Modulation of a heterologous immune response by the products of Ascaris suum

Infection and Immunity

Volumn 70, Issue 11, 2002, Pages 6058-6067

  Paterson, Jacqueline C M ^a   Garside, Paul ^a   Kennedy, Malcolm W ^a   Lawrence, Catherine E ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABA 1 PROTEIN; ALLERGEN; CYTOKINE; FATTY ACID BINDING PROTEIN; GAMMA INTERFERON; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; MONOCLONAL ANTIBODY; OVALBUMIN; PARASITE ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; ASCARIASIS; ASCARIS SUUM; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; FEMALE; HELMINTHIASIS; IMMUNE RESPONSE; IMMUNOMODULATION; INTESTINE PARASITE; LYMPHOCYTE CULTURE; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MOUSE; NONHUMAN; PARASITE; PRIORITY JOURNAL; TH2 CELL;

ALLERGENS; ANIMALS; ANTIGENS, HELMINTH; ASCARIS SUUM; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; FEMALE; HELMINTH PROTEINS; HYPERSENSITIVITY, DELAYED; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTERFERON TYPE II; INTERLEUKIN-10; INTERLEUKIN-4; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, INBRED BALB C; OVALBUMIN; T-LYMPHOCYTES;

EID: 0036841013     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.70.11.6058-6067.2002     Document Type: Article

References (61)

