytokine responses and nematode expulsion in normal and IL-4-deficient mice. Exp. Parasitol. 1996. 84: 65-73.
13. Finkleman, F. D., Shea-Donohue, T., Goldhill, J., Sullivan, C. A., Morris, S. C., Madden, K. B., Gause, W. C. and Urban, J. F., Jr., Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 1997. 15: 505-533.
14. Barner, M., Welte, M., Brombacher, F. and Kopf, M., Differences between IL-4Rα and IL-4-deficient mice reveal a novel role of IL-13 in the regulation of Th2 responses. Curr. Biol. 1998. 8: 669-672.
15. Urban, J. F., Jr., Noben-Trauth, N., Donaldson, D. D., Madden, K. B., Morris, S. C., Collins, M. and Finkelman, F. D., IL-13, IL-4Rα and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 1998. 8: 255-264.
16. McKenzie, G. J., Bancroft, A., Grencis, R. K. and McKenzie, A. N. J., A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr. Biol. 1998. 8: 339-342.
17. McKenzie, G. J., Fallen, P. G., Emson, C. L, Grencis, R. K. and McKenzie, A. N., Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J. Exp. Med. 1999. 189: 1565-1572.
18. Ogilvie, B. M., Mackenzie, C. D. and Love, R. J., Lymphocytes and eosinophils in the immune response of rats to initial and subsequent infections with Nippostrongylus brasiliensis. Am. J. Trop. Med. Hyg. 1977. 26: 61-67.
19. Coffman, R. L., Seymour, B. W. P., Hudak, S., Jackson, J. and Rennick, D., Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 1989. 245: 308-310.
20. Miller, H. R. P. and Jarrett, W. F. H., Immune reactions in mucous membranes. I. Intestinal mast cell response during helminth expulsion in the rat. Immunology 1971. 20: 277-288.
21. Kühn, R., Rajewsky, K. and Müller, W., Generation and analysis of interleukin-4 deficient mice. Science 1991. 254: 707-710.
22. Kopf, M., Le Gros, G., Bachmann, M., Lamers, M. C., Bluethmann, H. and Köhler, G., Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature 1993. 362: 245-248.
23. Maizels, R. M. and Holland, M. J., Parasite immunity: pathways for expelling intestinal parasites. Curr. Biol. 1998. 8: R711-R714.
24. Jarrett, E. E. E. and Stewart, D. C., Potentiation of rat reagenic (IgE) antibody by Nippostrongylus brasiliensis infection: effect of modifications of the life cycle of the parasite in the host. Clin. Exp. Immunol. 1973. 15: 79-85.
25. Kullberg, M. C., Pearce, E. J., Hieny, S. E., Sher, A. and Berzofsky, J. A., Infection with Schistosoma mansoni alters Th1/Th2 cytokine responses to a non-parasite antigen. J. Immunol. 1992. 148: 3264-3270.
26. + cytotoxic T-cell and Th1 cytokine responses as well as delayed virus clearance. Proc. Natl. Acad. Sci. USA 1993. 90: 948-952.
27. Sabin, E. A., Araujo, M. I., Carvalho, E. M. and Pearce, E. J., Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J. Infect. Dis. 1996. 173: 269-272.
28. Curry, A. J., Else, K. J., Bancroft, A., Grencis, R. K. and Dunne, D. W., Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. J. Exp. Med. 1995. 181: 769-774.
29. Cooke, A., Tonks, P., Jones, F. M., O'Shea, H., Hutchings, P., Fulford, A. J. and Dunne, D. W., Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in nonobese diabetic mice. Parasite Immunol. 1999. 21: 169-176.
30. H2 immunity in neonatal mice. Science 1996. 271: 1728-1730.
31. Yip, H. C., Karulin, A. Y., Tary-Lehmann, M., Hesse, M. D., Radeke, H., Heeger, P. S., Trezza, R. P., Heinzel, F. P., Forsthuber, T. and Lehmann, P. V., Adjuvant-guided type-1 and type-2 immunity: infectious/noninfectious dichotomy defines the class of response. J. Immunol. 1999. 162: 3942-3949.
32. H1 cell development. Science 1996. 271: 984-987.
33. Seder, R. A. and Paul, W. E., Acquisition of lymphokine-producing phenotype by CD4' T cells. Annu. Rev. Immunol. 1994. 12: 635-673.