1. Abbas, A. K., K. M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature 383:787-793.
2. + cytotoxic T-cell and Thl cytokine responses as well as delayed virus clearance. Proc. Natl. Acad. Sci. USA 90:948-952.
3. Agersborg, S. S., K. M. Garza, and K. S. Tung. 2001. Intestinal parasitism terminates self tolerance and enhances neonatal induction of autoimmune disease and memory. Eur. J. Immunol. 31:851-859.
4. Allen, J. E., R. A. Lawrence, and R. M. Maizels. 1996. APC from mice harbouring the filarial nematode, Brugia malayi, prevent cellular proliferation but not cytokine production. Int. Immunol. 8:143-151.
5. Allen, J. E., and A. S. MacDonald. 1998. Profound suppression of cellular proliferation mediated by the secretions of nematodes. Parasite Immunol. 20:241-247.
6. Asseman, C., S. Mauze, M. W. Leach, R. L. Coffman, and F. Powrie. 1999. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190:995-1004.
7. Blackburn, C. C., and M. E. Selkirk. 1992. Inactivation of platelet-activating factor by a putative acetylhydrolase from the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunology 75:41-46.
8. Bridoux, F., A. Badou, A. Saoudi, I. Bernard, E. Druet, R. Pasquier, P. Druet, and L. Pelletier. 1997. Transforming growth factor beta (TGF-beta)-dependent inhibition of T helper cell 2 (Th2)-induced autoimmunity by self-major histocompatibility complex (MHC) class II-specific, regulatory CD4(+) T cell lines. J. Exp. Med. 185:1769-1775.
9. Bundy, D. A. 1994. Immunoepidemiology of intestinal helminthic infections. 1. The global burden of intestinal nematode disease. Trans. R. Soc. Trop. Med. Hyg. 88:259-261.
10. Cher, D. J., and T. R. Mosmann. 1987. Two types of murine helper T cell clone. II. Delayed-type hypersensitivity is mediated by TH1 clones. J. Immunol. 138:3688-3694.
11. Cooper, P. J., M. Chico, C. Sandoval, I. Espinel, A. Guevara, M. M. Levine, G. E. Griffin, and T. B. Nutman. 2001. Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect. Immun. 69:1574-1580.
12. Culley, F. J., A. Brown, D. M. Conroy, I. Sabroe, D. I. Pritchard, and T. J. Williams. 2000. Eotaxin is specifically cleaved by hookworm metalloproteases, preventing its action in vitro and in vivo. J. Immunol. 165:6447-6453.
13. Deehan, M. R., M. M. Harnett, and W. Harnett. 1997. A filarial nematode secreted product differentially modulates expression and activation of protein kinase C isoforms in B lymphocytes. J. Immunol. 159:6105-6111.
14. Ehigiator, H. N., A. W. Stadnyk, and T. D. Lee. 2000. Extract of Nippostronglus brasiliensis stimulates polyclonal type-2 immunoglobulin response by inducing de novo class switch. Infect. Immun. 68:4913-4922.
15. Ehigiator, H. N., A. W. Stadnyk, and T. D. Lee. 2000. Modulation of B-cell proliferative response by a soluble extract of Nippostrongylus brasiliensis. Infect. Immun. 68:6154-6161.
16. Else, K. J., F. D. Finkelman, C. R. Maliszewski, and R. K. Grencis. 1994. Cytokine-mediated regulation of chronic intestinal helminth infection. J. Exp. Med. 179:347-351.
17. Falcone, F. H., A. G. Rossi, R. Sharkey, A. P. Brown, D. I. Pritchard, and R. M. Maizels. 2001. Ascaris suum-derived products induce human neutrophil activation via a G protein-coupled receptor that interacts with the interleukin-8 receptor pathway. Infect. Immun. 69:4007-4018.
18. Faquim-Mauro, E. L., and M. S. Macedo. 1998. The immunosuppressive activity of Ascaris suum is due to high molecular weight components. Clin. Exp. Immunol. 114:245-251.
19. Ferreira, A. P., E. S. Faquim, I. A. Abrahamsohn, and M. S. Macedo. 1995. Immunization with Ascaris suum extract impairs T cell functions in mice. Cell. Immunol. 162:202-210.
20. Fine, P. E. 1995. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346:1339-1345.
21. Fiorentino, D. F., A. Zlotnik, P. Vieira, T. R. Mosmann, M. Howard, K. W. Moore, and A. O'Garra. 1991. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J. Immunol. 146:3444-3451.
22. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389:737-742.
23. Harnett, W., and M. M. Harnett. 1993. Inhibition of murine B cell proliferation and down-regulation of protein kinase C levels by a phosphorylcholinecontaining filarial excretory-secretory product. J. Immunol. 151:4829-4837.