34. Del Prete, G. F., De Carli, M., Mastromauro, C., Biagiotti, R., Macchia, D., Falagiani, P., Picci, M. and Romagnani, S., Purified protein derivative of Mycobacterium tuberculosis and excretory-secretory antigen(s) of Toxocara canis expand human T cells with stable and opposite (type 1 T helper or type 2 T helper) profile of cytokine production. J. Clin. Invest. 1991. 88: 346-350.
35. Sartono, E., Kruize, Y. C. M., Kurniawan, A., Maizels, R. M. and Yazdanbakhsh, M., In Th2 biased lymphatic filarial patients, responses to PPD remain Th1. Eur. J. Immunol. 1996. 26: 501-504.
36. Yang, R. B., Mark, M. R., Gray, A., Huang, A., Xie, M. H., Zhang, M., Goddard, A., Wood, W., I., Gurney, A. L. and Godowski, P. J., Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 1998. 395: 284-288.
37. Maizels, R. M., Bundy, D. A. P., Selkirk, M. E., Smith, D. F. and Andersen, R. M., Immunological modulation and evasion by helminth parasites in human populations. Nature 1993. 365: 797-805.
38. Locksley, R. M., Th2 cells: help for helminths. J. Exp. Med. 1994. 179: 1405-1407.
39. Allen, J. E. and Maizels, R. M., Immunology of human helminth infection. Int. Arch. Allergy Immunol. 1996. 109: 3-10.
40. Pritchard, D. I., Hewitt, C. and Moqbel, R., The relationship between immunological responsiveness controlled by T-helper 2 lymphocytes and infections with parasitic helminths. Parasitology 1997. 115: S33-S44.
41. + T cell population to the T helper 2 cell pathway. J. Immunol. 1996. 157: 3260-3269.
42. Jarrett, E. E. E. and Stewart, D. C., Potentiation of rat reagenic (IgE) antibody by helminth infection. Simultaneous potentiation of separate reagins. Immunology 1972. 23: 749-755.
43. Macedo, M. S., Faquim-Mauro, E., Ferreira, A. P. and Abrahamsohn, I. A., Immunomodulation induced by Ascaris suum extract in mice: effect of anti-interleukin-4 and anti-interleukin-10 antibodies. Scand. J. Immunol. 1998. 47: 10-18.
44. Pearlman, E., Kazura, J. W., Hazlett, F. E., Jr. and Boom, W. H., Modulation of murine cytokine responses to mycobacterial antigens by helminth-induced T helper 2 cell responses. J. Immunol. 1993. 151: 4587-4864.
45. Urban, J. F., Jr., Madden, K. B., Cheever, A. W., Trotta, P. P., Katona, I. M. and Finkelman, F. D., IFN inhibits inflammatory responses and protective immunity in mice infected with the nematode parasite, Nippostrongylus brasiliensis. J. Immunol. 1993. 151: 7086-7094.
46. Finkelman, F. D., Madden, K. B., Cheever, A. W., Katona, I. M., Morris, S. C., Gately, M. K., Hubbard, B. R., Gause, W. C. and Urban, J. F., Jr., Effects of interleukin-12 on immune responses and host protection in mice infected with intestinal nematode parasites. J. Exp. Med. 1994. 179: 1563-1572.
47. Urban, J. F., Jr., Maliszewski, C. R., Madden, K. B., Katona, I. M. and Finkelman, F. D., IL-4 treatment can cure established gastrointestinal nematode infection in immunocompetent and immunodeficient mice. J. Immunol. 1995. 154: 4675-4684.
48. Taki, S., Sato, T., Ogasawara, K., Fukuda, T., Sato, M., Hida, S., Suzuki, G., Mitsuyama, M., Shin, E.-H., Kojima, S., Taniguchi, T. and Asano, Y., Multistage regulation of Th1-type immune responses by the transcription factor IRF-1. Immunity 1997. 6: 673-679.
49. Shin, E.-H., Osada, Y., Chai, J.-Y., Matsumoto, N., Takatsu, K. and Kojima, S., Protective roles of eosinophils in Nippostrongylus brasiliensis infection. Int. Arch. Allerg. Appl. Immunol. 1997. 114 (suppl 1): 45-50.