24. Harnett, W., and M. M. Harnett. 2001. Modulation of the host immune system by phosphorylcholine-containing glycoproteins secreted by parasitic filarial nematodes. Biochim. Biophys. Acta 1539:7-15.
25. Holland, M. J., Y. M. Harcus, P. L. Riches, and R. M. Maizels. 2000. Proteins secreted by the parasitic nematode Nippostrongvlus brasiliensis act as adjuvants for Th2 responses. Eur. J. Immunol. 30:1977-1987.
26. Houston, K. M., E. H. Wilson, L. Eyres, F. Brombacher, M. M. Harnett, J. Alexander, and W. Harnett. 2000. Presence of phosphorylcholine on a filarial nematode protein influences immunoglobulin G subclass response to the molecule by an interleukin-10-dependent mechanism. Infect. Immun. 68:5466-5468.
27. Jarrett, E. E., and H. R. Miller. 1982. Production and activities of IgE in helminth infection. Prog. Allergy 31:178-233.
28. Kasper, G., A. Brown, M. Eberl, L. Vallar, N. Kieffer, C. Berry, K. Girdwood, P. Eggleton, R. Quinnell, and D. I. Pritchard. 2001. A calreticulin-like molecule from the human hookworm Necator americanus interacts with C1q and the cytoplasmic signalling domains of some integrins. Parasite Immunol. 23:141-152.
29. Kennedy, M. W. 2000. The nematode polyprotein allergens/antigens. Parasitol. Today 16:373-380.
30. Kennedy, M. W., A. Brass, A. B. McCruden, N. C. Price, S. M. Kelly, and A. Cooper. 1995. The ABA-1 allergen of the parasitic nematode Ascaris suum: fatty acid and retinoid binding function and structural characterization. Biochemistry 34:6700-6710.
31. Kennedy, M. W., L. A. Tomlinson, E. M. Fraser, and J. F. Christie. 1990. The specificity of the antibody response to internal antigens of Ascaris: heterogeneity in infected humans, and MHC (H-2) control of the repertoire in mice. Clin. Exp. Immunol. 80:219-224.
32. King, C. L., V. Kumaraswami, R. W. Poindexter, S. Kumari, K. Jayaraman, D. W. Alling, E. A. Ottesen, and T. B. Nutman. 1992. Immunologic tolerance in lymphatic filariasis. Diminished parasite-specific T and B lymphocyte precursor frequency in the microfilaremic state. J. Clin. Investig. 89:1403-1410.
33. Lawrence, C. E., J. C. Paterson, L. M. Higgins, T. T. MacDonald, M. W. Kennedy, and P. Garside. 1998. IL-4-regulated enteropathy in an intestinal nematode infection. Eur. J. Immunol. 28:2672-2684.
34. Liwski, R., J. Zhou, V. McAlister, and T. D. Lee. 2000. Prolongation of allograft survival by Nippostrongvlus brasiliensis is associated with decreased allospecific cytotoxic T lymphocyte activity and development of T cytotoxic cell type 2 cells. Transplantation 69:1912-1922.
35. Lochnit, G., R. D. Dennis, H. Muntefehr, S. Nispel, and R. Geyer. 2001. Immunohistochemical localization and differentiation of phosphocholine-containing antigens of the porcine, parasitic nematode Ascaris suum. Parasitology 122:359-370.
36. Lochnit, G., R. D. Dennis, A. J. Ulmer, and R. Geyer. 1998. Structural elucidation and monokine-inducing activity of two biologically active zwitterionic glycosphingolipids derived from the porcine parasitic nematode Ascaris suum. J. Biol. Chem. 273:466-474.
37. MacDonald, A. S., R. M. Maizels, R. A. Lawrence, I. Dransfield, and J. E. Allen. 1998. Requirement for in vivo production of IL-4, but not IL-10, in the induction of proliferative suppression by filarial parasites. J. Immunol. 160:1304-1312.
38. Macedo, M. S., E. Faquim-Mauro, A. P. Ferreira, and I. A. Abrahamsohn. 1998. Immunomodulation induced by Ascaris suum extract in mice: effect of anti-interleukin-4 and anti-interleukin-10 antibodies. Scand. J. Immunol. 47:10-18.
39. Mahanty, S., C. L. King, V. Kumaraswami, J. Regunathan, A. Maya, K. Jayaraman, J. S. Abrams, E. A. Ottesen, and T. B. Nutman. 1993. IL-4- and IL-5-secreting lymphocyte populations are preferentially stimulated by parasite-derived antigens in human tissue invasive nematode infections. J. Immunol. 151:3704-3711.
40. McGibbon, A. M., J. F. Christie, M. W. Kennedy, and T. D. Lee. 1990. Identification of the major Ascaris allergen and its purification to homogeneity by high-performance liquid chromatography. Mol. Biochem. Parasitol. 39:163-171.