50. Dent, L. A., Daly, C. M., Mayrhofer, G., Zimmermann, T., Hallett, A., Bignold, L. P., Greaney, J. and Parsons, J. C., Interleukin-5 transgenic mice show enhanced resistance to primary infections with Nippostrongylus brasiliensis but not primary infections with Toxocara canis. Infect. Immun. 1999. 67: 989-993.
51. Pearce, E. J., Vasconcelos, J. P., Brunet, L. R. and Sabin, E. A., IL-4 in schistosomiasis. Exp. Parasitol. 1996. 84: 295-299.
52. Brunet, L. R., Dunne, D. W. and Pearce, E. J., Cytokine interaction and immune responses during Schistosoma mansoni infection. Parasitol. Today 1998. 14: 422-427.
53. Day, K. P., Howard, R. J., Prowse, S. J., Chapman, S. B. and Mitchell, G. F., Studies on chronic versus transient intestinal nematode infections in mice. I. A comparison of responses to excretory/secretory (ES) products of Nippostrongylus brasiliensis and Nematospiroides dubius worms. Parasite Immunol. 1979. 1: 217-239.
54. Yamada, M., Nakazawa, M. and Arizono, N., IgE and IgG2a antibody responses are induced by different antigen groups of the nematode Nippostrongylus brasiliensis in rats. Immunology 1993. 78: 298-302.
55. Ferrick, D. A., Schrenzel, M. D., Mulviana, T., Hsieh, B., Ferlin, W. G. and Lepper, H., Differential production of interferon-γ and interleukin-4 in response to Th1 - and Th2-stimulating pathogens by γδ T cells in vivo. Nature 1995. 373: 255-257.
56. Conrad, D. H., Ben-Sasson, S. Z., Le Gros, G., Finkelman, F. D. and Paul, W. E., Infection with Nippostrongylus brasiliensis or injection of anti-IgD antibodies markedly enhances Fc-receptormediated interleukin 4 production by non-B, non-T cells. J. Exp. Med. 1990. 171: 1497-1508.
57. + T cells are not essential for T helper cell 2 immune responses. J. Exp. Med. 1996. 184: 1295-1304.
58. Cui, J., Watanabe, N., Kawano, T., Yamashita, M., Kamata, T., Shimizu, C., Kimura, M., Shimizu, E., Koike, J., Koseki, H., Tanaka, Y., Taniguchi, M. and Nakayama, T., Inhibition of T helper cell type 2 cell differentiation and immunoglobulin E response by ligand-activated Vα14 natural killer T cells. J. Exp. Med. 1999. 190: 783-792.
59. Constant, P., Davodeau, F., Peyrat, M.-A., Poquet, Y., Puzo, G., Bonneville, M. and Fournié, J.-J., Stimulation of human γδ T cells by nonpeptidic mycobacterial ligands. Science 1994. 264: 267-270.
60. Burdin, N. and Kronenberg, M., CD1-mediated immune responses to glycolipids., Curr. Opin. Immunol. 1999. 11: 326-331.
61. Healer, J., Ashall, F. and Maizels, R. M., Characterization of proteolytic enzymes from larval and adult Nippostrongylus brasiliensis. Parasitology 1991. 103: 305-314.
62. Kamata, I., Yamada, M., Uchikawa, R., Matsuda, S. and Arizono, N., Cysteine protease of the nematode Nippostrongylus brasiliensis preferentially evokes an IgE/IgG1 antibody response in rats. Clin. Exp. Immunol. 1995. 102: 71-77.
63. Hussein, A. S., Chacon, M. R., Smith, A. M., Tosado-Acevedo, R. and Selkirk, M. E., Cloning, expression, and properties of a nonneuronal secreted acetylcholinesterase from the parasitic nematode Nippostrongylus brasiliensis. J. Biol. Chem. 1999. 274: 9312-9319.
64. Grigg, M. E., Gounaris, K. and Selkirk, M. E., Characterization of a platelet-activating factor acetylhydrolase secreted by the nematode parasite Nippostrongylus brasiliensis. Biochem. J. 1996. 317: 541-547.
65. Lawrence, R. A., Allen, J. E., Osborne, J. and Maizels, R. M., Adult and microfilarial stages of the filarial parasite Brugia malayi stimulate contrasting cytokine and immunoglobulin isotype responses in BALB/ mice. J. Immunol. 1994. 153: 1216-1224.