41. McSharry, C., Y. Xia, C. V. Holland, and M. W. Kennedy. 1999. Natural immunity to Ascaris lumbricoides associated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infect. Immun. 67:484-489.
42. Moyle, M., D. L. Foster, D. E. McGrath, S. M. Brown, Y. Laroche, J. De Meutter, P. Stanssens, C. A. Bogowitz, V. A. Fried, J. A. Ely, et al. 1994. A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD11b/CD18. J. Biol. Chem. 269:10008-10015.
43. Nacher, M., F. Gay, P. Singhasivanon, S. Krudsood, S. Treeprasertsuk, D. Mazier, I. Vouldoukis, and S. Looareesuwan. 2000. Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunol. 22:107-113.
44. Ogilvie, B. M., and D. de Savigny (ed.). 1982. Immune responses to nematodes. Blackwell Scientific Publications, London, United Kingdom.
45. Palanivel, V., C. Posey, A. M. Horauf, W. Solbach, W. F. Piessens, and D. A. Harn. 1996. B-cell outgrowth and ligand-specific production of IL-10 correlate with Th2 dominance in certain parasitic diseases. Exp. Parasitol. 84:168-177.
46. Pearlman, E., J. W. Kazura, F. E. Hazlett, Jr., and W. H. Boom. 1993. Modulation of murine cytokine responses to mycobacterial antigens by helminth-induced T helper 2 cell responses. J. Immunol. 151:4857-4864.
47. Powrie, F., S. Menon, and R. L. Coffman. 1993. Interleukin-4 and interleukin-10 synergize to inhibit cell-mediated immunity in vivo. Eur. J. Immunol. 23:3043-3049.
48. Pritchard, D. I., N. M. Ali, and J. M. Behnke. 1984. Analysis of the mechanism of immunodepression following heterologous antigenic stimulation during concurrent infection with Nematospiroides dubius. Immunology 51:633-642.
49. Pritchard, D. I., A. Brown, G. Kasper, P. McElroy, A. Loukas, C. Hewitt, C. Berry, R. Fullkrug, and E. Beck. 1999. A hookworm allergen which strongly resembles calreticulin. Parasite Immunol. 21:439-450.
50. Rhoads, M. L., R. H. Fetterer, D. E. Hill, and J. F. Urban, Jr. 2000. Trichuris suis: a secretory chymotrypsin/elastase inhibitor with potential as an immunomodulator. Exp. Parasitol. 95:36-44.
51. Rocken, M., J. F. Urban, and E. M. Shevach. 1992. Infection breaks T-cell tolerance. Nature 359:79-82.
52. Schulz, O., H. F. Sewell, and F. Shakib. 1998. Proteolytic cleavage of CD25, the alpha subunit of the human T cell interleukin 2 receptor, by Der p 1, a major mite allergen with cysteine protease activity. J. Exp. Med. 187:271-275.
53. Shi, H. N., C. J. Ingui, I. Dodge, and C. Nagler-Anderson. 1998. A helminth-induced mucosal Th2 response alters nonresponsiveness to oral administration of a soluble antigen. J. Immunol. 160:2449-2455.
54. + human T cells in vitro. J. Immunol. 160:351-360.
55. Stewart, G. R., M. Boussinesq, T. Coulson, L. Elson, T. Nutman, and J. E. Bradley. 1999. Onchocerciasis modulates the immune response to mycobacterial antigens. Clin. Exp. Immunol. 117:517-523.
56. Taiwo, F. A., P. M. Brophy, D. I. Pritchard, A. Brown, A. Wardlaw, and L. H. Patterson. 1999. Cu/Zn superoxide dismutase in excretory-secretory products of the human hookworm Necator americanus. An electron paramagnetic spectrometry study. Eur. J. Biochem. 264:434-438.
57. Tomlinson, L. A., J. F. Christie, E. M. Fraser, D. McLaughlin, A. E. McIntosh, and M. W. Kennedy. 1989. MHC restriction of the antibody repertoire to secretory antigens, and a major allergen, of the nematode parasite Ascaris. J. Immunol. 143:2349-2356.
58. Urban, J. F., Jr., K. B. Madden, A. W. Cheever, P. P. Trotta, I. M. Katona, and F. D. Finkelman. 1993. IFN inhibits inflammatory responses and protective immunity in mice infected with the nematode parasite Nippostrongylus brasiliensis. J. Immunol. 151:7086-7094.
59. +) outgrowth in murine schistosomiasis is genetically restricted and is largely due to activation by polylactosamine sugars. J. Immunol. 158:338-344.
60. World Health Organization. 1981. Intestinal protozoan and helminthic infections, vol. 666. World Health Organization, Geneva, Switzerland.
61. Xia, Y., H. J. Spence, J. Moore, N. Heaney, L. McDermott, A. Cooper, D. G. Watson, B. Mei, R. Komuniecki, and M. W. Kennedy. 2000. The ABA-1 allergen of Ascaris lumbricoides: sequence polymorphism, stage- and tissue-specific expression, lipid binding function, and protein biophysical properties. Parasitology 120:211-224.